The growing world of small heat shock proteins: from structure to functions

Cell Stress and Chaperones - Tập 22 Số 4 - Trang 601-611 - 2017
Serena Carra1, Simon Alberti2, Patrick A. Arrigo3, Justin L. P. Benesch4, Ivor J. Benjamin5, Wilbert C. Boelens6, Britta Bartelt‐Kirbach7, Bianca J.J.M. Brundel8, Johannes Büchner9, Bernd Bukau10, Ramesh Thakur11, Heath Ecroyd12, Cecilia Emanuelsson13, Stéphanie Finet14, Nikola Golenhofen7, Pierre Goloubinoff15, Nikolai B. Gusev16, Martin Haslbeck9, Lawrence E. Hightower17, Harm H. Kampinga18, Rachel E. Klevit19, Krzysztof Liberek20, Hassane S. Mchaourab21, Kathryn A. McMenimen22, Angelo Poletti23, Roy A. Quinlan24, Sergei V. Strelkov25, Melinda Tóth26, Elizabeth Vierling27, Robert M. Tanguay28
1Department of Biomedical, Metabolic and Neural Sciences, and Centre for Neuroscience and Neurotechnology, University of Modena and Reggio Emilia, via G. Campi 287, 41125, Modena, Italy
2Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
3Université de Lyon, 69622 Lyon, France
4Department of Chemistry, University of Oxford, Oxford OX1 3TA, UK
5Department of Biochemistry, University of Utah, Salt Lake City, UT, 84112-5650, USA
6Biomolecular Chemistry, 284, Radboud University, PO Box 9101, 6500 HB, Nijmegen, The Netherlands
7Institute of Anatomy and Cell Biology, University of Ulm, 89081, Ulm, Germany
8Department of Clinical Pharmacy and Pharmacology, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands
9Technische Universitat Munchen, Munich, Germany
10Center for Molecular Biology of the University of Heidelberg (ZMBH), DKFZ-ZMBH Alliance, Im Neuenheimer Feld 282, 69120 Heidelberg, Germany
11The Research School of Chemistry, The Australian National University, Acton, ACT, 2601, Australia
12Illawara Health and Medical Research Institute, School of Biological Sciences, University of Wollongong, Wollongong, NSW, 2522, Australia
13Department of Biochemistry and Structural Biology, Center for Molecular Protein Science, Lund University, 221 00 Lund, Sweden
14IMPMC UMR7590, CNRS, UPMC Paris 6, 4 place Jussieu, Paris, France
15Department of Plant Molecular Biology, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland
16Department of Biochemistry, School of Biology, Moscow State University, Moscow 119991, Russia
17Department of Molecular & Cell Biology, University of Connecticut, 91 North Eagleville Road, Storrs, CT, 06269-3125, USA
18Department of Cell Biology, University Medical Center Groningen, University of Groningen, 9713 GZ Groningen, the Netherlands
19Department of Biochemistry, University of Washington, Seattle, WA 98195 USA
20Department of Molecular and Cellular Biology, Intercollegiate Faculty of Biotechnology, University of Gdańsk and the Medical University of Gdańsk, Gdańsk, Poland
21Department of Molecular Physiology and Biophysics, Vanderbilt University, Nashville, TN 37232, USA
22Departments of Pathology, Biological Chemistry, and Medicinal Chemistry and the Life Sciences Institute, University of Michigan, Ann Arbor, MI, USA
23Dipartimento di Scienze Farmacologiche e Biomolecolari (DiSFeB), Centro di Eccellenza sulle Malattie Neurodegenerative, Università degli Studi di Milano, Milan, Italy
24Department of Biosciences and the Biophysical Sciences Institute, University of Durham, Durham, UK
25Laboratory for Biocrystallography, Department of Pharmaceutical and Pharmacological Sciences, KU Leuven, Leuven, Belgium
26Laboratory of Animal Genetics and Molecular Neurobiology, Institute of Biochemistry, Biological Research Centre, Szeged, Hungary
27Biochemistry and Molecular Biology, University of Massachusetts, Amherst, MA, 01003, USA
28Laboratory of Cell & Developmental Genetics, IBIS, and Department of Molecular Biology, Medical Biochemistry and Pathology, Medical School, Université Laval, Québec (Qc), G1V 0A6, Canada

