Abstract
Molecular chaperones are a group of structurally diverse and highly conserved ubiquitous proteins. They play crucial roles in facilitating the correct folding of proteins in vivo by preventing protein aggregation or facilitating the appropriate folding and assembly of proteins. Heat shock proteins form the major class of molecular chaperones that are responsible for protein folding events in the cell. This is achieved by ATP-dependent (folding machines) or ATP-independent mechanisms (holders). Heat shock proteins are induced by a variety of stresses, besides heat shock. The large and varied heat shock protein class is categorised into several subfamilies based on their sizes in kDa namely, small Hsps (HSPB), J domain proteins (Hsp40/DNAJ), Hsp60 (HSPD/E; Chaperonins), Hsp70 (HSPA), Hsp90 (HSPC), and Hsp100. Heat shock proteins are localised to different compartments in the cell to carry out tasks specific to their environment. Most heat shock proteins form large oligomeric structures, and their functions are usually regulated by a variety of cochaperones and cofactors. Heat shock proteins do not function in isolation but are rather part of the chaperone network in the cell. The general structural and functional features of the major heat shock protein families are discussed, including their roles in human disease. Their function is particularly important in disease due to increased stress in the cell. Vector-borne parasites affecting human health encounter stress during transmission between invertebrate vectors and mammalian hosts. Members of the main classes of heat shock proteins are all represented in Plasmodium falciparum, the causative agent of cerebral malaria, and they play specific functions in differentiation, cytoprotection, signal transduction, and virulence.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Acharya P, Kumar R, Tatu U (2007) Chaperoning a cellular upheaval in malaria: heat shock proteins in Plasmodium falciparum. Mol Biochem Parasitol 153(2):85–94. https://doi.org/10.1016/j.molbiopara.2007.01.009
Akerfelt M, Morimoto RI, Sistonen L (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 11(8):545–555. https://doi.org/10.1038/nrm2938
Albakova Z, Armeev GA, Kanevskiy LM, Kovalenko EI, Sapozhnikov AM (2020) HSP70 multi-functionality in cancer. Cells 9(3):587. https://doi.org/10.3390/cells9030587
Alderson TR, Roche J, Gastall HY, Dias DM, Pritišanac I, Ying J, Bax A, Benesch JLP, Baldwin AJ (2019) Local unfolding of the HSP27 monomer regulates chaperone activity. Nat Commun 10(1):1068. https://doi.org/10.1038/s41467-019-08557-8
Ali MM, Roe SM, Vaughan CK, Meyer P, Panaretou B, Piper PW, Prodromou C, Pearl LH (2006) Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 440(7087):1013–1017
Altieri DC, Stein GS, Lian JB, Languino LR (2012) TRAP-1, the mitochondrial Hsp90. Biochim Biophys Acta 1823(3):767–773. https://doi.org/10.1016/j.bbamcr.2011.08.007
Andreasson C, Fiaux J, Rampelt H, Druffel-Augustin S, Bukau B (2008) Insights into the structural dynamics of the Hsp110-Hsp70 interaction reveal the mechanism for nucleotide exchange activity. Proc Natl Acad Sci U S A 105(43):16519–16524. https://doi.org/10.1073/pnas.0804187105
Andreasson C, Rampelt H, Fiaux J, Druffel-Augustin S, Bukau B (2010) The endoplasmic reticulum Grp170 acts as a nucleotide exchange factor of Hsp70 via a mechanism similar to that of the cytosolic Hsp110. J Biol Chem 285(16):12445–12453. https://doi.org/10.1074/jbc.M109.096735
Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181(4096):223–230
Aoyagi S, Archer TK (2005) Modulating molecular chaperone Hsp90 functions through reversible acetylation. Trends Cell Biol 15(11):565–567
Archana G, Dhodapkar R, Kumar A (2017) Ecotoxicological risk assessment and seasonal variation of some pharmaceuticals and personal care products in the sewage treatment plant and surface water bodies (lakes). Environ Monit Assess 189(9):446. https://doi.org/10.1007/s10661-017-6148-3
Archer AE, Von Schulze AT, Geiger PC (2018) Exercise, heat shock proteins and insulin resistance. Philos Trans R Soc Lond B Biol Sci 373(1738):20160529. https://doi.org/10.1098/rstb.2016.0529
Argon Y, Simen BB (1999) GRP94, an ER chaperone with protein and peptide binding properties. Semin Cell Dev Biol 10(5):495–505
Aron R, Lopez N, Walter W, Craig EA, Johnson J (2005) In vivo bipartite interaction between the Hsp40 Sis1 and Hsp70 in Saccharomyces cerevisiae. Genetics 169(4):1873–1882. https://doi.org/10.1534/genetics.104.037242
Arsene F, Tomoyasu T, Bukau B (2000) The heat shock response of Escherichia coli. Int J Food Microbiol 55(1-3):3–9. https://doi.org/10.1016/s0168-1605(00)00206-3
Arts HJ, Hollema H, Lemstra W, Willemse PH, De Vries EG, Kampinga HH, Van der Zee AG (1999) Heat-shock-protein-27 (hsp27) expression in ovarian carcinoma: relation in response to chemotherapy and prognosis. Int J Cancer 84(3):234–238
Assenza S, Sassi AS, Kellner R, Schuler B, De Los RP, Barducci A (2019) Efficient conversion of chemical energy into mechanical work by Hsp70 chaperones. Elife 8:e48491. https://doi.org/10.7554/eLife.48491
Assimon VA, Gillies AT, Rauch JN, Gestwicki JE (2013) Hsp70 protein complexes as drug targets. Curr Pharm Des 19(3):404–417. https://doi.org/10.2174/138161213804143699
Avellaneda MJ, Franke KB, Sunderlikova V, Bukau B, Mogk A, Tans SJ (2020) Processive extrusion of polypeptide loops by a Hsp100 disaggregase. Nature 578(7794):317–320. https://doi.org/10.1038/s41586-020-1964-y
Bachman AB, Keramisanou D, Xu W, Beebe K, Moses MA, Vasantha Kumar MV, Gray G, Noor RE, van der Vaart A, Neckers L, Gelis I (2018) Phosphorylation induced cochaperone unfolding promotes kinase recruitment and client class-specific Hsp90 phosphorylation. Nat Commun 9(1):265. https://doi.org/10.1038/s41467-017-02711-w
Backe SJ, Sager RA, Woodford MR, Makedon AM, Mollapour M (2020) Post-translational modifications of Hsp90 and translating the chaperone code. J Biol Chem 295(32):11099–11117. https://doi.org/10.1074/jbc.REV120.011833
Baker-Williams AJ, Hashmi F, Budzyński MA, Woodford MR, Gleicher S, Himanen SV, Makedon AM, Friedman D, Cortes S, Namek S, Stetler-Stevenson WG, Bratslavsky G, Bah A, Mollapour M, Sistonen L, Bourboulia D (2019) Co-chaperones TIMP2 and AHA1 competitively regulate extracellular HSP90:Client MMP2 activity and matrix proteolysis. Cell Rep 28(7):1894–1906.e1896. https://doi.org/10.1016/j.celrep.2019.07.045
Ballinger CA, Connell P, Wu Y, Hu Z, Thompson LJ, Yin LY, Patterson C (1999) Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol Cell Biol 19(6):4535–4545. https://doi.org/10.1128/mcb.19.6.4535
Banumathy G, Singh V, Tatu U (2002) Host chaperones are recruited in membrane-bound complexes by Plasmodium falciparum. J Biol Chem 277(6):3902–3912
Banumathy G, Singh V, Pavithra SR, Tatu U (2003) Heat shock protein 90 function is essential for Plasmodium falciparum growth in human erythrocytes. J Biol Chem 278(20):18336–18345
Bayih AG, Pillai DR (2014) Mouse studies on inhibitors of Plasmodium falciparum Hsp90: progress and challenges. Parasitology 141(9):1216–1222. https://doi.org/10.1017/S0031182014000754
Bayih AG, Folefoc A, Mohon AN, Eagon S, Anderson M, Pillai DR (2016) In vitro and in vivo anti-malarial activity of novel harmine-analog heat shock protein 90 inhibitors: a possible partner for artemisinin. Malar J 15(1):579. https://doi.org/10.1186/s12936-016-1625-7
Becker J, Craig EA (1994) Heat-shock proteins as molecular chaperones. Eur J Biochem 219(1–2):11–23
Benesch JL, Ayoub M, Robinson CV, Aquilina JA (2008) Small heat shock protein activity is regulated by variable oligomeric substructure. J Biol Chem 283(42):28513–28517
Bentley SJ, Jamabo M, Boshoff A (2019) The Hsp70/J-protein machinery of the African trypanosome, Trypanosoma brucei. Cell Stress Chaperones 24(1):125–148. https://doi.org/10.1007/s12192-018-0950-x
Ben-Zvi A, Miller EA, Morimoto RI (2009) Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proc Natl Acad Sci U S A 106(35):14914–14919. https://doi.org/10.1073/pnas.0902882106
Beraldo FH, Soares IN, Goncalves DF, Fan J, Thomas AA, Santos TG, Mohammad AH, Roffe M, Calder MD, Nikolova S, Hajj GN, Guimaraes AL, Massensini AR, Welch I, Betts DH, Gros R, Drangova M, Watson AJ, Bartha R, Prado VF, Martins VR, Prado MA (2013) Stress-inducible phosphoprotein 1 has unique cochaperone activity during development and regulates cellular response to ischemia via the prion protein. FASEB J. https://doi.org/10.1096/fj.13-232280
Bertelsen EB, Chang L, Gestwicki JE, Zuiderweg ER (2009) Solution conformation of wild-type E. coli Hsp70 (DnaK) chaperone complexed with ADP and substrate. Proc Natl Acad Sci U S A 106(21):8471–8476. https://doi.org/10.1073/pnas.0903503106
Berthenet K, Bokhari A, Lagrange A, Marcion G, Boudesco C, Causse S, De Thonel A, Svrcek M, Goloudina AR, Dumont S, Hammann A, Biard DS, Demidov ON, Seigneuric R, Duval A, Collura A, Jego G, Garrido C (2017) HSP110 promotes colorectal cancer growth through STAT3 activation. Oncogene 36(16):2328–2336. https://doi.org/10.1038/onc.2016.403
Bhattacharya K, Weidenauer L, Luengo TM, Pieters EC, Echeverría PC, Bernasconi L, Wider D, Sadian Y, Koopman MB, Villemin M, Bauer C, Rüdiger SGD, Quadroni M, Picard D (2020) The Hsp70-Hsp90 co-chaperone Hop/Stip1 shifts the proteostatic balance from folding towards degradation. Nat Commun 11(1):5975. https://doi.org/10.1038/s41467-020-19783-w
Bhutani N, Udgaonkar JB (2000) A thermodynamic coupling mechanism can explain the GroEL-mediated acceleration of the folding of barstar. J Mol Biol 297(5):1037–1044. https://doi.org/10.1006/jmbi.2000.3648
Bhutani N, Udgaonkar JB (2001) GroEL channels the folding of thioredoxin along one kinetic route. J Mol Biol 314(5):1167–1179. https://doi.org/10.1006/jmbi.2000.5193
Bhutani N, Udgaonkar JB (2003) Folding subdomains of thioredoxin characterized by native-state hydrogen exchange. Protein Sci 12(8):1719–1731. https://doi.org/10.1110/ps.0239503
Bickel D, Gohlke H (2019) C-terminal modulators of heat shock protein of 90 kDa (HSP90): state of development and modes of action. Bioorg Med Chem 27(21):115080. https://doi.org/10.1016/j.bmc.2019.115080
Biebl MM, Buchner J (2019) Structure, function, and regulation of the Hsp90 machinery. Cold Spring Harb Perspect Biol 11(9):a034017. https://doi.org/10.1101/cshperspect.a034017
Bigotti MG, Clarke AR (2008) Chaperonins: the hunt for the Group II mechanism. Arch Biochem Biophys 474(2):331–339. https://doi.org/10.1016/j.abb.2008.03.015
Blatch GL, Lassle M (1999) The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21(11):932–939
Bohen SP (1998) Genetic and biochemical analysis of p23 and ansamycin antibiotics in the function of Hsp90-dependent signaling proteins. Mol Cell Biol 18(6):3330–3339
Bohush A, Bieganowski P, Filipek A (2019) Hsp90 and its co-chaperones in neurodegenerative diseases. Int J Mol Sci 20(20):4976. https://doi.org/10.3390/ijms20204976
Boisvert DC, Wang J, Otwinowski Z, Horwich AL, Sigler PB (1996) The 2.4 A crystal structure of the bacterial chaperonin GroEL complexed with ATP gamma S. Nat Struct Biol 3(2):170–177. https://doi.org/10.1038/nsb0296-170
Boncoraglio A, Minoia M, Carra S (2012) The family of mammalian small heat shock proteins (HSPBs): implications in protein deposit diseases and motor neuropathies. Int J Biochem Cell Biol 44(10):1657–1669. https://doi.org/10.1016/j.biocel.2012.03.011
Bonifati V (2014) Genetics of Parkinson’s disease--state of the art, 2013. Parkinsonism Relat Disord 20(Suppl 1):S23–S28. https://doi.org/10.1016/S1353-8020(13)70009-9
Borges JC, Fischer H, Craievich AF, Ramos CH (2005) Low resolution structural study of two human HSP40 chaperones in solution. DJA1 from subfamily A and DJB4 from subfamily B have different quaternary structures. J Biol Chem 280(14):13671–13681
Borkovich KA, Farrelly FW, Finkelstein DB, Taulien J, Lindquist S (1989) hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol Cell Biol 9(9):3919–3930
Botha M, Pesce ER, Blatch GL (2007) The Hsp40 proteins of Plasmodium falciparum and other apicomplexa: regulating chaperone power in the parasite and the host. Int J Biochem Cell Biol 39(10):1781–1803
Boudesco C, Cause S, Jego G, Garrido C (2018) Hsp70: a cancer target inside and outside the cell. Methods Mol Biol 1709:371–396. https://doi.org/10.1007/978-1-4939-7477-1_27
Braig K, Otwinowski Z, Hegde R, Boisvert DC, Joachimiak A, Horwich AL, Sigler PB (1994) The crystal structure of the bacterial chaperonin GroEL at 2.8 A. Nature 371(6498):578–586. https://doi.org/10.1038/371578a0
Brandvold KR, Morimoto RI (2015) The chemical biology of molecular chaperones--implications for modulation of proteostasis. J Mol Biol 427(18):2931–2947. https://doi.org/10.1016/j.jmb.2015.05.010
Brinker A, Scheufler C, Von Der Mulbe F, Fleckenstein B, Herrmann C, Jung G, Moarefi I, Hartl FU (2002) Ligand discrimination by TPR domains. Relevance and selectivity of EEVD-recognition in Hsp70 x Hop x Hsp90 complexes. J Biol Chem 277(22):19265–19275
Brodsky JL, Chiosis G (2006) Hsp70 molecular chaperones: emerging roles in human disease and identification of small molecule modulators. Curr Top Med Chem 6(11):1215–1225
Brodsky JL, Werner ED, Dubas ME, Goeckeler JL, Kruse KB, McCracken AA (1999) The requirement for molecular chaperones during endoplasmic reticulum-associated protein degradation demonstrates that protein export and import are mechanistically distinct. J Biol Chem 274(6):3453–3460. https://doi.org/10.1074/jbc.274.6.3453
Brychzy A, Rein T, Winklhofer KF, Hartl FU, Young JC, Obermann WM (2003) Cofactor Tpr2 combines two TPR domains and a J domain to regulate the Hsp70/Hsp90 chaperone system. Embo J 22(14):3613–3623
Buchberger A, Theyssen H, Schroder H, McCarty JS, Virgallita G, Milkereit P, Reinstein J, Bukau B (1995) Nucleotide-induced conformational changes in the ATPase and substrate binding domains of the DnaK chaperone provide evidence for interdomain communication. J Biol Chem 270(28):16903–16910. https://doi.org/10.1074/jbc.270.28.16903
