Skip to main content
SpringerLink
Log in

HSPB6 (Hsp20) as a Versatile Molecular Regulator

  • Chapter
The Big Book on Small Heat Shock Proteins

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

  • 1289 Accesses

Abstract

HspB6 (Hsp20) is a member of the large family of human small heat shock proteins. In contrast to other human small heat shock proteins (HspB1, HspB5) forming large oligomers, HspB6 predominantly forms stable dimers which tend to self-association. HspB6 is ubiquitously expressed in practically all human tissues, undergoes posttranslational modifications (such as phosphorylation and acetylation) and forms heterooligomeric complexes with two other human small heat shock proteins, HspB1 and HspB5. Possessing chaperone-like activity, HspB6 prevents aggregation of amyloid-β and α-synuclein, decreases cytotoxicity induced by accumulation of amyloids and, interacting with Bag3, modulates autophagosomal degradation of misfolded proteins. HspB6 protects cardiomyocytes from ischemia/reperfusion injuries, prevents cardiac hypertrophy and, possessing antiapoptotic activity, protects cardiomyocytes from different unfavorable conditions. Phosphorylation of HspB6 catalyzed by cyclic nucleotide-dependent protein kinases induces relaxation of different smooth muscle. Exact molecular mechanism underlying relaxation effect of phosphorylated HspB6 in smooth muscle remains enigmatic, but seems to be dependent on the remodeling of actin cytoskeleton. HspB6 is not a genuine actin-binding protein, but interacting with universal adapter protein 14-3-3 seems to be able indirectly affect activity of certain regulatory actin-binding proteins thus inducing cytoskeleton remodeling. Penetrating phosphorylated peptides of HspB6 were successfully used for relaxation of airway smooth muscle and prevention of vasospasm in human blood vessels. Full-size HspB6 and its short peptides modulate platelet aggregation. Versatility of HspB6 is awaiting further investigation, however it can be at least partially explained by the ability of phosphorylated HspB6 to interact with the universal adapter protein 14-3-3 and to displace different target proteins from their complexes with 14-3-3. This displacement may result in modulation of target protein activity and consequently can induce multiple and diverse effects.

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

  • An SS, Askovich PS, Zarembinski TI, Ahn K, Peltier JM, von Rechenberg M, Sahasrabudhe S, Fredberg JJ (2011) A novel small molecule target in human airway smooth muscle for potential treatment of obstructive lung diseases: a staged high-throughput biophysical screening. Respir Res 12:8. doi:10.1186/1465-9921-12-8

    CAS  PubMed Central  PubMed  Google Scholar 

  • Aquilina JA, Shrestha S, Morris AM, Ecroyd H (2013) Structural and functional aspects of hetero-oligomers formed by the small heat shock proteins alphaB-crystallin and HSP27. J Biol Chem 288(19):13602–13609. doi:10.1074/jbc.M112.443812

    CAS  PubMed Central  PubMed  Google Scholar 

  • Arndt V, Dick N, Tawo R, Dreiseidler M, Wenzel D, Hesse M, Furst DO, Saftig P, Saint R, Fleischmann BK, Hoch M, Hohfeld J (2010) Chaperone-assisted selective autophagy is essential for muscle maintenance. Curr Biol 20(2):143–148, S0960-9822(09)02000-4

    CAS  PubMed  Google Scholar 

  • Arrigo AP (2012) Pathology-dependent effects linked to small heat shock proteins expression: an update. Scientifica 2012:185641. doi:10.6064/2012/185641

    PubMed Central  PubMed  Google Scholar 

  • Arrigo AP (2013) Human small heat shock proteins: protein interactomes of homo- and hetero-oligomeric complexes: an update. FEBS Lett 587(13):1959–1969, S0014-5793(13)00353-0

    CAS  PubMed  Google Scholar 

  • Ba M, Singer CA, Tyagi M, Brophy C, Baker JE, Cremo C, Halayko A, Gerthoffer WT (2009) HSP20 phosphorylation and airway smooth muscle relaxation. Cell Health Cytoskeleton 2009(1):27–42

    PubMed Central  PubMed  Google Scholar 

  • Bagneris C, Bateman OA, Naylor CE, Cronin N, Boelens WC, Keep NH, Slingsby C (2009) Crystal structures of alpha-crystallin domain dimers of alphaB-crystallin and Hsp20. J Mol Biol 392(5):1242–1252, S0022-2836(09)00936-X

    CAS  PubMed  Google Scholar 

  • Bartelt-Kirbach B, Golenhofen N (2013) Reaction of small heat-shock proteins to different kinds of cellular stress in cultured rat hippocampal neurons. Cell Stress Chaperones. doi:10.1007/s12192-013-0452-9

    Google Scholar 

  • Basha E, O’Neill H, Vierling E (2012) Small heat shock proteins and alpha-crystallins: dynamic proteins with flexible functions. Trends Biochem Sci 37(3):106–117, S0968-0004(11)00190-3

    CAS  PubMed Central  PubMed  Google Scholar 

  • Beall AC, Kato K, Goldenring JR, Rasmussen H, Brophy CM (1997) Cyclic nucleotide-dependent vasorelaxation is associated with the phosphorylation of a small heat shock-related protein. J Biol Chem 272(17):11283–11287

    CAS  PubMed  Google Scholar 

  • Beall A, Bagwell D, Woodrum D, Stoming TA, Kato K, Suzuki A, Rasmussen H, Brophy CM (1999) The small heat shock-related protein, HSP20, is phosphorylated on serine 16 during cyclic nucleotide-dependent relaxation. J Biol Chem 274(16):11344–11351

    CAS  PubMed  Google Scholar 

  • Boluyt MO, Brevick JL, Rogers DS, Randall MJ, Scalia AF, Li ZB (2006) Changes in the rat heart proteome induced by exercise training: increased abundance of heat shock protein hsp20. Proteomics 6(10):3154–3169. doi:10.1002/pmic.200401356