Tóm tắt

Từ khóa


Tài liệu tham khảo

Ahrman, 2007, Small heat shock proteins prevent aggregation of citrate synthase and bind to the N-terminal region which is absent in thermostable forms of citrate synthase, Extremophiles, 11, 659, 10.1007/s00792-007-0080-3

Ahrman, 2007, Chemical cross-linking of the chloroplast localized small heat-shock protein, Hsp21, and the model substrate citrate synthase, Protein Sci, 16, 1464, 10.1110/ps.072831607

Aquilina, 2004, Phosphorylation of alphaB-crystallin alters chaperone function through loss of dimeric substructure, J Biol Chem, 279, 28675, 10.1074/jbc.M403348200

Arrigo, 2000, sHsp as novel regulators of programmed cell death and tumorigenicity, Pathologie-biologie, 48, 280

Arrigo, 2007, The cellular “networking” of mammalian Hsp27 and its functions in the control of protein folding, redox state and apoptosis, Adv Exp Med Biol, 594, 14, 10.1007/978-0-387-39975-1_2

Arrigo, 2013, Human small heat shock proteins: protein interactomes of homo- and hetero-oligomeric complexes: an update, FEBS Lett, 587, 1959, 10.1016/j.febslet.2013.05.011

Arrigo, 2002, Expression of the anti-apoptotic protein Hsp27 during both the keratinocyte differentiation and dedifferentiation of HaCat cells: expression linked to changes in intracellular protein organization?, Exp Gerontol, 37, 1247, 10.1016/S0531-5565(02)00131-6

Arrigo, 2012, HspB1 dynamic phospho-oligomeric structure dependent interactome as cancer therapeutic target, Curr Mol Med, 12, 1151, 10.2174/156652412803306693

Arrigo, 2014, HspB1, HspB5 and HspB4 in human cancers: potent oncogenic role of some of their client proteins, Cancers, 6, 333, 10.3390/cancers6010333

Baldwin, 2012, Probing dynamic conformations of the high-molecular-weight alphaB-crystallin heat shock protein ensemble by NMR spectroscopy, J Am Chem Soc, 134, 15343, 10.1021/ja307874r

Balogi, 2008, A mutant small heat shock protein with increased thylakoid association provides an elevated resistance against UV-B damage in synechocystis 6803, J Biol Chem, 283, 22983, 10.1074/jbc.M710400200

Bartelt-Kirbach, 2016, HspB5/alphaB-crystallin increases dendritic complexity and protects the dendritic arbor during heat shock in cultured rat hippocampal neurons, Cell Mol Life Sci, 73, 3761, 10.1007/s00018-016-2219-9

Benesch, 2012, The quaternary organization and dynamics of the molecular chaperone HSP26 are thermally regulated, Chem Biol, 17, 1008, 10.1016/j.chembiol.2010.06.016

Benesch, 2006, Tandem mass spectrometry reveals the quaternary organization of macromolecular assemblies, Chem Biol, 13, 597, 10.1016/j.chembiol.2006.04.006

Benjamin, 1997, Temporospatial expression of the small HSP/alpha B-crystallin in cardiac and skeletal muscle during mouse development, Dev Dyn, 208, 75, 10.1002/(SICI)1097-0177(199701)208:1<75::AID-AJA7>3.0.CO;2-Z

Boncoraglio, 2012, The family of mammalian small heat shock proteins (HSPBs): implications in protein deposit diseases and motor neuropathies, Int J Biochem Cell Biol, 44, 1657, 10.1016/j.biocel.2012.03.011

Bourrelle-Langlois, 2016, In vitro structural and functional characterization of the small heat shock proteins (sHSP) of the cyanophage S-ShM2 and its host, Synechococcus sp. WH7803, PLoS One, 11, e0162233, 10.1371/journal.pone.0162233

Bova, 1999, Mutation R120G in alphaB-crystallin, which is linked to a desmin-related myopathy, results in an irregular structure and defective chaperone-like function, Proc Natl Acad Sci U S A, 96, 6137, 10.1073/pnas.96.11.6137

Bruey, 2000, Differential regulation of HSP27 oligomerization in tumor cells grown in vitro and in vivo, Oncogene, 19, 4855, 10.1038/sj.onc.1203850

