Skip to main content
SpringerLink
Log in

Everything but the ACD, Functional Conservation of the Non-conserved Terminal Regions in sHSPs

  • Chapter
The Big Book on Small Heat Shock Proteins

Part of the book series: Heat Shock Proteins ((HESP,volume 8))

Abstract

At the primary level small heat shock proteins are commonly described as a conserved α-crystallin domain flanked by regions that have disparate sequence content. While this holds true when analysing simple pairwise alignments, it belittles the importance of these N-terminal and C-terminal extensions. Careful examination of their sequences, combined with an improved understanding of the structure and activity of these proteins, yields an alternative view where the N- and C-terminal arms play an important role in function. In this chapter we shall describe the current understanding of these two regions and highlight that they both demonstrate structural and functional properties that are highly conserved across all kingdoms of life.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ackerley S, James PA, Kalli A, French S, Davies KE, Talbot K (2006) A mutation in the small heat-shock protein HSPB1 leading to distal hereditary motor neuronopathy disrupts neurofilament assembly and the axonal transport of specific cellular cargoes. Hum Mol Genet 15:347–354

    CAS  PubMed  Google Scholar 

  • Ahrman E, Lambert W, Aquilina JA, Robinson CV, Emanuelsson CS (2007) Chemical cross-linking of the chloroplast localized small heat-shock protein, Hsp21, and the model substrate citrate synthase. Protein Sci 16:1464–1478

    PubMed Central  PubMed  Google Scholar 

  • Almeida-Souza L, Goethals S, de Winter V, Dierick I, Gallardo R, Van Durme J, Irobi J, Gettemans J, Rousseau F, Schymkowitz J, Timmerman V, Janssens S (2010) Increased monomerization of mutant HSPB1 leads to protein hyperactivity in Charcot-Marie-Tooth neuropathy. J Biol Chem 285:12778–12786

    CAS  PubMed Central  PubMed  Google Scholar 

  • Andley UP, Mathur S, Griest TA, Petrash JM (1996) Cloning, expression, and chaperone-like activity of human alphaA-crystallin. J Biol Chem 271:31973–31980

    CAS  PubMed  Google Scholar 

  • Andley UP, Malone JP, Townsend RR (2014) In vivo substrates of the lens molecular chaperones αA-crystallin and αB-crystallin. PLoS One 9:e95507

    PubMed Central  PubMed  Google Scholar 

  • Aquilina JA, Benesch JLP, Ding LL, Yaron O, Horwitz J, Robinson CV (2005) Subunit exchange of polydisperse proteins: mass spectrometry reveals consequences of alphaA-crystallin truncation. J Biol Chem 280:14485–14491

    CAS  PubMed  Google Scholar 

  • Arakawa T, Ejima D, Tsumoto K, Obeyama N, Tanaka Y, Kita Y, Timasheff SN (2007) Suppression of protein interactions by arginine: a proposed mechanism of the arginine effects. Biophys Chem 127:1–8

    CAS  PubMed  Google Scholar 

  • Bagnéris C, Bateman OA, Naylor CE, Cronin N, Boelens WC, Keep NH, Slingsby C (2009) Crystal structures of α-crystallin domain dimers of αB-crystallin and Hsp20. J Mol Biol 392:1242–1252

    PubMed  Google Scholar 

  • Baldwin AJ, Hilton GR, Lioe H, Bagnéris C, Benesch JLP, Kay LE (2011a) Quaternary dynamics of αB-crystallin as a direct consequence of localised tertiary fluctuations in the C-terminus. J Mol Biol 413:310–320

    CAS  PubMed  Google Scholar 

  • Baldwin AJ, Lioe H, Hilton GR, Baker LA, Rubinstein JL, Kay LE, Benesch JLP (2011b) The polydispersity of αB-crystallin is rationalized by an interconverting polyhedral architecture. Structure 19:1855–1863

    CAS  PubMed  Google Scholar 

  • Baranova EV, Weeks SD, Beelen S, Bukach OV, Gusev NB, Strelkov SV (2011) Three-dimensional structure of α-crystallin domain dimers of two human small heat shock proteins, HSPB1 and HSPB6. J Mol Biol 411:110–122

    CAS  PubMed  Google Scholar 

  • Basha E, Lee GJ, Breci LA, Hausrath AC, Buan NR, Giese KC, Vierling E (2004) The identity of proteins associated with a small heat shock protein during heat stress in vivo indicates that these chaperones protect a wide range of cellular functions. J Biol Chem 279:7566–7575

    CAS  PubMed  Google Scholar 

  • Basha E, Friedrich KL, Vierling E (2006) The N-terminal arm of small heat shock proteins is important for both chaperone activity and substrate specificity. J Biol Chem 281:39943–39952