    CAS  PubMed  Google Scholar 

  • Boros S, Kamps B, Wunderink L, de Bruijn W, de Jong WW, Boelens WC (2004) Transglutaminase catalyzes differential crosslinking of small heat shock proteins and amyloid-beta. FEBS Lett 576(1–2):57–62, S0014579304010816

    CAS  PubMed  Google Scholar 

  • Brophy CM, Dickinson M, Woodrum D (1999a) Phosphorylation of the small heat shock-related protein, HSP20, in vascular smooth muscles is associated with changes in the macromolecular associations of HSP20. J Biol Chem 274(10):6324–6329

    CAS  PubMed  Google Scholar 

  • Brophy CM, Lamb S, Graham A (1999b) The small heat shock-related protein-20 is an actin-associated protein. J Vasc Surg 29(2):326–333, S0741521499000427

    CAS  PubMed  Google Scholar 

  • Bruinsma IB, Bruggink KA, Kinast K, Versleijen AA, Segers-Nolten IM, Subramaniam V, Kuiperij HB, Boelens W, de Waal RM, Verbeek MM (2011) Inhibition of alpha-synuclein aggregation by small heat shock proteins. Proteins 79(10):2956–2967. doi:10.1002/prot.23152

    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(2):291–302, 3928

    CAS  PubMed  Google Scholar 

  • Bukach OV, Marston SB, Gusev NB (2005) Small heat shock protein with apparent molecular mass 20 kDa (Hsp20, HspB6) is not a genuine actin-binding protein. J Muscle Res Cell Motil 26(4–5):175–181. doi:10.1007/s10974-005-9008-7

    CAS  PubMed  Google Scholar 

  • Bukach OV, Glukhova AE, Seit-Nebi AS, Gusev NB (2009) Heterooligomeric complexes formed by human small heat shock proteins HspB1 (Hsp27) and HspB6 (Hsp20). Biochim Biophys Acta 1794(3):486–495, S1570-9639(08)00372-5

    CAS  PubMed  Google Scholar 

  • Caccamo D, Condello S, Ferlazzo N, Curro M, Griffin M, Ientile R (2013) Transglutaminase 2 interaction with small heat shock proteins mediate cell survival upon excitotoxic stress. Amino Acids 44(1):151–159. doi:10.1007/s00726-011-1083-z

    CAS  PubMed  Google Scholar 

  • Carra S, Seguin SJ, Landry J (2008) HspB8 and Bag3: a new chaperone complex targeting misfolded proteins to macroautophagy. Autophagy 4(2):237–239, 5407

    CAS  PubMed  Google Scholar 

  • Chen A, Karolczak-Bayatti M, Sweeney M, Treumann A, Morrissey K, Ulrich SM, Nicholas Europe-Finner G, Taggart MJ (2013) Lysine deacetylase inhibition promotes relaxation of arterial tone and C-terminal acetylation of HSPB6 (Hsp20) in vascular smooth muscle cells. Physiol Rep 1(6):e00127. doi:10.1002/phy2.127

    PubMed Central  PubMed  Google Scholar 

  • Chernik IS, Seit-Nebi AS, Marston SB, Gusev NB (2007) Small heat shock protein Hsp20 (HspB6) as a partner of 14-3-3 gamma. Mol Cell Biochem 295(1–2):9–17. doi:10.1007/s11010-006-9266-8

    CAS  PubMed  Google Scholar 

  • Clark AR, Naylor CE, Bagneris C, Keep NH, Slingsby C (2011) Crystal structure of R120G disease mutant of human alphaB-crystallin domain dimer shows closure of a groove. J Mol Biol 408(1):118–134, S0022-2836(11)00164-1

    CAS  PubMed Central  PubMed  Google Scholar 

  • Crippa V, Carra S, Rusmini P, Sau D, Bolzoni E, Bendotti C, De Biasi S, Poletti A (2010) A role of small heat shock protein B8 (HspB8) in the autophagic removal of misfolded proteins responsible for neurodegenerative diseases. Autophagy 6(7):958–960, 13042

    PubMed  Google Scholar 

  • Cross BE, O’Dea HM, MacPhee DJ (2007) Expression of small heat shock-related protein 20 (HSP20) in rat myometrium is markedly decreased during late pregnancy and labour. Reproduction 133(4):807–817, 133/4/807

    CAS  PubMed  Google Scholar 

  • Damer CK, Partridge J, Pearson WR, Haystead TA (1998) Rapid identification of protein phosphatase 1-binding proteins by mixed peptide sequencing and data base searching. Characterization of a novel holoenzymic form of protein phosphatase 1. J Biol Chem 273(38):24396–24405

    CAS  PubMed  Google Scholar 

  • Datskevich PN, Mymrikov EV, Gusev NB (2012a) Utilization of fluorescent chimeras for investigation of heterooligomeric complexes formed by human small heat shock proteins. Biochimie 94(8):1794–1784, S0300-9084(12)00146-0

    Google Scholar 

  • Datskevich PN, Mymrikov EV, Sluchanko NN, Shemetov AA, Sudnitsyna MV, Gusev NB (2012b) Expression, purification and some properties of fluorescent chimeras of human small heat shock proteins. Protein Expr Purif 82(1):45–54, S1046-5928(11)00313-5

    CAS  PubMed  Google Scholar 

  • Deighton RF, McGregor R, Kemp J, McCulloch J, Whittle IR (2010) Glioma pathophysiology: insights emerging from proteomics. Brain Pathol 20(4):691–703. doi:10.1111/j.1750-3639.2010.00376.x

    CAS  PubMed  Google Scholar 

  • Delbecq SP, Klevit RE (2013) One size does not fit all: the oligomeric states of alphaB crystallin. FEBS Lett 587(8):1073–1080, S0014-5793(13)00052-5

    CAS  PubMed  Google Scholar 

  • Delbecq SP, Jehle S, Klevit R (2012) Binding determinants of the small heat shock protein, alphaB-crystallin: recognition of the ‘IxI’ motif. EMBO J 31(24):4587–4594, emboj2012318

