Abstract
The review discusses the role of small heat shock proteins (sHsps) in human neurodegenerative disorders, such as Charcot-Marie-Tooth disease (CMT), Parkinson’s and Alzheimer’s diseases, and different forms of tauopathies. The effects of CMT-associated mutations in two small heat shock proteins (HspB1 and HspB8) on the protein stability, oligomeric structure, and chaperone-like activity are described. Mutations in HspB1 shift the equilibrium between different protein oligomeric forms, leading to the alterations in its chaperone-like activity and interaction with protein partners, which can induce damage of the cytoskeleton and neuronal death. Mutations in HspB8 affect its interaction with the adapter protein Bag3, as well as the process of autophagy, also resulting in neuronal death. The impact of sHsps on different forms of amyloidosis is discussed. Experimental studies have shown that sHsps interact with monomers or small oligomers of amyloidogenic proteins, stabilize their structure, prevent their aggregation, and/or promote their specific proteolytic degradation. This effect might be due to the interaction between the β-strands of sHsps and β-strands of target proteins, which prevents aggregation of the latter. In cooperation with the other heat shock proteins, sHsps can promote disassembly of oligomers formed by amyloidogenic proteins. Despite significant achievements, further investigations are required for understanding the role of sHsps in protection against various neurodegenerative diseases.
Similar content being viewed by others
Abbreviations
- ACD:
-
α-crystallin domain
- CMT:
-
Charcot-Marie-Tooth disease
- CTD:
-
C-terminal domain
- NTD:
-
N-terminal domain
- (s)Hsp:
-
(small) heat shock proteins
References
Vos, M. J., Hageman, J., Carra, S., and Kampinga, H. H. (2008) Structural and functional diversities between members of the human HSPB, HSPH, HSPA, and DNAJ chaperone families, Biochemistry, 47, 7001–7011; doi: https://doi.org/10.1021/bi800639z.
Vilasi, S., Bulone, D., Caruso Bavisotto, C., Campanella, C., Marino Gammazza, A., San Biagio, P. L., Cappello, F., Conway de Macario, E., and Macario, A. J. L. (2017) Chaperonin of group I: oligomeric spectrum and biochemical and biological implications, Front. Mol. Biosci., 4, 99; doi: https://doi.org/10.3389/fmolb.2017.00099.
Fontaine, J. M., Rest, J. S., Welsh, M. J., and Benndorf, R. (2003) The sperm outer dense fiber protein is the 10th member of the superfamily of mammalian small stress proteins, Cell Stress Chaperones, 8, 62–69.
Kappe, G., Franck, E., Verschuure, P., Boelens, W. C., Leunissen, J. A., and de Jong, W. W. (2003) The human genome encodes 10 alpha-crystallin-related small heat shock proteins: HspB1–10, Cell Stress Chaperones, 8, 53–61.
Mymrikov, E. V., Seit-Nebi, A. S., and Gusev, N. B. (2011) Large potentials of small heat shock proteins, Physiol. Rev., 91, 1123–1159; doi: 91/4/1123.
Bakthisaran, R., Tangirala, R., and Rao, C. M. (2015) Small heat shock proteins: role in cellular functions and pathology, Biochim. Biophys. Acta, 1854, 291–319; doi: https://doi.org/10.1016/j.bbapap.2014.12.019.
Bagneris, C., Bateman, O. A., Naylor, C. E., Cronin, N., Boelens, W. C., Keep, N. H., and Slingsby, C. (2009) Crystal structures of alpha-crystallin domain dimers of alphaB-crystallin and Hsp20, J. Mol. Biol., 392, 1242–1252; doi: S0022-2836(09)00936-X.
Baranova, E. V., Weeks, S. D., Beelen, S., Bukach, O. V., Gusev, N. B., and Strelkov, S. V. (2011) Three-dimensional structure of alpha-crystallin domain dimers of human small heat shock proteins HSPB1 and HSPB6, J. Mol. Biol., 411, 110–122; doi: S0022-2836(11)00574-2.
Mymrikov, E. V., Seit-Nebi, A. S., and Gusev, N. B. (2012) Heterooligomeric complexes of human small heat shock proteins, Cell Stress Chaperones, 17, 157–169; doi: https://doi.org/10.1007/s12192-011-0296-0.
