Abstract
All organisms and cells respond to various stress conditions such as environmental, metabolic, or pathophysiological stress by generally upregulating, among others, the expression and/or activation of a group of proteins called heat shock proteins (HSPs). Among the HSPs, special attention has been devoted to the mutations affecting the function of the αB-crystallin (HSPB5), a small heat shock protein (sHsp) playing a critical role in the modulation of several cellular processes related to survival and stress recovery, such as protein degradation, cytoskeletal stabilization, and apoptosis. Because of the emerging role in general health and disease conditions, the main objective of this mini-review is to provide a brief account on the role of HSPB5 in mammalian muscle physiopathology. Here, we report the current known state of the regulation and localization of HSPB5 in skeletal and cardiac tissue, making also a critical summary of all human HSPB5 mutations known to be strictly associated to specific skeletal and cardiac diseases, such as desmin-related myopathies (DRM), dilated (DCM) and restrictive (RCM) cardiomyopathy. Finally, pointing to putative strategies for HSPB5-based therapy to prevent or counteract these forms of human muscular disorders.
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References
Adhikari AS, Singh BN, Rao KS, Rao CM (2011) αB-crystallin, a small heat shock protein, modulates NF-κB activity in a phosphorylation-dependent manner and protects muscle myoblasts from TNF-α induced cytotoxicity. Biochim Biophys Acta 1813(8):1532–1542. https://doi.org/10.1016/j.bbamcr.2011.04.009
Aggeli IK, Beis I, Gaitanaki C (2008) Oxidative stress and calpain inhibition induce alpha B-crystallin phosphorylation via p38-MAPK and calcium signalling pathways in H9c2 cells. Cell Signal 20(7):1292–1302. https://doi.org/10.1016/j.cellsig.2008.02.019
Ahmad MF, Singh D, Taiyab A, Ramakrishna T, Raman B, Rao CM (2008) Selective Cu2+ binding, redox silencing, and cytoprotective effects of the small heat shock proteins alphaA- and alphaB-crystallin. J Mol Biol 382(3):812–824. https://doi.org/10.1016/j.jmb.2008.07.068
Ahmed K, Furusawa Y, Tabuchi Y, Emam HF, Piao JL, Hassan MA, Yamamoto T, Kondo T, Kadowaki M (2012) Chemical inducers of heat shock proteins derived from medicinal plants and cytoprotective genes response. Int J Hyperth 28(1):1–8. https://doi.org/10.3109/02656736.2011.627408
Arbustini E, Pasotti M, Pilotto A, Pellegrini C, Grasso M, Previtali S, Repetto A, Bellini O, Azan G, Scaffino M, Campana C, Piccolo G, Viganò M, Tavazzi L (2006) Desmin accumulation restrictive cardiomyopathy and atrioventricular block associated with desmin gene defects. Eur J Heart Fail 8(5):477–483. https://doi.org/10.1016/j.ejheart.2005.11.003
Arrigo AP (2013) Human small heat shock proteins: protein interactomes of homo- and hetero-oligomeric complexes: an update. FEBS Lett 587(13):1959–1969. https://doi.org/10.1016/j.febslet.2013.05.011
Arrigo AP, Gibert P (2014) HspB1, HspB5 and HspB4 in human cancers: potent oncogenic role of some of their client proteins. Cancers 6(1):333–365. https://doi.org/10.3390/cancers6010333
Arrigo AP, Gibert B (2013) Protein interactomes of three stress inducible small heat shock proteins: HspB1, HspB5 and HspB8. Int J Hyperth 29(5):409–422. https://doi.org/10.3109/02656736.2013.792956
Bagnéris 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. https://doi.org/10.1016/j.jmb.2009.07.069
Bakthisaran R, Tangirala R, Rao CM (2015) Small heat shock proteins: role in cellular functions and pathology. Biochim Biophys Acta 1854(4):291–319. https://doi.org/10.1016/j.bbapap.2014.12.019
Balchin D, Hayer-Hartl M, Hartl FU (2016) In vivo aspects of protein folding and quality control. Science 353: aac4354
Baldwin AJ, Lioe H, Robinson CV, Kay LE, Benesch JLP (2011) αBcrystallin polydispersity is a consequence of unbiased quaternary dynamics. J Mol Biol 413(2):297–309. https://doi.org/10.1016/j.jmb.2011.07.016
Banerjee Mustafi S, Grose JH, Zhang H, Pratt GW, Sadoshima J, Christians ES, Benjamin IJ (2014) Aggregate-prone R120GCRYAB triggers multifaceted modifications of the thioredoxin system. Antioxid Redox Signal 20(18):2891–2906. https://doi.org/10.1089/ars.2013.5340
Banerjee PR, Pande A, Shekhtman A, Pande J (2015) Molecular mechanism of the chaperone function of mini-alpha-Crystallin, a 19-residue peptide of human alpha-Crystallin. Biochemistry 54(2):505–515. https://doi.org/10.1021/bi5014479
Baranova EV, Weeks SD, Beelen S, Bukach OV, Gusev NB, Strelkov SV (2011) Three-dimensional structure of α-crystallin domain dimers of human small heat shock proteins HSPB1 and HSPB6. J Mol Biol 411(1):110–122. https://doi.org/10.1016/j.jmb.2011.05.024