Buchner J (1999) Hsp90 & Co. – a holding for folding. Trends Biochem Sci 24(4):136–141
Bukau B, Weissman J, Horwich A (2006) Molecular chaperones and protein quality control. Cell 125(3):443–451
Byrd KM, Subramanian C, Sanchez J, Motiwala HF, Liu W, Cohen MS, Holzbeierlein J, Blagg BS (2016) Synthesis and biological evaluation of novobiocin core analogues as Hsp90 inhibitors. Chemistry 22(20):6921–6931. https://doi.org/10.1002/chem.201504955
Byrd KM, Kent CN, Blagg BSJ (2017) Synthesis and biological evaluation of stilbene analogues as Hsp90 C-terminal inhibitors. ChemMedChem 12(24):2022–2029. https://doi.org/10.1002/cmdc.201700630
Calderwood SK (2018) Heat shock proteins and cancer: intracellular chaperones or extracellular signalling ligands? Philos Trans R Soc Lond B Biol Sci 373(1738):20160524. https://doi.org/10.1098/rstb.2016.0524
Calderwood SK, Neckers L (2016) Hsp90 in cancer: transcriptional roles in the nucleus. Adv Cancer Res 129:89–106. https://doi.org/10.1016/bs.acr.2015.08.002
Calderwood SK, Mambula SS, Gray PJ Jr (2007) Extracellular heat shock proteins in cell signaling and immunity. Ann N Y Acad Sci 1113:28–39
Callebaut I, Catelli MG, Portetelle D, Meng X, Cadepond F, Burny A, Baulieu EE, Mornon JP (1994) Redox mechanism for the chaperone activity of heat shock proteins HSPs 60, 70 and 90 as suggested by hydrophobic cluster analysis: hypothesis. C R Acad Sci III 317(8):721–729
Calloni G, Chen T, Schermann SM, Chang HC, Genevaux P, Agostini F, Tartaglia GG, Hayer-Hartl M, Hartl FU (2012) DnaK functions as a central hub in the E. coli chaperone network. Cell Rep 1(3):251–264. https://doi.org/10.1016/j.celrep.2011.12.007
Caplan AJ, Cyr DM, Douglas MG (1992) YDJ1p facilitates polypeptide translocation across different intracellular membranes by a conserved mechanism. Cell 71(7):1143–1155. https://doi.org/10.1016/s0092-8674(05)80063-7
Cappello F, Rappa F, David S, Anzalone R, Zummo G (2003) Immunohistochemical evaluation of PCNA, p53, HSP60, HSP10 and MUC-2 presence and expression in prostate carcinogenesis. Anticancer Res 23(2B):1325–1331
Cappello F, Marino Gammazza A, Palumbo Piccionello A, Campanella C, Pace A, Conway de Macario E, Macario AJ (2014) Hsp60 chaperonopathies and chaperonotherapy: targets and agents. Expert Opin Ther Targets 18(2):185–208. https://doi.org/10.1517/14728222.2014.856417
Carra S, Alberti S, Arrigo PA, Benesch JL, Benjamin IJ, Boelens W, Bartelt-Kirbach B, Brundel B, Buchner J, Bukau B, Carver JA, Ecroyd H, Emanuelsson C, Finet S, Golenhofen N, Goloubinoff P, Gusev N, Haslbeck M, Hightower LE, Kampinga HH, Klevit RE, Liberek K, McHaourab HS, McMenimen KA, Poletti A, Quinlan R, Strelkov SV, Toth ME, Vierling E, Tanguay RM (2017) The growing world of small heat shock proteins: from structure to functions. Cell Stress Chaperones 22(4):601–611. https://doi.org/10.1007/s12192-017-0787-8
Carra S, Alberti S, Benesch JLP, Boelens W, Buchner J, Carver JA, Cecconi C, Ecroyd H, Gusev N, Hightower LE, Klevit RE, Lee HO, Liberek K, Lockwood B, Poletti A, Timmerman V, Toth ME, Vierling E, Wu T, Tanguay RM (2019) Small heat shock proteins: multifaceted proteins with important implications for life. Cell Stress Chaperones 24(2):295–308. https://doi.org/10.1007/s12192-019-00979-z
Catlett MG, Kaplan KB (2006) Sgt1p is a unique co-chaperone that acts as a client adaptor to link Hsp90 to Skp1p. J Biol Chem 281(44):33739–33748
Chadli A, Bruinsma ES, Stensgard B, Toft D (2008) Analysis of Hsp90 cochaperone interactions reveals a novel mechanism for TPR protein recognition. Biochemistry 47(9):2850–2857
Chandra D, Choy G, Tang DG (2007) Cytosolic accumulation of HSP60 during apoptosis with or without apparent mitochondrial release: evidence that its pro-apoptotic or pro-survival functions involve differential interactions with caspase-3. J Biol Chem 282(43):31289–31301
Chandrasekhar GN, Tilly K, Woolford C, Hendrix R, Georgopoulos C (1986) Purification and properties of the groES morphogenetic protein of Escherichia coli. J Biol Chem 261(26):12414–12419
Chang HC, Nathan DF, Lindquist S (1997) In vivo analysis of the Hsp90 cochaperone Sti1 (p60). Mol Cell Biol 17(1):318–325
Charmpilas N, Kyriakakis E, Tavernarakis N (2017) Small heat shock proteins in ageing and age-related diseases. Cell Stress Chaperones 22(4):481–492. https://doi.org/10.1007/s12192-016-0761-x
Cheetham ME, Caplan AJ (1998) Structure, function and evolution of DnaJ: conservation and adaptation of chaperone function. Cell Stress Chaperones 3(1):28–36
Chen L, Sigler PB (1999) The crystal structure of a GroEL/peptide complex: plasticity as a basis for substrate diversity. Cell 99(7):757–768. https://doi.org/10.1016/s0092-8674(00)81673-6
Chen B, Piel WH, Gui L, Bruford E, Monteiro A (2005) The HSP90 family of genes in the human genome: insights into their divergence and evolution. Genomics 86(6):627–637
Chen HJ, Mitchell JC, Novoselov S, Miller J, Nishimura AL, Scotter EL, Vance CA, Cheetham ME, Shaw CE (2016) The heat shock response plays an important role in TDP-43 clearance: evidence for dysfunction in amyotrophic lateral sclerosis. Brain: J Neurol 139(Pt 5):1417–1432. https://doi.org/10.1093/brain/aww028
Chen W, Feng P, Liu T, Jin D (2019) Recent advances in machine learning methods for predicting heat shock proteins. Curr Drug Metab 20(3):224–228. https://doi.org/10.2174/1389200219666181031105916
Cheung-Flynn J, Roberts PJ, Riggs DL, Smith DF (2003) C-terminal sequences outside the tetratricopeptide repeat domain of FKBP51 and FKBP52 cause differential binding to Hsp90. J Biol Chem 278(19):17388–17394
Chi KN, Yu EY, Jacobs C, Bazov J, Kollmannsberger C, Higano CS, Mukherjee SD, Gleave ME, Stewart PS, Hotte SJ (2016) A phase I dose-escalation study of apatorsen (OGX-427), an antisense inhibitor targeting heat shock protein 27 (Hsp27), in patients with castration-resistant prostate cancer and other advanced cancers. Ann Oncol 27(6):1116–1122. https://doi.org/10.1093/annonc/mdw068
Chiappori F, Merelli I, Milanesi L, Colombo G, Morra G (2016) An atomistic view of Hsp70 allosteric crosstalk: from the nucleotide to the substrate binding domain and back. Sci Rep 6:23474. https://doi.org/10.1038/srep23474
Chiosis G, Rodina A, Moulick K (2006) Emerging Hsp90 inhibitors: from discovery to clinic. Anticancer Agents Med Chem 6(1):1–8
Chu F, Maynard JC, Chiosis G, Nicchitta CV, Burlingame AL (2006) Identification of novel quaternary domain interactions in the Hsp90 chaperone, GRP94. Protein Sci 15(6):1260–1269
Chukwuocha RU, Zhang B, Lai CJ, Scavulli JF, Albani S, Carson DA, Chen PP (1999) Isolation of an IgG monoclonal anti-dnaJ antibody from an immunoglobulin combinatorial library from a patient with rheumatoid arthritis. J Rheumatol 26(7):1439–1445
Clark MS, Peck LS (2009) Triggers of the HSP70 stress response: environmental responses and laboratory manipulation in an Antarctic marine invertebrate (Nacella concinna). Cell Stress Chaperones 14(6):649–660. https://doi.org/10.1007/s12192-009-0117-x
Cliff MJ, Harris R, Barford D, Ladbury JE, Williams MA (2006) Conformational diversity in the TPR domain-mediated interaction of protein phosphatase 5 with Hsp90. Structure 14(3):415–426
Corbett KD, Berger JM (2010) Structure of the ATP-binding domain of Plasmodium falciparum Hsp90. Proteins 78(13):2738–2744. https://doi.org/10.1002/prot.22799
Cox D, Ecroyd H (2017) The small heat shock proteins αB-crystallin (HSPB5) and Hsp27 (HSPB1) inhibit the intracellular aggregation of α-synuclein. Cell Stress Chaperones 22(4):589–600. https://doi.org/10.1007/s12192-017-0785-x
Cox D, Whiten DR, Brown JWP, Horrocks MH, San Gil R, Dobson CM, Klenerman D, van Oijen AM, Ecroyd H (2018) The small heat shock protein Hsp27 binds α-synuclein fibrils, preventing elongation and cytotoxicity. J Biol Chem 293(12):4486–4497. https://doi.org/10.1074/jbc.M117.813865
Criado-Marrero M, Rein T, Binder EB, Porter JT, Koren J 3rd, Blair LJ (2018) Hsp90 and FKBP51: complex regulators of psychiatric diseases. Philos Trans R Soc Lond B Biol Sci 373(1738):20160532. https://doi.org/10.1098/rstb.2016.0532
Csermely P, Schnaider T, Soti C, Prohaszka Z, Nardai G (1998) The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol Ther 79(2):129–168
Cupp-Vickery JR, Vickery LE (2000) Crystal structure of Hsc20, a J-type Co-chaperone from Escherichia coli. J Mol Biol 304(5):835–845
Cyr DM (1995) Cooperation of the molecular chaperone Ydj1 with specific Hsp70 homologs to suppress protein aggregation. FEBS Lett 359(2-3):129–132
Cyr DM, Lu X, Douglas MG (1992) Regulation of Hsp70 function by a eukaryotic DnaJ homolog. J Biol Chem 267(29):20927–20931
Das A, Syin C, Fujioka H, Zheng H, Goldman N, Aikawa M, Kumar N (1997) Molecular characterization and ultrastructural localization of Plasmodium falciparum Hsp 60. Mol Biochem Parasitol 88(1-2):95–104
Day J, Passecker A, Beck HP, Vakonakis I (2019) The Plasmodium falciparum Hsp70-x chaperone assists the heat stress response of the malaria parasite. Faseb j 33(12):14611–14624. https://doi.org/10.1096/fj.201901741R
de Koning-Ward TF, Drew DR, Chesson JM, Beeson JG, Crabb BS (2008) Truncation of Plasmodium berghei merozoite surface protein 8 does not affect in vivo blood-stage development. Mol Biochem Parasitol 159(1):69–72
de Koning-Ward TF, Gilson PR, Boddey JA, Rug M, Smith BJ, Papenfuss AT, Sanders PR, Lundie RJ, Maier AG, Cowman AF, Crabb BS (2009) A newly discovered protein export machine in malaria parasites. Nature 459(7249):945–949. https://doi.org/10.1038/nature08104
Dean ME, Johnson JL (2021) Human Hsp90 cochaperones: perspectives on tissue-specific expression and identification of cochaperones with similar in vivo functions. Cell Stress Chaperones 26(1):3–13. https://doi.org/10.1007/s12192-020-01167-0
Demand J, Luders J, Hohfeld J (1998) The carboxy-terminal domain of Hsc70 provides binding sites for a distinct set of chaperone cofactors. Mol Cell Biol 18(4):2023–2028. https://doi.org/10.1128/mcb.18.4.2023
den Engelsman J, Bennink EJ, Doerwald L, Onnekink C, Wunderink L, Andley UP, Kato K, de Jong WW, Boelens WC (2004) Mimicking phosphorylation of the small heat-shock protein alphaB-crystallin recruits the F-box protein FBX4 to nuclear SC35 speckles. Eur J Biochem 271(21):4195–4203
Devaney E, Gillan V (2016) Hsp90 Inhibitors in Parasitic Nematodes: Prospects and Challenges. Curr Top Med Chem 16(25):2805–2811
Dickey CA, Kamal A, Lundgren K, Klosak N, Bailey RM, Dunmore J, Ash P, Shoraka S, Zlatkovic J, Eckman CB, Patterson C, Dickson DW, Nahman NS Jr, Hutton M, Burrows F, Petrucelli L (2007) The high-affinity HSP90-CHIP complex recognizes and selectively degrades phosphorylated tau client proteins. J Clin Invest 117(3):648–658
Dobrzynski JK, Sternlicht ML, Farr GW, Sternlicht H (1996) Newly-synthesized beta-tubulin demonstrates domain-specific interactions with the cytosolic chaperonin. Biochemistry 35(49):15870–15882. https://doi.org/10.1021/bi961114j
Dollins DE, Warren JJ, Immormino RM, Gewirth DT (2007) Structures of GRP94-nucleotide complexes reveal mechanistic differences between the hsp90 chaperones. Mol Cell 28(1):41–56
Doong H, Vrailas A, Kohn EC (2002) What’s in the ‘BAG’? – a functional domain analysis of the BAG-family proteins. Cancer Letters 188(1–2):25–32. https://doi.org/10.1016/s0304-3835(02)00456-1
Dorard C, de Thonel A, Collura A, Marisa L, Svrcek M, Lagrange A, Jego G, Wanherdrick K, Joly AL, Buhard O, Gobbo J, Penard-Lacronique V, Zouali H, Tubacher E, Kirzin S, Selves J, Milano G, Etienne-Grimaldi MC, Bengrine-Lefevre L, Louvet C, Tournigand C, Lefevre JH, Parc Y, Tiret E, Flejou JF, Gaub MP, Garrido C, Duval A (2011) Expression of a mutant HSP110 sensitizes colorectal cancer cells to chemotherapy and improves disease prognosis. Nat Med 17(10):1283–1289. https://doi.org/10.1038/nm.2457
Doyle SM, Shorter J, Zolkiewski M, Hoskins JR, Lindquist S, Wickner S (2007) Asymmetric deceleration of ClpB or Hsp104 ATPase activity unleashes protein-remodeling activity. Nat Struct Mol Biol 14(2):114–122
Dragovic Z, Shomura Y, Tzvetkov N, Hartl FU, Bracher A (2006) Fes1p acts as a nucleotide exchange factor for the ribosome-associated molecular chaperone Ssb1p. Biol Chem 387(12):1593–1600. https://doi.org/10.1515/bc.2006.198
Duran EC, Weaver CL, Lucius AL (2017) Comparative analysis of the structure and function of AAA+ Motors ClpA, ClpB, and Hsp104: common threads and disparate functions. Front Mol Biosci 4:54. https://doi.org/10.3389/fmolb.2017.00054
Duval A, Olaru D, Campos L, Flandrin P, Nadal N, Guyotat D (2006) Expression and prognostic significance of heat-shock proteins in myelodysplastic syndromes. Haematologica 91(5):713–714
Duval M, Le Boeuf F, Huot J, Gratton JP (2007) Src-mediated phosphorylation of Hsp90 in response to vascular endothelial growth factor (VEGF) is required for VEGF receptor-2 signaling to endothelial NO synthase. Mol Biol Cell 18(11):4659–4668
Easton DP, Kaneko Y, Subjeck JR (2000) The hsp110 and Grp1 70 stress proteins: newly recognized relatives of the Hsp70s. Cell Stress Chaperones 5(4):276–290. https://doi.org/10.1379/1466-1268(2000)005<0276:thagsp>2.0.co;2
Echeverria PC, Bhattacharya K, Joshi A, Wang T, Picard D (2019) The sensitivity to Hsp90 inhibitors of both normal and oncogenically transformed cells is determined by the equilibrium between cellular quiescence and activity. PLoS One 14(2):e0208287. https://doi.org/10.1371/journal.pone.0208287
Edkins AL (2015) CHIP: a co-chaperone for degradation by the proteasome. Subcell Biochem 78:219–242. https://doi.org/10.1007/978-3-319-11731-7_11
Edkins AL (2016a) Hsp90 Co-chaperones as drug targets in cancer: current perspectives. In: McAlpine SR, Edkins AL (eds) Heat shock protein inhibitors: success stories, vol 19. Springer International Publishing, Switzerland, pp 21–54
