Introduction to small heat shock proteins

Small Stress Proteins and Human Diseases

Volumn , Issue , 2011, Pages 1-27

  van de Schootbrugge, Chantal ^a   Boelens, Wilbert C ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84895257192     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Editorial

References (187)

1. de Jong WW, Caspers GJ, Leunissen JA. Genealogy of the alpha-crystallin-small heat-shock protein superfamily. Int J Biol Macromol. 1998; 22(3-4):151-162.
2. Kappe G, Leunissen JA, de Jong WW. Evolution and diversity of prokaryotic small heat shock proteins. Prog Mol Subcell Biol. 2002; 28:1-17.
3. de Jong WW, Leunissen JA, Voorter CE. Evolution of the alpha-crystallin/small heat-shock protein family. Mol Biol Evol. 1993; 10(1):103-126.
4. Kappe G, Franck E, Verschuure P, Boelens WC, Leunissen JA, de Jong WW. The human genome encodes 10 alpha-crystallin-related small heat shock proteins: HspB1-10. Cell Stress Chaperones, 2003; 8(1):53-61.
5. Fontaine JM, Rest JS, Welsh MJ, Benndorf R. The sperm outer dense fiber protein is the 10th member of the superfamily of mammalian small stress proteins. Cell Stress & Chaperones, 2003; 8(1):62-69.
6. Kato K, Shinohara H, Kurobe N, Goto S, Inaguma Y, Ohshima K. Immunoreactive alpha A crystallin in rat non-lenticular tissues detected with a sensitive immunoassay method. Biochim Biophys Acta, 1991; 1080(2):173-180.
7. Mörner CT. Untersuchung der Proteinsubstanzen in den sichtbrechenden Medien de Auges. Hoppe-Seyler's Z Physiol.Chemie. 18, 16. 1894.
8. van der Ouderaa FJ, de Jong WW, Groenendijk GW, Bloemendal H. Sequence of the first 68 residues of the alpha B2 chain of bovine alpha-crystallin. Biochem Biophys Res Commun. 1974; 57(1):112-119.
9. van der Ouderaa FJ, de Jong WW, Bloemendal H. The amino-acid sequence of the alphaA2 chain of bovine alpha-crystallin. Eur J Biochem. 1973; 39(1):207-222.
10. Ingolia TD, Craig EA. Four small Drosophila heat shock proteins are related to each other and to mammalian alpha-crystallin. Proc Natl Acad Sci U S A, 1982; 79(7):2360-2364.
11. Horwitz J. Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci U S A, 1992; 89(21):10449-10453.
12. Bellyei S, Szigeti A, Pozsgai E, Boronkai A, Gomori E, Hocsak E et al. Preventing apoptotic cell death by a novel small heat shock protein. Eur J Cell Biol. 2007; 86(3):161-171.
13. Gough J, Karplus K, Hughey R, Chothia C. Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol. 2001; 313(4):903-919.
14. Ramelot TA, Raman S, Kuzin AP, Xiao R, Ma LC, Acton TB et al. Improving NMR protein structure quality by Rosetta refinement: a molecular replacement study. Proteins, 2009; 75(1):147-167.
15. Pasta SY, Raman B, Ramakrishna T, Rao C. The IXI/V motif in the C-terminal extension of alpha-crystallins: alternative interactions and oligomeric assemblies. Mol Vis. 2004; 10:655-662.
16. Pasta SY, Raman B, Ramakrishna T, Rao C. Role of the conserved SRLFDQFFG region of alpha-crystallin, a small heat shock protein. Effect on oligomeric size, subunit exchange, and chaperone-like activity. J Biol Chem. 2003; 278(51):51159-51166.
17. Iwaki A, Nagano T, Nakagawa M, Iwaki T, Fukumaki Y. Identification and characterization of the gene encoding a new member of the alpha-crystallin/small hsp family, closely linked to the alphaB-crystallin gene in a head-to-head manner. Genomics, 1997; 45(2):386-394.
18. Elicker KS, Hutson LD. Genome-wide analysis and expression profiling of the small heat shock proteins in zebrafish. Gene, 2007; 403(1-2):60-69.