Delbecq, S. P., Rosenbaum, J. C., and Klevit, R. E. (2015) A mechanism of subunit recruitment in human small heat shock protein oligomers, Biochemistry, 54, 4276–4284; doi: https://doi.org/10.1021/acs.biochem.5b00490.
Heirbaut, M., Lermyte, F., Martin, E. M., Beelen, S., Sobott, F., Strelkov, S. V., and Weeks, S. D. (2017) Specific sequences in the N-terminal domain of human small heat-shock protein HSPB6 dictate preferential hetero-oligomerization with the orthologue HSPB1, J. Biol. Chem., 292, 9944–9957; doi: https://doi.org/10.1074/jbc.M116.773515.
Carver, J. A., Ecroyd, H., Truscott, R. J. W., Thorn, D. C., and Holt, C. (2018) Proteostasis and the regulation of intra- and extracellular protein aggregation by ATP-independent molecular chaperones: lens alpha-crystallins and milk caseins, Acc. Chem. Res., 51, 745–752; doi: https://doi.org/10.1021/acs.accounts.7b00250.
Garvey, M., Ecroyd, H., Ray, N. J., Gerrard, J. A., and Carver, J. A. (2017) Functional amyloid protection in the eye lens: retention of alpha-crystallin molecular chaperone activity after modification into amyloid fibrils, Biomolecules, 7, E67; doi: https://doi.org/10.3390/biom7030067.
Tanaka, N., Tanaka, R., Tokuhara, M., Kunugi, S., Lee, Y. F., and Hamada, D. (2008) Amyloid fibril formation and chaperone-like activity of peptides from alphaA-crystallin, Biochemistry, 47, 2961–2967; doi: https://doi.org/10.1021/bi701823g.
Delbecq, S. P., Jehle, S., and Klevit, R. (2012) Binding determinants of the small heat shock protein, alphaB-crystallin: recognition of the ‘IxI’ motif, EMBO J., 31, 4587–4594; doi: emboj2012318.
Hochberg, G. K., and Benesch, J. L. (2014) Dynamical structure of alphaB-crystallin, Prog. Biophys. Mol. Biol., 115, 11–20; doi: https://doi.org/10.1016/j.pbiomolbio.2014.03.003.
Jovcevski, B., Kelly, M. A., Rote, A. P., Berg, T., Gastall, H. Y., Benesch, J. L., Aquilina, J. A., and Ecroyd, H. (2015) Phosphomimics destabilize Hsp27 oligomeric assemblies and enhance chaperone activity, Chem. Biol., 22, 186–195; doi: https://doi.org/10.1016/j.chembiol.2015.01.001.
Muranova, L. K., Weeks, S. D., Strelkov, S. V., and Gusev, N. B. (2015) Characterization of mutants of human small heat shock protein HspB1 carrying replacements in the N-terminal domain and associated with hereditary motor neuron diseases, PLoS One, 10, e0126248; doi: https://doi.org/10.1371/journal.pone.0126248.
Sluchanko, N. N., Beelen, S., Kulikova, A. A., Weeks, S. D., Antson, A. A., Gusev, N. B., and Strelkov, S. V. (2017) Structural basis for the interaction of a human small heat shock protein with the 14-3-3 universal signaling regulator, Structure, 25, 305–316; doi: https://doi.org/10.1016/j.str.2016.12.005.
Zwirowski, S., Klosowska, A., Obuchowski, I., Nillegoda, N. B., Pirog, A., Zietkiewicz, S., Bukau, B., Mogk, A., and Liberek, K. (2017) Hsp70 displaces small heat shock proteins from aggregates to initiate protein refolding, EMBO J., 36, 783–796; doi: https://doi.org/10.15252/embj.201593378.
Ahner, A., Gong, X., Schmidt, B. Z., Peters, K. W., Rabeh, W. M., Thibodeau, P. H., Lukacs, G. L., and Frizzell, R. A. (2013) Small heat shock proteins target mutant cystic fibrosis transmembrane conductance regulator for degradation via a small ubiquitin-like modifier-dependent pathway, Mol. Biol. Cell, 24, 74–84; doi: https://doi.org/10.1091/mbc.E12-09-0678.