Edkins AL (2016b) Hsp90 co-chaperones as drug targets in cancer: Current perspectives. Top Med Chem 19:33
Edkins AL, Price JT, Pockley AG, Blatch GL (2018) Heat shock proteins as modulators and therapeutic targets of chronic disease: an integrated perspective. Philos Trans R Soc Lond B Biol Sci 373(1738):20160521. https://doi.org/10.1098/rstb.2016.0521
Eggers DK, Welch WJ, Hansen WJ (1997) Complexes between nascent polypeptides and their molecular chaperones in the cytosol of mammalian cells. Mol Biol Cell 8(8):1559–1573. https://doi.org/10.1091/mbc.8.8.1559
Eisenhardt BD, Forreiter C (2012) Insights in small heat shock protein/client interaction by combined protection analysis of two different client proteins. FEBS Lett 586(13):1772–1777
Ellis RJ (2001) Macromolecular crowding: obvious but underappreciated. Trends Biochem Sci 26(10):597–604
Ellis RJ, Hartl FU (1999) Principles of protein folding in the cellular environment. Curr Opin Struct Biol 9(1):102–110
Elnatan D, Betegon M, Liu Y, Ramelot T, Kennedy MA, Agard DA (2017) Symmetry broken and rebroken during the ATP hydrolysis cycle of the mitochondrial Hsp90 TRAP1. Elife 6:e25235. https://doi.org/10.7554/eLife.25235
Emelyanov VV (2002) Phylogenetic relationships of organellar Hsp90 homologs reveal fundamental differences to organellar Hsp70 and Hsp60 evolution. Gene 299(1–2):125–133
Ernst BP, Wiesmann N, Gieringer R, Eckrich J, Brieger J (2020) HSP27 regulates viability and migration of cancer cell lines following irradiation. J Proteomics 226:103886. https://doi.org/10.1016/j.jprot.2020.103886
Eroglu B, Moskophidis D, Mivechi NF (2010) Loss of Hsp110 leads to age-dependent tau hyperphosphorylation and early accumulation of insoluble amyloid beta. Mol Cell Biol 30(19):4626–4643. https://doi.org/10.1128/MCB.01493-09
Ewalt KL, Hendrick JP, Houry WA, Hartl FU (1997) In vivo observation of polypeptide flux through the bacterial chaperonin system. Cell 90(3):491–500. https://doi.org/10.1016/s0092-8674(00)80509-7
Eyles SJ, Gierasch LM (2010) Nature's molecular sponges: small heat shock proteins grow into their chaperone roles. Proc Natl Acad Sci U S A 107(7):2727–2728
Fan CY, Lee S, Ren HY, Cyr DM (2004) Exchangeable chaperone modules contribute to specification of type I and type II Hsp40 cellular function. Mol Biol Cell 15(2):761–773
Fan AC, Bhangoo MK, Young JC (2006) Hsp90 functions in the targeting and outer membrane translocation steps of Tom70-mediated mitochondrial import. J Biol Chem 281(44):33313–33324
Farnsworth P, Singh K (2004) Structure function relationship among alpha-crystallin related small heat shock proteins. Exp Eye Res 79(6):787–794
Fayet O, Ziegelhoffer T, Georgopoulos C (1989) The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J Bacteriol 171(3):1379–1385
Felts SJ, Owen BA, Nguyen P, Trepel J, Donner DB, Toft DO (2000) The hsp90-related protein TRAP1 is a mitochondrial protein with distinct functional properties. J Biol Chem 275(5):3305–3312
Fink AL (1999) Chaperone-mediated protein folding. Physiol Rev 79:425–449
Flaherty KM, DeLuca-Flaherty C, McKay DB (1990) Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature 346(6285):623–628. https://doi.org/10.1038/346623a0
Flynn GC, Pohl J, Flocco MT, Rothman JE (1991) Peptide-binding specificity of the molecular chaperone BiP. Nature 353(6346):726–730. https://doi.org/10.1038/353726a0
Fontaine SN, Martin MD, Dickey CA (2016) Neurodegeneration and the heat shock protein 70 machinery: implications for therapeutic development. Curr Top Med Chem 16(25):2741–2752. https://doi.org/10.2174/1568026616666160413140741
Forsberg LK, Liu W, Holzbeierlein J, Blagg BSJ (2017) Modified biphenyl Hsp90 C-terminal inhibitors for the treatment of cancer. Bioorg Med Chem Lett 27(18):4514–4519. https://doi.org/10.1016/j.bmcl.2017.07.030
Freilich R, Betegon M, Tse E, Mok SA, Julien O, Agard DA, Southworth DR, Takeuchi K, Gestwicki JE (2018) Competing protein-protein interactions regulate binding of Hsp27 to its client protein tau. Nat Commun 9(1):4563. https://doi.org/10.1038/s41467-018-07012-4
Frey S, Leskovar A, Reinstein J, Buchner J (2007) The ATPase cycle of the endoplasmic chaperone Grp94. J Biol Chem 282(49):35612–35620
Frydman J (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 70:603–647. [pii]. https://doi.org/10.1146/annurev.biochem.70.1.603
Gao X, Carroni M, Nussbaum-Krammer C, Mogk A, Nillegoda NB, Szlachcic A, Guilbride DL, Saibil HR, Mayer MP, Bukau B (2015) Human Hsp70 disaggregase reverses parkinson’s-linked α-synuclein amyloid fibrils. Mol Cell 59(5):781–793. https://doi.org/10.1016/j.molcel.2015.07.012
Garg G, Khandelwal A, Blagg BS (2016) Anticancer Inhibitors of Hsp90 Function: Beyond the Usual Suspects. Adv Cancer Res 129:51–88. https://doi.org/10.1016/bs.acr.2015.12.001
Garnier C, Lafitte D, Tsvetkov PO, Barbier P, Leclerc-Devin J, Millot JM, Briand C, Makarov AA, Catelli MG, Peyrot V (2002) Binding of ATP to heat shock protein 90: evidence for an ATP-binding site in the C-terminal domain. J Biol Chem 277(14):12208–12214
Garrido C, Gurbuxani S, Ravagnan L, Kroemer G (2001) Heat shock proteins: endogenous modulators of apoptotic cell death. Biochem Biophys Res Commun 286(3):433–442. https://doi.org/10.1006/bbrc.2001.5427
Garrido C, Paul C, Seigneuric R, Kampinga HH (2006) The small heat shock proteins family: the long forgotten chaperones. Int J Biochem Cell Biol 44(10):1588–1592
Genest O, Hoskins JR, Kravats AN, Doyle SM, Wickner S (2015) Hsp70 and Hsp90 of E. coli directly interact for collaboration in protein remodeling. J Mol Biol 427(24):3877–3889. https://doi.org/10.1016/j.jmb.2015.10.010
Genest O, Wickner S, Doyle SM (2019) Hsp90 and Hsp70 chaperones: collaborators in protein remodeling. J Biol Chem 294(6):2109–2120. https://doi.org/10.1074/jbc.REV118.002806
Georgopoulos C, Welch WJ (1993) Role of the major heat shock proteins as molecular chaperones. Ann Rev Cell Biol 9:601–634. https://doi.org/10.1146/annurev.cb.09.110193.003125
Gestwicki JE, Shao H (2019) Inhibitors and chemical probes for molecular chaperone networks. J Biol Chem 294(6):2151–2161. https://doi.org/10.1074/jbc.TM118.002813
Gewirth DT (2016) Paralog specific Hsp90 inhibitors – a brief history and a bright future. Curr Top Med Chem 16(25):2779–2791. https://doi.org/10.2174/1568026616666160413141154
Gitau GW, Mandal P, Blatch GL, Przyborski J, Shonhai A (2012) Characterisation of the plasmodium falciparum Hsp70-Hsp90 organising protein (PfHop). Cell Stress Chaperones 17(2):191–202. https://doi.org/10.1007/s12192-011-0299-x
Glover JR, Lindquist S (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94(1):73–82. https://doi.org/10.1016/s0092-8674(00)81223-4
Goes FS, Martin J (2001) Hsp90 chaperone complexes are required for the activity and stability of yeast protein kinases Mik1, Wee1 and Swe1. Eur J Biochem 268(8):2281–2289
Goloubinoff P, Mogk A, Zvi AP, Tomoyasu T, Bukau B (1999) Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc Natl Acad Sci U S A 96(24):13732–13737
Gomez-Llorente Y, Jebara F, Patra M, Malik R, Nisemblat S, Chomsky-Hecht O, Parnas A, Azem A, Hirsch JA, Ubarretxena-Belandia I (2020) Structural basis for active single and double ring complexes in human mitochondrial Hsp60-Hsp10 chaperonin. Nat Commun 11(1):1916. https://doi.org/10.1038/s41467-020-15698-8
Gottesman S (2003) Proteolysis in bacterial regulatory circuits. Annu Rev Cell Dev Biol 19:565–587
Gracia L, Lora G, Blair LJ, Jinwal UK (2019) Therapeutic potential of the Hsp90/Cdc37 interaction in neurodegenerative diseases. Front Neurosci 13:1263. https://doi.org/10.3389/fnins.2019.01263
Grad I, McKee TA, Ludwig SM, Hoyle GW, Ruiz P, Wurst W, Floss T, Miller CA 3rd, Picard D (2006) The Hsp90 cochaperone p23 is essential for perinatal survival. Mol Cell Biol 26(23):8976–8983
Grad I, Cederroth CR, Walicki J, Grey C, Barluenga S, Winssinger N, De Massy B, Nef S, Picard D (2010) The molecular chaperone Hsp90alpha is required for meiotic progression of spermatocytes beyond pachytene in the mouse. PLoS One 5(12):e15770
Greene MK, Maskos K, Landry SJ (1998) Role of the J-domain in the cooperation of Hsp40 with Hsp70. Proc Natl Acad Sci U S A 95(11):6108–6113
Grenert JP, Sullivan WP, Fadden P, Haystead TA, Clark J, Mimnaugh E, Krutzsch H, Ochel HJ, Schulte TW, Sausville E, Neckers LM, Toft DO (1997) The amino-terminal domain of heat shock protein 90 (hsp90) that binds geldanamycin is an ATP/ADP switch domain that regulates hsp90 conformation. J Biol Chem 272(38):23843–23850
Grundtman C, Wick G (2011) The autoimmune concept of atherosclerosis. Curr Opin Lipidol 22(5):327–334. https://doi.org/10.1097/MOL.0b013e32834aa0c2
Gusev NB, Bogatcheva NV, Marston SB (2002) Structure and properties of small heat shock proteins (sHsp) and their interaction with cytoskeleton proteins. Biochemistry (Mosc) 67(5):511–519
Hageman J, Kampinga HH (2009) Computational analysis of the human HSPH/HSPA/DNAJ family and cloning of a human HSPH/HSPA/DNAJ expression library. Cell Stress Chaperones 14(1):1–21. https://doi.org/10.1007/s12192-008-0060-2
Hainzl O, Lapina MC, Buchner J, Richter K (2009) The charged linker region is an important regulator of Hsp90 function. J Biol Chem 284(34):22559–22567. https://doi.org/10.1074/jbc.M109.031658
Hakamada K, Nakamura M, Midorikawa R, Shinohara K, Noguchi K, Nagaoka H, Takashima E, Morishima K, Inoue R, Sugiyama M, Kawamoto A, Yohda M (2020) PV1 protein from plasmodium falciparum exhibits chaperone-like functions and cooperates with Hsp100s. Int J Mol Sci 21(22):8616. https://doi.org/10.3390/ijms21228616
Haldar S, Gupta AJ, Yan X, Miličić G, Hartl FU, Hayer-Hartl M (2015) Chaperonin-assisted protein folding: relative population of asymmetric and symmetric GroEL:GroES complexes. J Mol Biol 427(12):2244–2255. https://doi.org/10.1016/j.jmb.2015.04.009
Hamman BD, Hendershot LM, Johnson AE (1998) BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation. Cell 92(6):747–758. https://doi.org/10.1016/s0092-8674(00)81403-8
Harrison CJ, Hayer-Hartl M, Liberto MD, Hartl F-U, Kuriyan J (1997) Crystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK. Science 276(5311):431–435. https://doi.org/10.1126/science.276.5311.431
Harst A, Lin H, Obermann WM (2005) Aha1 competes with Hop, p50 and p23 for binding to the molecular chaperone Hsp90 and contributes to kinase and hormone receptor activation. Biochem J 387(Pt 3):789–796. https://doi.org/10.1042/BJ20041283
Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295(5561):1852–1858. https://doi.org/10.1126/science.1068408
Hartl FU, Martin J, Neupert W (1992) Protein folding in the cell: the role of molecular chaperones Hsp70 and Hsp60. Annu Rev Biophys Biomol Struct 21:293–322
Hawle P, Siepmann M, Harst A, Siderius M, Reusch HP, Obermann WM (2006) The middle domain of Hsp90 acts as a discriminator between different types of client proteins. Mol Cell Biol 26(22):8385–8395
Hayes D, Napoli V, Mazurkie A, Stafford WF, Graceffa P, Benesch JL, Ayoub M, Robinson CV, Aquilina JA, Lanneau D, Wettstein G, Bonniaud P, Garrido C, Parcellier A, Schmitt E, Brunet M, Hammann A, Solary E, Garrido C, den Engelsman J, Bennink EJ, Doerwald L, Onnekink C, Wunderink L, Andley UP, Kato K, de Jong WW, Boelens WC, Lee GJ, Roseman AM, Saibil HR, Vierling E, Koteiche HA, McHaourab HS, Irobi J, Van Impe K, Seeman P, Jordanova A, Dierick I, Verpoorten N, Michalik A, De Vriendt E, Jacobs A, Van Gerwen V, Vennekens K, Mazanec R, Tournev I, Hilton-Jones D, Talbot K, Kremensky I, Van Den Bosch L, Robberecht W, Van Vandekerckhove J, Van Broeckhoven C, Gettemans J, De Jonghe P, Timmerman V (2009) Phosphorylation dependence of hsp27 multimeric size and molecular chaperone function. J Biol Chem 284(28):18801–18807
Hayoun D, Kapp T, Edri-Brami M, Ventura T, Cohen M, Avidan A, Lichtenstein RG (2012) HSP60 is transported through the secretory pathway of 3-MCA-induced fibrosarcoma tumour cells and undergoes N-glycosylation. FEBS J 279(12):2083–2095. https://doi.org/10.1111/j.1742-4658.2012.08594.x
Hendrick JP, Hartl FU (1993) Molecular chaperone functions of heat-shock proteins. Annu Rev Biochem 62:349–384. https://doi.org/10.1146/annurev.bi.62.070193.002025
Hendrick JP, Langer T, Davis TA, Hartl FU, Wiedmann M (1993) Control of folding and membrane translocation by binding of the chaperone DnaJ to nascent polypeptides. Proc Natl Acad Sci U S A 90(21):10216–10220
Henics T, Nagy E, Oh HJ, Csermely P, von Gabain A, Subjeck JR (1999) Mammalian Hsp70 and Hsp110 proteins bind to RNA motifs involved in mRNA stability. J Biol Chem 274(24):17318–17324. https://doi.org/10.1074/jbc.274.24.17318
Hennessy F, Boshoff A, Blatch GL (2005) Rational mutagenesis of a 40 kDa heat shock protein from Agrobacterium tumefaciens identifies amino acid residues critical to its in vivo function. Int J Biochem Cell Biol 37(1):177–191
Hernandez MP, Chadli A, Toft DO (2002a) HSP40 binding is the first step in the HSP90 chaperoning pathway for the progesterone receptor. J Biol Chem 277(14):11873–11881
Hernandez MP, Sullivan WP, Toft DO (2002b) The assembly and intermolecular properties of the hsp70-Hop-hsp90 molecular chaperone complex. J Biol Chem 277(41):38294–38304
Hiller NL, Bhattacharjee S, van Ooij C, Liolios K, Harrison T, Lopez-Estraño C, Haldar K (2004) A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306(5703):1934–1937. https://doi.org/10.1126/science.1102737
Hohfeld J, Minami Y, Hartl FU (1995) Hip, a novel cochaperone involved in the eukaryotic Hsc70/Hsp40 reaction cycle. Cell 83(4):589–598. https://doi.org/10.1016/0092-8674(95)90099-3
Honoré FA, Méjean V, Genest O (2017) Hsp90 is essential under heat stress in the bacterium shewanella oneidensis. Cell Rep 19(4):680–687. https://doi.org/10.1016/j.celrep.2017.03.082
Horovitz A, Willison KR (2005) Allosteric regulation of chaperonins. Curr Opin Struct Biol 15(6):646–651. https://doi.org/10.1016/j.sbi.2005.10.001