Bruinsma, 2011, Inhibition of alpha-synuclein aggregation by small heat shock proteins, Proteins, 79, 2956, 10.1002/prot.23152

Bryantsev, 2002, Distribution, phosphorylation, and activities of Hsp25 in heat-stressed H9c2 myoblasts: a functional link to cytoprotection, Cell Stress Chaperones, 7, 146, 10.1379/1466-1268(2002)007<0146:DPAAOH>2.0.CO;2

Bult CJ et al. (1996) Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii Science (New York, NY 273:1058–1073

Candido, 2002, The small heat shock proteins of the nematode Caenorhabditis elegans: structure, regulation and biology, Prog Mol Subcell Biol, 28, 61, 10.1007/978-3-642-56348-5_4

Caspers, 1995, The expanding small heat-shock protein family, and structure predictions of the conserved “alpha-crystallin domain”, J Mol Evol, 40, 238, 10.1007/BF00163229

Cox, 2014, Preventing alpha-synuclein aggregation: the role of the small heat-shock molecular chaperone proteins, Biochim Biophys Acta, 1842, 1830, 10.1016/j.bbadis.2014.06.024

Cox, 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, 10.1074/jbc.M116.739250

Crippa, 2010, The small heat shock protein B8 (HspB8) promotes autophagic removal of misfolded proteins involved in amyotrophic lateral sclerosis (ALS), Hum Mol Genet, 19, 3440, 10.1093/hmg/ddq257

De Los, 2016, Hsp70 chaperones use ATP to remodel native protein oligomers and stable aggregates by entropic pulling, Nat Struct Mol Biol, 23, 766, 10.1038/nsmb.3283

de Marco, 2005, Native folding of aggregation-prone recombinant proteins in Escherichia coli by osmolytes, plasmid- or benzyl alcohol-overexpressed molecular chaperones, Cell Stress Chaperones, 10, 329, 10.1379/CSC-139R.1

Delbecq, 2013, One size does not fit all: the oligomeric states of alphaB crystallin, FEBS Lett, 587, 1073, 10.1016/j.febslet.2013.01.021

Delbecq, 2015, A mechanism of subunit recruitment in human small heat shock protein oligomers, Biochemistry, 54, 4276, 10.1021/acs.biochem.5b00490

den Engelsman, 2005, Nuclear import of {alpha}B-crystallin is phosphorylation-dependent and hampered by hyperphosphorylation of the myopathy-related mutant R120G, J Biol Chem, 280, 37139, 10.1074/jbc.M504106200

den Hoed, 2013, Identification of heart rate-associated loci and their effects on cardiac conduction and rhythm disorders, Nat Genet, 45, 621, 10.1038/ng.2610

Doshi, 2009, The role of Hsp27 and actin in the regulation of movement in human cancer cells responding to heat shock, Cell Stress Chaperones, 14, 445, 10.1007/s12192-008-0098-1

Ecroyd, 2009, Crystallin proteins and amyloid fibrils, Cell Mol Life Sci, 66, 62, 10.1007/s00018-008-8327-4

Ecroyd, 2007, Mimicking phosphorylation of alphaB-crystallin affects its chaperone activity, The Biochemical journal, 401, 129, 10.1042/BJ20060981

Evgrafov, 2004, Mutant small heat-shock protein 27 causes axonal Charcot-Marie-tooth disease and distal hereditary motor neuropathy, Nat Genet, 36, 602, 10.1038/ng1354

Eyles, 2010, Nature’s molecular sponges: small heat shock proteins grow into their chaperone roles, Proc Natl Acad Sci U S A, 107, 2727, 10.1073/pnas.0915160107

Fontaine, 2003, The sperm outer dense fiber protein is the 10th member of the superfamily of mammalian small stress proteins, Cell Stress Chaperones, 8, 62, 10.1379/1466-1268(2003)8<62:TSODFP>2.0.CO;2

Gaestel, 2002, sHsp-phosphorylation: enzymes, signaling pathways and functional implications, Prog Mol Subcell Biol, 28, 151, 10.1007/978-3-642-56348-5_8

Ghaoui, 2016, Mutations in HSPB8 causing a new phenotype of distal myopathy and motor neuropathy, Neurology, 86, 391, 10.1212/WNL.0000000000002324