Rusmini, P., Cristofani, R., Galbiati, M., Cicardi, M. E., Meroni, M., Ferrari, V., Vezzoli, G., Tedesco, B., Messi, E., Piccolella, M., Carra, S., Crippa, V., and Poletti, A. (2017) The role of the heat shock protein B8 (HSPB8) in motoneuron diseases, Front. Mol. Neurosci., 10, 176; doi: https://doi.org/10.3389/fnmol.2017.00176.
Carra, S., Crippa, V., Rusmini, P., Boncoraglio, A., Minoia, M., Giorgetti, E., Kampinga, H. H., and Poletti, A. (2012) Alteration of protein folding and degradation in motor neuron diseases: implications and protective functions of small heat shock proteins, Prog. Neurobiol., 97, 83–100; doi: S0301-0082(11)00176-6.
Torrente, M. P., and Shorter, J. (2013) The metazoan protein disaggregase and amyloid depolymerase system: Hsp110, Hsp70, Hsp40, and small heat shock proteins, Prion, 7, 457–463.
Weis, J., Claeys, K. G., Roos, A., Azzedine, H., Katona, I., Schroder, J. M., and Senderek, J. (2017) Towards a functional pathology of hereditary neuropathies, Acta Neuropathol., 133, 493–515; doi: https://doi.org/10.1007/s00401-016-1645-y.
Saporta, A. S., Sottile, S. L., Miller, L. J., Feely, S. M., Siskind, C. E., and Shy, M. E. (2011) Charcot-Marie-Tooth disease subtypes and genetic testing strategies, Ann. Neurol., 69, 22–33; doi: https://doi.org/10.1002/ana.22166.
Yoshimura, A., Yuan, J. H., Hashiguchi, A., Ando, M., Higuchi, Y., Nakamura, T., Okamoto, Y., Nakagawa, M., and Takashima, H. (2018) Genetic profile and onset features of 1005 patients with Charcot-Marie-Tooth disease in Japan, J. Neurol. Neurosurg. Psychiatry, 90, 195–202; doi: https://doi.org/10.1136/jnnp-2018-318839.
Echaniz-Laguna, A., Geuens, T., Petiot, P., Pereon, Y., Adriaenssens, E., Haidar, M., Capponi, S., Maisonobe, T., Fournier, E., Dubourg, O., Degos, B., Salachas, F., Lenglet, T., Eymard, B., Delmont, E., Pouget, J., Juntas Morales, R., Goizet, C., Latour, P., Timmerman, V., and Stojkovic, T. (2017) Axonal neuropathies due to mutations in small heat shock proteins: clinical, genetic, and functional insights into novel mutations, Hum. Mutat., 38, 556–568; doi: https://doi.org/10.1002/humu.23189.
Adriaenssens, E., Geuens, T., Baets, J., Echaniz-Laguna, A., and Timmerman, V. (2017) Novel insights in the disease biology of mutant small heat shock proteins in neuromuscular diseases, Brain, 140, 2541–2549; doi: https://doi.org/10.1093/brain/awx187.
Jovcevski, B., Kelly, M. A., Aquilina, J. A., Benesch, J. L. P., and Ecroyd, H. (2017) Evaluating the effect of phosphorylation on the structure and dynamics of Hsp27 dimers by means of ion mobility mass spectrometry, Anal. Chem., 89, 13275–13282; doi: https://doi.org/10.1021/acs.analchem.7b03328.
Clark, A. R., Lubsen, N. H., and Slingsby, C. (2012) sHSP in the eye lens: crystallin mutations, cataract and proteostasis, Int. J. Biochem. Cell Biol., 44, 1687–1697; doi: https://doi.org/10.1016/j.biocel.2012.02.015.
Nefedova, V. V., Sudnitsyna, M. V., Strelkov, S. V., and Gusev, N. B. (2013) Structure and properties of G84R and L99M mutants of human small heat shock protein HspB1 correlating with motor neuropathy, Arch. Biochem. Biophys., 538, 16–24; doi: https://doi.org/10.1016/j.abb.2013.07.028.
Nefedova, V. V., Datskevich, P. N., Sudnitsyna, M. V., Strelkov, S. V., and Gusev, N. B. (2013) Physico-chemical properties of R140G and K141Q mutants of human small heat shock protein HspB1 associated with hereditary peripheral neuropathies, Biochimie, 95, 1582–1592; doi: https://doi.org/10.1016/j.biochi.2013.04.014.