Barbash O, Diehl JA (2008) SCF(Fbx4/alphaB-crystallin) E3 ligase: when one is not enough. Cell Cycle 7(19):2983–2986. https://doi.org/10.4161/cc.7.19.6775
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297. https://doi.org/10.1016/S0092-8674(04)00045-5
Beltran Valls MR, Dimauro I, Brunelli A, Tranchita E, Ciminelli E, Caserotti P, Duranti G, Sabatini S, Parisi P, Parisi A, Caporossi D (2014) Explosive type of moderate-resistance training induces functional, cardiovascular, and molecular adaptations in the elderly. Age (Dordr) 36(2):759–772. https://doi.org/10.1007/s11357-013-9584-1
Beltran Valls MR, Wilkinson DJ, Narici MV, Smith K, Phillips BE, Caporossi D, Atherton PJ (2015) Protein carbonylation and heat shock proteins in human skeletal muscle: relationships to age and sarcopenia. J Gerontol A Biol Sci Med Sci 70(2):174–181. https://doi.org/10.1093/gerona/glu007
Bhat SP, Nagineni CN (1989) αB subunit of lens-specific protein α-crystallin is present in other ocular and non-ocular tissue. Biochem Biophys Res Commun 158(1):319–325. https://doi.org/10.1016/S0006-291X(89)80215-3
Bhattacharyya J, Padmanabha Udupa EG, Wang J, Sharma KK (2006) Mini-alphaBcrystallin: a functional element of alphaB-crystallin with chaperone-like activity. Biochemistry 45(9):3069–3076. https://doi.org/10.1021/bi0518141
Bhuiyan MS, Pattison JS, Osinska H, James J, Gulick J, McLendon PM, Hill JA, Sadoshima J, Robbins J (2013) Enhanced autophagy ameliorates cardiac proteinopathy. J Clin Invest 123(12):5284–5297. https://doi.org/10.1172/JCI70877
Bornman L, Steinmann CML, Gericke GS, Polla BS (1998) In vivo heat shock protects rat myocardial mitochondria. Biochem Biophys Res Commun 246(3):836–840. https://doi.org/10.1006/bbrc.1998.8717
Bova MP, Yaron O, Huang Q, Ding L, Haley DA, Stewart PL, Horwitz J (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(11):6137–6142. https://doi.org/10.1073/pnas.96.11.6137
Bradbury J (2003) Chaperones: keeping a close eye on protein folding. Lancet 361(9364):1194–1195. https://doi.org/10.1016/S0140-6736(03)12975-3
Brady JP, Garland DL, Green DE, Tamm ER, Giblin FJ, Wawrousek EF (2001) AlphaB-crystallin in lens development and muscle integrity: a gene knockout approach. Invest Ophthalmol Vis Sci 42(12):2924–2934
Braun N, Zacharias M, Peschek J, Kastenmüller A, Zou J, Hanzlik M (2011) Multiple molecular architectures of the eye lens chaperone αB-crystallin elucidated by a triple hybrid approach. Proc Natl Acad Sci U.S.A 108:20491–20496
Brodehl A, Ferrier RA, Hamilton SJ, Greenway SC, Brundler MA, Yu W, Gibson WT, McKinnon ML, McGillivray B, Alvarez N, Giuffre M, Schwartzentruber J, FORGE Canada Consortium, Gerull B (2016) Mutations in FLNC are associated with familial restrictive cardiomyopathy. Hum Mutat 37(3):269–279. https://doi.org/10.1002/humu.22942
Brodehl A, Gaertner-Rommel A, Klauke B, Grewe SA, Schirmer I, Peterschröder A, Faber L, Vorgerd M, Gummert J, Anselmetti D, Schulz U, Paluszkiewicz L, Milting H (2017) The novel αB-crystallin (CRYAB) mutation p.D109G causes restrictive cardiomyopathy. Hum Mutat 38(8):947–952. https://doi.org/10.1002/humu.23248
Brunelli A, Dimauro I, Sgrò P et al (2012) Acute exercise modulates BDNF and pro-BDNF protein content in immune cells. Med Sci Sports Exerc 44(10):1871–1880. https://doi.org/10.1249/MSS.0b013e31825ab69b
Bucley PA, Konigsberg IR (1974) Myogenic fusion and the duration of the post-mitotic gap (G1). Dev Biol 37(1):193–212. https://doi.org/10.1016/0012-1606(74)90179-1
Cabet E, Batonnet-Pichon S, Delort F, Gausser’es B, Vicart P, Lilienbaum A (2015) Antioxidant treatment and induction of autophagy cooperate to reduce desmin aggregation in a cellular model of desminopathy. PLoS One 10(9):e0137009. https://doi.org/10.1371/journal.pone.0137009
Carra S, Alberti S, Arrigo PA, Benesch JL, Benjamin IJ, Boelens W, Bartelt-Kirbach B, Brundel BJJM, Buchner J, Bukau B, Carver JA, Ecroyd H, Emanuelsson C, Finet S, Golenhofen N, Goloubinoff P, Gusev N, Haslbeck M, Hightower l, Kampinga HH, Klevit RE, Liberek K, Mchaourab HS, McMenimen KA, Poletti A, Quinlan R, Strelkov SV, Toth ME, Vierling E, Tanguay RM (2017) The growing world of small heat shock proteins: from structure to functions. Cell Stress Chaperones 22(4):601–611. https://doi.org/10.1007/s12192-017-0787-8
Ceci R, Beltran Valls MR, Duranti G, Dimauro I, Quaranta F, Pittaluga M, Sabatini S, Caserotti P, Parisi P, Parisi A, Caporossi D (2014) Oxidative stress responses to a graded maximal exercise test in older adults following explosive-type resistance training. Redox Biol 2:65–72. https://doi.org/10.1016/j.redox.2013.12.004
Chalova AS, Sudnitsyna MV, Semenyuk PI, Orlov VN, Gusev NB (2014) Effect of disulfide crosslinking on thermal transitions and chaperone-like activity of human small heat shock protein HspB1. Cell Stress Chaperones 19(6):963–972. https://doi.org/10.1007/s12192-014-0520-9