    CAS  PubMed  Google Scholar 

  • Benndorf R, Hayess K, Ryazantsev S, Wieske M, Behlke J, Lutsch G (1994) Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J Biol Chem 269:20780–20784

    CAS  PubMed  Google Scholar 

  • Benndorf R, Martin JL, Kosakovsky Pond SL, Wertheim JO (2014) Neuropathy- and myopathy-associated mutations in human small heat shock proteins: characteristics and evolutionary history of the mutation sites. Mutat Res Rev Mutat Res. doi:10.1016/j.mrrev.2014.02.004

    PubMed  Google Scholar 

  • Bepperling A, Alte F, Kriehuber T, Braun N, Weinkauf S, Groll M, Haslbeck M, Buchner J (2012) Alternative bacterial two-component small heat shock protein systems. Proc Natl Acad Sci U S A 109:20407–20412

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bondino HG, Valle EM, Ten Have A (2011) Evolution and functional diversification of the small heat shock protein/α-crystallin family in higher plants. Planta 235:1299–1313

    PubMed  Google Scholar 

  • Braun N, Zacharias M, Peschek J, Kastenmüller A, Zou J, Hanzlik M, Haslbeck M, Rappsilber J, Buchner J, Weinkauf S (2011) Multiple molecular architectures of the eye lens chaperone αB-crystallin elucidated by a triple hybrid approach. Proc Natl Acad Sci U S A 108:20491–20496

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bruinsma IB, Bruggink KA, Kinast K, Versleijen AAM, Segers-Nolten IMJ, Subramaniam V, Kuiperij HB, Boelens W, de Waal RMW, Verbeek MM (2011) Inhibition of α-synuclein aggregation by small heat shock proteins. Proteins 79:2956–2967

    CAS  PubMed  Google Scholar 

  • Bukach OV, Seit-Nebi AS, Marston SB, Gusev NB (2004) Some properties of human small heat shock protein Hsp20 (HspB6). Eur J Biochem 271:291–302

    CAS  PubMed  Google Scholar 

  • Campanella JJ, Bitincka L, Smalley J (2003) MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinformatics 4:29

    PubMed Central  PubMed  Google Scholar 

  • Cheng G, Basha E, Wysocki VH, Vierling E (2008) Insights into small heat shock protein and substrate structure during chaperone action derived from hydrogen/deuterium exchange and mass spectrometry. J Biol Chem 283:26634–26642

    CAS  PubMed Central  PubMed  Google Scholar 

  • Clauwaert J, Ellerton HD, Koretz JF, Thomson K, Augusteyn RC (1989) The effect of temperature on the renaturation of alpha-crystallin. Curr Eye Res 8:397–403

    CAS  PubMed  Google Scholar 

  • Crabbe MJ, Goode D (1994) Alpha-crystallin: chaperoning and aggregation. Biochem J 297(Pt 3):653–654

    CAS  PubMed Central  PubMed  Google Scholar 

  • Crack JA, Mansour M, Sun Y, MacRae TH (2002) Functional analysis of a small heat shock/alpha-crystallin protein from Artemia franciscana. Oligomerization and thermotolerance. Eur J Biochem 269:933–942

    CAS  PubMed  Google Scholar 

  • Crooks GE, Hon G, Chandonia J-M, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190

    CAS  PubMed Central  PubMed  Google Scholar 

  • De Jong WW, Caspers GJ, Leunissen JA (1998) Genealogy of the alpha-crystallin–small heat-shock protein superfamily. Int J Biol Macromol 22:151–162

    PubMed  Google Scholar 

  • Delbecq SP, Jehle S, Klevit R (2012) Binding determinants of the small heat shock protein, αB-crystallin: recognition of the “IxI” motif. EMBO J 31:4587–4594

    CAS  PubMed Central  PubMed  Google Scholar 

  • Derham BK, van Boekel MA, Muchowski PJ, Clark JI, Horwitz J, Hepburne-Scott HW, de Jong WW, Crabbe MJ, Harding JJ (2001) Chaperone function of mutant versions of alpha A- and alpha B-crystallin prepared to pinpoint chaperone binding sites. Eur J Biochem 268:713–721

    CAS  PubMed  Google Scholar 

  • Dreiza CM, Brophy CM, Komalavilas P, Furnish EJ, Joshi L, Pallero MA, Murphy-Ullrich JE, von Rechenberg M, Ho YJ, Richardson B, Xu N, Zhen Y, Peltier JM, Panitch A (2005) Transducible heat shock protein 20 (HSP20) phosphopeptide alters cytoskeletal dynamics. FASEB J 19:261–263