Horrocks P, Newbold CI (2000) Intraerythrocytic polyubiquitin expression in Plasmodium falciparum is subjected to developmental and heat-shock control. Mol Biochem Parasitol 105(1):115–125
Horwich AL, Fenton WA, Chapman E, Farr GW (2007) Two families of chaperonin: physiology and mechanism. Annu Rev Cell Dev Biol 23:115–145
Hoter A, El-Sabban ME, Naim HY (2018) The HSP90 family: structure, regulation, function, and implications in health and disease. Int J Mol Sci 19(9):2560. https://doi.org/10.3390/ijms19092560
Houry WA, Frishman D, Eckerskorn C, Lottspeich F, Hartl FU (1999) Identification of in vivo substrates of the chaperonin GroEL. Nature 402(6758):147–154
Hu J, Wu Y, Li J, Qian X, Fu Z, Sha B (2008) The crystal structure of the putative peptide-binding fragment from the human Hsp40 protein Hdj1. BMC Struct Biol 8:3
Immormino RM, Dollins DE, Shaffer PL, Soldano KL, Walker MA, Gewirth DT (2004) Ligand-induced conformational shift in the N-terminal domain of GRP94, an Hsp90 chaperone. J Biol Chem 279(44):46162–46171
Immormino RM, Metzger LE, Reardon PN, Dollins DE, Blagg BS, Gewirth DT (2009) Different poses for ligand and chaperone in inhibitor-bound Hsp90 and GRP94: implications for paralog-specific drug design. J Mol Biol 388(5):1033–1042
Inda C, Bolaender A, Wang T, Gandu SR, Koren J 3rd (2016) Stressing out Hsp90 in neurotoxic proteinopathies. Curr Top Med Chem 16(25):2829–2838
Ingolia TD, Craig EA (1982) Drosophila gene related to the major heat shock-induced gene is transcribed at normal temperatures and not induced by heat shock. Proc Natl Acad Sci U S A 79(2):525–529. https://doi.org/10.1073/pnas.79.2.525
Irmer H, Hohfeld J (1997) Characterization of functional domains of the eukaryotic co-chaperone Hip. J Biol Chem 272(4):2230–2235. https://doi.org/10.1074/jbc.272.4.2230
Irobi J, Van Impe K, Seeman P, Jordanova A, Dierick I, Verpoorten N, Michalik A, De Vriendt E, Jacobs A, Van Gerwen V, Vennekens K, Mazanec R, Tournev I, Hilton-Jones D, Talbot K, Kremensky I, Van Den Bosch L, Robberecht W, Van Vandekerckhove J, Van Broeckhoven C, Gettemans J, De Jonghe P, Timmerman V (2004) Hot-spot residue in small heat-shock protein 22 causes distal motor neuropathy. Nat Genet 36(6):597–601
Jahn M, Rehn A, Pelz B, Hellenkamp B, Richter K, Rief M, Buchner J, Hugel T (2014) The charged linker of the molecular chaperone Hsp90 modulates domain contacts and biological function. Proc Natl Acad Sci U S A 111(50):17881–17886. https://doi.org/10.1073/pnas.1414073111
Jakob U, Gaestel M, Engel K, Buchner J (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268(3):1517–1520
Jan RL, Yang SC, Liu YC, Yang RC, Tsai SP, Huang SE, Yeh JL, Hsu JH (2020) Extracellular heat shock protein HSC70 protects against lipopolysaccharide-induced hypertrophic responses in rat cardiomyocytes. Biomed Pharmacother 128:110370. https://doi.org/10.1016/j.biopha.2020.110370
Jhaveri K, Taldone T, Modi S, Chiosis G (2012) Advances in the clinical development of heat shock protein 90 (Hsp90) inhibitors in cancers. Biochim Biophys Acta 1823(3):742–755. https://doi.org/10.1016/j.bbamcr.2011.10.008
Jiang J, Taylor AB, Prasad K, Ishikawa-Brush Y, Hart PJ, Lafer EM, Sousa R (2003) Structure-function analysis of the auxilin J-domain reveals an extended Hsc70 interaction interface. Biochemistry 42(19):5748–5753
Jiang J, Prasad K, Lafer EM, Sousa R (2005) Structural basis of interdomain communication in the Hsc70 chaperone. Mol Cell 20(4):513–524. https://doi.org/10.1016/j.molcel.2005.09.028
Jiang J, Lafer EM, Sousa R (2006) Crystallization of a functionally intact Hsc70 chaperone. Acta Crystallogr Sect F Struct Biol Cryst Commun 62(Pt 1):39–43. https://doi.org/10.1107/S1744309105040303
Jiang J, Maes EG, Taylor AB, Wang L, Hinck AP, Lafer EM, Sousa R (2007) Structural basis of J cochaperone binding and regulation of Hsp70. Mol Cell 28(3):422–433. https://doi.org/10.1016/j.molcel.2007.08.022
Jing XY, Li FM (2020) Identifying Heat Shock Protein Families from Imbalanced Data by Using Combined Features. Comput Math Methods Med 2020:8894478. https://doi.org/10.1155/2020/8894478
Johnson JL, Craig EA (2001) An essential role for the substrate-binding region of Hsp40s in Saccharomyces cerevisiae. J Cell Biol 152(4):851–856. https://doi.org/10.1083/jcb.152.4.851
Johnson JL, Toft DO (1995) Binding of p23 and hsp90 during assembly with the progesterone receptor. Mol Endocrinol 9(6):670–678
Johnson BD, Schumacher RJ, Ross ED, Toft DO (1998) Hop modulates Hsp70/Hsp90 interactions in protein folding. J Biol Chem 273(6):3679–3686
Joshi A, Dai L, Liu Y, Lee J, Ghahhari NM, Segala G, Beebe K, Jenkins LM, Lyons GC, Bernasconi L, Tsai FTF, Agard DA, Neckers L, Picard D (2020) The mitochondrial HSP90 paralog TRAP1 forms an OXPHOS-regulated tetramer and is involved in mitochondrial metabolic homeostasis. BMC Biol 18(1):10. https://doi.org/10.1186/s12915-020-0740-7
Juhasz K, Lipp AM, Nimmervoll B, Sonnleitner A, Hesse J, Haselgruebler T, Balogi Z (2013) The complex function of hsp70 in metastatic cancer. Cancers (Basel) 6(1):42–66. https://doi.org/10.3390/cancers6010042
Kabani M, Martineau CN (2008) Multiple hsp70 isoforms in the eukaryotic cytosol: mere redundancy or functional specificity? Curr Genomics 9(5):338–248. https://doi.org/10.2174/138920208785133280
Kabani M, McLellan C, Raynes DA, Guerriero V, Brodsky JL (2002) HspBP1, a homologue of the yeast Fes1 and Sls1 proteins, is an Hsc70 nucleotide exchange factor. FEBS Letters 531(2):339–342. https://doi.org/10.1016/s0014-5793(02)03570-6
Kadota Y, Amigues B, Ducassou L, Madaoui H, Ochsenbein F, Guerois R, Shirasu K (2008) Structural and functional analysis of SGT1-HSP90 core complex required for innate immunity in plants. EMBO Rep 9(12):1209–1215
Kamal A, Thao L, Sensintaffar J, Zhang L, Boehm MF, Fritz LC, Burrows FJ (2003) A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425(6956):407–410
Kampinga HH, Craig EA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11(8):579–592. https://doi.org/10.1038/nrm2941
Kampinga HH, Garrido C (2012) HSPBs: small proteins with big implications in human disease. Int J Biochem Cell Biol 44(10):1706–1710. https://doi.org/10.1016/j.biocel.2012.06.005
Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM, Bruford EA, Cheetham ME, Chen B, Hightower LE (2009) Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 14(1):105–111. https://doi.org/10.1007/s12192-008-0068-7
Kampinga HH, Andreasson C, Barducci A, Cheetham ME, Cyr D, Emanuelsson C, Genevaux P, Gestwicki JE, Goloubinoff P, Huerta-Cepas J, Kirstein J, Liberek K, Mayer MP, Nagata K, Nillegoda NB, Pulido P, Ramos C, De Los RP, Rospert S, Rosenzweig R, Sahi C, Taipale M, Tomiczek B, Ushioda R, Young JC, Zimmermann R, Zylicz A, Zylicz M, Craig EA, Marszalek J (2019) Function, evolution, and structure of J-domain proteins. Cell Stress Chaperones 24(1):7–15. https://doi.org/10.1007/s12192-018-0948-4
Kanazawa Y, Isomoto H, Oka M, Yano Y, Soda H, Shikuwa S, Takeshima F, Omagari K, Mizuta Y, Murase K, Nakagoe T, Ohtsuka K, Kohno S (2003) Expression of heat shock protein (Hsp) 70 and Hsp 40 in colorectal cancer. Med Oncol 20(2):157–164. https://doi.org/10.1385/MO:20:2:157
Kannan R, Sreekumar PG, Hinton DR (2012) Novel roles for alpha-crystallins in retinal function and disease. Prog Retin Eye Res 31(6):576–604. https://doi.org/10.1016/j.preteyeres.2012.06.001
Kase S, Parikh JG, Rao NA (2009) Expression of heat shock protein 27 and alpha-crystallins in human retinoblastoma after chemoreduction. Br J Ophthalmol 93(4):541–544
Kędzierska-Mieszkowska S, Arent Z (2020) AAA+ molecular chaperone ClpB in Leptospira interrogans: its role and significance in leptospiral virulence and pathogenesis of leptospirosis. Int J Mol Sci 21(18):6645. https://doi.org/10.3390/ijms21186645
Kelley WL, Georgopoulos C (1997) Positive control of the two-component RcsC/B signal transduction network by DjlA: a member of the DnaJ family of molecular chaperones in Escherichia coli. Mol Microbiol 25(5):913–931
Kerner MJ, Naylor DJ, Ishihama Y, Maier T, Chang HC, Stines AP, Georgopoulos C, Frishman D, Hayer-Hartl M, Mann M, Hartl FU (2005) Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122(2):209–220
Kimura Y, Rutherford SL, Miyata Y, Yahara I, Freeman BC, Yue L, Morimoto RI, Lindquist S (1997) Cdc37 is a molecular chaperone with specific functions in signal transduction. Genes Dev 11(14):1775–1785
Kityk R, Kopp J, Sinning I, Mayer MP (2012) Structure and dynamics of the ATP-bound open conformation of Hsp70 chaperones. Mol Cell 48(6):863–874. https://doi.org/10.1016/j.molcel.2012.09.023
Kityk R, Kopp J, Mayer MP (2018) Molecular mechanism of J-domain-triggered ATP hydrolysis by Hsp70 chaperones. Mol Cell 69(2):227–237.e224. https://doi.org/10.1016/j.molcel.2017.12.003
Kluger HM, Chelouche Lev D, Kluger Y, McCarthy MM, Kiriakova G, Camp RL, Rimm DL, Price JE (2005) Using a xenograft model of human breast cancer metastasis to find genes associated with clinically aggressive disease. Cancer Res 65(13):5578–5587. https://doi.org/10.1158/0008-5472.CAN-05-0108
Klumpp M, Baumeister W, Essen LO (1997) Structure of the substrate binding domain of the thermosome, an archaeal group II chaperonin. Cell 91(2):263–270. https://doi.org/10.1016/s0092-8674(00)80408-0
Koike-Takeshita A, Arakawa T, Taguchi H, Shimamura T (2014) Crystal structure of a symmetric football-shaped GroEL:GroES2-ATP14 complex determined at 3.8Å reveals rearrangement between two GroEL rings. J Mol Biol 426(21):3634–3641. https://doi.org/10.1016/j.jmb.2014.08.017
Koteiche HA, McHaourab HS (2006) Mechanism of a hereditary cataract phenotype. Mutations in alphaA-crystallin activate substrate binding. J Biol Chem 281(20):14273–14279
Kourtis N, Tavernarakis N (2018) Small heat shock proteins and neurodegeneration: recent developments. Biomol Concepts 9(1):94–102. https://doi.org/10.1515/bmc-2018-0009
Kramer G, Patzelt H, Rauch T, Kurz TA, Vorderwulbecke S, Bukau B, Deuerling E (2004) Trigger factor peptidyl-prolyl cis/trans isomerase activity is not essential for the folding of cytosolic proteins in Escherichia coli. J Biol Chem 279(14):14165–14170
Kravats AN, Hoskins JR, Reidy M, Johnson JL, Doyle SM, Genest O, Masison DC, Wickner S (2018) Functional and physical interaction between yeast Hsp90 and Hsp70. Proc Natl Acad Sci U S A 115(10):E2210–e2219. https://doi.org/10.1073/pnas.1719969115
Kroeger H, Messah C, Ahern K, Gee J, Joseph V, Matthes MT, Yasumura D, Gorbatyuk MS, Chiang WC, LaVail MM, Lin JH (2012) Induction of endoplasmic reticulum stress genes, BiP and chop, in genetic and environmental models of retinal degeneration. Invest Ophthalmol Vis Sci 53(12):7590–7599. https://doi.org/10.1167/iovs.12-10221
Kumar R, Pavithra SR, Tatu U (2007) Three-dimensional structure of heat shock protein 90 from Plasmodium falciparum: molecular modelling approach to rational drug design against malaria. J Biosci 32(3):531–536
Lackie RE, Maciejewski A, Ostapchenko VG, Marques-Lopes J, Choy WY, Duennwald ML, Prado VF, Prado MAM (2017) The Hsp70/Hsp90 chaperone machinery in neurodegenerative diseases. Front Neurosci 11:254. https://doi.org/10.3389/fnins.2017.00254
Langer T, Lu C, Echols H, Flanagan J, Hayer MK, Hartl FU (1992) Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding. Nature 356(6371):683–689
Lanneau D, de Thonel A, Maurel S, Didelot C, Garrido C (2007) Apoptosis versus cell differentiation: role of heat shock proteins HSP90, HSP70 and HSP27. Prion 1(1):53–60
Lanneau D, Wettstein G, Bonniaud P, Garrido C (2010) Heat shock proteins: cell protection through protein triage. Sci World J 10:1543–1552
Lauwers E, Wang YC, Gallardo R, Van der Kant R, Michiels E, Swerts J, Baatsen P, Zaiter SS, McAlpine SR, Gounko NV, Rousseau F, Schymkowitz J, Verstreken P (2018) Hsp90 mediates membrane deformation and exosome release. Mol Cell 71(5):689–702. e689. https://doi.org/10.1016/j.molcel.2018.07.016
Lawson B, Brewer JW, Hendershot LM (1998) Geldanamycin, an hsp90/GRP94-binding drug, induces increased transcription of endoplasmic reticulum (ER) chaperones via the ER stress pathway. J Cell Physiol 174(2):170–178
Lee GJ, Roseman AM, Saibil HR, Vierling E (1997) A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. Embo J 16(3):659–671
Lee S, Fan CY, Younger JM, Ren H, Cyr DM (2002) Identification of essential residues in the type II Hsp40 Sis1 that function in polypeptide binding. J Biol Chem 277(24):21675–21682
Lee S, Sowa ME, Watanabe YH, Sigler PB, Chiu W, Yoshida M, Tsai FT (2003) The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state. Cell 115(2):229–240
Lee P, Shabbir A, Cardozo C, Caplan AJ (2004) Sti1 and Cdc37 can stabilize Hsp90 in chaperone complexes with a protein kinase. Mol Biol Cell 15(4):1785–1792. https://doi.org/10.1091/mbc.E03-07-0480
Lee CT, Graf C, Mayer FJ, Richter SM, Mayer MP (2012) Dynamics of the regulation of Hsp90 by the co-chaperone Sti1. EMBO J 31(6):1518–1528. https://doi.org/10.1038/emboj.2012.37
Lee K, Sharma R, Shrestha OK, Bingman CA, Craig EA (2016) Dual interaction of the Hsp70 J-protein cochaperone Zuotin with the 40S and 60S ribosomal subunits. Nat Struct Mol Biol 23(11):1003–1010. https://doi.org/10.1038/nsmb.3299
Lee JC, Sim DY, Lee HJ, Im E, Choi JB, Park JE, Park WY, Jung JH, Shim BS, Kim SH (2020) MicroRNA216b mediated downregulation of HSP27/STAT3/AKT signaling is critically involved in lambertianic acid induced apoptosis in human cervical cancers. Phytother Res. https://doi.org/10.1002/ptr.6842
Lee-Yoon D, Easton D, Murawski M, Burd R, Subjeck JR (1995) Identification of a major subfamily of large hsp70-like proteins through the cloning of the mammalian 110-kDa heat shock protein. J Biol Chem 270(26):15725–15733. https://doi.org/10.1074/jbc.270.26.15725
Leroux MR, Fändrich M, Klunker D, Siegers K, Lupas AN, Brown JR, Schiebel E, Dobson CM, Hartl FU (1999) MtGimC, a novel archaeal chaperone related to the eukaryotic chaperonin cofactor GimC/prefoldin. Embo j 18(23):6730–6743. https://doi.org/10.1093/emboj/18.23.6730