Chen SJ, Sun TX, Akhtar NJ, Liang JJ (2001) Oxidation of human lens recombinant alphaA-crystallin and cysteine-deficient mutants. J Mol Biol 305(4):969–976. https://doi.org/10.1006/jmbi.2000.4348
Chiesi M, Longoni S, Limbruno U (1990) Cardiac alpha-crystallin: involvement during heart ischemia. Mol Cell Biochem 97(2):129–136
Chung J, Nguyen AK, Henstridge DC et al (2008) HSP72 protects against obesity-induced insulin resistance. Proc Natl Acad Sci U S A 5:1739–1744
Cornford PA, Dodson AR, Parsons KF, Desmond AD, Woolfenden A, Fordham M, Neoptolemos JP, Ke Y, Foster CS (2000) Heat shock protein expression independently predicts clinical outcome in prostate cancer. Cancer Res 60(24):7099–7105
Cumming KT, Raastad T, Holden G et al (2014) Effects of vitamin C and E supplementation on endogenous antioxidant systems and heat shock proteins in response to endurance training. Physiol Rep 2. pii: e12142. https://doi.org/10.14814/phy2.12142
Dalakas MC, Dagvadorj A, Goudeau B, Park KY, Takeda K, Simon-Casteras M, Vasconcelos O, Sambuughin N, Shatunov A, Nagle JW, Sivakumar K, Vicart P, Goldfarb LG (2003) Progressive skeletal myopathy, a phenotypic variant of desmin myopathy associated with desmin mutations. Neuromuscul Disord 13(3):252–258. https://doi.org/10.1016/s0960-8966(02)00271-7
Delbecq SP, Klevit RE (2013) One size does not fit all: the oligomeric states of αB crystallin. FEBS Lett 587(8):1073–1080. https://doi.org/10.1016/j.febslet.2013.01.021
Delbecq SP, Rosenbaum JC, Klevit RE (2015) A mechanism of subunit recruitment in human small heat shock protein oligomers. Biochemistry 54(28):4276–4284. https://doi.org/10.1021/acs.biochem.5b00490
Del Bigio MR, Chudley AE, Sarnat HB, Campbell C, Goobie S, Chodirker BN, Selcen D (2011) Infantile muscular dystrophy in Canadian aboriginals is an αB-crystallinopathy. Ann Neurol 69(5):866–871. https://doi.org/10.1002/ana.22331
den Engelsman J, Gerrits D, de Jong WW, Robbins J, Kato K, Boelens WC (2005) Nuclear import of {alpha}B-crystallin is phosphorylation-dependent and hampered by hyperphosphorylation of the myopathy-related mutant R120G. J Biol Chem 280(44):37139–37148. https://doi.org/10.1074/jbc.M504106200
Dimauro I, Grasso L, Fittipaldi S, Fantini C, Mercatelli N, Racca S, Geuna S, di Gianfrancesco A, Caporossi D, Pigozzi F, Borrione P (2014) Platelet-rich plasma and skeletal muscle healing: a molecular analysis of the early phases of the regeneration process in an experimental animal model. PLoS One 9(7):e102993. https://doi.org/10.1371/journal.pone.0102993
Dimauro I, Mercatelli N, Caporossi D (2016a) Exercise-induced ROS in heat shock proteins response. Free Radic Biol Med 98:46–55. https://doi.org/10.1016/j.freeradbiomed.2016.03.028
Dimauro I, Scalabrin M, Fantini C et al (2016b) Resistance training and redox homeostasis: correlation with age-associated genomic changes. Redox Bio l10:34–44. https://doi.org/10.1016/j.redox.2016.09.008
Dimauro I, Sgura A, Pittaluga et al (2017) Regular exercise participation improves genomic stability in diabetic patients: an exploratory study to analyse telomere length and DNA damage. Sci Rep 7:4137. doi: https://doi.org/10.1038/s41598-017-04448-4, 1.
Djuranovic S, Nahvi A, Green R (2011) A parsimonious model for gene regulation by miRNAs. Science 331(6017):550–553. https://doi.org/10.1126/science.1191138
Doran P, Gannon J, O'Connell K, Ohlendieck K (2007) Aging skeletal muscle shows a drastic increase in the small heat shock proteins alphaB-crystallin/HspB5 and cvHsp/HspB7. Eur J Cell Biol 86(10):629–640. https://doi.org/10.1016/j.ejcb.2007.07.003
Dubin RA, Ally A, Chung S, Piatigorsky J (1990) Human alpha-β-crystallin gene and preferential promoter function in lens. Genomics 7(4):594–601. https://doi.org/10.1016/0888-7543(90)90204-8
Eaton P, Fuller W, Bell JR, Shattock MJ (2001) AlphaB crystallin translocation and phosphorylation: signal transduction pathways and preconditioning in the isolated rat heart. J Mol Cell Cardiol 33(9):1659–1671. https://doi.org/10.1006/jmcc.2001.1418
Eaton P, Fuller W, Shattock MJ (2002) S-thiolation of HSP27 regulates its multimeric aggregate size independently of phosphorylation. J Biol Chem 277(24):21189–21196. https://doi.org/10.1074/jbc.M200591200
Enomoto Y, Adachi S, Matsushima-Nishiwaki R et al (2009) αB-crystallin extracellularly suppresses ADP-induced granule secretion from human platelets. FEBS Lett 583:2464e2468
Esser C, Alberti S, Hohfeld J (2004) Cooperation of molecular chaperones with the ubiquitin/proteasome system. Biochim Biophys Acta 1695(1-3):171–188. https://doi.org/10.1016/j.bbamcr.2004.09.020