19. Franck E, Madsen O, van Rheede T, Ricard G, Huynen MA, de Jong WW. Evolutionary diversity of vertebrate small heat shock proteins. J Mol Evol. 2004; 59(6):792-805.
20. Gusev NB, Bogatcheva NV, Marston SB. Structure and properties of small heat shock proteins (sHsp) and their interaction with cytoskeleton proteins. Biochemistry, (Mosc) 2002; 67(5):511-519.
21. van den Oetelaar PJ, van Someren PF, Thomson JA, Siezen RJ, Hoenders HJ. A dynamic quaternary structure of bovine alpha-crystallin as indicated from intermolecular exchange of subunits. Biochemistry, 1990; 29(14):3488-3493.
22. Bova MP, Ding LL, Horwitz J, Fung BK. Subunit exchange of alphaA-crystallin. J Biol Chem. 1997; 272(47):29511-29517.
23. Koteiche HA, Mchaourab HS. Folding pattern of the alpha-crystallin domain in alphaA-crystallin determined by site-directed spin labeling. J Mol Biol. 1999; 294(2):561-577.
24. Jehle S, van Rossum B, Stout JR, Noguchi SM, Falber K, Rehbein K et al. alphaB-crystallin: a hybrid solid-state/solution-state NMR investigation reveals structural aspects of the heterogeneous oligomer. J Mol Biol. 2009; 385(5):1481-1497.
25. Kim KK, Kim R, Kim SH. Crystal structure of a small heat-shock protein. Nature, 1998; 394(6693):595-599.
26. van Montfort RL, Basha E, Friedrich KL, Slingsby C, Vierling E. Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Biol. 2001; 8(12):1025-1030.
27. Stamler R, Kappe G, Boelens W, Slingsby C. Wrapping the alpha-crystallin domain fold in a chaperone assembly. J Mol Biol. 2005; 353(1):68-79.
28. Morris AM, Treweek TM, Aquilina JA, Carver JA, Walker MJ. Glutamic acid residues in the C-terminal extension of small heat shock protein 25 are critical for structural and functional integrity. FEBS J. 2008; 275(23):5885-5898.
29. Li Y, Schmitz KR, Salerno JC, Koretz JF. The role of the conserved COOH-terminal triad in alphaA-crystallin aggregation and functionality. Mol Vis. 2007; 13:1758-1768.
30. Saji H, Iizuka R, Yoshida T, Abe T, Kidokoro S, Ishii N et al. Role of the IXI/V motif in oligomer assembly and function of StHsp14.0, a small heat shock protein from the acidothermophilic archaeon, Sulfolobus tokodaii strain 7. Proteins, 2008; 71(2):771-782.
31. Kennaway CK, Benesch JL, Gohlke U, Wang L, Robinson CV, Orlova EV et al. Dodecameric structure of the small heat shock protein Acr1 from Mycobacterium tuberculosis. J Biol Chem. 2005; 280(39):33419-33425.
32. Haslbeck M, Kastenmuller A, Buchner J, Weinkauf S, Braun N. Structural dynamics of archaeal small heat shock proteins. J Mol Biol. 2008; 378(2):362-374.
33. White HE, Orlova EV, Chen S, Wang L, Ignatiou A, Gowen B et al. Multiple distinct assemblies reveal conformational flexibility in the small heat shock protein Hsp26. Structure, 2006; 14(7):1197-1204.
34. Carver JA, Aquilina JA, Truscott RJ, Ralston GB. Identification by 1H NMR spectroscopy of flexible C-terminal extensions in bovine lens alpha-crystallin. FEBS Lett. 1992; 311(2):143-149.
35. Haslbeck M, Franzmann T, Weinfurtner D, Buchner J. Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol. 2005; 12(10):842-846.
36. Haley DA, Bova MP, Huang QL, Mchaourab HS, Stewart PL. Small heat-shock protein structures reveal a continuum from symmetric to variable assemblies. J Mol Biol. 2000; 298(2):261-272.
37. Benesch JL, Ayoub M, Robinson CV, Aquilina JA. Small heat shock protein activity is regulated by variable oligomeric substructure. J Biol Chem. 2008; 283(42):28513-28517.
38. Wang K, Spector A. The chaperone activity of bovine alpha crystallin. Interaction with other lens crystallins in native and denatured states. J Biol Chem. 1994; 269(18):13601-13608.