Giese, 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, 10.1073/pnas.0506169103

Giese, 2002, Changes in oligomerization are essential for the chaperone activity of a small heat shock protein in vivo and in vitro, J Biol Chem, 277, 46310, 10.1074/jbc.M208926200

Golenhofen, 2016, The impact of small heat shock proteins (HspBs) in Alzheimer’s and other neurological diseases, Curr Pharm Des, 22, 4050, 10.2174/1381612822666160519113339

Haslbeck, 2016, Structure and function of alpha-crystallins: traversing from in vitro to in vivo, Biochim Biophys Acta, 1860, 149, 10.1016/j.bbagen.2015.06.008

Haslbeck, 2015, A first line of stress defense: small heat shock proteins and their function in protein homeostasis, J Mol Biol, 427, 1537, 10.1016/j.jmb.2015.02.002

Heirbaut, 2014, Dissecting the functional role of the N-terminal domain of the human small heat shock protein HSPB6, PLoS One, 9, e105892, 10.1371/journal.pone.0105892

Heirbaut, 2016, The preferential heterodimerization of human small heat shock proteins HSPB1 and HSPB6 is dictated by the N-terminal domain, Arch Biochem Biophys, 610, 41, 10.1016/j.abb.2016.10.002

Hishiya, 2010, BAG3 directly interacts with mutated alphaB-crystallin to suppress its aggregation and toxicity, PLoS One, 6, e16828, 10.1371/journal.pone.0016828

Hochberg, 2014, The structured core domain of alphaB-crystallin can prevent amyloid fibrillation and associated toxicity, Proc Natl Acad Sci U S A, 111, E1562, 10.1073/pnas.1322673111

Hong, 2000, Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress, Proc Natl Acad Sci U S A, 97, 4392, 10.1073/pnas.97.8.4392

Hoogstra-Berends, 2012, Heat shock protein-inducing compounds as therapeutics to restore proteostasis in atrial fibrillation, Trends in cardiovascular medicine, 22, 62, 10.1016/j.tcm.2012.06.013

Irobi, 2004, Hot-spot residue in small heat-shock protein 22 causes distal motor neuropathy, Nat Genet, 36, 597, 10.1038/ng1328

Jaspard, 2016, sHSPdb: a database for the analysis of small heat shock proteins, BMC Plant Biol, 16, 135, 10.1186/s12870-016-0820-6

Kamradt, 2002, The small heat shock protein alpha B-crystallin negatively regulates apoptosis during myogenic differentiation by inhibiting caspase-3 activation, J Biol Chem, 277, 38731, 10.1074/jbc.M201770200

Kamradt, 2005, The small heat shock protein alpha B-crystallin is a novel inhibitor of TRAIL-induced apoptosis that suppresses the activation of caspase-3, J Biol Chem, 280, 11059, 10.1074/jbc.M413382200

Kappe, 2003, The human genome encodes 10 alpha-crystallin-related small heat shock proteins: HspB1-10, Cell Stress Chaperones, 8, 53, 10.1379/1466-1268(2003)8<53:THGECS>2.0.CO;2

Ke, 2011, HSPB1, HSPB6, HSPB7 and HSPB8 protect against RhoA GTPase-induced remodeling in tachypaced atrial myocytes, PLoS One, 6, e20395, 10.1371/journal.pone.0020395

Kim, 1998, Crystal structure of a small heat-shock protein, Nature, 394, 595, 10.1038/29106

Klosowska A, Chamera T, Liberek K (2016) Adenosine diphosphate restricts the protein remodeling activity of the Hsp104 chaperone to Hsp70 assisted disaggregation eLife 5

Kolb, 2010, Mutant small heat shock protein B3 causes motor neuropathy: utility of a candidate gene approach, Neurology, 74, 502, 10.1212/WNL.0b013e3181cef84a

Kondrat, 2015, Native mass spectrometry: towards high-throughput structural proteomics, Methods in molecular biology (Clifton, NJ), 1261, 349, 10.1007/978-1-4939-2230-7_18

Lambert, 1999, HSP27 multimerization mediated by phosphorylation-sensitive intermolecular interactions at the amino terminus, J Biol Chem, 274, 9378, 10.1074/jbc.274.14.9378