Weeks, S. D., Muranova, L. K., Heirbaut, M., Beelen, S., Strelkov, S. V., and Gusev, N. B. (2018) Characterization of human small heat shock protein HSPB1 alpha-crystallin domain localized mutants associated with hereditary motor neuron diseases, Sci. Rep., 8, 688; doi: https://doi.org/10.1038/s41598-017-18874-x.
Chalova, A. S., Sudnitsyna, M. V., Strelkov, S. V., and Gusev, N. B. (2014) Characterization of human small heat shock protein HspB1 that carries C-terminal domain mutations associated with hereditary motor neuron diseases, Biochim. Biophys. Acta, 1844, 2116–2126; doi: https://doi.org/10.1016/j.bbapap.2014.09.005.
Carver, J. A., Grosas, A. B., Ecroyd, H., and Quinlan, R. A. (2017) The functional roles of the unstructured N- and C-terminal regions in alphaB-crystallin and other mammalian small heat-shock proteins, Cell Stress Chaperones, 22, 627–638; doi: https://doi.org/10.1007/s12192-017-0789-6.
Dahiya, V., and Buchner, J. (2019) Functional principles and regulation of molecular chaperones, Adv. Protein. Chem. Struct. Biol., 114, 1–60; doi: https://doi.org/10.1016/bs.apcsb.2018.10.001.
Bucci, C., Bakke, O., and Progida, C. (2012) Charcot-Marie-Tooth disease and intracellular traffic, Prog. Neurobiol., 99, 191–225; doi: https://doi.org/10.1016/j.pneurobio.2012.03.003.
Pareyson, D., Saveri, P., Sagnelli, A., and Piscosquito, G. (2015) Mitochondrial dynamics and inherited peripheral nerve diseases, Neurosci. Lett., 596, 66–77; doi: https://doi.org/10.1016/j.neulet.2015.04.001.
Almeida-Souza, L., Asselbergh, B., d’Ydewalle, C., Moonens, K., Goethals, S., de Winter, V., Azmi, A., Irobi, J., Timmermans, J. P., Gevaert, K., Remaut, H., Van Den Bosch, L., Timmerman, V., and Janssens, S. (2011) Small heat-shock protein HSPB1 mutants stabilize microtubules in Charcot-Marie-Tooth neuropathy, J. Neurosci., 31, 15320–15328; doi: 31/43/15320.
d’Ydewalle, C., Krishnan, J., Chiheb, D. M., Van Damme, P., Irobi, J., Kozikowski, A. P., Vanden Berghe, P., Timmerman, V., Robberecht, W., and Van Den Bosch, L. (2011) HDAC6 inhibitors reverse axonal loss in a mouse model of mutant HSPB1-induced Charcot-Marie-Tooth disease, Nat. Med., 17, 968–974; doi: https://doi.org/10.1038/nm.2396.
Benedetti, S., Previtali, S. C., Coviello, S., Scarlato, M., Cerri, F., Di Pierri, E., Piantoni, L., Spiga, I., Fazio, R., Riva, N., Natali Sora, M. G., Dacci, P., Malaguti, M. C., Munerati, E., Grimaldi, L. M., Marrosu, M. G., De Pellegrin, M., Ferrari, M., Comi, G., Quattrini, A., and Bolino, A. (2010) Analyzing histopathological features of rare Charcot-Marie-Tooth neuropathies to unravel their pathogenesis, Arch. Neurol., 67, 1498–1505; doi: https://doi.org/10.1001/archneurol.2010.303.
Almeida-Souza, L., Timmerman, V., and Janssens, S. (2011) Microtubule dynamics in the peripheral nervous system: a matter of balance, Bioarchitecture, 1, 267–270; doi: https://doi.org/10.4161/bioa.1.6.19198.
Benoy, V., Vanden Berghe, P., Jarpe, M., Van Damme, P., Robberecht, W., and Van Den Bosch, L. (2017) Development of improved HDAC6 inhibitors as pharmacological therapy for axonal Charcot-Marie-Tooth disease, Neurotherapeutics, 14, 417–428; doi: https://doi.org/10.1007/s13311-016-0501-z.