Leskovar A, Wegele H, Werbeck ND, Buchner J, Reinstein J (2008) The ATPase cycle of the mitochondrial Hsp90 analog Trap1. J Biol Chem 283(17):11677–11688
Li J, Sha B (2005) Structure-based mutagenesis studies of the peptide substrate binding fragment of type I heat-shock protein 40. Biochem J 386(Pt 3):453–460
Li J, Wu Y, Qian X, Sha B (2006) Crystal structure of yeast Sis1 peptide-binding fragment and Hsp70 Ssa1 C-terminal complex. Biochem J 398(3):353–360. https://doi.org/10.1042/bj20060618
Li J, Qian X, Hu J, Sha B (2009) Molecular chaperone Hsp70/Hsp90 prepares the mitochondrial outer membrane translocon receptor Tom71 for preprotein loading. J Biol Chem 284(35):23852–23859. https://doi.org/10.1074/jbc.M109.023986
Liberek K, Marszalek J, Ang D, Georgopoulos C, Zylicz M (1991) Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc Natl Acad Sci U S A 88(7):2874–2878. https://doi.org/10.1073/pnas.88.7.2874
Liu Q, Hendrickson WA (2007) Insights into Hsp70 chaperone activity from a crystal structure of the yeast Hsp110 Sse1. Cell 131(1):106–120. https://doi.org/10.1016/j.cell.2007.08.039
Liu L, Srikakulam R, Winkelmann DA (2008) Unc45 activates Hsp90-dependent folding of the myosin motor domain. J Biol Chem 283(19):13185–13193
Liu B, Yang Y, Qiu Z, Staron M, Hong F, Li Y, Wu S, Li Y, Hao B, Bona R, Han D, Li Z (2010) Folding of Toll-like receptors by the HSP90 paralogue gp96 requires a substrate-specific cochaperone. Nat Commun 1:79. https://doi.org/10.1038/ncomms1070
Liu Z, Liu Y, Long Y, Liu B, Wang X (2020) Role of HSP27 in the multidrug sensitivity and resistance of colon cancer cells. Oncol Lett 19(3):2021–2027. https://doi.org/10.3892/ol.2020.11255
Longshaw VM, Dirr HW, Blatch GL, Lassle M (2000) The in vitro phosphorylation of the co-chaperone mSTI1 by cell cycle kinases substantiates a predicted casein kinase II-p34cdc2-NLS (CcN) motif. Biol Chem 381(11):1133–1138. https://doi.org/10.1515/BC.2000.139
Lopez T, Dalton K, Frydman J (2015) The mechanism and function of group II chaperonins. J Mol Biol 427(18):2919–2930. https://doi.org/10.1016/j.jmb.2015.04.013
López A, Elimelech AR, Klimm K, Sattler M (2020) The charged linker modulates the conformations and molecular interactions of Hsp90. Chembiochem. https://doi.org/10.1002/cbic.202000699
Lotz GP, Lin H, Harst A, Obermann WM (2003) Aha1 binds to the middle domain of Hsp90, contributes to client protein activation, and stimulates the ATPase activity of the molecular chaperone. J Biol Chem 278(19):17228–17235
Lu Z, Cyr DM (1998) The conserved carboxyl terminus and zinc finger-like domain of the co-chaperone Ydj1 assist Hsp70 in protein folding. J Biol Chem 273(10):5970–5978
Lu XA, Wang X, Zhuo W, Jia L, Jiang Y, Fu Y, Luo Y (2014) The regulatory mechanism of a client kinase controlling its own release from Hsp90 chaperone machinery through phosphorylation. Biochem J 457(1):171–183. https://doi.org/10.1042/bj20130963
Lyon MS, Milligan C (2019) Extracellular heat shock proteins in neurodegenerative diseases: new perspectives. Neurosci Lett 711:134462. https://doi.org/10.1016/j.neulet.2019.134462
Macario AJ, de Macario EC (2020) Molecular mechanisms in chaperonopathies: clues to understanding the histopathological abnormalities and developing novel therapies. J Pathol 250(1):9–18. https://doi.org/10.1002/path.5349
Macario AJ, Brocchieri L, Shenoy AR, Conway de Macario E (2006) Evolution of a protein-folding machine: genomic and evolutionary analyses reveal three lineages of the archaeal hsp70(dnaK) gene. J Mol Evol 63(1):74–86. https://doi.org/10.1007/s00239-005-6207-1
MacLean M, Picard D (2003) Cdc37 goes beyond Hsp90 and kinases. Cell Stress Chaperones 8(2):114–119
Magen D, Georgopoulos C, Bross P, Ang D, Segev Y, Goldsher D, Nemirovski A, Shahar E, Ravid S, Luder A, Heno B, Gershoni-Baruch R, Skorecki K, Mandel H (2008) Mitochondrial hsp60 chaperonopathy causes an autosomal-recessive neurodegenerative disorder linked to brain hypomyelination and leukodystrophy. Am J Hum Genet 83(1):30–42. https://doi.org/10.1016/j.ajhg.2008.05.016
Maharaj KA, Que NL, Hong F, Huck JD, Gill SK, Wu S, Li Z, Gewirth DT (2016) Exploring the functional complementation between Grp94 and Hsp90. PLoS One 11(11):e0166271. https://doi.org/10.1371/journal.pone.0166271
Maier AG, Rug M, O'Neill MT, Brown M, Chakravorty S, Szestak T, Chesson J, Wu Y, Hughes K, Coppel RL, Newbold C, Beeson JG, Craig A, Crabb BS, Cowman AF (2008) Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell 134(1):48–61. https://doi.org/10.1016/j.cell.2008.04.051
Maier AG, Cooke BM, Cowman AF, Tilley L (2009) Malaria parasite proteins that remodel the host erythrocyte. Nat Rev Microbiol 7(5):341–354
Marcu MG, Neckers LM (2003) The C-terminal half of heat shock protein 90 represents a second site for pharmacologic intervention in chaperone function. Curr Cancer Drug Targets 3(5):343–347
Marcu MG, Chadli A, Bouhouche I, Catelli M, Neckers LM (2000a) The heat shock protein 90 antagonist novobiocin interacts with a previously unrecognized ATP-binding domain in the carboxyl terminus of the chaperone. J Biol Chem 275(47):37181–37186. https://doi.org/10.1074/jbc.M003701200
Marcu MG, Schulte TW, Neckers L (2000b) Novobiocin and related coumarins and depletion of heat shock protein 90-dependent signaling proteins. J Natl Cancer Inst 92(3):242–248
Martinez-Ruiz A, Villanueva L, Gonzalez de Orduna C, Lopez-Ferrer D, Higueras MA, Tarin C, Rodriguez-Crespo I, Vazquez J, Lamas S (2005) S-nitrosylation of Hsp90 promotes the inhibition of its ATPase and endothelial nitric oxide synthase regulatory activities. Proc Natl Acad Sci U S A 102(24):8525–8530
Martinez-Yamout MA, Venkitakrishnan RP, Preece NE, Kroon G, Wright PE, Dyson HJ (2006) Localization of sites of interaction between p23 and Hsp90 in solution. J Biol Chem 281(20):14457–14464
Marzec M, Eletto D, Argon Y (2012) GRP94: An HSP90-like protein specialized for protein folding and quality control in the endoplasmic reticulum. Biochim Biophys Acta 1823(3):774–787. https://doi.org/10.1016/j.bbamcr.2011.10.013
Matz JM, Matuschewski K, Kooij TW (2013) Two putative protein export regulators promote Plasmodium blood stage development in vivo. Mol Biochem Parasitol 191(1):44–52. https://doi.org/10.1016/j.molbiopara.2013.09.003
Mayer MP (2010a) Gymnastics of molecular chaperones. Mol Cell 39(3):321–331
Mayer MP (2010b) Phosphotyrosine confers client specificity to Hsp90. Mol Cell 37(3):295–296. https://doi.org/10.1016/j.molcel.2010.01.028
Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62(6):670–684. https://doi.org/10.1007/s00018-004-4464-6
Mayer MP, Schröder H, Rüdiger S, Paal K, Laufen T, Bukau B (2000) Multistep mechanism of substrate binding determines chaperone activity of Hsp70. Nat Struct Biol 7(7):586–593. https://doi.org/10.1038/76819
Mayer MP, Nikolay R, Bukau B (2002) Aha, another regulator for hsp90 chaperones. Mol Cell 10(6):1255–1256
McCarty JS, Buchberger A, Reinstein J, Bukau B (1995) The role of ATP in the functional cycle of the DnaK chaperone system. J Mol Biol 249(1):126–137. https://doi.org/10.1006/jmbi.1995.0284
McClellan AJ, Tam S, Kaganovich D, Frydman J (2005) Protein quality control: chaperones culling corrupt conformations. Nat Cell Biol 7(8):736–741
McCormack EA, Altschuler GM, Dekker C, Filmore H, Willison KR (2009) Yeast phosducin-like protein 2 acts as a stimulatory co-factor for the folding of actin by the chaperonin CCT via a ternary complex. J Mol Biol 391(1):192–206. https://doi.org/10.1016/j.jmb.2009.06.003
McDonald ET, Bortolus M, Koteiche HA, McHaourab HS (2012) Sequence, structure, and dynamic determinants of Hsp27 (HspB1) equilibrium dissociation are encoded by the N-terminal domain. Biochemistry 51(6):1257–1268
McLaughlin SH, Smith HW, Jackson SE (2002) Stimulation of the weak ATPase activity of human hsp90 by a client protein. J Mol Biol 315(4):787–798
McLaughlin SH, Sobott F, Yao ZP, Zhang W, Nielsen PR, Grossmann JG, Laue ED, Robinson CV, Jackson SE (2006) The co-chaperone p23 arrests the Hsp90 ATPase cycle to trap client proteins. J Mol Biol 356(3):746–758
Medana IM, Turner GD (2006) Human cerebral malaria and the blood-brain barrier. Int J Parasitol 36(5):555–568
Meyer P, Prodromou C, Hu B, Vaughan C, Roe SM, Panaretou B, Piper PW, Pearl LH (2003) Structural and functional analysis of the middle segment of hsp90: implications for ATP hydrolysis and client protein and cochaperone interactions. Mol Cell 11(3):647–658
Meyer P, Prodromou C, Liao C, Hu B, Mark Roe S, Vaughan CK, Vlasic I, Panaretou B, Piper PW, Pearl LH (2004) Structural basis for recruitment of the ATPase activator Aha1 to the Hsp90 chaperone machinery. Embo J 23(3):511–519
Mishra RC, Grover A (2016) ClpB/Hsp100 proteins and heat stress tolerance in plants. Crit Rev Biotechnol 36(5):862–874. https://doi.org/10.3109/07388551.2015.1051942
Mitra A, Shevde LA, Samant RS (2009) Multi-faceted role of HSP40 in cancer. Clin Exp Metastasis 26(6):559–567. https://doi.org/10.1007/s10585-009-9255-x
Moffatt NS, Bruinsma E, Uhl C, Obermann WM, Toft D (2008) Role of the cochaperone Tpr2 in Hsp90 chaperoning. Biochemistry 47(31):8203–8213
Mogk A, Bukau B, Kampinga HH (2018) Cellular handling of protein aggregates by disaggregation machines. Mol Cell 69(2):214–226. https://doi.org/10.1016/j.molcel.2018.01.004
Mollapour M, Bourboulia D, Beebe K, Woodford MR, Polier S, Hoang A, Chelluri R, Li Y, Guo A, Lee MJ, Fotooh-Abadi E, Khan S, Prince T, Miyajima N, Yoshida S, Tsutsumi S, Xu W, Panaretou B, Stetler-Stevenson WG, Bratslavsky G, Trepel JB, Prodromou C, Neckers L (2014) Asymmetric Hsp90 N domain SUMOylation recruits Aha1 and ATP-competitive inhibitors. Mol Cell 53(2):317–329. https://doi.org/10.1016/j.molcel.2013.12.007
Morán Luengo T, Mayer MP, Rüdiger SGD (2019) The Hsp70-Hsp90 chaperone cascade in protein folding. Trends Cell Biol 29(2):164–177. https://doi.org/10.1016/j.tcb.2018.10.004
Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12(24):3788–3796. https://doi.org/10.1101/gad.12.24.3788
Morishima Y, Kanelakis KC, Murphy PJ, Lowe ER, Jenkins GJ, Osawa Y, Sunahara RK, Pratt WB (2003) The hsp90 cochaperone p23 is the limiting component of the multiprotein hsp90/hsp70-based chaperone system in vivo where it acts to stabilize the client protein: hsp90 complex. J Biol Chem 278(49):48754–48763
Moroni E, Agard DA, Colombo G (2018) The structural asymmetry of mitochondrial Hsp90 (Trap1) determines fine tuning of functional dynamics. J Chem Theory Comput 14(2):1033–1044. https://doi.org/10.1021/acs.jctc.7b00766
Morshauser RC, Hu W, Wang H, Pang Y, Flynn GC, Zuiderweg ER (1999) High-resolution solution structure of the 18 kDa substrate-binding domain of the mammalian chaperone protein Hsc70. J Mol Biol 289(5):1387–1403. https://doi.org/10.1006/jmbi.1999.2776
Mounier N, Arrigo AP (2002) Actin cytoskeleton and small heat shock proteins: how do they interact? Cell Stress Chaperones 7(2):167–176
Mróz D, Wyszkowski H, Szablewski T, Zawieracz K, Dutkiewicz R, Bury K, Wortmann SB, Wevers RA, Ziętkiewicz S (2020) CLPB (caseinolytic peptidase B homolog), the first mitochondrial protein refoldase associated with human disease. Biochim Biophys Acta Gen Subj 1864(4):129512. https://doi.org/10.1016/j.bbagen.2020.129512
Muller P, Ruckova E, Halada P, Coates PJ, Hrstka R, Lane DP, Vojtesek B (2013) C-terminal phosphorylation of Hsp70 and Hsp90 regulates alternate binding to co-chaperones CHIP and HOP to determine cellular protein folding/degradation balances. Oncogene 32(25):3101–3110. https://doi.org/10.1038/onc.2012.314
Muralidharan V, Oksman A, Pal P, Lindquist S, Goldberg DE (2012) Plasmodium falciparum heat shock protein 110 stabilizes the asparagine repeat-rich parasite proteome during malarial fevers. Nat Commun 3:1310. https://doi.org/10.1038/ncomms2306
Mylvaganam S, Earnshaw R, Heymann G, Kalia SK, Kalia LV (2020) C-terminus of Hsp70 Interacting Protein (CHIP) and Neurodegeneration: Lessons from the Bench and Bedside. Curr Neuropharmacol. https://doi.org/10.2174/1570159X18666201116145507
Nachman E, Wentink AS, Madiona K, Bousset L, Katsinelos T, Allinson K, Kampinga H, McEwan WA, Jahn TR, Melki R, Mogk A, Bukau B, Nussbaum-Krammer C (2020) Disassembly of Tau fibrils by the human Hsp70 disaggregation machinery generates small seeding-competent species. J Biol Chem 295(28):9676–9690. https://doi.org/10.1074/jbc.RA120.013478
Nahas EA, Nahas-Neto J, Orsatti CL, Tardivo AP, Uemura G, Peracoli MT, Witkin SS (2014) The 60- and 70-kDa heat-shock proteins and their correlation with cardiovascular risk factors in postmenopausal women with metabolic syndrome. Cell Stress Chaperones 19(4):559–568. https://doi.org/10.1007/s12192-013-0483-2
Narberhaus F (2002) Alpha-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol Mol Biol Rev 66(1):64–93. table of contents
Neckers L, Kern A, Tsutsumi S (2007) Hsp90 inhibitors disrupt mitochondrial homeostasis in cancer cells. Chem Biol 14(11):1204–1206
Neckers L, Blagg B, Haystead T, Trepel JB, Whitesell L, Picard D (2018) Methods to validate Hsp90 inhibitor specificity, to identify off-target effects, and to rethink approaches for further clinical development. Cell Stress Chaperones 23(4):467–482. https://doi.org/10.1007/s12192-018-0877-2
Nelson GM, Huffman H, Smith DF (2003) Comparison of the carboxy-terminal DP-repeat region in the co-chaperones Hop and Hip. Cell Stress Chaperones 8(2):125–133
Nemoto T, Sato N (1998) Oligomeric forms of the 90-kDa heat shock protein. Biochem J 330(Pt 2):989–995
Nielsen KL, Cowan NJ (1998) A single ring is sufficient for productive chaperonin-mediated folding in vivo. Mol Cell 2(1):93–99. https://doi.org/10.1016/s1097-2765(00)80117-3
Nikolay R, Wiederkehr T, Rist W, Kramer G, Mayer MP, Bukau B (2004) Dimerization of the human E3 ligase CHIP via a coiled-coil domain is essential for its activity. J Biol Chem 279(4):2673–2678. https://doi.org/10.1074/jbc.M311112200