Lambert, 2011, Subunit arrangement in the dodecameric chloroplast small heat shock protein Hsp21, Protein Sci, 20, 291, 10.1002/pro.560

Lavoie, 1993, Induction of Chinese hamster HSP27 gene expression in mouse cells confers resistance to heat shock. HSP27 stabilization of the microfilament organization, J Biol Chem, 268, 3420, 10.1016/S0021-9258(18)53711-X

Lavoie, 1995, Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat shock protein 27, Mol Cell Biol, 15, 505, 10.1128/MCB.15.1.505

Litt, 1998, Autosomal dominant congenital cataract associated with a missense mutation in the human alpha crystallin gene CRYAA, Hum Mol Genet, 7, 471, 10.1093/hmg/7.3.471

Maaroufi, 2013, Analysis and phylogeny of small heat shock proteins from marine viruses and their cyanobacteria host, PLoS One, 8, e81207, 10.1371/journal.pone.0081207

Mainz, 2015, The chaperone alphaB-crystallin uses different interfaces to capture an amorphous and an amyloid client, Nat Struct Mol Biol, 22, 898, 10.1038/nsmb.3108

McDonald, 2012, Sequence, structure, and dynamic determinants of Hsp27 (HspB1) equilibrium dissociation are encoded by the N-terminal domain, Biochemistry, 51, 1257, 10.1021/bi2017624

McHaourab, 2002, Mechanism of chaperone function in small heat shock proteins. Two-mode binding of the excited states of T4 lysozyme mutants by alphaA-crystallin, J Biol Chem, 277, 40557, 10.1074/jbc.M206250200

McLoughlin, 2016, Class I and II small heat shock proteins together with HSP101 protect protein translation factors during heat stress, Plant Physiol, 172, 1221

Mehlen, 1997, Large unphosphorylated aggregates as the active form of hsp27 which controls intracellular reactive oxygen species and glutathione levels and generates a protection against TNFalpha in NIH-3T3-ras cells, Biochem Biophys Res Commun, 241, 187, 10.1006/bbrc.1997.7635

Michaud, 2008, The nuclear localization of Drosophila Hsp27 is dependent on a monopartite arginine-rich NLS and is uncoupled from its association to nuclear speckles, Biochim Biophys Acta, 1783, 1200, 10.1016/j.bbamcr.2008.01.031

Mitzelfelt, 2016, The human 343delT HSPB5 chaperone associated with early-onset skeletal myopathy causes defects in protein solubility, J Biol Chem, 291, 14939, 10.1074/jbc.M116.730481

Morrison, 2003, Mimicking phosphorylation of alphaB-crystallin on serine-59 is necessary and sufficient to provide maximal protection of cardiac myocytes from apoptosis, Circ Res, 92, 203, 10.1161/01.RES.0000052989.83995.A5

Morrow, 2015, Small heat shock proteins: big folding machines, Cell Stress Chaperones, 20, 207, 10.1007/s12192-014-0561-0

Moutaoufik, 2016, Oligomerization and chaperone-like activity of Drosophila melanogaster small heat shock protein DmHsp27 and three arginine mutants in the alpha-crystallin domain, Cell Stress Chaperones

Mymrikov EV, Daake M, Richter B, Haslbeck M, Buchner J (2016) The chaperone activity and substrate spectrum of human small heat shock proteins The Journal of biological chemistry

Nefedova, 2016, Interaction of small heat shock proteins with light component of neurofilaments (NFL), Cell Stress Chaperones

Nicholl, 1994, Chaperone activity of alpha-crystallins modulates intermediate filament assembly, EMBO J, 13, 945, 10.1002/j.1460-2075.1994.tb06339.x

Painter, 2008, Real-time monitoring of protein complexes reveals their quaternary organization and dynamics, Chem Biol, 15, 246, 10.1016/j.chembiol.2008.01.009

Parcellier, 2006, HSP27 favors ubiquitination and proteasomal degradation of p27Kip1 and helps S-phase re-entry in stressed cells, FASEB J, 20, 1179, 10.1096/fj.05-4184fje