Zhai, J., Lin, H., Julien, J. P., and Schlaepfer, W. W. (2007) Disruption of neurofilament network with aggregation of light neurofilament protein: a common pathway leading to motor neuron degeneration due to Charcot-Marie-Tooth disease-linked mutations in NFL and HSPB1, Hum. Mol. Genet., 16, 3103–3116; doi: https://doi.org/10.1093/hmg/ddm272.
Ackerley, S., James, P. A., Kalli, A., French, S., Davies, K. E., and 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; doi: https://doi.org/10.1093/hmg/ddi452.
Holmgren, A., Bouhy, D., De Winter, V., Asselbergh, B., Timmermans, J. P., Irobi, J., and Timmerman, V. (2013) Charcot-Marie-Tooth causing HSPB1 mutations increase Cdk5-mediated phosphorylation of neurofilaments, Acta Neuropathol., 126, 93–108; doi: https://doi.org/10.1007/s00401-013-1133-6.
Srivastava, A. K., Renusch, S. R., Naiman, N. E., Gu, S., Sneh, A., Arnold, W. D., Sahenk, Z., and Kolb, S. J. (2012) Mutant HSPB1 overexpression in neurons is sufficient to cause age-related motor neuronopathy in mice, Neurobiol. Dis., 47, 163–173; doi: S0969-9961(12)00124-6.
Lee, J., Jung, S. C., Joo, J., Choi, Y. R., Moon, H. W., Kwak, G., Yeo, H. K., Lee, J. S., Ahn, H. J., Jung, N., Hwang, S., Rheey, J., Woo, S. Y., Kim, J. Y., Hong, Y. B., and Choi, B. O. (2015) Overexpression of mutant HSP27 causes axonal neuropathy in mice, J. Biomed. Sci., 22, 43; doi: https://doi.org/10.1186/s12929-015-0154-y.
Kim, M. V., Seit-Nebi, A. S., Marston, S. B., and Gusev, N. B. (2004) Some properties of human small heat shock protein Hsp22 (H11 or HspB8), Biochem. Biophys. Res. Commun., 315, 796–801; doi: https://doi.org/10.1016/j.bbrc.2004.01.130.
Chowdary, T. K., Raman, B., Ramakrishna, T., and Rao, C. M. (2004) Mammalian Hsp22 is a heat-inducible small heat-shock protein with chaperone-like activity, Biochem. J., 381, 379–387; doi: https://doi.org/10.1042/BJ20031958.
Kim, M. V., Kasakov, A. S., Seit-Nebi, A. S., Marston, S. B., and Gusev, N. B. (2006) Structure and properties of K141E mutant of small heat shock protein HSP22 (HspB8, H11) that is expressed in human neuromuscular disorders, Arch. Biochem. Biophys., 454, 32–41; doi: S0003-9861(06)00267-0.
Shemetov, A. A., and Gusev, N. B. (2011) Biochemical characterization of small heat shock protein HspB8 (Hsp22)-Bag3 interaction, Arch. Biochem. Biophys., 513, 1–9; doi: S0003-9861(11)00249-9.
Carra, S., Boncoraglio, A., Kanon, B., Brunsting, J. F., Minoia, M., Rana, A., Vos, M. J., Seidel, K., Sibon, O. C., and Kampinga, H. H. (2010) Identification of the Drosophila ortholog of HSPB8: implication of HSPB8 loss of function in protein folding diseases, J. Biol. Chem., 285, 37811–37822; doi: https://doi.org/10.1074/jbc.M110.127498.
Haidar, M., Asselbergh, B., Adriaenssens, E., De Winter, V., Timmermans, J. P., Auer-Grumbach, M., Juneja, M., and Timmerman, V. (2019) Neuropathy-causing mutations in HSPB1 impair autophagy by disturbing the formation of SQSTM1/p62 bodies, Autophagy, 15, 1051–1068; doi: https://doi.org/10.1080/15548627.2019.1569930.
Sharma, S. K., and Priya, S. (2017) Expanding role of molecular chaperones in regulating alpha-synuclein mis-folding; implications in Parkinson’s disease, Cell. Mol. Life Sci., 74, 617–629; doi: https://doi.org/10.1007/s00018-016-2340-9.