Nitika, Truman AW (2017) Cracking the Chaperone Code: Cellular Roles for Hsp70 Phosphorylation. Trends Biochem Sci 42(12):932–935. https://doi.org/10.1016/j.tibs.2017.10.002
Nitika, Porter CM, Truman AW, Truttmann MC (2020) Post-translational modifications of Hsp70 family proteins: Expanding the chaperone code. J Biol Chem 295(31):10689–10708. https://doi.org/10.1074/jbc.REV120.011666
Njunge JM, Ludewig MH, Boshoff A, Pesce ER, Blatch GL (2013) Hsp70s and J proteins of Plasmodium parasites infecting rodents and primates: structure, function, clinical relevance, and drug targets. Curr Pharm Des 19(3):387–403
Nokin MJ, Durieux F, Peixoto P, Chiavarina B, Peulen O, Blomme A, Turtoi A, Costanza B, Smargiasso N, Baiwir D, Scheijen JL, Schalkwijk CG, Leenders J, De Tullio P, Bianchi E, Thiry M, Uchida K, Spiegel DA, Cochrane JR, Hutton CA, De Pauw E, Delvenne P, Belpomme D, Castronovo V, Bellahcène A (2016) Methylglyoxal, a glycolysis side-product, induces Hsp90 glycation and YAP-mediated tumor growth and metastasis. Elife 5:e19375. https://doi.org/10.7554/eLife.19375
Nyalwidhe J, Lingelbach K (2006) Proteases and chaperones are the most abundant proteins in the parasitophorous vacuole of Plasmodium falciparum-infected erythrocytes. Proteomics 6(5):1563–1573
Obermann WM, Sondermann H, Russo AA, Pavletich NP, Hartl FU (1998) In vivo function of Hsp90 is dependent on ATP binding and ATP hydrolysis. J Cell Biol 143(4):901–910
Odunuga OO, Hornby JA, Bies C, Zimmermann R, Pugh DJ, Blatch GL (2003) Tetratricopeptide repeat motif-mediated Hsc70-mSTI1 interaction. Molecular characterization of the critical contacts for successful binding and specificity. J Biol Chem 278(9):6896–6904. https://doi.org/10.1074/jbc.M206867200
Ogura T, Wilkinson AJ (2001) AAA+ superfamily ATPases: common structure--diverse function. Genes Cells 6(7):575–597
Oh HJ, Chen X, Subjeck JR (1997) Hsp110 protects heat-denatured proteins and confers cellular thermoresistance. J Biol Chem 272(50):31636–31640. https://doi.org/10.1074/jbc.272.50.31636
Oh HJ, Easton D, Murawski M, Kaneko Y, Subjeck JR (1999) The chaperoning activity of hsp110. Identification of functional domains by use of targeted deletions. J Biol Chem 274(22):15712–15718. https://doi.org/10.1074/jbc.274.22.15712
Oh JH, Hyun JY, Varshavsky A (2017) Control of Hsp90 chaperone and its clients by N-terminal acetylation and the N-end rule pathway. Proc Natl Acad Sci U S A 114(22):E4370–e4379. https://doi.org/10.1073/pnas.1705898114
Ohto-Fujita E, Fujita Y, Atomi Y (2007) Analysis of the alphaB-crystallin domain responsible for inhibiting tubulin aggregation. Cell Stress Chaperones 12(2):163–171
Onuoha SC, Coulstock ET, Grossmann JG, Jackson SE (2008) Structural studies on the co-chaperone Hop and its complexes with Hsp90. J Mol Biol 379(4):732–744
Padma Priya P, Grover M, Tatu US, Natarajan V (2015) Characterization of Precursor PfHsp60 in Plasmodium falciparum Cytosol during Its Asexual Development in Human Erythrocytes. PLoS One 10(8):e0136401. https://doi.org/10.1371/journal.pone.0136401
Pallavi R, Roy N, Nageshan RK, Talukdar P, Pavithra SR, Reddy R, Venketesh S, Kumar R, Gupta AK, Singh RK, Yadav SC, Tatu U (2010) Heat shock protein 90 as a drug target against protozoan infections: biochemical characterization of HSP90 from Plasmodium falciparum and Trypanosoma evansi and evaluation of its inhibitor as a candidate drug. J Biol Chem 285(49):37964–37975. https://doi.org/10.1074/jbc.M110.155317
Palleros DR, Reid KL, Shi L, Welch WJ, Fink AL (1993) ATP-induced protein-Hsp70 complex dissociation requires K+ but not ATP hydrolysis. Nature 365(6447):664–666. https://doi.org/10.1038/365664a0
Panaretou B, Prodromou C, Roe SM, O'Brien R, Ladbury JE, Piper PW, Pearl LH (1998) ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo. Embo J 17(16):4829–4836
Panaretou B, Siligardi G, Meyer P, Maloney A, Sullivan JK, Singh S, Millson SH, Clarke PA, Naaby-Hansen S, Stein R, Cramer R, Mollapour M, Workman P, Piper PW, Pearl LH, Prodromou C (2002) Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1. Mol Cell 10(6):1307–1318
Parcellier A, Schmitt E, Brunet M, Hammann A, Solary E, Garrido C (2005) Small heat shock proteins HSP27 and alphaB-crystallin: cytoprotective and oncogenic functions. Antioxid Redox Signal 7(3-4):404–413
Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496
Pavithra SR, Banumathy G, Joy O, Singh V, Tatu U (2004) Recurrent fever promotes Plasmodium falciparum development in human erythrocytes. J Biol Chem 279(45):46692–46699
Pavithra SR, Kumar R, Tatu U (2007) Systems analysis of chaperone networks in the malarial parasite Plasmodium falciparum. PLoS Comput Biol 3(9):1701–1715
Pearl LH, Prodromou C, Workman P (2008) The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem J 410(3):439–453
Pellecchia M, Szyperski T, Wall D, Georgopoulos C, Wuthrich K (1996) NMR structure of the J-domain and the Gly/Phe-rich region of the Escherichia coli DnaJ chaperone. J Mol Biol 260(2):236–250
Pesce ER, Blatch GL (2014) Plasmodial Hsp40 and Hsp70 chaperones: current and future perspectives. Parasitology 141(9):1167–1176. https://doi.org/10.1017/S003118201300228X
Pesce ER, Cockburn IL, Goble JL, Stephens LL, Blatch GL (2010) Malaria heat shock proteins: drug targets that chaperone other drug targets. Infect Disord Drug Targets 10(3):147–157
Pirkl F, Buchner J (2001) Functional analysis of the Hsp90-associated human peptidyl prolyl cis/trans isomerases FKBP51, FKBP52 and Cyp40. J Mol Biol 308(4):795–806
Pockley AG, Henderson B (2018) Extracellular cell stress (heat shock) proteins-immune responses and disease: an overview. Philos Trans R Soc Lond B Biol Sci 373(1738):20160522. https://doi.org/10.1098/rstb.2016.0522
Pockley AG, Henderson B, Multhoff G (2014) Extracellular cell stress proteins as biomarkers of human disease. Biochem Soc Trans 42(6):1744–1751. https://doi.org/10.1042/BST20140205
Polier S, Dragovic Z, Hartl FU, Bracher A (2008a) Structural basis for the cooperation of Hsp70 and Hsp110 chaperones in protein folding. Cell 133(6):1068–1079. https://doi.org/10.1016/j.cell.2008.05.022
Polier S, Dragovic Z, Hartl FU, Bracher A (2008b) Structural basis for the cooperation of Hsp70 and Hsp110 chaperones in protein folding. Cell 133(6):1068–1079. https://doi.org/10.1016/j.cell.2008.05.022
Pratt WB, Toft DO (2003) Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med (Maywood) 228(2):111–133
Pratt WB, Morishima Y, Peng HM, Osawa Y (2010) Proposal for a role of the Hsp90/Hsp70-based chaperone machinery in making triage decisions when proteins undergo oxidative and toxic damage. Exp Biol Med (Maywood) 235(3):278–289. https://doi.org/10.1258/ebm.2009.009250
Prince T, Sun L, Matts RL (2005) Cdk2: a genuine protein kinase client of Hsp90 and Cdc37. Biochemistry 44(46):15287–15295. https://doi.org/10.1021/bi051423m
Prodromou C (2016) Mechanisms of Hsp90 regulation. Biochem J 473(16):2439–2452. https://doi.org/10.1042/bcj20160005
Prodromou C, Roe SM, O'Brien R, Ladbury JE, Piper PW, Pearl LH (1997) Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90(1):65–75
Prodromou C, Siligardi G, O'Brien R, Woolfson DN, Regan L, Panaretou B, Ladbury JE, Piper PW, Pearl LH (1999) Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain co-chaperones. Embo J 18(3):754–762
Przyborski JM, Diehl M, Blatch GL (2015) Plasmodial HSP70s are functionally adapted to the malaria parasite life cycle. Front Mol Biosci 2:34. https://doi.org/10.3389/fmolb.2015.00034
Pulido P, Llamas E, Llorente B, Ventura S, Wright LP, Rodríguez-Concepción M (2016) Specific Hsp100 chaperones determine the fate of the first enzyme of the plastidial isoprenoid pathway for either refolding or degradation by the stromal clp protease in arabidopsis. PLoS Genet 12(1):e1005824. https://doi.org/10.1371/journal.pgen.1005824
Qi R, Sarbeng EB, Liu Q, Le KQ, Xu X, Xu H, Yang J, Wong JL, Vorvis C, Hendrickson WA, Zhou L, Liu Q (2013) Allosteric opening of the polypeptide-binding site when an Hsp70 binds ATP. Nat Struct Mol Biol 20(7):900–907. https://doi.org/10.1038/nsmb.2583
Qian YQ, Patel D, Hartl FU, McColl DJ (1996) Nuclear magnetic resonance solution structure of the human Hsp40 (HDJ-1) J-domain. J Mol Biol 260(2):224–235
Qian SB, McDonough H, Boellmann F, Cyr DM, Patterson C (2006) CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature 440(7083):551–555. https://doi.org/10.1038/nature04600
Rampelt H, Kirstein-Miles J, Nillegoda NB, Chi K, Scholz SR, Morimoto RI, Bukau B (2012) Metazoan Hsp70 machines use Hsp110 to power protein disaggregation. Embo j 31(21):4221–4235. https://doi.org/10.1038/emboj.2012.264
Ranek MJ, Stachowski MJ, Kirk JA, Willis MS (2018) The role of heat shock proteins and co-chaperones in heart failure. Philos Trans R Soc Lond B Biol Sci 373(1738):20160530. https://doi.org/10.1098/rstb.2016.0530
Ranson NA, White HE, Saibil HR (1998) Chaperonins. Biochem J 333(Pt 2):233–242. https://doi.org/10.1042/bj3330233
Rao R, Fiskus W, Yang Y, Lee P, Joshi R, Fernandez P, Mandawat A, Atadja P, Bradner JE, Bhalla K (2008) HDAC6 inhibition enhances 17-AAG--mediated abrogation of hsp90 chaperone function in human leukemia cells. Blood 112(5):1886–1893. https://doi.org/10.1182/blood-2008-03-143644. [pii]
Rauch JN, Gestwicki JE (2014) Binding of human nucleotide exchange factors to heat shock protein 70 (Hsp70) generates functionally distinct complexes in vitro. J Biol Chem 289(3):1402–1414. https://doi.org/10.1074/jbc.M113.521997
Raviol H, Sadlish H, Rodriguez F, Mayer MP, Bukau B (2006) Chaperone network in the yeast cytosol: Hsp110 is revealed as an Hsp70 nucleotide exchange factor. EMBO J 25(11):2510–2518. https://doi.org/10.1038/sj.emboj.7601139
Reddy VS, Madala SK, Trinath J, Reddy GB (2018) Extracellular small heat shock proteins: exosomal biogenesis and function. Cell Stress Chaperones 23(3):441–454. https://doi.org/10.1007/s12192-017-0856-z
Rehn A, Lawatscheck J, Jokisch ML, Mader SL, Luo Q, Tippel F, Blank B, Richter K, Lang K, Kaila VRI, Buchner J (2020) A methylated lysine is a switch point for conformational communication in the chaperone Hsp90. Nat Commun 11(1):1219. https://doi.org/10.1038/s41467-020-15048-8
Reid BG, Fenton WA, Horwich AL, Weber-Ban EU (2001) ClpA mediates directional translocation of substrate proteins into the ClpP protease. Proc Natl Acad Sci U S A 98(7):3768–3772
Requena JM, Montalvo AM, Fraga J (2015) Molecular chaperones of leishmania: central players in many stress-related and -unrelated physiological processes. Biomed Res Int 2015:301326. https://doi.org/10.1155/2015/301326
Riggs DL, Roberts PJ, Chirillo SC, Cheung-Flynn J, Prapapanich V, Ratajczak T, Gaber R, Picard D, Smith DF (2003) The Hsp90-binding peptidylprolyl isomerase FKBP52 potentiates glucocorticoid signaling in vivo. Embo J 22(5):1158–1167
Ritossa F (1996) Discovery of the heat shock response. Cell Stress Chaperones 1(2):97–98. https://doi.org/10.1379/1466-1268(1996)001<0097:dothsr>2.3.co;2
Rodina A, Wang T, Yan P, Gomes ED, Dunphy MP, Pillarsetty N, Koren J, Gerecitano JF, Taldone T, Zong H, Caldas-Lopes E, Alpaugh M, Corben A, Riolo M, Beattie B, Pressl C, Peter RI, Xu C, Trondl R, Patel HJ, Shimizu F, Bolaender A, Yang C, Panchal P, Farooq MF, Kishinevsky S, Modi S, Lin O, Chu F, Patil S, Erdjument-Bromage H, Zanzonico P, Hudis C, Studer L, Roboz GJ, Cesarman E, Cerchietti L, Levine R, Melnick A, Larson SM, Lewis JS, Guzman ML, Chiosis G (2016) The epichaperome is an integrated chaperome network that facilitates tumour survival. Nature 538(7625):397–401. https://doi.org/10.1038/nature19807
Roe SM, Ali MM, Meyer P, Vaughan CK, Panaretou B, Piper PW, Prodromou C, Pearl LH (2004) The Mechanism of Hsp90 regulation by the protein kinase-specific cochaperone p50(cdc37). Cell 116(1):87–98
Rogalla T, Ehrnsperger M, Preville X, Kotlyarov A, Lutsch G, Ducasse C, Paul C, Wieske M, Arrigo AP, Buchner J, Gaestel M (1999) Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor alpha by phosphorylation. J Biol Chem 274(27):18947–18956
Roseman AM, Chen S, White H, Braig K, Saibil HR (1996) The chaperonin ATPase cycle: mechanism of allosteric switching and movements of substrate-binding domains in GroEL. Cell 87(2):241–251. https://doi.org/10.1016/s0092-8674(00)81342-2
Rosenzweig R, Nillegoda NB, Mayer MP, Bukau B (2019) The Hsp70 chaperone network. Nat Rev Mol Cell Biol 20(11):665–680. https://doi.org/10.1038/s41580-019-0133-3
Rosser MF, Washburn E, Muchowski PJ, Patterson C, Cyr DM (2007) Chaperone functions of the E3 ubiquitin ligase CHIP. J Biol Chem 282(31):22267–22277
Rotanova TV, Andrianova AG, Kudzhaev AM, Li M, Botos I, Wlodawer A, Gustchina A (2019) New insights into structural and functional relationships between LonA proteases and ClpB chaperones. FEBS Open Bio 9(9):1536–1551. https://doi.org/10.1002/2211-5463.12691
Rudiger S, Buchberger A, Bukau B (1997) Interaction of Hsp70 chaperones with substrates. Nat Struct Biol 4(5):342–349. https://doi.org/10.1038/nsb0597-342
Rug M, Maier AG (2011) The heat shock protein 40 family of the malaria parasite Plasmodium falciparum. IUBMB Life 63(12):1081–1086
Rye HS, Burston SG, Fenton WA, Beechem JM, Xu Z, Sigler PB, Horwich AL (1997) Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature 388(6644):792–798. https://doi.org/10.1038/42047
Sager RA, Woodford MR, Backe SJ, Makedon AM, Baker-Williams AJ, DiGregorio BT, Loiselle DR, Haystead TA, Zachara NE, Prodromou C, Bourboulia D, Schmidt LS, Linehan WM, Bratslavsky G, Mollapour M (2019) Post-translational regulation of FNIP1 creates a rheostat for the molecular chaperone Hsp90. Cell Rep 26(5):1344–1356.e1345. https://doi.org/10.1016/j.celrep.2019.01.018
Saibil H (2000) Molecular chaperones: containers and surfaces for folding, stabilising or unfolding proteins. Curr Opin Struct Biol 10(2):251–258. https://doi.org/10.1016/s0959-440x(00)00074-9