Fichna JP, Potulska-Chromik A, Miszta P, Redowicz MJ, Kaminska AM, Zekanowski C, Filipek S (2016) A novel dominant D109A CRYAB mutation in a family with myofibrillar myopathy affects αB-crystallin structure. BBA Clin 7:1–7. https://doi.org/10.1016/j.bbacli.2016.11.004
Fittipaldi S, Dimauro I, Mercatelli N, Caporossi D (2014) Role of exercise-induced reactive oxygen species in the modulation of heat shock protein response. Free Radic Res 48(1):52–70. https://doi.org/10.3109/10715762.2013.835047
Fittipaldi S, Mercatelli N, Dimauro I, Jackson MJ, Paronetto MP, Caporossi D (2015) Alpha B-crystallin induction in skeletal muscle cells under redox imbalance is mediated by a JNK-dependent regulatory mechanism. Free Radic Biol Med 86:331–342. https://doi.org/10.1016/j.freeradbiomed.2015.05.035
Forrest KM, Al-Sarraj S, Sewry C et al (2011) Infantile onset myofibrillar myopathy due to recessive CRYAB mutations. Neuromuscul Disord 21(1):37–40. https://doi.org/10.1016/j.nmd.2010.11.003
Gabai VL, Sherman MY (2002) Interplay between molecular chaperones and signaling pathways in survival of heat shock. J Appl Physiol 92(4):1743–1748. https://doi.org/10.1152/japplphysiol.01101.2001
Gamerdinger M, Carra S, Behl C (2011) Emerging roles of molecular chaperones and co-chaperones in selective autophagy: focus on BAG proteins. J Mol Med 89(12):1175–1182. https://doi.org/10.1007/s00109-011-0795-6
Gangalum RK, Atanasov IC, Zhou ZH, Bhat SP (2011) αB-crystallin is found in detergent-resistant membrane microdomains and is secreted via exosomes from human retinal pigment epithelial cells. J Biol Chem 286:3261e3269
Ganguly S, Mitra A, Sarkar S (2014) Role of α-crystallin B in regulation of stress induced cardiomyocyte apoptosis. Cardiovasc Hematol Agents Med Chem 12(2):60–65. https://doi.org/10.2174/1871525713666150123151731
Garrido C, Paul C, Seigneuric R, Kampinga HH (2012) The small heat shock proteins family: the long forgotten chaperones. Int J Biochem Cell Biol 44(10):1588–1592. https://doi.org/10.1016/j.biocel.2012.02.022
Geeraert C, Ratier A, Pfisterer SG, Perdiz D, Cantaloube I, Rouault A, Pattingre S, Proikas-Cezanne T, Codogno P, Poüs C (2010) Starvation-induced hyperacetylation of tubulin is required for the stimulation of autophagy by nutrient deprivation. J Biol Chem 285(31):24184–24194. https://doi.org/10.1074/jbc.M109.091553
Ghosh JG, Estrada MR, Clark JI (2005) Interactive domains for chaperone activity in the small heat shock protein, human alphaB crystallin. Biochemistry 44(45):14854–14869. https://doi.org/10.1021/bi0503910
Golenhofen N, Arbeiter A, Koob R, Drenckhahn D (2002) Ischemia induced association of the stress protein alpha B-crystallin with Iband portion of cardiac titin. J Mol Cell Cardiol 34(3):309–319. https://doi.org/10.1006/jmcc.2001.1513
Golenhofen N, Htun P, Ness W, Koob R, Schaper W, Drenckhahn D (1999) Binding of the stress protein alpha B-crystallin to cardiac myofibrils correlates with the degree of myocardial damage during ischemia/reperfusion in vivo. J Mol Cell Cardiol 31(3):569–580. https://doi.org/10.1006/jmcc.1998.0892
Gopal-Srivastava R, Piatigorsky J (1993) The murine B-crystallin/small heat shock protein enhancer: identification of BE-1, BE-2, BE-3, and MRF control elements. Mol Cell Biol 13(11):7144–7152. https://doi.org/10.1128/MCB.13.11.7144
Groenendyk J, Sreenivasaiah PK, Kim DH, Agellon LB, Michalak M (2010) Biology of endoplasmic reticulum stress in the heart. Circ Res 107(10):1185–1197. https://doi.org/10.1161/CIRCRESAHA.110.227033
Gupta R, Srivastava OP (2004) Deamidation affects structural and functional properties of human alphaA-crystallin and its oligomerization with alphaB-crystallin. J Biol Chem 279(43):44258–44269. https://doi.org/10.1074/jbc.M405648200
Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12(10):842–846. https://doi.org/10.1038/nsmb993
Haslbeck M, Weinkauf S, Buchner J (2015) Regulation of the chaperone function of small Hsps. In: Hightower LE (ed) Tanguay RM. Springer International Publishing, Switzerland, The Small HSP World. Cham. isbn:978-3-319-16076-4
Hayes D, Napoli V, Mazurkie A, Stafford WF, Graceffa P (2009) Phosphorylation dependence of hsp27 multimeric size and molecular chaperone function. J Biol Chem 284(28):18801–18807. https://doi.org/10.1074/jbc.M109.011353
Hoover HE, Thuerauf DJ, Martindale JJ, Glembotski CC (2000) Alpha B-crystallin gene induction and phosphorylation by MKK6-activated p38. A potential role for alpha B-crystallin as a target of the p38 branch of the cardiac stress response. J Biol Chem 275(31):23825–23833. https://doi.org/10.1074/jbc.M003864200
Houck SA1, Landsbury A, Clark JI, Quinlan RA (2011). Multiple sites in αB-crystallin modulate its interactions with desmin filaments assembled in vitro. PLoS One 6:e25859. doi: https://doi.org/10.1371/journal.pone.0025859.