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dohke T, Wada A, Isono T, Fujii M, Yamamoto T, Tsutamoto T, Horie M (2006) Proteomic analysis reveals significant alternations of cardiac small heat shock protein expression in congestive heart failure. J Card Fail 12(1):77–84, S1071-9164(05)00703-7

    CAS  PubMed  Google Scholar 

  • Dreiza CM, Brophy CM, Komalavilas P, Furnish EJ, Joshi L, Pallero MA, Murphy-Ullrich JE, von Rechenberg M, Ho YS, Richardson B, Xu N, Zhen Y, Peltier JM, Panitch A (2005) Transducible heat shock protein 20 (HSP20) phosphopeptide alters cytoskeletal dynamics. FASEB J 19(2):261–263, 04-2911fje

    CAS  PubMed  Google Scholar 

  • Dreiza CM, Komalavilas P, Furnish EJ, Flynn CR, Sheller MR, Smoke CC, Lopes LB, Brophy CM (2010) The small heat shock protein, HSPB6, in muscle function and disease. Cell Stress Chaperones 15(1):1–11. doi:10.1007/s12192-009-0127-8

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dubinska-Magiera M, Jablonska J, Saczko J, Kulbacka J, Jagla T, Daczewska M (2014) Contribution of small heat shock proteins to muscle development and function. FEBS Lett. doi:10.1016/j.febslet.2014.01.005

    PubMed  Google Scholar 

  • Edwards HV, Cameron RT, Baillie GS (2011) The emerging role of HSP20 as a multifunctional protective agent. Cell Signal 23(9):1447–1454, S0898-6568(11)00146-X

    CAS  PubMed  Google Scholar 

  • Edwards HV, Scott JD, Baillie GS (2012a) The A-kinase anchoring protein AKAP-Lbc facilitates cardioprotective PKA phosphorylation of Hsp20 on Serine 16. Biochem J 446(3):437–443, BJ20120570

    Google Scholar 

  • Edwards HV, Scott JD, Baillie GS (2012b) PKA phosphorylation of the small heat-shock protein Hsp20 enhances its cardioprotective effects. Biochem Soc Trans 40(1):210–214, BST20110673

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fan GC, Kranias EG (2011) Small heat shock protein 20 (HspB6) in cardiac hypertrophy and failure. J Mol Cell Cardiol 51(4):574–577, S0022-2828(10)00344-5

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fan GC, Chu G, Mitton B, Song Q, Yuan Q, Kranias EG (2004) Small heat-shock protein Hsp20 phosphorylation inhibits beta-agonist-induced cardiac apoptosis. Circ Res 94(11):1474–1482. doi:10.1161/01.RES.0000129179.66631.00

    CAS  PubMed  Google Scholar 

  • Fan GC, Chu G, Kranias EG (2005a) Hsp20 and its cardioprotection. Trends Cardiovasc Med 15(4):138–141, S1050-1738(05)00058-7

    CAS  PubMed  Google Scholar 

  • Fan GC, Ren X, Qian J, Yuan Q, Nicolaou P, Wang Y, Jones WK, Chu G, Kranias EG (2005b) Novel cardioprotective role of a small heat-shock protein, Hsp20, against ischemia/reperfusion injury. Circulation 111(14):1792–1799, 01.CIR.0000160851.41872.C6

    CAS  PubMed  Google Scholar 

  • Fan GC, Yuan Q, Song G, Wang Y, Chen G, Qian J, Zhou X, Lee YJ, Ashraf M, Kranias EG (2006) Small heat-shock protein Hsp20 attenuates beta-agonist-mediated cardiac remodeling through apoptosis signal-regulating kinase 1. Circ Res 99(11):1233–1242, 01.RES.0000251074.19348.af

    CAS  PubMed  Google Scholar 

  • Fan GC, Zhou X, Wang X, Song G, Qian J, Nicolaou P, Chen G, Ren X, Kranias EG (2008) Heat shock protein 20 interacting with phosphorylated Akt reduces doxorubicin-triggered oxidative stress and cardiotoxicity. Circ Res 103(11):1270–1279, CIRCRESAHA.108.182832

    CAS  PubMed Central  PubMed  Google Scholar 

  • Flynn CR, Komalavilas P, Tessier D, Thresher J, Niederkofler EE, Dreiza CM, Nelson RW, Panitch A, Joshi L, Brophy CM (2003) Transduction of biologically active motifs of the small heat shock-related protein HSP20 leads to relaxation of vascular smooth muscle. FASEB J 17(10):1358–1360. doi:10.1096/fj.02-1028fje

    CAS  PubMed  Google Scholar 

  • Flynn CR, Smoke CC, Furnish E, Komalavilas P, Thresher J, Yi Z, Mandarino LJ, Brophy CM (2007) Phosphorylation and activation of a transducible recombinant form of human HSP20 in Escherichia coli. Protein Expr Purif 52(1):50–58, S1046-5928(06)00263-4

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fontaine JM, Rest JS, Welsh MJ, 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(1):62–69

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fontaine JM, Sun X, Benndorf R, Welsh MJ (2005) Interactions of HSP22 (HSPB8) with HSP20, alphaB-crystallin, and HSPB3. Biochem Biophys Res Commun 337(3):1006–1011, S0006-291X(05)02180-7

    CAS  PubMed  Google Scholar 

  • Fontaine JM, Sun X, Hoppe AD, Simon S, Vicart P, Welsh MJ, Benndorf R (2006) Abnormal small heat shock protein interactions involving neuropathy-associated HSP22 (HSPB8) mutants. FASEB J 20(12):2168–2170, fj.06-5911fje

    CAS  PubMed  Google Scholar 

  • Freeman AK, Morrison DK (2011) 14-3-3 Proteins: diverse functions in cell proliferation and cancer progression. Semin Cell Dev Biol 22(7):681–687. doi:10.1016/j.semcdb.2011.08.009