Park AM et al (2016) Heat shock protein 27 plays a pivotal role in myofibroblast differentiation and in the development of bleomycin-induced pulmonary fibrosis. PLoS One 11:e0148998. doi:10.1371/journal.pone.0148998

Perng, 1999, Intermediate filament interactions can be altered by HSP27 and alphaB-crystallin, J Cell Sci, 112, 2099, 10.1242/jcs.112.13.2099

Perng, 2016, Purification of protein chaperones and their functional assays with intermediate filaments, Methods Enzymol, 569, 155, 10.1016/bs.mie.2015.07.025

Perng, 1999, The cardiomyopathy and lens cataract mutation in alphaB-crystallin alters its protein structure, chaperone activity, and interaction with intermediate filaments in vitro, J Biol Chem, 274, 33235, 10.1074/jbc.274.47.33235

Perng, 2004, Desmin aggregate formation by R120G alphaB-crystallin is caused by altered filament interactions and is dependent upon network status in cells, Mol Biol Cell, 15, 2335, 10.1091/mbc.e03-12-0893

Peschek, 2009, The eye lens chaperone alpha-crystallin forms defined globular assemblies, Proc Natl Acad Sci U S A, 106, 13272, 10.1073/pnas.0902651106

Qian, 2009, Blockade of Hsp20 phosphorylation exacerbates cardiac ischemia/reperfusion injury by suppressed autophagy and increased cell death, Circ Res, 105, 1223, 10.1161/CIRCRESAHA.109.200378

Quinlan, 1999, Fatal attraction: when chaperone turns harlot, Nat Med, 5, 25, 10.1038/4704

Rajagopal P, Tse E, Borst AJ, Delbecq SP, Shi L, Southworth DR, Klevit RE (2015) A conserved histidine modulates HSPB5 structure to trigger chaperone activity in response to stress-related acidosis eLife 4

Rajasekaran, 2007, Human alpha B-crystallin mutation causes oxido-reductive stress and protein aggregation cardiomyopathy in mice, Cell, 130, 427, 10.1016/j.cell.2007.06.044

Richter, 2010, The heat shock response: life on the verge of death, Mol Cell, 40, 253, 10.1016/j.molcel.2010.10.006

Rogalla, 1999, Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor alpha by phosphorylation, J Biol Chem, 274, 18947, 10.1074/jbc.274.27.18947

Rouse, 1994, A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins, Cell, 78, 1027, 10.1016/0092-8674(94)90277-1

Rusmini, 2013, Clearance of the mutant androgen receptor in motoneuronal models of spinal and bulbar muscular atrophy, Neurobiol Aging, 34, 2585, 10.1016/j.neurobiolaging.2013.05.026

Schmidt, 2016, Induction and phosphorylation of the small heat shock proteins HspB1/Hsp25 and HspB5/alphaB-crystallin in the rat retina upon optic nerve injury, Cell Stress Chaperones, 21, 167, 10.1007/s12192-015-0650-8

Shi, 2012, 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, 10.1074/jbc.M112.388132

Simon, 2007, Myopathy-associated alphaB-crystallin mutants: abnormal phosphorylation, intracellular location, and interactions with other small heat shock proteins, J Biol Chem, 282, 34276, 10.1074/jbc.M703267200

Sluchanko, 2012, Monomeric 14-3-3zeta has a chaperone-like activity and is stabilized by phosphorylated HspB6, Biochemistry, 51, 6127, 10.1021/bi300674e

Sluchanko, 2014, Chaperone-like activity of monomeric human 14-3-3zeta on different protein substrates, Arch Biochem Biophys, 549, 32, 10.1016/j.abb.2014.03.008

Sluchanko, 2011, Properties of the monomeric form of human 14-3-3zeta protein and its interaction with tau and HspB6, Biochemistry, 50, 9797, 10.1021/bi201374s

Stengel, 2012, Dissecting heterogeneous molecular chaperone complexes using a mass spectrum deconvolution approach, Chem Biol, 19, 599, 10.1016/j.chembiol.2012.04.007

Stengel, 2010, Quaternary dynamics and plasticity underlie small heat shock protein chaperone function, Proc Natl Acad Sci U S A, 107, 2007, 10.1073/pnas.0910126107