WF Hu, Gong L, Cao Z et al (2012) alphaA- and alphaB-crystallins interact with caspase-3 and Bax to guard mouse lens development. Curr Mol Med 12:177–187
Inagaki N, Hayashi T, Arimura T, Koga Y, Takahashi M, Shibata H, Teraoka K, Chikamori T, Yamashina A, Kimura A (2006) Alpha B-crystallin mutation in dilated cardiomyopathy. Biochem Biophys Res Commun 342(2):379–386. https://doi.org/10.1016/j.bbrc.2006.01.154
Ito H, Okamoto K, Nakayama H, Isobe T, Kato K (1997) Phosphorylation of alphaB-crystallin in response to various types of stress. J Biol Chem 272(47):29934–29941. https://doi.org/10.1074/jbc.272.47.29934
Ivanov O, Chen F, Wiley EL, Keswani A, Diaz LK, Memmel HC, Rademaker A, Gradishar WJ, Morrow M, Khan SA, Cryns VL (2008) alphaB-crystallin is a novel predictor of resistance to neoadjuvant chemotherapy in breast cancer. Breast Cancer Res Treat 111(3):411–417. https://doi.org/10.1007/s10549-007-9796-0
Janu’e A, Oliv’e M, Ferrer I (2007) Oxidative stress in desminopathies and myotilinopathies: a link between oxidative damage and abnormal protein aggregation. Brain Pathol 17(4):377–388. https://doi.org/10.1111/j.1750-3639.2007.00087.x
Jehle S, Vollmar BS, Bardiaux B, Dove KK, Rajagopal P, Gonen T, Oschkinat H, Klevit RE (2011) N-terminal domain of alphaB-crystallin provides a conformational switch for multimerization and structural heterogeneity. Proc Natl Acad Sci U S A 108(16):6409–6414. https://doi.org/10.1073/pnas.1014656108
Kamradt MC, Chen F, Cryns VL (2001) The small heat shock protein alpha B-crystallin negatively regulates cytochrome c- and caspase-8- dependent activation of caspase-3 by inhibiting its autoproteolytic maturation. J Biol Chem 276(19):16059–16063. https://doi.org/10.1074/jbc.C100107200
Kappé G, Franck E, Verschuure P, Boelens WC, Leunissen JAM, 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. https://doi.org/10.1379/1466-1268(2003)8%3C53:THGECS%3E2.0.CO;2
Karin M, Lin A (2002) NF-kappaB at the crossroads of life and death. Nat Immunol 3(3):221–227. https://doi.org/10.1038/ni0302-221
Kato K, Ito H, Kamei K, Inaguma Y, Iwamoto I, Saga S (1998) Phosphorylation of alpha beta-crystallin in mitotic cells and identification enzymatic activities responsible for phosphorylation. J Biol Chem 273(43):28346–28354. https://doi.org/10.1074/jbc.273.43.28346
Kim KK, Kim R, Kim SH (1998) Crystal structure of a small heatshock protein. Nature 394(6693):595–599. https://doi.org/10.1038/29106
Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, Kominami E, Tanaka K, Chiba T (2005) Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 169(3):425–434. https://doi.org/10.1083/jcb.200412022
Kriehuber T, Rattei T, Weinmaier T, Bepperling A, Haslbeck M, Buchner J (2010) Independent evolution of the core domain and its flanking sequences in small heat shock proteins. FASEB J 24(10):3633–3642. https://doi.org/10.1096/fj.10-156992
Laganowsky A, Benesch JLP, Landau M, Ding L, Sawaya MR, Cascio D, Huang Q, Robinson CV, Horwitz J, Eisenberg D (2010) Crystal structures of truncated alphaA and alphaB crystallins reveal structural mechanisms of polydispersity important for eye lens function. Protein Sci 19(5):1031–1043. https://doi.org/10.1002/pro.380
Launay N, Goudeau B, Kato K, Vicart P, Lilienbaum A (2006) Cell signaling pathways to alphaB-crystallin following stresses of the cytoskeleton. Expt. Cell Res 312(18):3570–3584. https://doi.org/10.1016/j.yexcr.2006.07.025
Li J, Horak KM, Su H, Sanbe A, Robbins J, Wang X (2011) Enhancement of proteasomal function protects against cardiac proteinopathy and ischemia/reperfusion injury in mice. J Clin Invest 121(9):3689–3700. https://doi.org/10.1172/JCI45709
Li DW, Liu JP, Mao YW, Xiang H, Wang J, Ma WY, Dong Z, Pike HM, Brown RE, Reed JC (2005) Calcium-activated RAF/MEK/ERK signaling pathway mediates p53-dependent apoptosis and is abrogated by alpha B-crystallin through inhibition of RAS activation. Mol Biol Cell 16(9):4437–4453. https://doi.org/10.1091/mbc.E05-01-0010
Li Y, Shin D, Kwon SH (2013) Histone deacetylase 6 plays a role as a distinct regulator of diverse cellular processes. FEBS J 280(3):775–793. https://doi.org/10.1111/febs.12079
Lin DI, Barbash O, Kumar KG et al (2006) Phosphorylation-dependent ubiquitination of cyclin D1 by the SCF (FBX4-alphaB crystallin) complex. Mol Cell 24(3):355–366. https://doi.org/10.1016/j.molcel.2006.09.007
Liu S, Li J, Tao Y, Xiao X (2007) Small heat shock protein alphaB-crystallin binds to p53 to sequester its translocation to mitochondria during hydrogen peroxide induced apoptosis. Biochem Biophys Res Commun 354(1):109–114. https://doi.org/10.1016/j.bbrc.2006.12.152