    CAS  PubMed Central  PubMed  Google Scholar 

  • Frobert O, Buus CL, Rembold CM (2005) HSP20 phosphorylation and interstitial metabolites in hypoxia-induced dilation of swine coronary arteries. Acta Physiol Scand 184(1):37–44, APS1426

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fuchs M, Poirier DJ, Seguin SJ, Lambert H, Carra S, Charette SJ, Landry J (2010) Identification of the key structural motifs involved in HspB8/HspB6-Bag3 interaction. Biochem J 425(1):245–255, BJ20090907

    CAS  Google Scholar 

  • Furnish EJ, Brophy CM, Harris VA, Macomson S, Winger J, Head GA, Shaver EG (2010) Treatment with transducible phosphopeptide analogues of the small heat shock-related protein, HSP20, after experimental subarachnoid hemorrhage: prevention and reversal of delayed decreases in cerebral perfusion. J Neurosurg 112(3):631–639. doi:10.3171/2009.7.JNS09730

    CAS  PubMed  Google Scholar 

  • Gohla A, Bokoch GM (2002) 14-3-3 regulates actin dynamics by stabilizing phosphorylated cofilin. Curr Biol 12(19):1704–1710, S0960982202011843

    CAS  PubMed  Google Scholar 

  • Golenhofen N, Perng MD, Quinlan RA, Drenckhahn D (2004) Comparison of the small heat shock proteins alphaB-crystallin, MKBP, HSP25, HSP20, and cvHSP in heart and skeletal muscle. Histochem Cell Biol 122(5):415–425. doi:10.1007/s00418-004-0711-z

    CAS  PubMed  Google Scholar 

  • Grebenova D, Roselova P, Pluskalova M, Halada P, Rosel D, Suttnar J, Brodska B, Otevrelova P, Kuzelova K (2012) Proteins implicated in the increase of adhesivity induced by suberoylanilide hydroxamic acid in leukemic cells. J Proteomics 77:406–422. doi:10.1016/j.jprot.2012.09.014

    CAS  PubMed  Google Scholar 

  • Hocking KM, Baudenbacher FJ, Putumbaka G, Venkatraman S, Cheung-Flynn J, Brophy CM, Komalavilas P (2013) Role of cyclic nucleotide-dependent actin cytoskeletal dynamics: Ca(2+)](i) and force suppression in forskolin-pretreated porcine coronary arteries. PLoS One 8(4):e60986. doi:10.1371/journal.pone.0060986

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hojlund K, Bowen BP, Hwang H, Flynn CR, Madireddy L, Geetha T, Langlais P, Meyer C, Mandarino LJ, Yi Z (2009) In vivo phosphoproteome of human skeletal muscle revealed by phosphopeptide enrichment and HPLC-ESI-MS/MS. J Proteome Res 8(11):4954–4965. doi:10.1021/pr9007267

    CAS  PubMed Central  PubMed  Google Scholar 

  • Huey KA, Thresher JS, Brophy CM, Roy RR (2004) Inactivity-induced modulation of Hsp20 and Hsp25 content in rat hindlimb muscles. Muscle Nerve 30(1):95–101. doi:10.1002/mus.20063

    CAS  PubMed  Google Scholar 

  • Inaguma Y, Hasegawa K, Kato K, Nishida Y (1996) cDNA cloning of a 20-kDa protein (p20) highly homologous to small heat shock proteins: developmental and physiological changes in rat hindlimb muscles. Gene 178(1–2):145–150

    CAS  PubMed  Google Scholar 

  • Islamovic E, Duncan A, Bers DM, Gerthoffer WT, Mestril R (2007) Importance of small heat shock protein 20 (hsp20) C-terminal extension in cardioprotection. J Mol Cell Cardiol 42(4):862–869, S0022-2828(07)00004-1

    CAS  PubMed  Google Scholar 

  • Kanno Y, Matsuno H (2006) The possibility of novel antiplatelet peptides: the physiological effects of low molecular weight HSPs on platelets. Curr Pharm Des 12(7):887–892

    CAS  PubMed  Google Scholar 

  • Kappe G, Verschuure P, Philipsen RL, Staalduinen AA, Van de Boogaart P, Boelens WC, De Jong WW (2001) Characterization of two novel human small heat shock proteins: protein kinase-related HspB8 and testis-specific HspB9. Biochim Biophys Acta 1520(1):1–6

    CAS  PubMed  Google Scholar 

  • Kappe G, Franck E, Verschuure P, Boelens WC, Leunissen JA, de Jong WW (2003) The human genome encodes 10 alpha-crystallin-related small heat shock proteins: HspB1-10. Cell Stress Chaperones 8(1):53–61

    CAS  PubMed Central  PubMed  Google Scholar 

  • Karolczak-Bayatti M, Sweeney M, Cheng J, Edey L, Robson SC, Ulrich SM, Treumann A, Taggart MJ, Europe-Finner GN (2011) Acetylation of heat shock protein 20 (Hsp20) regulates human myometrial activity. J Biol Chem 286(39):34346–34355. doi:10.1074/jbc.M111.278549

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kato K, Goto S, Inaguma Y, Hasegawa K, Morishita R, Asano T (1994) Purification and characterization of a 20-kDa protein that is highly homologous to alpha B crystallin. J Biol Chem 269(21):15302–15309

    CAS  PubMed  Google Scholar 

  • Kim NK, Joh JH, Park HR, Kim OH, Park BY, Lee CS (2004) Differential expression profiling of the proteomes and their mRNAs in porcine white and red skeletal muscles. Proteomics 4(11):3422–3428. doi:10.1002/pmic.200400976

    CAS  PubMed  Google Scholar 

  • Kirbach BB, Golenhofen N (2011) Differential expression and induction of small heat shock proteins in rat brain and cultured hippocampal neurons. J Neurosci Res 89(2):162–175. doi:10.1002/jnr.22536

