The role of αB-crystallin in skeletal and cardiac muscle tissues

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.

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

Fig. 1
Fig. 2

References

  1. 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

    PubMed  CAS  Article  Google Scholar 

  2. 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

    PubMed  CAS  Article  Google Scholar 

  3. 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

    PubMed  CAS  Article  Google Scholar 

  4. 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

    CAS  Article  Google Scholar 

  5. 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

    PubMed  CAS  Article  Google Scholar 

  6. 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

    PubMed  CAS  Article  Google Scholar 

  7. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  8. 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

    CAS  Article  Google Scholar 

  9. 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

    PubMed  CAS  Article  Google Scholar 

  10. 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

    PubMed  CAS  Article  Google Scholar 

  11. Balchin D, Hayer-Hartl M, Hartl FU (2016) In vivo aspects of protein folding and quality control. Science 353: aac4354

  12. 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

    PubMed  CAS  Article  Google Scholar 

  13. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  14. 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

    PubMed  CAS  Article  Google Scholar 

  15. 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

    PubMed  CAS  Article  Google Scholar 

  16. 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

    PubMed  CAS  Article  Google Scholar 

  17. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297. https://doi.org/10.1016/S0092-8674(04)00045-5

    PubMed  CAS  Article  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. 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

    PubMed  CAS  Article  Google Scholar 

  20. 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

    PubMed  CAS  Article  Google Scholar 

  21. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  22. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  23. 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

    PubMed  CAS  Article  Google Scholar 

  24. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  25. 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

    PubMed  Article  Google Scholar 

  26. 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

    PubMed  CAS  Google Scholar 

  27. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  28. 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

    PubMed  CAS  Article  Google Scholar 

  29. 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

    PubMed  CAS  Article  Google Scholar 

  30. 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

    PubMed  CAS  Article  Google Scholar 

  31. 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

    Article  Google Scholar 

  32. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  33. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  34. 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

    PubMed  CAS  Article  Google Scholar 

  35. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  36. 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

    PubMed  CAS  Article  Google Scholar 

  37. Chiesi M, Longoni S, Limbruno U (1990) Cardiac alpha-crystallin: involvement during heart ischemia. Mol Cell Biochem 97(2):129–136

    PubMed  CAS  Article  Google Scholar 

  38. 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

    Article  Google Scholar 

  39. 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

    PubMed  CAS  Google Scholar 

  40. 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

  41. 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

    PubMed  Article  Google Scholar 

  42. 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

    PubMed  CAS  Article  Google Scholar 

  43. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  44. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  45. 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

    CAS  Article  Google Scholar 

  46. 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

    PubMed  PubMed Central  Article  Google Scholar 

  47. 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

    PubMed  CAS  Article  Google Scholar 

  48. 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

    CAS  Article  Google Scholar 

  49. 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.

  50. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  51. 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

    PubMed  CAS  Article  Google Scholar 

  52. 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

    PubMed  CAS  Article  Google Scholar 

  53. 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

    PubMed  CAS  Article  Google Scholar 

  54. 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

    PubMed  CAS  Article  Google Scholar 

  55. 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

    Article  Google Scholar 

  56. 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

    PubMed  CAS  Article  Google Scholar 

  57. 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

    PubMed  PubMed Central  Article  Google Scholar 

  58. 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

    PubMed  CAS  Article  Google Scholar 

  59. 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

    PubMed  CAS  Article  Google Scholar 

  60. 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

    PubMed  Article  Google Scholar 

  61. 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

    PubMed  CAS  Article  Google Scholar 

  62. 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

    PubMed  CAS  Article  Google Scholar 

  63. 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

    Article  Google Scholar 

  64. 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

    PubMed  CAS  Article  Google Scholar 

  65. 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

    PubMed  CAS  Article  Google Scholar 

  66. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  67. 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

    PubMed  CAS  Article  Google Scholar 

  68. 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

    PubMed  CAS  Article  Google Scholar 

  69. 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

    PubMed  CAS  Article  Google Scholar 

  70. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  71. 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

    PubMed  CAS  Article  Google Scholar 

  72. 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

    PubMed  CAS  Article  Google Scholar 

  73. 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

    PubMed  CAS  Article  Google Scholar 

  74. 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

  75. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  76. 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

    PubMed  CAS  Article  Google Scholar 

  77. 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.