39. Dillmann WH. Small heat shock proteins and protection against injury. Ann N Y Acad Sci. 1999; 874:66-68.
40. Verschuure P, Tatard C, Boelens WC, Grongnet JF, David JC. Expression of small heat shock proteins HspB2, HspB8, Hsp20 and cvHsp in different tissues of the perinatal developing pig. Eur J Cell Biol. 2003; 82(10):523-530.
41. Tallot P, Grongnet JF, David JC. Dual perinatal and developmental expression of the small heat shock proteins [FC12]aB-crystallin and Hsp27 in different tissues of the developing piglet. Biol Neonate. 2003; 83(4):281-288.
42. van de Klundert FA, Gijsen ML, van den Ijssel PR, Snoeckx LH, de Jong WW. alpha B-crystallin and hsp25 in neonatal cardiac cells--differences in cellular localization under stress conditions. Eur J Cell Biol. 1998; 75(1):38-45.
43. Simkhovich BZ, Marjoram P, Poizat C, Kedes L, Kloner RA. Brief episode of ischemia activates protective genetic program in rat heart: a gene chip study. Cardiovasc Res. 2003; 59(2):450-459.
44. Lutsch G, Vetter R, Offhauss U, Wieske M, Grone HJ, Klemenz R et al. Abundance and location of the small heat shock proteins HSP25 and alphaB-crystallin in rat and human heart. Circulation, 1997; 96(10):3466-3476.
45. Ciocca DR, Oesterreich S, Chamness GC, McGuire WL, Fuqua SA. Biological and clinical implications of heat shock protein 27,000 (Hsp27): a review. J Natl Cancer Inst. 1993; 85(19):1558-1570.
46. Efthymiou CA, Mocanu MM, de Belleroche J, Wells DJ, Latchmann DS, Yellon DM. Heat shock protein 27 protects the heart against myocardial infarction. Basic Res Cardiol. 2004; 99(6):392-394.
47. Srinivasan AN, Nagineni CN, Bhat SP. alpha A-crystallin is expressed in non-ocular tissues. J Biol Chem. 1992; 267(32):23337-23341.
48. Egwuagu CE, Chepelinsky AB. Extralenticular expression of the alpha A-crystallin promoter/gamma interferon transgene. Exp Eye Res. 1997; 64(3):491-495.
49. Dubin RA, Wawrousek EF, Piatigorsky J. Expression of the murine alpha B-crystallin gene is not restricted to the lens. Mol Cell Biol. 1989; 9(3):1083-1091.
50. Bhat SP, Nagineni CN. alpha B subunit of lens-specific protein alpha-crystallin is present in other ocular and non-ocular tissues. Biochem Biophys Res Commun. 1989; 158(1):319-325.
51. Lam WY, Wing Tsui SK, Law PT, Luk SC, Fung KP, Lee CY et al. Isolation and characterization of a human heart cDNA encoding a new member of the small heat shock protein family--HSPL27. Biochim Biophys Acta, 1996; 1314(1-2):120-124.
52. Sugiyama Y, Suzuki A, Kishikawa M, Akutsu R, Hirose T, Waye MM et al. Muscle develops a specific form of small heat shock protein complex composed of MKBP/HSPB2 and HSPB3 during myogenic differentiation. J Biol Chem. 2000; 275(2):1095-1104.
53. Golenhofen N, Perng MD, Quinlan RA, Drenckhahn D. Comparison of the small heat shock proteins alphaB-crystallin, MKBP, HSP25, HSP20, and cvHSP in heart and skeletal muscle. Histochem Cell Biol. 2004; 122(5):415-425.
54. Swamynathan SK, Piatigorsky J. Regulation of the mouse alphaB-crystallin and MKBP/HspB2 promoter activities by shared and gene specific intergenic elements: the importance of context dependency. Int J Dev Biol. 2007; 51(8):689-700.
55. Doerwald L, van Rheede T, Dirks RP, Madsen O, Rexwinkel R, van Genesen ST et al. Sequence and functional conservation of the intergenic region between the head-to-head genes encoding the small heat shock proteins alphaB-crystallin and HspB2 in the mammalian lineage. J Mol Evol. 2004; 59(5):674-686.