    CAS  PubMed  Google Scholar 

  • Koga Y, Pelizzola M, Cheng E, Krauthammer M, Sznol M, Ariyan S, Narayan D, Molinaro AM, Halaban R, Weissman SM (2009) Genome-wide screen of promoter methylation identifies novel markers in melanoma. Genome Res 19(8):1462–1470. doi:10.1101/gr.091447.109

    CAS  PubMed Central  PubMed  Google Scholar 

  • Komalavilas P, Penn RB, Flynn CR, Thresher J, Lopes LB, Furnish EJ, Guo M, Pallero MA, Murphy-Ullrich JE, Brophy CM (2008) The small heat shock-related protein, HSP20, is a cAMP-dependent protein kinase substrate that is involved in airway smooth muscle relaxation. Am J Physiol Lung Cell Mol Physiol 294(1):L69–L78. doi:10.1152/ajplung.00235.2007

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kozawa O, Matsuno H, Niwa M, Hatakeyama D, Oiso Y, Kato K, Uematsu T (2002) HSP20, low-molecular-weight heat shock-related protein, acts extracellularly as a regulator of platelet functions: a novel defense mechanism. Life Sci 72(2):113–124, S0024320502021446

    CAS  PubMed  Google Scholar 

  • Laganowsky A, Eisenberg D (2010) Non-3D domain swapped crystal structure of truncated zebrafish alphaA crystallin. Protein Sci. doi:10.1002/pro.471

    Google Scholar 

  • Laganowsky A, Benesch JL, 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(5):1031–1043. doi:10.1002/pro.380

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lopes LB, Furnish EJ, Komalavilas P, Flynn CR, Ashby P, Hansen A, Ly DP, Yang GP, Longaker MT, Panitch A, Brophy CM (2009) Cell permeant peptide analogues of the small heat shock protein, HSP20, reduce TGF-beta1-induced CTGF expression in keloid fibroblasts. J Invest Dermatol 129(3):590–598, jid2008264

    CAS  PubMed Central  PubMed  Google Scholar 

  • Matsuno H, Kozawa O, Niwa M, Usui A, Ito H, Uematsu T, Kato K (1998) A heat shock-related protein, p20, plays an inhibitory role in platelet activation. FEBS Lett 429(3):327–329, S0014-5793(98)00626-7

    CAS  PubMed  Google Scholar 

  • Matsuno H, Ishisaki A, Nakajima K, Kato K, Kozawa O (2003) A peptide isolated from alpha B-crystallin is a novel and potent inhibitor of platelet aggregation via dual prevention of PAR-1 and GPIb/V/IX. J Thromb Haemost 1(12):2636–2642

    CAS  PubMed  Google Scholar 

  • Matsushima-Nishiwaki R, Kumada T, Nagasawa T, Suzuki M, Yasuda E, Okuda S, Maeda A, Kaneoka Y, Toyoda H, Kozawa O (2013) Direct association of heat shock protein 20 (HSPB6) with phosphoinositide 3-kinase (PI3K) in human hepatocellular carcinoma: regulation of the PI3K activity. PLoS One 8(11):e78440. doi:10.1371/journal.pone.0078440

    CAS  PubMed Central  PubMed  Google Scholar 

  • McCollum AK, Casagrande G, Kohn EC (2010) Caught in the middle: the role of Bag3 in disease. Biochem J 425(1):e1–e3, BJ20091739

    CAS  Google Scholar 

  • McHaourab HS, Godar JA, Stewart PL (2009) Structure and mechanism of protein stability sensors: chaperone activity of small heat shock proteins. Biochemistry 48(18):3828–3837. doi:10.1021/bi900212j

    CAS  PubMed Central  PubMed  Google Scholar 

  • McLemore EC, Tessier DJ, Flynn CR, Furnish EJ, Komalavilas P, Thresher JS, Joshi L, Stone WM, Fowl RJ, Brophy CM (2004) Transducible recombinant small heat shock-related protein, HSP20, inhibits vasospasm and platelet aggregation. Surgery 136(3):573–578. doi:10.1016/j.surg.2004.04.024

    PubMed  Google Scholar 

  • Meeks MK, Ripley ML, Jin Z, Rembold CM (2005) Heat shock protein 20-mediated force suppression in forskolin-relaxed swine carotid artery. Am J Physiol Cell Physiol 288(3):C633–C639, 00269.2004

    CAS  PubMed  Google Scholar 

  • Mizuno K (2013) Signaling mechanisms and functional roles of cofilin phosphorylation and dephosphorylation. Cell Signal 25(2):457–469. doi:10.1016/j.cellsig.2012.11.001

    CAS  PubMed  Google Scholar 

  • Mymrikov EV, Bukach OV, Seit-Nebi AS, Gusev NB (2010) The pivotal role of the beta 7 strand in the intersubunit contacts of different human small heat shock proteins. Cell Stress Chaperones 15(4):365–377. doi:10.1007/s12192-009-0151-8

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mymrikov EV, Seit-Nebi AS, Gusev NB (2011) Large potentials of small heat shock proteins. Physiol Rev 91(4):1123–1159, 91/4/1123

    CAS  PubMed  Google Scholar 

  • Mymrikov EV, Seit-Nebi AS, Gusev NB (2012) Heterooligomeric complexes of human small heat shock proteins. Cell Stress Chaperones 17(2):157–169. doi:10.1007/s12192-011-0296-0

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nefedova VV, Datskevich PN, Sudnitsyna MV, Strelkov SV, Gusev NB (2013a) Physico-chemical properties of R140G and K141Q mutants of human small heat shock protein HspB1 associated with hereditary peripheral neuropathies. Biochimie 95(8):1582–1592. doi:10.1016/j.biochi.2013.04.014

    CAS  PubMed  Google Scholar 

  • Nefedova VV, Sudnitsyna MV, Strelkov SV, Gusev NB (2013b) Structure and properties of G84R and L99M mutants of human small heat shock protein HspB1 correlating with motor neuropathy. Arch Biochem Biophys 538(1):16–24. doi:10.1016/j.abb.2013.07.028