Cox, D., Carver, J. A., and Ecroyd, H. (2014) Preventing alpha-synuclein aggregation: the role of the small heat-shock molecular chaperone proteins, Biochim. Biophys. Acta, 1842, 1830–1843; doi: https://doi.org/10.1016/j.bbadis.2014.06.024.
Leak, R. K. (2014) Heat shock proteins in neurodegenerative disorders and aging, J. Cell Commun. Signal., 8, 293–310; doi: https://doi.org/10.1007/s12079-014-0243-9.
Cox, D., Selig, E., Griffin, M. D., Carver, J. A., and Ecroyd, H. (2016) Small heat-shock proteins prevent alpha-synuclein aggregation via transient interactions and their efficacy is affected by the rate of aggregation, J. Biol. Chem., 291, 22618–22629; doi: https://doi.org/10.1074/jbc.M116.739250.
Cox, D., and Ecroyd, H. (2017) The small heat shock proteins alphaB-crystallin (HSPB5) and Hsp27 (HSPB1) inhibit the intracellular aggregation of alpha-synuclein, Cell Stress Chaperones, 22, 589–600; doi: https://doi.org/10.1007/s12192-017-0785-x.
Cox, D., Whiten, D. R., Brown, J. W. P., Horrocks, M. H., San Gil, R., Dobson, C. M., Klenerman, D., van Oijen, A. M., and Ecroyd, H. (2018) The small heat shock protein Hsp27 binds alpha-synuclein fibrils, preventing elongation and cytotoxicity, J. Biol. Chem., 293, 4486–4497; doi: https://doi.org/10.1074/jbc.M117.813865.
Mainz, A., Peschek, J., Stavropoulou, M., Back, K. C., Bardiaux, B., Asami, S., Prade, E., Peters, C., Weinkauf, S., Buchner, J., and Reif, B. (2015) The chaperone alphaB-crystallin uses different interfaces to capture an amorphous and an amyloid client, Nat. Struct. Mol. Biol., 22, 898–905; doi: https://doi.org/10.1038/nsmb.3108.
Alperstein, A. M., Ostrander, J. S., Zhang, T. O., and Zanni, M. T. (2019) Amyloid found in human cataracts with two-dimensional infrared spectroscopy, Proc. Natl. Acad. Sci. USA, 116, 6602–6607; doi: https://doi.org/10.1073/pnas.1821534116.
Lu, S. Z., Guo, Y. S., Liang, P. Z., Zhang, S. Z., Yin, S., Yin, Y. Q., Wang, X. M., Ding, F., Gu, X. S., and Zhou, J. W. (2019) Suppression of astrocytic autophagy by alphaB-crystallin contributes to alpha-synuclein inclusion formation, Transl. Neurodegener., 8, 3; doi: https://doi.org/10.1186/s40035-018-0143-7.
Boros, S., Kamps, B., Wunderink, L., de Bruijn, W., de Jong, W. W., and Boelens, W. C. (2004) Transglutaminase catalyzes differential crosslinking of small heat shock proteins and amyloid-beta, FEBS Lett., 576, 57–62; doi: S0014579304010816.
Wilhelmus, M. M., Otte-Holler, I., Wesseling, P., de Waal, R. M., Boelens, W. C., and Verbeek, M. M. (2006) Specific association of small heat shock proteins with the pathological hallmarks of Alzheimer’s disease brains, Neuropathol. Appl. Neurobiol., 32, 119–130; doi: https://doi.org/10.1111/j.1365-2990.2006.00689.x.
Zerovnik, E. (2017) Co-chaperoning by amyloid-forming proteins: cystatins vs. crystallins, Eur. Biophys. J., 46, 789–793; doi: https://doi.org/10.1007/s00249-017-1214-x.
Nafar, F., Williams, J. B., and Mearow, K. M. (2016) Astrocytes release HspB1 in response to amyloid-beta exposure in vitro, J. Alzheimers Dis., 49, 251–263; doi: https://doi.org/10.3233/JAD-150317.