56. Taylor RP, Benjamin IJ. Small heat shock proteins: a new classification scheme in mammals. J Mol Cell Cardiol. 2005; 38(3):433-444.
57. Louapre P, Grongnet JF, Tanguay RM, David JC. Effects of hypoxia on stress proteins in the piglet heart at birth. Cell Stress Chaperones, 2005; 10(1):17-23.
58. Nefti O, Grongnet JF, David JC. Overexpression of alphaB crystallin in the gastrointestinal tract of the newborn piglet after hypoxia. Shock, 2005; 24(5):455-461.
59. Golenhofen N, Ness W, Wawrousek EF, Drenckhahn D. Expression and induction of the stress protein alpha-B-crystallin in vascular endothelial cells. Histochem Cell Biol. 2002; 117(3):203-209.
60. Yu AL, Fuchshofer R, Birke M, Priglinger SG, Eibl KH, Kampik A et al. Hypoxia/reoxygenation and TGF-beta increase alphaB-crystallin expression in human optic nerve head astrocytes. Exp Eye Res. 2007; 84(4):694-706.
61. Omar R, Pappolla M. Oxygen free radicals as inducers of heat shock protein synthesis in cultured human neuroblastoma cells: relevance to neurodegenerative disease. Eur Arch Psychiatry Clin Neurosci. 1993; 242(5):262-267.
62. Hawse JR, Cumming JR, Oppermann B, Sheets NL, Reddy VN, Kantorow M. Activation of metallothioneins and alpha-crystallin/sHSPs in human lens epithelial cells by specific metals and the metal content of aging clear human lenses. Invest Ophthalmol Vis Sci 2003; 44(2):672-679.
63. Boluyt MO, Brevick JL, Rogers DS, Randall MJ, Scalia AF, Li ZB. Changes in the rat heart proteome induced by exercise training: Increased abundance of heat shock protein hsp20. Proteomics, 2006; 6(10):3154-3169.
64. Vissing K, Bayer ML, Overgaard K, Schjerling P, Raastad T. Heat shock protein translocation and expression response is attenuated in response to repeated eccentric exercise. Acta Physiol. (Oxf) 2008.
65. Wilhelmus MM, Otte-Holler I, Wesseling P, de Waal RM, Boelens WC, Verbeek MM. Specific association of small heat shock proteins with the pathological hallmarks of Alzheimer's disease brains. Neuropathol Appl Neurobiol. 2006; 32(2):119-130.
66. Wang J, Martin E, Gonzales V, Borchelt DR, Lee MK. Differential regulation of small heat shock proteins in transgenic mouse models of neurodegenerative diseases. Neurobiol Aging, 2008; 29(4):586-597.
67. Arrigo AP, Simon S, Gibert B, Kretz-Remy C, Nivon M, Czekalla A et al. Hsp27 (HspB1) and alphaB-crystallin (HspB5) as therapeutic targets. FEBS Lett. 2007; 581(19):3665-3674.
68. Hishiya A, Takayama S. Molecular chaperones as regulators of cell death. Oncogene. 2008; 27(50):6489-6506.
69. Aggeli IK, Beis I, Gaitanaki C. Oxidative stress and calpain inhibition induce alpha B-crystallin phosphorylation via p38-MAPK and calcium signalling pathways in H9c2 cells. Cell Signal, 2008; 20(7):1292-1302.
70. Golenhofen N, Ness W, Koob R, Htun P, Schaper W, Drenckhahn D. Ischemia-induced phosphorylation and translocation of stress protein alpha B-crystallin to Z lines of myocardium. Am J Physiol. 1998; 274(5 Pt 2):H1457-H1464.
71. Ito H, Okamoto K, Nakayama H, Isobe T, Kato K. Phosphorylation of alphaB-crystallin in response to various types of stress. J Biol Chem. 1997; 272(47):29934-29941.
72. Landry J, Lambert H, Zhou M, Lavoie JN, Hickey E, Weber LA et al. Human HSP27 is phosphorylated at serines 78 and 82 by heat shock and mitogen-activated kinases that recognize the same amino acid motif as S6 kinase II. J Biol Chem. 1992; 267(2):794-803.