    CAS  PubMed  Google Scholar 

  • Nicolaou P, Knoll R, Haghighi K, Fan GC, Dorn GW 2nd, Hasenfub G, Kranias EG (2008) Human mutation in the anti-apoptotic heat shock protein 20 abrogates its cardioprotective effects. J Biol Chem 283(48):33465–33471, M802307200

    CAS  PubMed Central  PubMed  Google Scholar 

  • Niwa M, Kozawa O, Matsuno H, Kato K, Uematsu T (2000) Small molecular weight heat shock-related protein, HSP20, exhibits an anti-platelet activity by inhibiting receptor-mediated calcium influx. Life Sci 66(1):PL7–PL12, S0024320599005664

    CAS  PubMed  Google Scholar 

  • Noda T, Kumada T, Takai S, Matsushima-Nishiwaki R, Yoshimi N, Yasuda E, Kato K, Toyoda H, Kaneoka Y, Yamaguchi A, Kozawa O (2007) Expression levels of heat shock protein 20 decrease in parallel with tumor progression in patients with hepatocellular carcinoma. Oncol Rep 17(6):1309–1314

    CAS  PubMed  Google Scholar 

  • O’Connor MJ, Rembold CM (2002) Heat-induced force suppression and HSP20 phosphorylation in swine carotid media. J Appl Physiol 93(2):484–488. doi:10.1152/japplphysiol.00009.2002

    PubMed  Google Scholar 

  • Pipkin W, Johnson JA, Creazzo TL, Burch J, Komalavilas P, Brophy C (2003) Localization, macromolecular associations, and function of the small heat shock-related protein HSP20 in rat heart. Circulation 107(3):469–476

    CAS  PubMed  Google Scholar 

  • Pozuelo Rubio M, Geraghty KM, Wong BH, Wood NT, Campbell DG, Morrice N, Mackintosh C (2004) 14-3-3-affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation and trafficking. Biochem J 379(Pt 2):395–408. doi:10.1042/BJ20031797

    PubMed Central  PubMed  Google Scholar 

  • Qian J, Ren X, Wang X, Zhang P, Jones WK, Molkentin JD, Fan GC, Kranias EG (2009) Blockade of Hsp20 phosphorylation exacerbates cardiac ischemia/reperfusion injury by suppressed autophagy and increased cell death. Circ Res 105(12):1223–1231, CIRCRESAHA.109.200378

    CAS  PubMed Central  PubMed  Google Scholar 

  • Qian J, Vafiadaki E, Florea SM, Singh VP, Song W, Lam CK, Wang Y, Yuan Q, Pritchard TJ, Cai W, Haghighi K, Rodriguez P, Wang HS, Sanoudou D, Fan GC, Kranias EG (2011) Small heat shock protein 20 interacts with protein phosphatase-1 and enhances sarcoplasmic reticulum calcium cycling. Circ Res 108(12):1429–1438, CIRCRESAHA.110.237644

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rembold CM, Zhang E (2001) Localization of heat shock protein 20 in swine carotid artery. BMC Physiol 1:10

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rembold CM, Foster DB, Strauss JD, Wingard CJ, Eyk JE (2000) cGMP-mediated phosphorylation of heat shock protein 20 may cause smooth muscle relaxation without myosin light chain dephosphorylation in swine carotid artery. J Physiol 524(Pt 3):865–878, PHY_0041

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ren XP, Wu J, Wang X, Sartor MA, Qian J, Jones K, Nicolaou P, Pritchard TJ, Fan GC (2009) MicroRNA-320 is involved in the regulation of cardiac ischemia/reperfusion injury by targeting heat-shock protein 20. Circulation 119(17):2357–2366. doi:10.1161/CIRCULATIONAHA.108.814145

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rosati A, Graziano V, De Laurenzi V, Pascale M, Turco MC (2011) BAG3: a multifaceted protein that regulates major cell pathways. Cell Death Dis 2:e141, cddis201124

    CAS  PubMed Central  PubMed  Google Scholar 

  • Salinthone S, Tyagi M, Gerthoffer WT (2008) Small heat shock proteins in smooth muscle. Pharmacol Ther 119(1):44–54, S0163-7258(08)00080-6

    CAS  PubMed Central  PubMed  Google Scholar 

  • Seit-Nebi AS, Gusev NB (2010) Versatility of the small heat shock protein HSPB6 (Hsp20). Cell Stress Chaperones 15(3):233–236. doi:10.1007/s12192-009-0141-x

    CAS  PubMed Central  PubMed  Google Scholar 

  • Selcen D, Muntoni F, Burton BK, Pegoraro E, Sewry C, Bite AV, Engel AG (2009) Mutation in BAG3 causes severe dominant childhood muscular dystrophy. Ann Neurol 65(1):83–89. doi:10.1002/ana.21553

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shemetov AA, Gusev NB (2011) Biochemical characterization of small heat shock protein HspB8 (Hsp22)-Bag3 interaction. Arch Biochem Biophys 513(1):1–9, S0003-9861(11)00249-9

    Google Scholar 

  • Simon S, Fontaine JM, Martin JL, Sun X, Hoppe AD, Welsh MJ, Benndorf R, Vicart P (2007) Myopathy-associated alphaB-crystallin mutants: abnormal phosphorylation, intracellular location, and interactions with other small heat shock proteins. J Biol Chem 282(47):34276–34287, M703267200

    CAS  PubMed  Google Scholar 

  • Sin YY, Edwards HV, Li X, Day JP, Christian F, Dunlop AJ, Adams DR, Zaccolo M, Houslay MD, Baillie GS (2011) Disruption of the cyclic AMP phosphodiesterase-4 (PDE4)-HSP20 complex attenuates the beta-agonist induced hypertrophic response in cardiac myocytes. J Mol Cell Cardiol 50(5):872–883. doi:10.1016/j.yjmcc.2011.02.006