    CAS  PubMed  Google Scholar 

  • Dreiza C, Komalavilas P, Furnish E, Flynn C, Sheller M, Smoke C, Lopes L, Brophy C (2010) The small heat shock protein, HSPB6, in muscle function and disease. Cell Stress Chaperones 15:1–11

    CAS  PubMed Central  PubMed  Google Scholar 

  • Feil IK, Malfois M, Hendle J, van Der Zandt H, Svergun DI (2001) A novel quaternary structure of the dimeric alpha-crystallin domain with chaperone-like activity. J Biol Chem 276:12024–12029

    CAS  PubMed  Google Scholar 

  • Fernando P, Heikkila JJ (2000) Functional characterization of Xenopus small heat shock protein, Hsp30C: the carboxyl end is required for stability and chaperone activity. Cell Stress Chaperones 5:148–159

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fernando P, Abdulle R, Mohindra A, Guillemette JG, Heikkila JJ (2002) Mutation or deletion of the C-terminal tail affects the function and structure of Xenopus laevis small heat shock protein, hsp30. Comp Biochem Physiol B Biochem Mol Biol 133:95–103

    CAS  PubMed  Google Scholar 

  • Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230

    CAS  PubMed Central  PubMed  Google Scholar 

  • Franck E, Madsen O, Rheede T, Ricard G, Huynen MA, Jong WW (2004) Evolutionary diversity of vertebrate small heat shock proteins. J Mol Evol 59:792–805

    CAS  PubMed  Google Scholar 

  • Fu X, Zhang H, Zhang X, Cao Y, Jiao W, Liu C, Song Y, Abulimiti A, Chang Z (2005) A dual role for the N-terminal region of Mycobacterium tuberculosis Hsp16.3 in self-oligomerization and binding denaturing substrate proteins. J Biol Chem 280:6337–6348

    CAS  PubMed  Google Scholar 

  • Fu X, Shi X, Yin L, Liu J, Joo K, Lee J, Chang Z (2013) Small heat shock protein IbpB acts as a robust chaperone in living cells by hierarchically activating its multi-type substrate-binding residues. J Biol Chem 288:11897–11906

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fujii N, Awakura M, Takemoto L, Inomata M, Takata T, Fujii N, Saito T (2003) Characterization of alphaA-crystallin from high molecular weight aggregates in the normal human lens. Mol Vis 9:315–322

    CAS  PubMed  Google Scholar 

  • Ghosh JG, Clark JI (2005) Insights into the domains required for dimerization and assembly of human alphaB crystallin. Protein Sci 14:684–695

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ghosh JG, Estrada MR, Clark JI (2005) Interactive domains for chaperone activity in the small heat shock protein, human alphaB crystallin. Biochemistry 44:14854–14869

    CAS  PubMed  Google Scholar 

  • Ghosh JG, Shenoy AK, Clark JI (2006) N- and C-Terminal motifs in human alphaB crystallin play an important role in the recognition, selection, and solubilization of substrates. Biochemistry 45:13847–13854

    CAS  PubMed  Google Scholar 

  • Giese KC, Vierling E (2004) Mutants in a small heat shock protein that affect the oligomeric state. Analysis and allele-specific suppression. J Biol Chem 279:32674–32683

    CAS  PubMed  Google Scholar 

  • Giese KC, Basha E, Catague BY, Vierling E (2005) Evidence for an essential function of the N terminus of a small heat shock protein in vivo, independent of in vitro chaperone activity. Proc Natl Acad Sci U S A 102:18896–18901

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224

    CAS  PubMed  Google Scholar 

  • Groenen PJ, Merck KB, de Jong WW, Bloemendal H (1994) Structure and modifications of the junior chaperone alpha-crystallin. From lens transparency to molecular pathology. Eur J Biochem 225:1–19

    CAS  PubMed  Google Scholar 

  • Guo Z, Cooper LF (2000) An N-terminal 33-amino-acid-deletion variant of hsp25 retains oligomerization and functional properties. Biochem Biophys Res Commun 270:183–189

    CAS  PubMed  Google Scholar 

  • Gustavsson N, Kokke BP, Anzelius B, Boelens WC, Sundby C (2001) Substitution of conserved methionines by leucines in chloroplast small heat shock protein results in loss of redox-response but retained chaperone-like activity. Protein Sci 10:1785–1793

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hanazono Y, Takeda K, Yohda M, Miki K (2012) Structural studies on the oligomeric transition of a small heat shock protein, StHsp14.0. J Mol Biol 422:100–108