73. Kato K, Ito H, Kamei K, Inaguma Y, Iwamoto I, Saga S. Phosphorylation of alphaB-crystallin in mitotic cells and identification of enzymatic activities responsible for phosphorylation. J Biol Chem. 1998; 273(43):28346-28354.
74. Beall A, Bagwell D, Woodrum D, Stoming TA, Kato K, Suzuki A et al. The small heat shock-related protein, HSP20, is phosphorylated on serine 16 during cyclic nucleotide-dependent relaxation. J Biol Chem. 1999; 274(16):11344-11351.
75. Shemetov AA, Seit-Nebi AS, Bukach OV, Gusev NB. Phosphorylation by cyclic AMP-dependent protein kinase inhibits chaperone-like activity of human HSP22 in vitro. Biochemistry-Moscow, 2008; 73(2):200-208.
76. Rosales JL, Sarker K, Ho N, Broniewska M, Wong P, Cheng M et al. ODF1 phosphorylation by Cdk5/p35 enhances ODF1-OIP1 interaction. Cell Physiol Biochem. 2007; 20(5):311-318.
77. Kato K, Hasegawa K, Goto S, Inaguma Y. Dissociation as a result of phosphorylation of an aggregated form of the small stress protein, hsp27. J Biol Chem. 1994; 269(15):11274-11278.
78. Ito H, Kamei K, Iwamoto I, Inaguma Y, Nohara D, Kato K. Phosphorylation-induced change of the oligomerization state of alpha B-crystallin. J Biol Chem. 2001; 276(7):5346-5352.
79. Benndorf R, Hayess K, Ryazantsev S, Wieske M, Behlke J, Lutsch G. Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J Biol Chem. 1994; 269(32):20780-20784.
80. Lavoie JN, Gingras-Breton G, Tanguay RM, Landry J. Induction of Chinese hamster HSP27 gene expression in mouse cells confers resistance to heat shock. HSP27 stabilization of the microfilament organization. J Biol Chem. 1993; 268(5):3420-3429.
81. Ahmad MF, Raman B, Ramakrishna T, Rao C. Effect of phosphorylation on alpha B-crystallin: differences in stability, subunit exchange and chaperone activity of homo and mixed oligomers of alpha B-crystallin and its phosphorylation-mimicking mutant. J Mol Biol. 2008; 375(4):1040-1051.
82. den Engelsman J, Bennink EJ, Doerwald L, Onnekink C, Wunderink L, Andley UP et al. Mimicking phosphorylation of the small heat-shock protein alphaB-crystallin recruits the F-box protein FBX4 to nuclear SC35 speckles. Eur J Biochem. 2004; 271(21):4195-4203.
83. Bryantsev AL, Kurchashova SY, Golyshev SA, Polyakov VY, Wunderink HF, Kanon B et al. Regulation of stress-induced intracellular sorting and chaperone function of Hsp27 (HspB1) in mammalian cells. Biochem J. 2007; 407(3):407-417.
84. Bryantsev AL, Chechenova MB, Shelden EA. Recruitment of phosphorylated small heat shock protein Hsp27 to nuclear speckles without stress. Exp Cell Res. 2007; 313(1):195-209.
85. Maddala R, Rao VP. alpha-Crystallin localizes to the leading edges of migrating lens epithelial cells. Exp Cell Res. 2005; 306(1):203-215.
86. Launay N, Goudeau B, Kato K, Vicart P, Lilienbaum A. Cell signaling pathways to alphaB-crystallin following stresses of the cytoskeleton. Exp Cell Res. 2006; 312(18):3570-3584.
87. Flynn CR, Smoke CC, Furnish E, Komalavilas P, Thresher J, Yi Z et al. Phosphorylation and activation of a transducible recombinant form of human HSP20 in Escherichia coli. Protein Expr Purif. 2007; 52(1):50-58.
88. Gupta R, Srivastava OP. Deamidation affects structural and functional properties of human alphaA-crystallin and its oligomerization with alphaB-crystallin. J Biol Chem. 2004; 279(43):44258-44269.
89. Kamei A, Iwase H, Masuda K. Cleavage of amino acid residue(s) from the N-terminal region of alpha A- and alpha B-crystallins in human crystalline lens during aging. Biochem Biophys Res Commun. 1997; 231(2):373-378.