    CAS  PubMed  Google Scholar 

  • Sluchanko NN, Gusev NB (2010) 14-3-3 proteins and regulation of cytoskeleton. Biochemistry 75(13):1528–1546

    CAS  PubMed  Google Scholar 

  • Sluchanko NN, Gusev NB (2012) Oligomeric structure of 14-3-3 protein: what do we know about monomers? FEBS Lett 586(24):4249–4256. doi:10.1016/j.febslet.2012.10.048

    CAS  PubMed  Google Scholar 

  • Sluchanko NN, Sudnitsyna MV, Chernik IS, Seit-Nebi AS, Gusev NB (2011a) Phosphomimicking mutations of human 14-3-3zeta affect its interaction with tau protein and small heat shock protein HspB6. Arch Biochem Biophys 506(1):24–34, S0003-9861(10)00463-7

    CAS  PubMed  Google Scholar 

  • Sluchanko NN, Sudnitsyna MV, Seit-Nebi AS, Antson AA, Gusev NB (2011b) Properties of the monomeric form of human 14-3-3zeta protein and its interaction with tau and HspB6. Biochemistry 50(45):9797–9808. doi:10.1021/bi201374s

    CAS  PubMed  Google Scholar 

  • Sluchanko NN, Artemova NV, Sudnitsyna MV, Safenkova IV, Antson AA, Levitsky DI, Gusev NB (2012) Monomeric 14-3-3zeta has a chaperone-like activity and is stabilized by phosphorylated HspB6. Biochemistry 51(31):6127–6138. doi:10.1021/bi300674e

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sluchanko NN, Chebotareva NA, Gusev NB (2013) Modulation of 14-3-3/phosphotarget interaction by physiological concentrations of phosphate and glycerophosphates. PLoS One 8(8):e72597. doi:10.1371/journal.pone.0072597

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sudnitsyna MV, Mymrikov EV, Seit-Nebi AS, Gusev NB (2012a) The role of intrinsically disordered regions in the structure and functioning of small heat shock proteins. Curr Protein Pept Sci 13(1):76–85, BSP/CPPS/E-Pub/163

    CAS  PubMed  Google Scholar 

  • Sudnitsyna MV, Seit-Nebi AS, Gusev NB (2012b) Cofilin weakly interacts with 14-3-3 and therefore can only indirectly participate in regulation of cell motility by small heat shock protein HspB6 (Hsp20). Arch Biochem Biophys 521(1–2):62–70, S0003-9861(12)00101-4

    CAS  PubMed  Google Scholar 

  • Sugiyama Y, Suzuki A, Kishikawa M, Akutsu R, Hirose T, Waye MM, Tsui SK, Yoshida S, Ohno S (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(2):1095–1104

    CAS  PubMed  Google Scholar 

  • Takayama S, Reed JC (2001) Molecular chaperone targeting and regulation by BAG family proteins. Nat Cell Biol 3(10):E237–E241. doi:10.1038/ncb1001-e237

    CAS  PubMed  Google Scholar 

  • Taylor RP, Benjamin IJ (2005) Small heat shock proteins: a new classification scheme in mammals. J Mol Cell Cardiol 38(3):433–444, S0022-2828(05)00003-9

    CAS  PubMed  Google Scholar 

  • Tessier DJ, Komalavilas P, Panitch A, Joshi L, Brophy CM (2003) The small heat shock protein (HSP) 20 is dynamically associated with the actin cross-linking protein actinin. J Surg Res 111(1):152–157, S0022480403001136

    CAS  PubMed  Google Scholar 

  • Tessier DJ, Komalavilas P, Liu B, Kent CK, Thresher JS, Dreiza CM, Panitch A, Joshi L, Furnish E, Stone W, Fowl R, Brophy CM (2004) Transduction of peptide analogs of the small heat shock-related protein HSP20 inhibits intimal hyperplasia. J Vasc Surg 40(1):106–114. doi:10.1016/j.jvs.2004.03.028

    PubMed  Google Scholar 

  • Tyson EK, Macintyre DA, Smith R, Chan EC, Read M (2008) Evidence that a protein kinase A substrate, small heat-shock protein 20, modulates myometrial relaxation in human pregnancy. Endocrinology 149(12):6157–6165, en.2008-0593

    CAS  PubMed  Google Scholar 

  • Uhart M, Bustos DM (2013) Human 14-3-3 paralogs differences uncovered by cross-talk of phosphorylation and lysine acetylation. PLoS One 8(2):e55703. doi:10.1371/journal.pone.0055703

    CAS  PubMed Central  PubMed  Google Scholar 

  • van de Klundert FA, Smulders RH, Gijsen ML, Lindner RA, Jaenicke R, Carver JA, de Jong WW (1998) The mammalian small heat-shock protein Hsp20 forms dimers and is a poor chaperone. Eur J Biochem 258(3):1014–1021

    PubMed  Google Scholar 

  • van de Klundert F, van den Ijssel P, Stege GJ, de Jong WW (1999) Rat Hsp20 confers thermoresistance in a clonal survival assay, but fails to protect coexpressed luciferase in Chinese hamster ovary cells. Biochem Biophys Res Commun 254(1):164–168, S0006291X9899917X

    Google Scholar 

  • van Noort JM, Bsibsi M, Nacken P, Gerritsen WH, Amor S (2012) The link between small heat shock proteins and the immune system. Int J Biochem Cell Biol 44(10):1670–1679. doi:10.1016/j.biocel.2011.12.010

    PubMed  Google Scholar 

  • Verschuure P, Tatard C, Boelens WC, Grongnet JF, David JC (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(10):523–530

    CAS  PubMed  Google Scholar 

  • 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. doi:10.1021/bi800639z

    CAS  PubMed  Google Scholar 

  • Vos MJ, Zijlstra MP, Carra S, Sibon OC, Kampinga HH (2011) Small heat shock proteins, protein degradation and protein aggregation diseases. Autophagy 7(1):101–103, 13935