Liu Y, Zhang X, Luo L, Wu M, Zeng R, Cheng G, Hu B, Liu B, Liang JJ, Shang F (2006) A novel αB-crystallincmutation associated with autosomal dominant congenital lamellar cataract. Invest Ophthalmol Vis Sci 47(3):1069–1075. https://doi.org/10.1167/iovs.05-1004
Longoni S, James P, Chiesi M (1990) Cardiac alpha-crystallin: isolation and identification. Mol Cell Biochem 97:113–120
Lutsch G, Vetter R, Offhauss U, Wieske M, Grone HJ, Klemenz R, Schimke I, Stahl J, Benndorf R (1997) Abundance and location of the small heat shock proteins HSP25 and alphaB-crystallin in rat and human heart. Circulation 96(10):3466–3476. https://doi.org/10.1161/01.CIR.96.10.3466
Maloyan A, Gulick J, Glabe CG, Kayed R, Robbins J (2007) Exercise reverses preamyloid oligomer and prolongs survival in alphaB-crystallin-based desmin-related cardiomyopathy. Proc Natl Acad Sci U S A 104(14):5995–6000. https://doi.org/10.1073/pnas.0609202104
Maloyan A, Osinska H, Lammerding J, Lee RT, Cingolani OH, Kass d, Lorenz JN, Robbins J (2009) Biochemical and mechanical dysfunction in a mouse model of desmin-related myopathy. Circ Res 104(8):1021–1028. https://doi.org/10.1161/CIRCRESAHA.108.193516
Mao YW, Liu JP, Xiang H, Li DW (2004) Human alphaA- and alphaB- crystallins bind to Bax and Bcl-X(S) to sequester their translocation during staurosporine-induced apoptosis. Cell Death Differ 11(5):512–526. https://doi.org/10.1038/sj.cdd.4401384
Maulik N, Watanabe M, YL Z et al (1996) Ischemic preconditioning triggers the activation of MAP kinases and MAPKAP kinase 2 in rat hearts. FEBS Lett 396(2-3):233–237. https://doi.org/10.1016/0014-5793(96)01109-X
McLendon PM, Ferguson BS, Osinska H, Bhuiyan MS, James J, McKinsey TA, Robbins J (2014) Tubulin hyperacetylation is adaptive in cardiac proteotoxicity by promoting autophagy. Proc Natl Acad Sci U S A 111(48):E5178–E5186. https://doi.org/10.1073/pnas.1415589111
McLendon PM, Robbins J (2011) Desmin-related cardiomyopathy: an unfolding story. Am J Physiol Heart Circ Physiol 301(4):H1220–H1228. https://doi.org/10.1152/ajpheart.00601.2011
Melkani GC, Cammarato A, Bernstein SI (2006) αBcrystallin maintains skeletal muscle myosin enzymatic activity and prevents its aggregation under heat-shock stress. J Mol Biol 3:635–645
Mercatelli N, Dimauro I, Ciafré SA, Farace MG, Caporossi D (2010) AlphaB-crystallin is involved in oxidative stress protection determined by VEGF in skeletal myoblasts. Free Radic Biol Med 49(3):374–382. https://doi.org/10.1016/j.freeradbiomed.2010.04.027
Michiel M, Skouri-Panet F, Duprat E, Simon S, Férard C, Tardieu A, Finet S (2009) Abnormal assemblies and subunit exchange of alphaB-crystallin R120 mutants could be associated with destabilization of the dimeric substructure. Biochemistry 48(2):442–453. https://doi.org/10.1021/bi8014967.
Mitra A, Basak T, Datta K, Naskar S, Sengupta S, Sarkar S (2013) Role of a-crystallin B as a regulatory switch in modulating cardiomyocyte apoptosis by mitochondria or endoplasmic reticulum during cardiac hypertrophy and myocardial infarction. Cell Death Dis 4(4):e582. https://doi.org/10.1038/cddis.2013.114
Morrison LE, Hoover HE, Thuerauf DJ, Glembotski CC (2003) Mimicking phosphorylation of αB-Crystallin on Serine-59 is necessary and sufficient to provide maximal protection of cardiac myocytes from apoptosis. Circ Res 92(2):203–211. https://doi.org/10.1161/01.RES.0000052989.83995.A5
Morrison LE, Whittaker RJ, Klepper RE, Wawrousek EF, Glembotski CC (2004) Roles for alphaB-crystallin and HSPB2 in protecting the myocardium from ischemia-reperfusion-induced damage in a KO mouse model. Am J Physiol Heart Circ Physiol 286(3):H847–H855. https://doi.org/10.1152/ajpheart.00715.2003
Mymrikov EV, Daake M, Richter B, Haslbeck M, Buchner J (2017) The chaperone activity and substrate spectrum of human small heat shock proteins. J Biol Chem 292(2):672–684. https://doi.org/10.1074/jbc.M116.760413
Mymrikov EV, Seit-Nebi AS, Gusev NB (2011) Large potentials of small heat shock proteins. Physiol Rev 91(4):1123–1159. https://doi.org/10.1152/physrev.00023.2010
N’edellec P, Edling Y, Perret E, Fardeau M, Vicart P (2002) Glucocorticoid treatment induces expression of small heat shock proteins in human satellite cell populations: consequences for a desmin-related myopathy involving the R120G alpha B-crystallin mutation. Neuromuscul Disord 12(5):457–465. https://doi.org/10.1016/S0960-8966(01)00306-6
Neppl RL, Kataoka M, Wang DZ (2014) Crystallin-αB regulates skeletal muscle homeostasis via modulation of argonaute2 activity. J Biol Chem 289(24):17240–17248. https://doi.org/10.1074/jbc.M114.549584
Nicholl ID, Quinlan RA (1994) Chaperone activity of alpha-crystallins modulates intermediate filament assembly. EMBO J 13(4):945–953