    CAS  PubMed  Google Scholar 

  • Hanazono Y, Takeda K, Oka T, Abe T, Tomonari T, Akiyama N, Aikawa Y, Yohda M, Miki K (2013) Nonequivalence observed for the 16-meric structure of a small heat shock protein, SpHsp16.0, from Schizosaccharomyces pombe. Structure 21:220–228

    CAS  PubMed  Google Scholar 

  • Härndahl U, Kokke BP, Gustavsson N, Linse S, Berggren K, Tjerneld F, Boelens WC, Sundby C (2001) The chaperone-like activity of a small heat shock protein is lost after sulfoxidation of conserved methionines in a surface-exposed amphipathic alpha-helix. Biochim Biophys Acta 1545:227–237

    PubMed  Google Scholar 

  • Haslbeck M, Ignatiou A, Saibil H, Helmich S, Frenzl E, Stromer T, Buchner J (2004) A domain in the N-terminal part of Hsp26 is essential for chaperone function and oligomerization. J Mol Biol 343:445–455

    CAS  PubMed  Google Scholar 

  • Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12:842–846

    CAS  PubMed  Google Scholar 

  • Heirbaut M, Beelen S, Strelkov SV, Weeks SD (2014) Dissection the functional role of the N-terminal domain of the human small heat shock protein HSPB6. PLoS One 9:e105892

    PubMed Central  PubMed  Google Scholar 

  • Hilario E, Martin FJM, Bertolini MC, Fan L (2011) Crystal structures of xanthomonas small heat shock protein provide a structural basis for an active molecular chaperone oligomer. J Mol Biol 408:74–86

    CAS  PubMed  Google Scholar 

  • Hilton GR, Hochberg GKA, Laganowsky A, McGinnigle SI, Baldwin AJ, Benesch JLP (2013) C-terminal interactions mediate the quaternary dynamics of αB-crystallin. Philos Trans R Soc Lond B Biol Sci 368:20110405

    PubMed Central  PubMed  Google Scholar 

  • Hochberg GKA, Ecroyd H, Liu C, Cox D, Cascio D, Sawaya MR, Collier MP, Stroud J, Carver JA, Baldwin AJ, Robinson CV, Eisenberg DS, Benesch JLP, Laganowsky A (2014) The structured core domain of αB-crystallin can prevent amyloid fibrillation and associated toxicity. Proc Natl Acad Sci U S A 111:E1562–E1570

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hooi MYS, Raftery MJ, Truscott RJW (2013) Age-dependent racemization of serine residues in a human chaperone protein. Protein Sci 22:93–100

    CAS  PubMed Central  PubMed  Google Scholar 

  • Horwitz J (2003) Alpha-crystallin. Exp Eye Res 76:145–153

    CAS  PubMed  Google Scholar 

  • Horwitz J, Bova M, Huang QL, Ding L, Yaron O, Lowman S (1998) Mutation of alpha B-crystallin: effects on chaperone-like activity. Int J Biol Macromol 22:263–269

    CAS  PubMed  Google Scholar 

  • Jaya N, Garcia V, Vierling E (2009) Substrate binding site flexibility of the small heat shock protein molecular chaperones. Proc Natl Acad Sci U S A 106:15604–15609

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jehle S, Rajagopal P, Bardiaux B, Markovic S, Kühne R, Stout JR, Higman VA, Klevit RE, van Rossum B-J, Oschkinat H (2010) Solid-state NMR and SAXS studies provide a structural basis for the activation of alphaB-crystallin oligomers. Nat Struct Mol Biol 17:1037–1042

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jehle S, Vollmar BS, Bardiaux B, Dove KK, Rajagopal P, Gonen T, Oschkinat H, Klevit RE (2011) N-terminal domain of alphaB-crystallin provides a conformational switch for multimerization and structural heterogeneity. Proc Natl Acad Sci U S A 108:6409–6414

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jiao W, Qian M, Li P, Zhao L, Chang Z (2005) The essential role of the flexible termini in the temperature-responsiveness of the oligomeric state and chaperone-like activity for the polydisperse small heat shock protein IbpB from Escherichia coli. J Mol Biol 347:871–884

    CAS  PubMed  Google Scholar 

  • Kallur LS, Aziz A, Abraham EC (2008) C-Terminal truncation affects subunit exchange of human alphaA-crystallin with alphaB-crystallin. Mol Cell Biochem 308:85–91

    CAS  PubMed  Google Scholar 

  • Kelley PB, Abraham EC (2003) Thermally induced disintegration of the oligomeric structure of alphaB-crystallin mutant F28S is associated with diminished chaperone activity. Mol Cell Biochem 252:273–278