    PubMed  Google Scholar 

  • Wang Y, Xu A, Pearson RB, Cooper GJ (1999) Insulin and insulin antagonists evoke phosphorylation of P20 at serine 157 and serine 16 respectively in rat skeletal muscle. FEBS Lett 462(1–2):25–30, S0014-5793(99)01496-9

    CAS  PubMed  Google Scholar 

  • Wang X, Zingarelli B, O’Connor M, Zhang P, Adeyemo A, Kranias EG, Wang Y, Fan GC (2009) Overexpression of Hsp20 prevents endotoxin-induced myocardial dysfunction and apoptosis via inhibition of NF-kappaB activation. J Mol Cell Cardiol 47(3):382–390, S0022-2828(09)00227-2

    CAS  PubMed Central  PubMed  Google Scholar 

  • Weeks SD, Baranova EV, Heirbaut M, Beelen S, Shkumatov AV, Gusev NB, Strelkov SV (2013) Molecular structure and dynamics of the dimeric human small heat shock protein HSPB6. J Struct Biol. doi:10.1016/j.jsb.2013.12.009

    PubMed  Google Scholar 

  • Wilhelmus MM, Boelens WC, Otte-Holler I, Kamps B, de Waal RM, Verbeek MM (2006a) Small heat shock proteins inhibit amyloid-beta protein aggregation and cerebrovascular amyloid-beta protein toxicity. Brain Res 1089(1):67–78, S0006-8993(06)00762-1

    CAS  PubMed  Google Scholar 

  • Wilhelmus MM, Boelens WC, Otte-Holler I, Kamps B, Kusters B, Maat-Schieman ML, de Waal RM, Verbeek MM (2006b) Small heat shock protein HspB8: its distribution in Alzheimer’s disease brains and its inhibition of amyloid-beta protein aggregation and cerebrovascular amyloid-beta toxicity. Acta Neuropathol 111(2):139–149. doi:10.1007/s00401-005-0030-z

    CAS  PubMed  Google Scholar 

  • Wilhelmus MM, Otte-Holler I, Wesseling P, de Waal RM, Boelens WC, Verbeek MM (2006c) Specific association of small heat shock proteins with the pathological hallmarks of Alzheimer’s disease brains. Neuropathol Appl Neurobiol 32(2):119–130, NAN689

    CAS  PubMed  Google Scholar 

  • Willis MS, Patterson C (2010) Hold me tight: role of the heat shock protein family of chaperones in cardiac disease. Circulation 122(17):1740–1751. doi:10.1161/CIRCULATIONAHA.110.942250

    PubMed Central  PubMed  Google Scholar 

  • Woodrum DA, Brophy CM, Wingard CJ, Beall A, Rasmussen H (1999) Phosphorylation events associated with cyclic nucleotide-dependent inhibition of smooth muscle contraction. Am J Physiol 277(3 Pt 2):H931–H939

    CAS  PubMed  Google Scholar 

  • Woodrum D, Pipkin W, Tessier D, Komalavilas P, Brophy CM (2003) Phosphorylation of the heat shock-related protein, HSP20, mediates cyclic nucleotide-dependent relaxation. J Vasc Surg 37(4):874–881. doi:10.1067/mva.2003.153

    PubMed  Google Scholar 

  • Yaffe MB, Rittinger K, Volinia S, Caron PR, Aitken A, Leffers H, Gamblin SJ, Smerdon SJ, Cantley LC (1997) The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91(7):961–971

    CAS  PubMed  Google Scholar 

  • Yap YL, Lam DC, Luc G, Zhang XW, Hernandez D, Gras R, Wang E, Chiu SW, Chung LP, Lam WK, Smith DK, Minna JD, Danchin A, Wong MP (2005) Conserved transcription factor binding sites of cancer markers derived from primary lung adenocarcinoma microarrays. Nucleic Acids Res 33(1):409–421. doi:10.1093/nar/gki188

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zeng L, Tan J, Lu W, Hu Z (2013) Blockade of Ser16-Hsp20 phosphorylation attenuates neuroprotection dependent upon Bcl-2 and Bax. Curr Neurovasc Res 10(3):208–215

    CAS  PubMed  Google Scholar 

  • Zhang X, Wang X, Zhu H, Kranias EG, Tang Y, Peng T, Chang J, Fan GC (2012) Hsp20 functions as a novel cardiokine in promoting angiogenesis via activation of VEGFR2. PLoS One 7(3):e32765. doi:10.1371/journal.pone.0032765

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgement

This investigation was supported by Russian Foundation for Basic Research (14-04-00146 to NNS and 13-04-00015 to NBG).Note The recently published data indicate that under crowding conditions HspB6 tends to self-association and that phosphorylation abrogates this tendency (Sluchanko NN, Chebotareva NA, Gusev NB (2015) Quaternary structure of human small heat shock protein HSPB6 (Hsp20) in crowded media modeled by trimethylamine N-oxide (TMAO): Effect of protein phosphorylation. Biochimie 108:68–75. doi:10.1016/j.biochi.2014.11.001).

Author information

Authors and Affiliations

  1. Department of Biochemistry, School of Biology, Moscow State University, Moscow, 119991, Russian Federation

    Maria V. Sudnitsyna & Nikolai B. Gusev

  2. A. N. Bach Institute of Biochemistry, Russian Academy of Sciences, Moscow, 119071, Russian Federation

    Nikolai N. Sluchanko

Authors
  1. Maria V. Sudnitsyna
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nikolai N. Sluchanko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nikolai B. Gusev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nikolai B. Gusev .

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

Sudnitsyna, M.V., Sluchanko, N.N., Gusev, N.B. (2015). HSPB6 (Hsp20) as a Versatile Molecular Regulator. 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_9

Download citation

Publish with us

Policies and ethics

Search

Navigation