Wilhelmus, M. M., Boelens, W. C., Otte-Holler, I., Kamps, B., de Waal, R. M., and Verbeek, M. M. (2006) Small heat shock proteins inhibit amyloid-beta protein aggregation and cerebrovascular amyloid-beta protein toxicity, Brain Res., 1089, 67–78; doi: S0006-8993(06)00762-1.
Cameron, R. T., Quinn, S. D., Cairns, L. S., MacLeod, R., Samuel, I. D., Smith, B. O., Carlos Penedo, J., and Baillie, G. S. (2014) The phosphorylation of Hsp20 enhances its association with amyloid-beta to increase protection against neuronal cell death, Mol. Cell. Neurosci., 61, 46–55; doi: https://doi.org/10.1016/j.mcn.2014.05.002.
Sotiropoulos, I., Galas, M. C., Silva, J. M., Skoulakis, E., Wegmann, S., Maina, M. B., Blum, D., Sayas, C. L., Mandelkow, E. M., Mandelkow, E., Spillantini, M. G., Sousa, N., Avila, J., Medina, M., Mudher, A., and Buee, L. (2017) Atypical, non-standard functions of the microtubule associated tau protein, Acta Neuropathol. Commun., 5, 91; doi: https://doi.org/10.1186/s40478-017-0489-6.
Sierra-Fonseca, J. A., and Gosselink, K. L. (2018) Tauopathy and neurodegeneration: a role for stress, Neurobiol. Stress, 9, 105–112; doi: https://doi.org/10.1016/j.ynstr.2018.08.009.
Zabik, N. L., Imhof, M. M., and Martic-Milne, S. (2017) Structural evaluations of tau protein conformation: methodologies and approaches, Biochem. Cell Biol., 95, 338–349; doi: https://doi.org/10.1139/bcb-2016-0227.
Shimura, H., Miura-Shimura, Y., and Kosik, K. S. (2004) Binding of tau to heat shock protein 27 leads to decreased concentration of hyperphosphorylated tau and enhanced cell survival, J. Biol. Chem., 279, 17957–17962; doi: https://doi.org/10.1074/jbc.M400351200.
Kumar, P., Jha, N. K., Jha, S. K., Ramani, K., and Ambasta, R. K. (2015) Tau phosphorylation, molecular chaperones, and ubiquitin E3 ligase: clinical relevance in Alzheimer’s disease, J. Alzheimers Dis., 43, 341–361; doi: https://doi.org/10.3233/JAD-140933.
Abisambra, J. F., Blair, L. J., Hill, S. E., Jones, J. R., Kraft, C., Rogers, J., Koren, J., 3rd, Jinwal, U. K., Lawson, L., Johnson, A. G., Wilcock, D., O’Leary, J. C., Jansen-West, K., Muschol, M., Golde, T. E., Weeber, E. J., Banko, J., and Dickey, C. A. (2010) Phosphorylation dynamics regulate Hsp27-mediated rescue of neuronal plasticity deficits in tau transgenic mice, J. Neurosci., 30, 15374–15382; doi: https://doi.org/10.1523/JNEUROSCI.3155-10.2010.
Baughman, H. E. R., Clouser, A. F., Klevit, R. E., and Nath, A. (2018) HspB1 and Hsc70 chaperones engage distinct tau species and have different inhibitory effects on amyloid formation, J. Biol. Chem., 293, 2687–2700; doi: https://doi.org/10.1074/jbc.M117.803411.
Janowska, M. K., Baughman, H. E. R., Woods, C. N., and Klevit, R. E. (2019) Mechanisms of small heat shock proteins, Cold Spring Harb. Perspect. Biol., a034025; doi: https://doi.org/10.1101/cshperspect.a034025.
Hashiguchi, M., Sobue, K., and Paudel, H. K. (2000) 14-3-3zeta is an effector of tau protein phosphorylation, J. Biol. Chem., 275, 25247–25254; doi: https://doi.org/10.1074/jbc.M003738200.
Sadik, G., Tanaka, T., Kato, K., Yamamori, H., Nessa, B. N., Morihara, T., and Takeda, M. (2009) Phosphorylation of tau at Ser214 mediates its interaction with 14-3-3 protein: implications for the mechanism of tau aggregation, J. Neurochem., 108, 33–43; doi: https://doi.org/10.1111/j.1471-4159.2008.05716.x.