Oya-Ito T, Liu BF, Nagaraj RH (2006) Effect of methylglyoxal modification and phosphorylation on the chaperone and anti-apoptotic properties of heat shock protein 27. J Cell Biochem 99(1):279–291. https://doi.org/10.1002/jcb.20781
Pauly M, Daussin F, Burelle Y, Li T, Godin R, Fauconnier J, Koechlin-Ramonatxo C, Hugon G, Lacampagne A, Coisy-Quivy M, Liang F, Hussain S, Matecki S, Petrof BJ (2012) AMPK activation stimulates autophagy and ameliorates muscular dystrophy in the mdx mouse diaphragm. Am J Pathol 181(2):583–592. https://doi.org/10.1016/j.ajpath.2012.04.004
Pereira MB, Santos AM, Gonçalves DC et al (2015) Corrigendum: αB-crystallin interacts with and prevents stress-activated proteolysis of focal adhesion kinase by calpain in cardiomyocytes. Nat Commun 6:6508. https://doi.org/10.1038/ncomms7508
Perkins ND, Gilmore TD (2006) Good cop, bad cop: the different faces of NF-κB. Cell Death Differ 13(5):759–772. https://doi.org/10.1038/sj.cdd.4401838
Peschek J, Braun N, Rohrberg J et al (2013) Regulated structural transitions unleash the chaperone activity of aB-crystallin. Proc Natl Acad Sci U S A 110(E3780e):E3789
Pilotto A, Marziliano N, Pasotti M, Grasso M, Costante AM, Arbustini E (2006) alphaB-crystallin mutation in dilated cardiomyopathies: low prevalence in a consecutive series of 200 unrelated probands. Biochem Biophys Res Commun 346(4):1115–1117. https://doi.org/10.1016/j.bbrc.2006.05.203
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. https://doi.org/10.1161/01.CIR.0000044386.27444.5A
Pittaluga M, Sgadari A, Dimauro I, Tavazzi B, Parisi P, Caporossi D (2015) Physical exercise and redox balance in type 2 diabetics: effects of moderate training on biomarkers of oxidative stress and DNA damage evaluated through comet assay. Oxidative Med Cell Longev 2015:981242–981247. https://doi.org/10.1155/2015/981242
Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S, Massey DCO, Menzies FM, Moreau K, Narayanan U, Renna M, Siddiqi FH, Underwood BR, Winslow AR, Rubinsztein DC (2010) Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 90(4):1383–1435. https://doi.org/10.1152/physrev.00030.2009
Reddy VS, Jakhotia S, Reddy PY, Reddy GB (2015) Hyperglycemia induced expression, phosphorylation, and translocation of αB-crystallin in rat skeletal muscle. IUBMB Life 67(4):291–299. https://doi.org/10.1002/iub.1370
Reddy VS, Reddy GB (2015) Emerging role for αB-crystallin as a therapeutic agent: pros and cons. Curr Mol Med 15(1):47–61. https://doi.org/10.2174/1566524015666150114112853
Reilich P, Schoser B, Schramm N, Krause S, Schessl J, Kress W, Müller-Höcker J, Walter MC, Lochmuller H (2010) The p. G154S mutation of the Alpha-B crystallin gene (CRYAB) causes late-onset distal myopathy. Neuromuscul Disord 20(4):255–259. https://doi.org/10.1016/j.nmd.2010.01.012
Richardson P, McKenna W, Bristow M, Maisch B, Mautner B, O'Connell J, Olsen E, Thiene G, Goodwin J, Gyarfas I, Martin I, Nordet P (1996) Report of the 1995 World Health Organization/International Society and Federation of Cardiology Task Force on the definition and classification of cardiomyopathies. Circulation 93(5):841–842
Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. Mol Cell 22:253–266
Rogalla T, Ehrnsperger M, Preville X, Kotlyarov A, Lutsch G, Ducasse C, Paul C, Wieske M, Arrigo AP, Buchner J, Gaestel M (1999) Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor a by phosphorylation. J Biol Chem 274(27):18947–18956. https://doi.org/10.1074/jbc.274.27.18947
Rothbard JB, Kurnellas MP, Brownell S et al (2012) Therapeutic effects of systemic administration of chaperone aB-crystallin associated with binding proinflammatory plasma proteins. J Biol Chem 287:9708e9721
Rubinsztein DC, Codogno P, Levine B (2012) Autophagy modulation as a potential therapeutic target for diverse diseases. Nat Rev Drug Discov 11(9):709–730. https://doi.org/10.1038/nrd3802
Sacconi S, Féasson L, Antoine JC, Pécheux C, Bernard R, Cobo AM, Casarin A, Salviati L, Desnuelle C, Urtizberea A (2012) A novel CRYAB mutation resulting in multisystemic disease. Neuromuscul Disord 22(1):66–72. https://doi.org/10.1016/j.nmd.2011.07.004
Sammut IA, Harrison JC (2003) Cardiac mitochondrial complex activity is enhanced by heats hock proteins. Clin Exp Pharm Phys 30(1-2):110–115. https://doi.org/10.1046/j.1440-1681.2003.03799.x
Sanbe A, Daicho T, Mizutani R, Endo T, Miyauchi N, Yamauchi J, Tanonaka K, Glabe C, Tanoue A (2009) Protective effect of geranylgeranylacetone via enhancement of HSPB8 induction in desmin-related cardiomyopathy. PLoS One 4(4):e5351. https://doi.org/10.1371/journal.pone.0005351