    CAS  PubMed  Google Scholar 

  • Kim KK, Kim R, Kim SH (1998) Crystal structure of a small heat-shock protein. Nature 394:595–599

    CAS  PubMed  Google Scholar 

  • Kim R, Lai L, Lee H-H, Cheong G-W, Kim KK, Wu Z, Yokota H, Marqusee S, Kim S-H (2003) On the mechanism of chaperone activity of the small heat-shock protein of Methanococcus jannaschii. Proc Natl Acad Sci U S A 100:8151–8155

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kirschner M, Winkelhaus S, Thierfelder JM, Nover L (2000) Transient expression and heat-stress-induced co-aggregation of endogenous and heterologous small heat-stress proteins in tobacco protoplasts. Plant J 24:397–411

    CAS  PubMed  Google Scholar 

  • Kriehuber T, Rattei T, Weinmaier T, Bepperling A, Haslbeck M, Buchner J (2010) Independent evolution of the core domain and its flanking sequences in small heat shock proteins. FASEB J 24:3633–3642

    CAS  PubMed  Google Scholar 

  • Kundu M, Sen PC, Das KP (2007) Structure, stability, and chaperone function of alphaA-crystallin: role of N-terminal region. Biopolymers 86:177–192

    CAS  PubMed  Google Scholar 

  • Laganowsky A, Eisenberg D (2010) Non-3D domain swapped crystal structure of truncated zebrafish alphaA crystallin. Protein Sci 19:1978–1984

    CAS  PubMed Central  PubMed  Google Scholar 

  • Laganowsky A, Benesch JLP, Landau M, Ding L, Sawaya MR, Cascio D, Huang Q, Robinson CV, Horwitz J, Eisenberg D (2010) Crystal structures of truncated alphaA and alphaB crystallins reveal structural mechanisms of polydispersity important for eye lens function. Protein Sci 19:1031–1043

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lambert H, Charette SJ, Bernier AF, Guimond A, Landry J (1999) HSP27 multimerization mediated by phosphorylation-sensitive intermolecular interactions at the amino terminus. J Biol Chem 274:9378–9385

    CAS  PubMed  Google Scholar 

  • Laskowski RA, Swindells MB (2011) LigPlot+: multiple ligand-protein interaction diagrams for drug discovery. J Chem Inf Model 51:2778–2786

    CAS  PubMed  Google Scholar 

  • Lelj-Garolla B, Mauk AG (2005) Self-association of a small heat shock protein. J Mol Biol 345:631–642

    CAS  PubMed  Google Scholar 

  • Lelj-Garolla B, Mauk AG (2012) Roles of the N- and C-terminal sequences in Hsp27 self-association and chaperone activity. Protein Sci 21:122–133

    CAS  PubMed Central  PubMed  Google Scholar 

  • Leroux MR, Melki R, Gordon B, Batelier G, Candido EP (1997) Structure-function studies on small heat shock protein oligomeric assembly and interaction with unfolded polypeptides. J Biol Chem 272:24646–24656

    CAS  PubMed  Google Scholar 

  • Li H, Li C, Lu Q, Su T, Ke T, Li DW-C, Yuan M, Liu J, Ren X, Zhang Z, Zeng S, Wang QK, Liu M (2008) Cataract mutation P20S of alphaB-crystallin impairs chaperone activity of alphaA-crystallin and induces apoptosis of human lens epithelial cells. Biochim Biophys Acta 1782:303–309

    CAS  PubMed  Google Scholar 

  • Liao J-H, Lee J-S, Wu S-H, Chiou S-H (2009) COOH-terminal truncations and site-directed mutations enhance thermostability and chaperone-like activity of porcine alphaB-crystallin. Mol Vis 15:1429–1444

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lindner RA, Carver JA, Ehrnsperger M, Buchner J, Esposito G, Behlke J, Lutsch G, Kotlyarov A, Gaestel M (2000) Mouse Hsp25, a small shock protein. The role of its C-terminal extension in oligomerization and chaperone action. Eur J Biochem 267:1923–1932

    CAS  PubMed  Google Scholar 

  • Liu Z, Yao P, Guo X, Xu B (2014) Two small heat shock protein genes in Apis cerana cerana: characterization, regulation, and developmental expression. Gene 545:205–214

    CAS  PubMed  Google Scholar 

  • Maaroufi H, Tanguay RM (2013) Analysis and phylogeny of small heat shock proteins from marine viruses and their cyanobacteria host. PLoS One 8:e81207

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 51:1257–1268

    CAS  PubMed Central  PubMed  Google Scholar 

  • Morrow G, Heikkila JJ, Tanguay RM (2006) Differences in the chaperone-like activities of the four main small heat shock proteins of Drosophila melanogaster. Cell Stress Chaperones 11:51–60