Sanchez Y, Lindquist SL (1990) HSP104 required for induced thermotolerance. Science 248(4959):1112–1115
Sanchez Y, Taulien J, Borkovich KA, Lindquist S (1992) Hsp104 is required for tolerance to many forms of stress. Embo J 11(6):2357–2364
Sanchez J, Carter TR, Cohen MS, Blagg BSJ (2020) Old and New Approaches to Target the Hsp90 Chaperone. Curr Cancer Drug Targets 20(4):253–270. https://doi.org/10.2174/1568009619666191202101330
Sargeant TJ, Marti M, Caler E, Carlton JM, Simpson K, Speed TP, Cowman AF (2006) Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol 7(2):R12. https://doi.org/10.1186/gb-2006-7-2-r12
Sawarkar R, Sievers C, Paro R (2012) Hsp90 globally targets paused RNA polymerase to regulate gene expression in response to environmental stimuli. Cell 149(4):807–818. https://doi.org/10.1016/j.cell.2012.02.061
Scheufler C, Brinker A, Bourenkov G, Pegoraro S, Moroder L, Bartunik H, Hartl FU, Moarefi I (2000) Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101(2):199–210
Schirmer EC, Glover JR, Singer MA, Lindquist S (1996) HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem Sci 21(8):289–296
Schirmer EC, Queitsch C, Kowal AS, Parsell DA, Lindquist S (1998) The ATPase activity of Hsp104, effects of environmental conditions and mutations. J Biol Chem 273(25):15546–15552
Schirmer EC, Ware DM, Queitsch C, Kowal AS, Lindquist SL (2001) Subunit interactions influence the biochemical and biological properties of Hsp104. Proc Natl Acad Sci U S A 98(3):914–919
Schmid AB, Lagleder S, Grawert MA, Rohl A, Hagn F, Wandinger SK, Cox MB, Demmer O, Richter K, Groll M, Kessler H, Buchner J (2012) The architecture of functional modules in the Hsp90 co-chaperone Sti1/Hop. EMBO J 31(6):1506–1517. https://doi.org/10.1038/emboj.2011.472
Schmidt J, Vakonakis I (2020) Structure of the substrate-binding domain of Plasmodium falciparum heat-shock protein 70-x. Acta Crystallogr F Struct Biol Commun 76(Pt 10):495–500. https://doi.org/10.1107/s2053230x2001208x
Schopf FH, Biebl MM, Buchner J (2017) The HSP90 chaperone machinery. Nat Rev Mol Cell Biol 18(6):345–360. https://doi.org/10.1038/nrm.2017.20
Schuermann JP, Jiang J, Cuellar J, Llorca O, Wang L, Gimenez LE, Jin S, Taylor AB, Demeler B, Morano KA, Hart PJ, Valpuesta JM, Lafer EM, Sousa R (2008) Structure of the Hsp110:Hsc70 nucleotide exchange machine. Mol Cell 31(2):232–243. https://doi.org/10.1016/j.molcel.2008.05.006
Scior A, Buntru A, Arnsburg K, Ast A, Iburg M, Juenemann K, Pigazzini ML, Mlody B, Puchkov D, Priller J, Wanker EE, Prigione A, Kirstein J (2018) Complete suppression of Htt fibrilization and disaggregation of Htt fibrils by a trimeric chaperone complex. Embo J 37(2):282–299. https://doi.org/10.15252/embj.201797212
Selig EE, Zlatic CO, Cox D, Mok YF, Gooley PR, Ecroyd H, Griffin MDW (2020) N- and C-terminal regions of αB-crystallin and Hsp27 mediate inhibition of amyloid nucleation, fibril binding, and fibril disaggregation. J Biol Chem 295(29):9838–9854. https://doi.org/10.1074/jbc.RA120.012748
Seo MK, Straume O, Akslen LA, Cairns J (2020) HSP27 Expression as a Novel Predictive Biomarker for Bevacizumab: is it Cost Effective? Pharmacoecon Open 4(3):529–539. https://doi.org/10.1007/s41669-019-00193-8
Seraphim TV, Chakafana G, Shonhai A, Houry WA (2019) Plasmodium falciparum R2TP complex: driver of parasite Hsp90 function. Biophys Rev 11(6):1007–1015. https://doi.org/10.1007/s12551-019-00605-3
Sha B, Lee S, Cyr DM (2000) The crystal structure of the peptide-binding fragment from the yeast Hsp40 protein Sis1. Structure 8(8):799–807
Shaner L, Sousa R, Morano KA (2006) Characterization of Hsp70 binding and nucleotide exchange by the yeast Hsp110 chaperone Sse1. Biochemistry 45(50):15075–15084. https://doi.org/10.1021/bi061279k
Shao J, Hartson SD, Matts RL (2002) Evidence that protein phosphatase 5 functions to negatively modulate the maturation of the Hsp90-dependent heme-regulated eIF2alpha kinase. Biochemistry 41(21):6770–6779
Sharma YD (1992) Structure and possible function of heat-shock proteins in Falciparum malaria. Comp Biochem Physiol B, Comp Biochem 102(3):437–444
Sharma SK, Priya S (2017) Expanding role of molecular chaperones in regulating alpha-synuclein misfolding; implications in Parkinson's disease. Cell Mol Life Sci 74(4):617–629. https://doi.org/10.1007/s00018-016-2340-9
Shelton LB, Koren J 3rd, Blair LJ (2017) Imbalances in the Hsp90 chaperone machinery: implications for tauopathies. Front Neurosci 11:724. https://doi.org/10.3389/fnins.2017.00724
Sherman MY, Goldberg AL (2001) Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron 29(1):15–32. https://doi.org/10.1016/s0896-6273(01)00177-5
Shevtsov M, Huile G, Multhoff G (2018) Membrane heat shock protein 70: a theranostic target for cancer therapy. Philos Trans R Soc Lond B Biol Sci 373(1738):20160526. https://doi.org/10.1098/rstb.2016.0526
Shi YY, Hong XG, Wang CC (2005) The C-terminal (331-376) sequence of Escherichia coli DnaJ is essential for dimerization and chaperone activity: a small angle X-ray scattering study in solution. J Biol Chem 280(24):22761–22768
Shomura Y, Dragovic Z, Chang H-C, Tzvetkov N, Young JC, Brodsky JL, Guerriero V, Hartl FU, Bracher A (2005) Regulation of Hsp70 function by HspBP1: structural analysis reveals an alternate mechanism for Hsp70 nucleotide exchange. Molecular Cell 17(3):367–379. https://doi.org/10.1016/j.molcel.2004.12.023
Shonhai A, Boshoff A, Blatch GL (2005) Plasmodium falciparum heat shock protein 70 is able to suppress the thermosensitivity of an Escherichia coli DnaK mutant strain. Mol Genet Genomics 274(1):70–78. https://doi.org/10.1007/s00438-005-1150-9
Shonhai A, Boshoff A, Blatch GL (2007) The structural and functional diversity of Hsp70 proteins from Plasmodium falciparum. Protein Sci 16(9):1803–1818. https://doi.org/10.1110/ps.072918107
Shonhai A, Maier AG, Przyborski JM, Blatch GL (2010) Intracellular protozoan parasites of humans: the role of molecular chaperones in development and pathogenesis. Protein Pept Lett 18(2):143–157
Shrestha OK, Sharma R, Tomiczek B, Lee W, Tonelli M, Cornilescu G, Stolarska M, Nierzwicki L, Czub J, Markley JL, Marszalek J, Ciesielski SJ, Craig EA (2019) Structure and evolution of the 4-helix bundle domain of Zuotin, a J-domain protein co-chaperone of Hsp70. PLoS One 14(5):e0217098. https://doi.org/10.1371/journal.pone.0217098
Siegers K, Waldmann T, Leroux MR, Grein K, Shevchenko A, Schiebel E, Hartl FU (1999) Compartmentation of protein folding in vivo: sequestration of non-native polypeptide by the chaperonin-GimC system. Embo j 18(1):75–84. https://doi.org/10.1093/emboj/18.1.75
Siligardi G, Panaretou B, Meyer P, Singh S, Woolfson DN, Piper PW, Pearl LH, Prodromou C (2002) Regulation of Hsp90 ATPase activity by the co-chaperone Cdc37p/p50cdc37. J Biol Chem 277(23):20151–20159
Siligardi G, Hu B, Panaretou B, Piper PW, Pearl LH, Prodromou C (2004) Co-chaperone regulation of conformational switching in the Hsp90 ATPase cycle. J Biol Chem 279(50):51989–51998
Silva NSM, Torricillas MS, Minari K, Barbosa LRS, Seraphim TV, Borges JC (2020) Solution structure of Plasmodium falciparum Hsp90 indicates a high flexible dimer. Arch Biochem Biophys 690:108468. https://doi.org/10.1016/j.abb.2020.108468
Silverstein AM, Galigniana MD, Chen MS, Owens-Grillo JK, Chinkers M, Pratt WB (1997) Protein phosphatase 5 is a major component of glucocorticoid receptor.hsp90 complexes with properties of an FK506-binding immunophilin. J Biol Chem 272(26):16224–16230
Sima S, Richter K (2018) Regulation of the Hsp90 system. Biochim Biophys Acta Mol Cell Res 1865(6):889–897. https://doi.org/10.1016/j.bbamcr.2018.03.008
Singh MK, Sharma B, Tiwari PK (2017) The small heat shock protein Hsp27: present understanding and future prospects. J Therm Biol 69:149–154. https://doi.org/10.1016/j.jtherbio.2017.06.004
Skowyra D, Georgopoulos C, Zylicz M (1990) The E. coli dnaK gene product, the hsp70 homolog, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis-dependent manner. Cell 62(5):939–944. https://doi.org/10.1016/0092-8674(90)90268-j
Slepenkov SV, Witt SN (2002) The unfolding story of the Escherichia coli Hsp70 DnaK: is DnaK a holdase or an unfoldase? Mol Microbiol 45(5):1197–1206. https://doi.org/10.1046/j.1365-2958.2002.03093.x
Sliutz G, Karlseder J, Tempfer C, Orel L, Holzer G, Simon MM (1996) Drug resistance against gemcitabine and topotecan mediated by constitutive hsp70 overexpression in vitro: implication of quercetin as sensitiser in chemotherapy. Br J Cancer 74(2):172–177. https://doi.org/10.1038/bjc.1996.334
Sondermann H, Scheufler C, Schneider C, Hohfeld J, Hartl FU, Moarefi I (2001) Structure of a Bag/Hsc70 complex: convergent functional evolution of Hsp70 nucleotide exchange factors. Science 291(5508):1553–1557. https://doi.org/10.1126/science.1057268
Soti C, Vermes A, Haystead TA, Csermely P (2003) Comparative analysis of the ATP-binding sites of Hsp90 by nucleotide affinity cleavage: a distinct nucleotide specificity of the C-terminal ATP-binding site. Eur J Biochem 270(11):2421–2428
Sreedhar AS, Kalmar E, Csermely P, Shen YF (2004) Hsp90 isoforms: functions, expression and clinical importance. FEBS Lett 562(1–3):11–15
Srikakulam R, Liu L, Winkelmann DA (2008) Unc45b forms a cytosolic complex with Hsp90 and targets the unfolded myosin motor domain. PLoS ONE 3(5):e2137
Stebbins CE, Russo AA, Schneider C, Rosen N, Hartl FU, Pavletich NP (1997) Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 89(2):239–250
Sternlicht H, Farr GW, Sternlicht ML, Driscoll JK, Willison K, Yaffe MB (1993) The t-complex polypeptide 1 complex is a chaperonin for tubulin and actin in vivo. Proc Natl Acad Sci U S A 90(20):9422–9426. https://doi.org/10.1073/pnas.90.20.9422
Sterrenberg JN, Blatch GL, Edkins AL (2011) Human DNAJ in cancer and stem cells. Cancer Lett 312(2):129–142. https://doi.org/10.1016/j.canlet.2011.08.019
Stoldt V, Rademacher F, Kehren V, Ernst JF, Pearce DA, Sherman F (1996) Review: the Cct eukaryotic chaperonin subunits of Saccharomyces cerevisiae and other yeasts. Yeast 12(6):523–529
Suhane T, Laskar S, Advani S, Roy N, Varunan S, Bhattacharyya D, Bhattacharyya S, Bhattacharyya MK (2015) Both the charged linker region and ATPase domain of Hsp90 are essential for Rad51-dependent DNA repair. Eukaryot Cell 14(1):64–77. https://doi.org/10.1128/ec.00159-14
Sullivan WP, Owen BA, Toft DO (2002) The influence of ATP and p23 on the conformation of hsp90. J Biol Chem 277(48):45942–45948
Sun Y, MacRae TH (2005) The small heat shock proteins and their role in human disease. FEBS J 272(11):2613–2627. https://doi.org/10.1111/j.1742-4658.2005.04708.x
Suzuki H, Noguchi S, Arakawa H, Tokida T, Hashimoto M, Satow Y (2010) Peptide-binding sites as revealed by the crystal structures of the human Hsp40 Hdj1 C-terminal domain in complex with the octapeptide from human Hsp70. Biochemistry 49(39):8577–8584. https://doi.org/10.1021/bi100876n
Swain JF, Dinler G, Sivendran R, Montgomery DL, Stotz M, Gierasch LM (2007) Hsp70 chaperone ligands control domain association via an allosteric mechanism mediated by the interdomain linker. Mol Cell 26(1):27–39. https://doi.org/10.1016/j.molcel.2007.02.020
Taguwa S, Maringer K, Li X, Bernal-Rubio D, Rauch JN, Gestwicki JE, Andino R, Fernandez-Sesma A, Frydman J (2015) Defining Hsp70 subnetworks in dengue virus replication reveals key vulnerability in flavivirus infection. Cell 163(5):1108–1123. https://doi.org/10.1016/j.cell.2015.10.046
Taldone T, Gozman A, Maharaj R, Chiosis G (2008) Targeting Hsp90: small-molecule inhibitors and their clinical development. Curr Opin Pharmacol 8(4):370–374
Tang X, Chang C, Guo J, Lincoln V, Liang C, Chen M, Woodley DT, Li W (2019) Tumour-secreted Hsp90alpha on external surface of exosomes mediates tumour – stromal cell communication via autocrine and paracrine mechanisms. Sci Rep 9(1):15108. https://doi.org/10.1038/s41598-019-51704-w
Terasawa K, Minami M, Minami Y (2005) Constantly updated knowledge of Hsp90. J Biochem 137(4):443–447
Thakur SS, Swiderski K, Ryall JG, Lynch GS (2018) Therapeutic potential of heat shock protein induction for muscular dystrophy and other muscle wasting conditions. Philos Trans R Soc Lond B Biol Sci 373(1738):20160528. https://doi.org/10.1098/rstb.2016.0528
Tissieres A, Mitchell HK, Tracy UM (1974) Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. J Mol Biol 84(3):389–398. https://doi.org/10.1016/0022-2836(74)90447-1
Tomasello G, Rodolico V, Zerilli M, Martorana A, Bucchieri F, Pitruzzella A, Marino Gammazza A, David S, Rappa F, Zummo G, Damiani P, Accomando S, Rizzo M, de Macario EC, Macario AJ, Cappello F (2011) Changes in immunohistochemical levels and subcellular localization after therapy and correlation and colocalization with CD68 suggest a pathogenetic role of Hsp60 in ulcerative colitis. Appl Immunohistochem Mol Morphol: AIMM 19(6):552–561. https://doi.org/10.1097/PAI.0b013e3182118e5f
Tomiczek B, Delewski W, Nierzwicki L, Stolarska M, Grochowina I, Schilke B, Dutkiewicz R, Uzarska MA, Ciesielski SJ, Czub J, Craig EA, Marszalek J (2020) Two-step mechanism of J-domain action in driving Hsp70 function. PLoS Comput Biol 16(6):e1007913. https://doi.org/10.1371/journal.pcbi.1007913
Trepel J, Mollapour M, Giaccone G, Neckers L (2010) Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer 10(8):537–549. https://doi.org/10.1038/nrc2887
Tsai J, Douglas MG (1996) A conserved HPD sequence of the J-domain is necessary for YDJ1 stimulation of Hsp70 ATPase activity at a site distinct from substrate binding. J Biol Chem 271(16):9347–9354
Tsan MF, Gao B (2009) Heat shock proteins and immune system. J Leukoc Biol 85(6):905–910. https://doi.org/10.1189/jlb.0109005
Tukaj S, Kotlarz A, Jozwik A, Smolenska Z, Bryl E, Witkowski JM, Lipinska B (2010) Hsp40 proteins modulate humoral and cellular immune response in rheumatoid arthritis patients. Cell Stress Chaperones 15(5):555–566. https://doi.org/10.1007/s12192-010-0168-z