Sluchanko, N. N., Seit-Nebi, A. S., and Gusev, N. B. (2009) Effect of phosphorylation on interaction of human tau protein with 14-3-3zeta, Biochem. Biophys. Res. Commun., 379, 990–994; doi: S0006-291X(09)00007-2.
Sluchanko, N. N., Seit-Nebi, A. S., and Gusev, N. B. (2009) Phosphorylation of more than one site is required for tight interaction of human tau protein with 14-3-3zeta, FEBS Lett., 583, 2739–2742; doi: S0014-5793(09)00593-6.
Sluchanko, N. N., and Gusev, N. B. (2011) Probable participation of 14-3-3 in tau protein oligomerization and aggregation, J. Alzheimers Dis., 27, 467–476; doi: https://doi.org/10.3233/JAD-2011-110692.
Sluchanko, N. N., Sudnitsyna, M. V., Chernik, I. S., Seit-Nebi, A. S., and Gusev, N. B. (2011) Phosphomimicking mutations of human 14-3-3zeta affect its interaction with tau protein and small heat shock protein HspB6, Arch. Biochem. Biophys., 506, 24–34; doi: S0003-9861(10)00463-7.
Wang, K., Zhang, J., Xu, Y., Ren, K., Xie, W. L., Yan, Y. E., Zhang, B. Y., Shi, Q., Liu, Y., and Dong, X. P. (2013) Abnormally upregulated alphaB-crystallin was highly coincidental with the astrogliosis in the brains of scrapie-infected hamsters and human patients with prion diseases, J. Mol. Neurosci., 51, 734–748; doi: https://doi.org/10.1007/s12031-013-0057-x.
Duennwald, M. L., Echeverria, A., and Shorter, J. (2012) Small heat shock proteins potentiate amyloid dissolution by protein disaggregases from yeast and humans, PLoS Biol., 10, e1001346; doi: https://doi.org/10.1371/journal.pbio.1001346.
Rothbard, J. B., Rothbard, J. J., Soares, L., Fathman, C. G., and Steinman, L. (2018) Identification of a common immune regulatory pathway induced by small heat shock proteins, amyloid fibrils, and nicotine, Proc. Natl. Acad. Sci. USA, 115, 7081–7086; doi: https://doi.org/10.1073/pnas.1804599115.
Rothbard, J. B., Kurnellas, M. P., Ousman, S. S., Brownell, S., Rothbard, J. J., and Steinman, L. (2018) Small heat shock proteins, amyloid fibrils, and nicotine stimulate a common immune suppressive pathway with implications for future therapies, Cold Spring Harb. Perspect. Med., 9, a034223; doi: https://doi.org/10.1101/cshperspect.a034223.
Liu, Z., Wang, C., Li, Y., Zhao, C., Li, T., Li, D., Zhang, S., and Liu, C. (2018) Mechanistic insights into the switch of alphaB-crystallin chaperone activity and self-multimerization, J. Biol. Chem., 293, 14880–14890; doi: https://doi.org/10.1074/jbc.RA118.004034.
Acknowledgements
All authors of this paper are alumni of the Department of Biochemistry, School of Biology, Moscow State University. Our investigation would have been impossible if not based on the knowledge and skills obtained in the course of our study at our department, on traditions laid by the founder of our department Academician Sergei E. Severin. In the year of the 80th anniversary of the Department of Biochemistry, we would like to wish our department great achievements and to voice the hope that in the future, despite all difficulties, the Department of Biochemistry will be able to educate interested and skillful biochemists.
Funding
This study was supported by the Russian Foundation for Basic Research (project 19-04-00038).
Author information
Authors and Affiliations
Corresponding author
Additional information
Conflict of interest
The authors declare no conflict of interest in financial or any other area.
Compliance with ethical norms
This article does not contain studies with human participants or animals performed by any of the authors.
Published in Russian in Biokhimiya, 2019, Vol. 84, No. 11, pp. 1564–1577.
Rights and permissions
About this article
Cite this article
Muranova, L.K., Ryzhavskaya, A.S., Sudnitsyna, M.V. et al. Small Heat Shock Proteins and Human Neurodegenerative Diseases. Biochemistry Moscow 84, 1256–1267 (2019). https://doi.org/10.1134/S000629791911004X
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S000629791911004X