    CAS  PubMed Central  PubMed  Google Scholar 

  • Numoto N, Kita A, Fujii N, Miki K (2012) A P39R mutation at the N-terminal domain of human αB-crystallin regulates its oligomeric state and chaperone-like activity. Biochem Biophys Res Commun 425:601–606

    CAS  PubMed  Google Scholar 

  • Pasta SY, Raman B, Ramakrishna T, Rao CM (2003) Role of the conserved SRLFDQFFG region of alpha-crystallin, a small heat shock protein. Effect on oligomeric size, subunit exchange, and chaperone-like activity. J Biol Chem 278:51159–51166

    CAS  PubMed  Google Scholar 

  • Pasta SY, Raman B, Ramakrishna T, Rao CM (2004) The IXI/V motif in the C-terminal extension of alpha-crystallins: alternative interactions and oligomeric assemblies. Mol Vis 10:655–662

    CAS  PubMed  Google Scholar 

  • Plater ML, Goode D, Crabbe MJ (1996) Effects of site-directed mutations on the chaperone-like activity of alphaB-crystallin. J Biol Chem 271:28558–28566

    CAS  PubMed  Google Scholar 

  • Poulain P, Gelly J-C, Flatters D (2010) Detection and architecture of small heat shock protein monomers. PLoS One 5:e9990

    PubMed Central  PubMed  Google Scholar 

  • Qian J, Vafiadaki E, Florea SM, Singh VP, Song W, Kung Lam C, Wang Y, Yuan Q, Pritchard TJ, Cai W, Haghighi K, Rodriguez P, Wang H-S, Sanoudou D, Fan G-C, Kranias EG (2011) Small heat shock protein 20 interacts with protein phosphatase-1 and enhances sarcoplasmic reticulum calcium cycling. Circ Res 108:1429–1438

    CAS  PubMed Central  PubMed  Google Scholar 

  • Quinlan RA, Zhang Y, Lansbury A, Williamson I, Pohl E, Sun F (2013) Changes in the quaternary structure and function of MjHSP16.5 attributable to deletion of the IXI motif and introduction of the substitution, R107G, in the α-crystallin domain. Philos Trans R Soc Lond B Biol Sci 368:20120327

    PubMed Central  PubMed  Google Scholar 

  • Raman B, Ban T, Sakai M, Pasta SY, Ramakrishna T, Naiki H, Goto Y, Rao CM (2005) AlphaB-crystallin, a small heat-shock protein, prevents the amyloid fibril growth of an amyloid beta-peptide and beta2-microglobulin. Biochem J 392:573–581

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ren J, Wen L, Gao X, Jin C, Xue Y, Yao X (2009) DOG 1.0: illustrator of protein domain structures. Cell Res 19:271–273

    CAS  PubMed  Google Scholar 

  • Saha S, Das KP (2004) Relationship between chaperone activity and oligomeric size of recombinant human alphaA- and alphaB-crystallin: a tryptic digestion study. Proteins 57:610–617

    CAS  PubMed  Google Scholar 

  • Saji H, Iizuka R, Yoshida T, Abe T, Kidokoro S-I, Ishii N, Yohda M (2008) Role of the IXI/V motif in oligomer assembly and function of StHsp14.0, a small heat shock protein from the acidothermophilic archaeon, Sulfolobus tokodaii strain 7. Proteins 71:771–782

    CAS  PubMed  Google Scholar 

  • Santhoshkumar P, Murugesan R, Sharma KK (2009) Deletion of (54)FLRAPSWF(61) residues decreases the oligomeric size and enhances the chaperone function of alphaB-crystallin. Biochemistry 48:5066–5073

    CAS  PubMed Central  PubMed  Google Scholar 

  • Scharf KD, Siddique M, Vierling E (2001) The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing alpha-crystallin domains (Acd proteins). Cell Stress Chaperones 6:225–237

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shah D, Li J, Shaikh AR, Rajagopalan R (2012) Arginine-aromatic interactions and their effects on arginine-induced solubilization of aromatic solutes and suppression of protein aggregation. Biotechnol Prog 28:223–231

    CAS  PubMed  Google Scholar 

  • Sharma KK, Santhoshkumar P (2009) Lens aging: effects of crystallins. Biochim Biophys Acta 1790:1095–1108

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shashidharamurthy R, Koteiche HA, Dong J, McHaourab HS (2005) Mechanism of chaperone function in small heat shock proteins: dissociation of the HSP27 oligomer is required for recognition and binding of destabilized T4 lysozyme. J Biol Chem 280:5281–5289