Sanbe A, Osinska H, Saffitz JE, Glabe CG, Kayed R, Maloyan A, Robbins J (2004) Desmin-related cardiomyopathy in transgenic mice: a cardiac amyloidosis. Proc Natl Acad Sci U S A 101(27):10132–10136. https://doi.org/10.1073/pnas.0401900101
Satish Kumar M, Mrudula T, Mitra N, Bhanuprakash Reddy G (2004) Enhanced degradation and decreased stability of eye lens alpha-crystallin upon methylglyoxal modification. Exp Eye Res 79(4):577–583. https://doi.org/10.1016/j.exer.2004.07.003
Segard BD, Delort F, Bailleux V, Simon S, Leccia E, Gausseres B, Briki F, Vicart P, Batonnet-Pichon S (2013) N-acetyl-L-cysteine prevents stress-induced desmin aggregation in cellular models of desminopathy. PLoS One 8(10):e76361. https://doi.org/10.1371/journal.pone.0076361
Selcen D, Engel AG (2003) Myofibrillar myopathy caused by novel dominant negative alpha B-crystallin mutations. Ann Neurol 54(6):804–810. https://doi.org/10.1002/ana.10767
Sharma KK, Kumar GS, Murphy AS, Kester K (1998) Identification of 1,1′-bi(4-anilino) naphthalene-5,5′-disulfonic acid binding sequences in alpha-crystallin. J Biol Chem 273(25):15474–15478. https://doi.org/10.1074/jbc.273.25.15474
Singh BN, Rao KS, Ramakrishna T, Rangaraj N, Rao CM (2007) Association of alphaB-crystallin, a small heat shock protein, with actin: role in modulating actin filament dynamics in vivo. J Mol Biol 366(3):756–767. https://doi.org/10.1016/j.jmb.2006.12.012
Singh BN, Rao KS, Rao CM (2010) Ubiquitin–proteasome-mediated degradation and synthesis of MyoD is modulated by alphaB-crystallin, a small heat shock protein, during muscle differentiation. Biochim Biophys Acta 1803(2):288–299. https://doi.org/10.1016/j.bbamcr.2009.11.009
Smith DA, Carland CR, Guo Y, Bernstein SI (2014) Getting folded: chaperone proteins in muscle development, maintenance and disease. Anat Rec (Hoboken) 297(9):1637–1649. https://doi.org/10.1002/ar.22980
Tannous P, Zhu H, Johnstone JL, Shelton JM, Rajasekaran NS, Benjamin IJ, Nguyen L, Gerard RD, Levine B, Rothermel BA, Hill JA (2008) Autophagy is an adaptive response in desmin-related cardiomyopathy. Proc Natl Acad Sci U S A 105(28):9745–9750. https://doi.org/10.1073/pnas.0706802105
Thornell E, Aquilina A (2015) Regulation of αA- and αB-crystallins via phosphorylation in cellular homeostasis. Cell Mol Life Sci 72(21):4127–4137. https://doi.org/10.1007/s00018-015-1996-x
Treweek TM, Rekas A, Walker MJ, Carver JA (2010) A quantitative NMR spectroscopic examination of the flexibility of the C-terminal extensions of the molecular chaperones, alphaA- and alphaB-crystallin. Exp Eye Res 91(5):691–699. https://doi.org/10.1016/j.exer.2010.08.015
Tupling AR, Gramolini AO, Duhamel TA et al (2004) HSP70 binds to the fast-twitch skeletal muscle sarco(endo)plasmic reticulum Ca2þ-ATPase(SERCA1a) and prevents thermal inactivation. J Biol Chem 50:52382–52389
Tyedmers J, Mogk A, Bukau B (2010) Cellular strategies for controlling protein aggregation. Nat Rev. Mol Cell Biol 11:777–788
Vicart P, Caron A, Guicheney P, Li Z, Prévost MC, Faure A, Chateau D, Chapon F, Tomé F, Dupret JM, Paulin D, Fardeau M (1998) A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat Genet 20(1):92–95. https://doi.org/10.1038/1765
Voss OH, Batra S, Kolattukudy SJ, Gonzalez-Mejia ME, Smith JB, Doseff AI (2007) Binding of caspase-3 prodomain to heat shock protein 27 regulates monocyte apoptosis by inhibiting caspase-3 proteolytic activation. J Biol Chem 282(34):25088–25099. https://doi.org/10.1074/jbc.M701740200
Warburton DE, Nicol CW, Bredin SS (2006) Health benefits of physical activity: the evidence. CMAJ 174(6):801–809. https://doi.org/10.1503/cmaj.051351
Webster KA (2003) Serine phosphorylation and suppression of apoptosis by the small heat shock protein alphaB-crystallin. Circ Res 92(2):130–132. https://doi.org/10.1161/01.RES.0000056967.51841.21
Welch WJ (2003) Role of quality control pathways in human diseases involving protein misfolding. Semin Cell Dev Biol 15:31–38
Wu W, Lu C, Wang Y et al (2015) Novel phenotype-genotype correlations of restrictive cardiomyopathy with myosin-binding protein C (MYBPC3) gene mutations tested by next generation sequencing. Journal of the American Heart Association 4. pii:e001879
Zantema A, Vries MVD, Maasdam D, Bol S, Eb A.v.d. (1992) Heat shock protein 27 and alphaB-cristallin can form a complex, which dissociates by heat shock. J Biol Chem 267(18):12936–12941
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Dimauro, I., Antonioni, A., Mercatelli, N. et al. The role of αB-crystallin in skeletal and cardiac muscle tissues. Cell Stress and Chaperones 23, 491–505 (2018). https://doi.org/10.1007/s12192-017-0866-x
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DOI: https://doi.org/10.1007/s12192-017-0866-x