Stromer, 2004, Analysis of the regulation of the molecular chaperone Hsp26 by temperature-induced dissociation: the N-terminal domain is important for oligomer assembly and the binding of unfolding proteins, J Biol Chem, 279, 11222, 10.1074/jbc.M310149200

Strozecka, 2012, Importance of N- and C-terminal regions of IbpA, Escherichia coli small heat shock protein, for chaperone function and oligomerization, J Biol Chem, 287, 2843, 10.1074/jbc.M111.273847

Sudnitsyna, 2011, The role of intrinsically disordered regions in the structure and functioning of small heat shock proteins, Curr Protein Pept Sci, 13, 76, 10.2174/138920312799277875

Sugiyama, 2000, Muscle develops a specific form of small heat shock protein complex composed of MKBP/HSPB2 and HSPB3 during myogenic differentiation, J Biol Chem, 275, 1095, 10.1074/jbc.275.2.1095

Suzuki, 1998, MKBP, a novel member of the small heat shock protein family, binds and activates the myotonic dystrophy protein kinase, J Cell Biol, 140, 1113, 10.1083/jcb.140.5.1113

Takayama, 2003, Heat-shock proteins as regulators of apoptosis, Oncogene, 22, 9041, 10.1038/sj.onc.1207114

Tanguay RM, Hightower LE (2015) The big book on small heat shock proteins vol 8. Heat shock proteins 8, Series Editors: Alexzander A.A. Asea, Stuart K. Calderwood edn. Springer

Theriault, 2004, Essential role of the NH2-terminal WD/EPF motif in the phosphorylation-activated protective function of mammalian Hsp27, J Biol Chem, 279, 23463, 10.1074/jbc.M402325200

Toivola, 2010, Intermediate filaments take the heat as stress proteins, Trends Cell Biol, 20, 79, 10.1016/j.tcb.2009.11.004

Toth, 2010, Neuroprotective effect of small heat shock protein, Hsp27, after acute and chronic alcohol administration, Cell Stress Chaperones, 15, 807, 10.1007/s12192-010-0188-8

Toth, 2014, Alcohol stress, membranes, and chaperones, Cell Stress Chaperones, 19, 299, 10.1007/s12192-013-0472-5

Treweek, 2015, Small heat-shock proteins: important players in regulating cellular proteostasis, Cell Mol Life Sci, 72, 429, 10.1007/s00018-014-1754-5

Treweek, 2005, R120G alphaB-crystallin promotes the unfolding of reduced alpha-lactalbumin and is inherently unstable, FEBS J, 272, 711, 10.1111/j.1742-4658.2004.04507.x

Ungelenk, 2016, Small heat shock proteins sequester misfolding proteins in near-native conformation for cellular protection and efficient refolding, Nat Commun, 7, 13673, 10.1038/ncomms13673

van Montfort, 2001, Crystal structure and assembly of a eukaryotic small heat shock protein, Nat Struct Biol, 8, 1025, 10.1038/nsb722

Verschuure, 2003, Expression of small heat shock proteins HspB2, HspB8, Hsp20 and cvHsp in different tissues of the perinatal developing pig, Eur J Cell Biol, 82, 523, 10.1078/0171-9335-00337

Vicart, 1998, A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy, Nat Genet, 20, 92, 10.1038/1765

Vos, 2008, Structural and functional diversities between members of the human HSPB, HSPH, HSPA, and DNAJ chaperone families Biochemistry, 47, 7001

Webster, 2003, Serine phosphorylation and suppression of apoptosis by the small heat shock protein alphaB-crystallin, Circ Res, 92, 130, 10.1161/01.RES.0000056967.51841.21

Weeks, 2014, Molecular structure and dynamics of the dimeric human small heat shock protein HSPB6, J Struct Biol, 185, 342, 10.1016/j.jsb.2013.12.009

Wu SY, Zou P, Fuller AW, Mishra S, Wang Z, Schey KL, McHaourab HS (2016) Expression of cataract-linked gamma-crystallin variants in zebrafish reveals a proteostasis network that senses protein stability. J Biol Chem 291:25387–25397

Zhu, 2009, Single molecule force spectroscopy of the cardiac titin N2B element: effects of the molecular chaperone alphaB-crystallin with disease-causing mutations, J Biol Chem, 284, 13914, 10.1074/jbc.M809743200