    CAS  PubMed  Google Scholar 

  • Shi J, Koteiche HA, McDonald ET, Fox TL, Stewart PL, McHaourab HS (2013) Cryoelectron microscopy analysis of small heat shock protein 16.5 (Hsp16.5) complexes with T4 lysozyme reveals the structural basis of multimode binding. J Biol Chem 288:4819–4830

    CAS  PubMed Central  PubMed  Google Scholar 

  • Siddique M, Gernhard S, von Koskull-Döring P, Vierling E, Scharf K-D (2008) The plant sHSP superfamily: five new members in Arabidopsis thaliana with unexpected properties. Cell Stress Chaperones 13:183–197

    CAS  PubMed Central  PubMed  Google Scholar 

  • Smulders RH, Carver JA, Lindner RA, van Boekel MA, Bloemendal H, de Jong WW (1996) Immobilization of the C-terminal extension of bovine alphaA-crystallin reduces chaperone-like activity. J Biol Chem 271:29060–29066

    CAS  Google Scholar 

  • Soskić V, Groebe K, Schrattenholz A (2008) Nonenzymatic posttranslational protein modifications in ageing. Exp Gerontol 43:247–257

    PubMed  Google Scholar 

  • Stromer T, Fischer E, Richter K, Haslbeck M, Buchner J (2004) Analysis of the regulation of the molecular chaperone Hsp26 by temperature-induced dissociation: the N-terminal domail is important for oligomer assembly and the binding of unfolding proteins. J Biol Chem 279:11222–11228

    CAS  PubMed  Google Scholar 

  • Studer S, Obrist M, Lentze N, Narberhaus F (2002) A critical motif for oligomerization and chaperone activity of bacterial alpha-heat shock proteins. Eur J Biochem 269:3578–3586

    CAS  PubMed  Google Scholar 

  • Sun Y, MacRae TH (2005) Characterization of novel sequence motifs within N- and C-terminal extensions of p26, a small heat shock protein from Artemia franciscana. FEBS J 272:5230–5243

    CAS  PubMed  Google Scholar 

  • Sun Y, Mansour M, Crack JA, Gass GL, MacRae TH (2004) Oligomerization, chaperone activity, and nuclear localization of p26, a small heat shock protein from Artemia franciscana. J Biol Chem 279:39999–40006

    CAS  PubMed  Google Scholar 

  • Takeda K, Hayashi T, Abe T, Hirano Y, Hanazono Y, Yohda M, Miki K (2011) Dimer structure and conformational variability in the N-terminal region of an archaeal small heat shock protein, StHsp14.0. J Struct Biol 174:92–99

    CAS  PubMed  Google Scholar 

  • Theriault JR (2004) Essential role of the NH2-terminal WD/EPF motif in the phosphorylation-activated protective function of mammalian Hsp27. J Biol Chem 279:23463–23471

    CAS  PubMed  Google Scholar 

  • Tomoyasu T, Tabata A, Nagamune H (2010) Investigation of the chaperone function of the small heat shock protein-AgsA. BMC Biochem 11:27

    PubMed Central  PubMed  Google Scholar 

  • Treweek TM, Ecroyd H, Williams DM, Meehan S, Carver JA, Walker MJ (2007) Site-directed mutations in the C-terminal extension of human alphaB-crystallin affect chaperone function and block amyloid fibril formation. PLoS One 2:e1046

    PubMed Central  PubMed  Google Scholar 

  • Usui K, Hatipoglu OF, Ishii N, Yohda M (2004) Role of the N-terminal region of the crenarchaeal sHsp, StHsp14.0, in thermal-induced disassembly of the complex and molecular chaperone activity. Biochem Biophys Res Commun 315:113–118

    CAS  PubMed  Google Scholar 

  • Van Boekel MA, Hoogakker SE, Harding JJ, de Jong WW (1996) The influence of some post-translational modifications on the chaperone-like activity of alpha-crystallin. Ophthalmic Res 28(Suppl 1):32–38

    PubMed  Google Scholar 

  • Van Der Ouderaa FJ, De Jong WW, Hilderink A, Bloemendal H (1974) The amino-acids sequence of the alphaB2 chain of bovine alpha-crystallin. Eur J Biochem 49:157–168

    Google Scholar 

  • Van Montfort RL, Basha E, Friedrich KL, Slingsby C, Vierling E (2001) Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Biol 8:1025–1030

    PubMed  Google Scholar 

  • Vos MJ, Kanon B, Kampinga HH (2009) HSPB7 is a SC35 speckle resident small heat shock protein. Biochim Biophys Acta 1793:1343–1353