Turturici G, Sconzo G, Geraci F (2011) Hsp70 and its molecular role in nervous system diseases. Biochem Res Int 2011:618127. https://doi.org/10.1155/2011/618127
Turturici G, Tinnirello R, Sconzo G, Asea A, Savettieri G, Ragonese P, Geraci F (2014) Positive or negative involvement of heat shock proteins in multiple sclerosis pathogenesis: an overview. J Neuropathol Exp Neurol 73(12):1092–1106. https://doi.org/10.1097/NEN.0000000000000136
Ungewickell E, Ungewickell H, Holstein SE, Lindner R, Prasad K, Barouch W, Martin B, Greene LE, Eisenberg E (1995) Role of auxilin in uncoating clathrin-coated vesicles. Nature 378(6557):632–635. https://doi.org/10.1038/378632a0
van Eden W (2018) Immune tolerance therapies for autoimmune diseases based on heat shock protein T-cell epitopes. Philos Trans R Soc Lond B Biol Sci 373(1738):20160531. https://doi.org/10.1098/rstb.2016.0531
Vaughan CK, Mollapour M, Smith JR, Truman A, Hu B, Good VM, Panaretou B, Neckers L, Clarke PA, Workman P, Piper PW, Prodromou C, Pearl LH (2008) Hsp90-dependent activation of protein kinases is regulated by chaperone-targeted dephosphorylation of Cdc37. Mol Cell 31(6):886–895. https://doi.org/10.1016/j.molcel.2008.07.021
Vertii A, Hakim C, Kotlyarov A, Gaestel M (2006) Analysis of properties of small heat shock protein Hsp25 in MAPK-activated protein kinase 2 (MK2)-deficient cells: MK2-dependent insolubilization of Hsp25 oligomers correlates with susceptibility to stress. J Biol Chem 281(37):26966–26975
Vicente Miranda H, Chegão A, Oliveira MS, Fernandes Gomes B, Enguita FJ, Outeiro TF (2020) Hsp27 reduces glycation-induced toxicity and aggregation of alpha-synuclein. Faseb j 34(5):6718–6728. https://doi.org/10.1096/fj.201902936R
Vogel M, Mayer MP, Bukau B (2006) Allosteric regulation of Hsp70 chaperones involves a conserved interdomain linker. J Biol Chem 281(50):38705–38711. https://doi.org/10.1074/jbc.M609020200
Vos MJ, Hageman J, Carra S, Kampinga HH (2008) Structural and functional diversities between members of the human HSPB, HSPH, HSPA, and DNAJ chaperone families. Biochemistry 47(27):7001–7011
Voss AK, Thomas T, Gruss P (2000) Mice lacking HSP90beta fail to develop a placental labyrinth. Development 127(1):1–11
Wakabayashi Y, Kobayashi M, Akashi-Takamura S, Tanimura N, Konno K, Takahashi K, Ishii T, Mizutani T, Iba H, Kouro T, Takaki S, Takatsu K, Oda Y, Ishihama Y, Saitoh S, Miyake K (2006) A protein associated with toll-like receptor 4 (PRAT4A) regulates cell surface expression of TLR4. J Immunol 177(3):1772–1779
Walsh P, Bursac D, Law YC, Cyr D, Lithgow T (2004) The J-protein family: modulating protein assembly, disassembly and translocation. EMBO Rep 5(6):567–571
Wandinger SK, Richter K, Buchner J (2008) The Hsp90 chaperone machinery. J Biol Chem 283(27):18473–18477
Wang K, Shang Y, Dou F (2018) Brain aging: Hsp90 and neurodegenerative diseases. Adv Exp Med Biol 1086:93–103. https://doi.org/10.1007/978-981-13-1117-8_6
Wang J, Wang G, Cheng D, Huang S, Chang A, Tan X, Wang Q, Zhao S, Wu D, Liu AT, Yang S, Xiang R, Sun P (2020) Her2 promotes early dissemination of breast cancer by suppressing the p38-MK2-Hsp27 pathway that is targetable by Wip1 inhibition. Oncogene 39(40):6313–6326. https://doi.org/10.1038/s41388-020-01437-2
Wang L, Fu Y, Yu B, Jiang X, Liu H, Liu J, Zha B, Chu Y (2021) HSP70, a novel regulatory molecule in B cell-mediated suppression of autoimmune diseases. J Mol Biol 433(1):166634. https://doi.org/10.1016/j.jmb.2020.08.019
Ward BK, Allan RK, Mok D, Temple SE, Taylor P, Dornan J, Mark PJ, Shaw DJ, Kumar P, Walkinshaw MD, Ratajczak T (2002) A structure-based mutational analysis of cyclophilin 40 identifies key residues in the core tetratricopeptide repeat domain that mediate binding to Hsp90. J Biol Chem 277(43):40799–40809
Wei YJ, Huang YX, Shen Y, Cui CJ, Zhang XL, Zhang H, Hu SS (2009) Proteomic analysis reveals significant elevation of heat shock protein 70 in patients with chronic heart failure due to arrhythmogenic right ventricular cardiomyopathy. Mol Cell Biochem 332(1-2):103–111. https://doi.org/10.1007/s11010-009-0179-1
Whitesell L, Lindquist SL (2005) HSP90 and the chaperoning of cancer. Nat Rev Cancer 5(10):761–772
Wider D, Peli-Gulli MP, Briand PA, Tatu U, Picard D (2009) The complementation of yeast with human or Plasmodium falciparum Hsp90 confers differential inhibitor sensitivities. Mol Biochem Parasitol 164(2):147–152
Winkler J, Tyedmers J, Bukau B, Mogk A (2012) Hsp70 targets Hsp100 chaperones to substrates for protein disaggregation and prion fragmentation. J Cell Biol 198(3):387–404. https://doi.org/10.1083/jcb.201201074
Wisniewska M, Karlberg T, Lehtio L, Johansson I, Kotenyova T, Moche M, Schuler H (2010) Crystal structures of the ATPase domains of four human Hsp70 isoforms: HSPA1L/Hsp70-hom, HSPA2/Hsp70-2, HSPA6/Hsp70B’, and HSPA5/BiP/GRP78. PLoS One 5(1):e8625. https://doi.org/10.1371/journal.pone.0008625
Wittung-Stafshede P, Guidry J, Horne BE, Landry SJ (2003) The J-domain of Hsp40 couples ATP hydrolysis to substrate capture in Hsp70. Biochemistry 42(17):4937–4944. https://doi.org/10.1021/bi027333o
Wolmarans A, Kwantes A, LaPointe P (2019) A novel method for site-specific chemical SUMOylation: SUMOylation of Hsp90 modulates co-chaperone binding in vitro. Biol Chem 400(4):487–500. https://doi.org/10.1515/hsz-2018-0251
Wong DS, Jay DG (2016) Emerging roles of extracellular Hsp90 in cancer. Adv Cancer Res 129:141–163. https://doi.org/10.1016/bs.acr.2016.01.001
Woodford MR, Dunn DM, Ciciarelli JG, Beebe K, Neckers L, Mollapour M (2016) Targeting Hsp90 in Non-Cancerous Maladies. Curr Top Med Chem 16(25):2792–2804
Wortmann SB, Ziętkiewicz S, Kousi M, Szklarczyk R, Haack TB, Gersting SW, Muntau AC, Rakovic A, Renkema GH, Rodenburg RJ, Strom TM, Meitinger T, Rubio-Gozalbo ME, Chrusciel E, Distelmaier F, Golzio C, Jansen JH, van Karnebeek C, Lillquist Y, Lücke T, Õunap K, Zordania R, Yaplito-Lee J, van Bokhoven H, Spelbrink JN, Vaz FM, Pras-Raves M, Ploski R, Pronicka E, Klein C, Willemsen MA, de Brouwer AP, Prokisch H, Katsanis N, Wevers RA (2015) CLPB mutations cause 3-methylglutaconic aciduria, progressive brain atrophy, intellectual disability, congenital neutropenia, cataracts, movement disorder. Am J Hum Genet 96(2):245–257. https://doi.org/10.1016/j.ajhg.2014.12.013
Wu Y, Li J, Jin Z, Fu Z, Sha B (2005) The crystal structure of the C-terminal fragment of yeast Hsp40 Ydj1 reveals novel dimerization motif for Hsp40. J Mol Biol 346(4):1005–1011
Wu CT, Ou LS, Yeh KW, Lee WI, Huang JL (2011) Serum heat shock protein 60 can predict remission of flare-up in juvenile idiopathic arthritis. Clin Rheumatol 30(7):959–965. https://doi.org/10.1007/s10067-011-1709-2
Xu Z, Horwich AL, Sigler PB (1997) The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature 388(6644):741–750. https://doi.org/10.1038/41944
Xu Z, Page RC, Gomes MM, Kohli E, Nix JC, Herr AB, Patterson C, Misra S (2008) Structural basis of nucleotide exchange and client binding by the Hsp70 cochaperone Bag2. Nat Struct Mol Biol 15(12):1309–1317. https://doi.org/10.1038/nsmb.1518
Xu W, Beebe K, Chavez JD, Boysen M, Lu Y, Zuehlke AD, Keramisanou D, Trepel JB, Prodromou C, Mayer MP, Bruce JE, Gelis I, Neckers L (2019) Hsp90 middle domain phosphorylation initiates a complex conformational program to recruit the ATPase-stimulating cochaperone Aha1. Nat Commun 10(1):2574. https://doi.org/10.1038/s41467-019-10463-y
Yang Y, Rao R, Shen J, Tang Y, Fiskus W, Nechtman J, Atadja P, Bhalla K (2008) Role of acetylation and extracellular location of heat shock protein 90alpha in tumor cell invasion. Cancer Res 68(12):4833–4842. [pii]. https://doi.org/10.1158/0008-5472.CAN-08-0644
Young JC, Hartl FU (2000) Polypeptide release by Hsp90 involves ATP hydrolysis and is enhanced by the co-chaperone p23. Embo J 19(21):5930–5940
Young JC, Obermann WM, Hartl FU (1998) Specific binding of tetratricopeptide repeat proteins to the C-terminal 12-kDa domain of hsp90. J Biol Chem 273(29):18007–18010
Young JC, Hoogenraad NJ, Hartl FU (2003) Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112(1):41–50
Young JC, Agashe VR, Siegers K, Hartl FU (2004) Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 5(10):781–791. https://doi.org/10.1038/nrm1492
Young ZT, Rauch JN, Assimon VA, Jinwal UK, Ahn M, Li X, Dunyak BM, Ahmad A, Carlson GA, Srinivasan SR, Zuiderweg ER, Dickey CA, Gestwicki JE (2016) Stabilizing the Hsp70-Tau complex promotes turnover in models of tauopathy. Cell Chem Biol 23(8):992–1001. https://doi.org/10.1016/j.chembiol.2016.04.014
Yu EY, Ellard SL, Hotte SJ, Gingerich JR, Joshua AM, Gleave ME, Chi KN (2018) A randomized phase 2 study of a HSP27 targeting antisense, apatorsen with prednisone versus prednisone alone, in patients with metastatic castration resistant prostate cancer. Invest New Drugs 36(2):278–287. https://doi.org/10.1007/s10637-017-0553-x
Zarouchlioti C, Parfitt DA, Li W, Gittings LM, Cheetham ME (2018) DNAJ Proteins in neurodegeneration: essential and protective factors. Philos Trans R Soc Lond B Biol Sci 373(1738):20160534. https://doi.org/10.1098/rstb.2016.0534
Zhang W, Hirshberg M, McLaughlin SH, Lazar GA, Grossmann JG, Nielsen PR, Sobott F, Robinson CV, Jackson SE, Laue ED (2004) Biochemical and structural studies of the interaction of Cdc37 with Hsp90. J Mol Biol 340(4):891–907. https://doi.org/10.1016/j.jmb.2004.05.007
Zhang C, Xu Z, He XR, Michael LH, Patterson C (2005) CHIP, a cochaperone/ubiquitin ligase that regulates protein quality control, is required for maximal cardioprotection after myocardial infarction in mice. Am J Physiol Heart Circ Physiol 288(6):H2836–H2842
Zhang M, Boter M, Li K, Kadota Y, Panaretou B, Prodromou C, Shirasu K, Pearl LH (2008) Structural and functional coupling of Hsp90- and Sgt1-centred multi-protein complexes. Embo J 27(20):2789–2798
Zhang X, Liu T, Zheng S, Liu Q, Shen T, Han X, Zhang Q, Yang L, Lu X (2020) SUMOylation of HSP27 regulates PKM2 to promote esophageal squamous cell carcinoma progression. Oncol Rep 44(4):1355–1364. https://doi.org/10.3892/or.2020.7711
Zhao L, Vecchi G, Vendruscolo M, Korner R, Hayer-Hartl M, Hartl FU (2019) The Hsp70 chaperone system stabilizes a thermo-sensitive subproteome in E. coli. Cell Rep 28(5):1335–1345. e1336. https://doi.org/10.1016/j.celrep.2019.06.081
Zhu X, Zhao X, Burkholder WF, Gragerov A, Ogata CM, Gottesman ME, Hendrickson WA (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272(5268):1606–1614
Zininga T, Shonhai A (2019) Small molecule inhibitors targeting the heat shock protein system of human obligate protozoan parasites. Int J Mol Sci 20(23):5930. https://doi.org/10.3390/ijms20235930
Zininga T, Achilonu I, Hoppe H, Prinsloo E, Dirr HW, Shonhai A (2015a) Overexpression, purification and characterisation of the plasmodium falciparum Hsp70-z (PfHsp70-z) Protein. PLoS One 10(6):e0129445. https://doi.org/10.1371/journal.pone.0129445
Zininga T, Makumire S, Gitau GW, Njunge JM, Pooe OJ, Klimek H, Scheurr R, Raifer H, Prinsloo E, Przyborski JM, Hoppe H, Shonhai A (2015b) Plasmodium falciparum Hop (PfHop) interacts with the Hsp70 chaperone in a nucleotide-dependent fashion and exhibits ligand selectivity. PLoS One 10(8):e0135326. https://doi.org/10.1371/journal.pone.0135326
Zininga T, Achilonu I, Hoppe H, Prinsloo E, Dirr HW, Shonhai A (2016) Plasmodium falciparum Hsp70-z, an Hsp110 homologue, exhibits independent chaperone activity and interacts with Hsp70-1 in a nucleotide-dependent fashion. Cell Stress Chaperones 21(3):499–513. https://doi.org/10.1007/s12192-016-0678-4
Zolkiewski M (2006) A camel passes through the eye of a needle: protein unfolding activity of Clp ATPases. Mol Microbiol 61(5):1094–1100
Zougbede S, Miller F, Ravassard P, Rebollo A, Ciceron L, Couraud PO, Mazier D, Moreno A (2011) Metabolic acidosis induced by Plasmodium falciparum intraerythrocytic stages alters blood-brain barrier integrity. J Cereb Blood Flow Metab 31(2):514–526
Zuehlke A, Johnson JL (2010) Hsp90 and co-chaperones twist the functions of diverse client proteins. Biopolymers 93(3):211–217. https://doi.org/10.1002/bip.21292
Zuehlke AD, Reidy M, Lin C, LaPointe P, Alsomairy S, Lee DJ, Rivera-Marquez GM, Beebe K, Prince T, Lee S, Trepel JB, Xu W, Johnson J, Masison D, Neckers L (2017) An Hsp90 co-chaperone protein in yeast is functionally replaced by site-specific posttranslational modification in humans. Nat Commun 8:15328. https://doi.org/10.1038/ncomms15328
Zuehlke AD, Moses MA, Neckers L (2018) Heat shock protein 90: its inhibition and function. Philos Trans R Soc Lond B Biol Sci 373(1738):20160527. https://doi.org/10.1098/rstb.2016.0527
Zuiderweg ER, Hightower LE, Gestwicki JE (2017) The remarkable multivalency of the Hsp70 chaperones. Cell Stress Chaperones 22(2):173–189. https://doi.org/10.1007/s12192-017-0776-y
Zuo D, Subjeck J, Wang XY (2016) Unfolding the role of large heat shock proteins: new insights and therapeutic implications. Front Immunol 7:75. https://doi.org/10.3389/fimmu.2016.00075
Zylicz M, Ang D, Liberek K, Georgopoulos C (1989) Initiation of lambda DNA replication with purified host- and bacteriophage-encoded proteins: the role of the dnaK, dnaJ and grpE heat shock proteins. EMBO J 8(5):1601–1608
Author information
Authors and Affiliations
Corresponding authors
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Edkins, A.L., Boshoff, A. (2021). General Structural and Functional Features of Molecular Chaperones. In: Shonhai, A., Picard, D., Blatch, G.L. (eds) Heat Shock Proteins of Malaria. Advances in Experimental Medicine and Biology, vol 1340. Springer, Cham. https://doi.org/10.1007/978-3-030-78397-6_2
Download citation
DOI: https://doi.org/10.1007/978-3-030-78397-6_2
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-78396-9
Online ISBN: 978-3-030-78397-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)