  78. 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

    Article  Google Scholar 

  79. 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

    PubMed  CAS  Article  Google Scholar 

  80. 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

    PubMed  CAS  Article  Google Scholar 

  81. 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

    PubMed  CAS  Article  Google Scholar 

  82. 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

    CAS  Article  Google Scholar 

  83. 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

    PubMed  PubMed Central  Article  Google Scholar 

  84. 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

    PubMed  CAS  Article  Google Scholar 

  85. 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

    PubMed  PubMed Central  Article  Google Scholar 

  86. 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

    PubMed  CAS  Article  Google Scholar 

  87. 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

    PubMed  CAS  Article  Google Scholar 

  88. 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

    PubMed  CAS  Article  Google Scholar 

  89. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  90. 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

    PubMed  CAS  Article  Google Scholar 

  91. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  92. 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

    CAS  Article  Google Scholar 

  93. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  94. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  95. 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

    PubMed  CAS  Article  Google Scholar 

  96. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  97. 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

    PubMed  CAS  Article  Google Scholar 

  98. 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

    PubMed  PubMed Central  Article  Google Scholar 

  99. Longoni S, James P, Chiesi M (1990) Cardiac alpha-crystallin: isolation and identification. Mol Cell Biochem 97:113–120

    CAS  Article  Google Scholar 

  100. 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

    PubMed  CAS  Article  Google Scholar 

  101. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  102. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  103. 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

    PubMed  CAS  Article  Google Scholar 

  104. 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

    PubMed  CAS  Article  Google Scholar 

  105. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  106. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  107. 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

    Article  Google Scholar 

  108. 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

    PubMed  CAS  Article  Google Scholar 

  109. 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.

    PubMed  CAS  Article  Google Scholar 

  110. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  111. 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

    PubMed  CAS  Article  Google Scholar 

  112. 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

    PubMed  CAS  Article  Google Scholar 

  113. 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

    PubMed  CAS  Article  Google Scholar 

  114. 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

    PubMed  CAS  Article  Google Scholar 

  115. 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

    Article  Google Scholar 

  116. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  117. Nicholl ID, Quinlan RA (1994) Chaperone activity of alpha-crystallins modulates intermediate filament assembly. EMBO J 13(4):945–953

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  118. 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

    PubMed  CAS  Article  Google Scholar 

  119. 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

    PubMed  CAS  Article  Google Scholar 

  120. 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

    PubMed  CAS  Article  Google Scholar 

  121. 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

    PubMed  CAS  Article  Google Scholar 

  122. 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

    Google Scholar 

  123. 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

    PubMed  CAS  Article  Google Scholar 

  124. 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

    PubMed  CAS  Article  Google Scholar 

  125. 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

    Article  Google Scholar 

  126. 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

    PubMed  CAS  Article  Google Scholar 

  127. 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

    PubMed  CAS  Article  Google Scholar 

  128. 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

    PubMed  CAS  Article  Google Scholar 

  129. 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

    PubMed  Article  Google Scholar 

  130. 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

    PubMed  CAS  Article  Google Scholar 

  131. Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. Mol Cell 22:253–266

    Article  Google Scholar 

  132. 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

    PubMed  CAS  Article  Google Scholar 

  133. 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

    Article  Google Scholar 

  134. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  135. 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

    PubMed  Article  Google Scholar 

  136. 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

    CAS  Article  Google Scholar 

  137. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  138. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  139. 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

    PubMed  CAS  Article  Google Scholar 

  140. 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

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  141. 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

    PubMed  CAS  Article  Google Scholar 

  142. 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

    PubMed  CAS  Article  Google Scholar 

  143. 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

    PubMed  CAS  Article  Google Scholar 

  144. 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

    PubMed  CAS  Article  Google Scholar 

  145. 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

    CAS  Article  Google Scholar 

  146. 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

    PubMed  PubMed Central  Article  Google Scholar 

  147. 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

    PubMed  CAS  Article  Google Scholar 

  148. 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

    PubMed  CAS  Article  Google Scholar 

  149. 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

    Article  Google Scholar 

  150. Tyedmers J, Mogk A, Bukau B (2010) Cellular strategies for controlling protein aggregation. Nat Rev. Mol Cell Biol 11:777–788

    PubMed  CAS  Article  Google Scholar 

  151. 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

    PubMed  CAS  Article  Google Scholar 

  152. 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

    PubMed  CAS  Article  Google Scholar 

  153. 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

    PubMed  PubMed Central  Article  Google Scholar 

  154. 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

    PubMed  CAS  Article  Google Scholar 

  155. Welch WJ (2003) Role of quality control pathways in human diseases involving protein misfolding. Semin Cell Dev Biol 15:31–38

    Article  Google Scholar 

  156. 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

  157. 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

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr. Timothy Pearson for the English revision.

Funding

The work has been supported by grant from University of Rome Foro Italico, Research Grant 2015.

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Ivan Dimauro or Daniela Caporossi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Keywords

  • Heat shock proteins
  • Disease
  • Physical activity
  • Chaperones
  • Crystallinopathies