    CAS  PubMed  Google Scholar 

  • Voss OH, Batra S, Kolattukudy SJ, Gonzalez-Mejia ME, Smith JB, Doseff AI (2007) Binding of caspase-3 prodomain to heat shock protein 27 regulates monocyte apoptosis by inhibiting caspase-3 proteolytic activation. J Biol Chem 282:25088–25099

    CAS  PubMed  Google Scholar 

  • Vucetic S, Brown CJ, Dunker AK, Obradovic Z (2003) Flavors of protein disorder. Proteins 52:573–584

    CAS  PubMed  Google Scholar 

  • Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview version 2–a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191

    CAS  PubMed Central  PubMed  Google Scholar 

  • Waters ER (2013) The evolution, function, structure, and expression of the plant sHSPs. J Exp Bot 64:391–403

    CAS  PubMed  Google Scholar 

  • Waters ER, Vierling E (1999a) Chloroplast small heat shock proteins: evidence for atypical evolution of an organelle-localized protein. Proc Natl Acad Sci U S A 96:14394–14399

    CAS  PubMed Central  PubMed  Google Scholar 

  • Waters ER, Vierling E (1999b) The diversification of plant cytosolic small heat shock proteins preceded the divergence of mosses. Mol Biol Evol 16:127–139

    CAS  PubMed  Google Scholar 

  • Waters ER, Aevermann BD, Sanders-Reed Z (2008) Comparative analysis of the small heat shock proteins in three angiosperm genomes identifies new subfamilies and reveals diverse evolutionary patterns. Cell Stress Chaperones 13:127–142

    CAS  PubMed Central  PubMed  Google Scholar 

  • Waudby CA, Knowles TPJ, Devlin GL, Skepper JN, Ecroyd H, Carver JA, Welland ME, Christodoulou J, Dobson CM, Meehan S (2010) The interaction of alphaB-crystallin with mature alpha-synuclein amyloid fibrils inhibits their elongation. Biophys J 98:843–851

    CAS  PubMed Central  PubMed  Google Scholar 

  • Weeks SD, Baranova EV, Heirbaut M, Beelen S, Shkumatov AV, Gusev NB, Strelkov SV (2014) Molecular structure and dynamics of the dimeric human small heat shock protein HSPB6. J Struct Biol 185:342–354

    CAS  PubMed  Google Scholar 

  • White HE, Orlova EV, Chen S, Wang L, Ignatiou A, Gowen B, Stromer T, Franzmann TM, Haslbeck M, Buchner J, Saibil HR (2006) Multiple distinct assemblies reveal conformational flexibility in the small heat shock protein Hsp26. Structure 14:1197–1204

    CAS  PubMed  Google Scholar 

  • Wieske M, Benndorf R, Behlke J, Dölling R, Grelle G, Bielka H, Lutsch G (2001) Defined sequence segments of the small heat shock proteins HSP25 and alphaB-crystallin inhibit actin polymerization. Eur J Biochem 268:2083–2090

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

M.H. is funded by the Department of Pharmaceutical and Pharmacological Sciences, KU Leuven. S.D.W. acknowledges the support of Marie Curie Reintegration Grant. This research was further supported by the grant OT13/097 from the KU Leuven, and the grant G.0936.15 from the Research Foundation Flanders/FWO, both awarded to S.V.S. The authors would like to thank Drs. Alexander Shkumatov and Nikolai Sluchanko for their careful review of the chapter and useful suggestions.

Author information

Authors and Affiliations

  1. Laboratory for Biocrystallography, Department of Pharmaceutical and Pharmacological Sciences, KU Leuven, Leuven, Belgium

    Michelle Heirbaut, Sergei V. Strelkov & Stephen D. Weeks

Authors
  1. Michelle Heirbaut
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sergei V. Strelkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephen D. Weeks
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stephen D. Weeks .

Editor information

Editors and Affiliations

  1. Department of Molecular Biology, Medical Biochemistry & Pathology Medical School Lab Cell & Developmental Genetics IBIS, Université Laval, Quebec, Québec, Canada

    Robert M. Tanguay

  2. Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut, USA

    Lawrence E. Hightower

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Heirbaut, M., Strelkov, S.V., Weeks, S.D. (2015). Everything but the ACD, Functional Conservation of the Non-conserved Terminal Regions in sHSPs. In: Tanguay, R., Hightower, L. (eds) The Big Book on Small Heat Shock Proteins. Heat Shock Proteins, vol 8. Springer, Cham. https://doi.org/10.1007/978-3-319-16077-1_8

Download citation

Publish with us

Policies and ethics

Search

Navigation