90. Takeuchi N, Ouchida A, Kamei A. C-terminal truncation of alpha-crystallin in hereditary cataractous rat lens. Biol Pharm Bull. 2004; 27(3):308-314.
91. Chen SJ, Sun TX, Akhtar NJ, Liang JJ. Oxidation of human lens recombinant alphaA-crystallin and cysteine-deficient mutants. J Mol Biol. 2001; 305(4):969-976.
92. Blakytny R, Carver JA, Harding JJ, Kilby GW, Sheil MM. A spectroscopic study of glycated bovine alpha-crystallin: investigation of flexibility of the C-terminal extension, chaperone activity and evidence for diglycation. Biochim Biophys Acta, 1997; 1343(2):299-315.
93. Nagaraj RH, Oya-Ito T, Padayatti PS, Kumar R, Mehta S, West K et al. Enhancement of chaperone function of alpha-crystallin by methylglyoxal modification. Biochemistry, 2003; 42(36):10746-10755.
94. Satish KM, Mrudula T, Mitra N, Bhanuprakash RG. Enhanced degradation and decreased stability of eye lens alpha-crystallin upon methylglyoxal modification. Exp Eye Res. 2004; 79(4):577-583.
95. Seidler NW, Yeargans GS, Morgan TG. Carnosine disaggregates glycated alpha-crystallin: an in vitro study. Arch Biochem Biophys. 2004; 427(1):110-115.
96. Fujii N, Matsumoto S, Hiroki K, Takemoto L. Inversion and isomerization of Asp-58 residue in human alphaA-crystallin from normal aged lenses and cataractous lenses. Biochim Biophys Acta, 2001; 1549(2):179-187.
97. Stromer T, Ehrnsperger M, Gaestel M, Buchner J. Analysis of the interaction of small heat shock proteins with unfolding proteins. J Biol Chem. 2003; 278(20):18015-18021.
98. Cuesta R, Laroia G, Schneider RJ. Chaperone hsp27 inhibits translation during heat shock by binding eIF4G and facilitating dissociation of cap-initiation complexes. Genes Dev 2000; 14(12):1460-1470.
99. Quinlan RA, Brenner M, Goldman JE, Messing A. GFAP and its role in Alexander disease. Exp Cell Res 2007; 313(10):2077-2087.
100. Outeiro TF, Klucken J, Strathearn KE, Liu F, Nguyen P, Rochet JC et al. Small heat shock proteins protect against alpha-synuclein-induced toxicity and aggregation. Biochem Biophys Res Commun. 2006; 351(3):631-638.
101. Sharma MC, Goebel HH. Protein aggregate myopathies. Neurol India, 2005; 53(3):273-279.
102. Lee GJ, Vierling E. A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol. 2000; 122(1):189-198.
103. Matuszewska M, Kuczynska-Wisnik D, Laskowska E, Liberek K. The small heat shock protein IbpA of Escherichia coli cooperates with IbpB in stabilization of thermally aggregated proteins in a disaggregation competent state. J Biol Chem. 2005; 280(13):12292-12298.
104. Mogk A, Deuerling E, Vorderwulbecke S, Vierling E, Bukau B. Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol Microbiol. 2003; 50(2):585-595.
105. Haslbeck M, Miess A, Stromer T, Walter S, Buchner J. Disassembling protein aggregates in the yeast cytosol. The cooperation of Hsp26 with Ssa1 and Hsp104. J Biol Chem. 2005; 280(25):23861-23868.
106. Cashikar AG, Duennwald M, Lindquist SL. A chaperone pathway in protein disaggregation. Hsp26 alters the nature of protein aggregates to facilitate reactivation by Hsp104. J Biol Chem. 2005; 280(25):23869-23875.
107. Kato K, Goto S, Inaguma Y, Hasegawa K, Morishita R, Asano T. Purification and characterization of a 20-kDa protein that is highly homologous to alpha B crystallin. J Biol Chem. 1994; 269(21):15302-15309.
108. Bukach OV, Glukhova AE, Seit-Nebi AS, Gusev NB. Heterooligomeric complexes formed by human small heat shock proteins HspB1 (Hsp27) and HspB6 (Hsp20). Biochim Biophys Acta, 2008.
109. Zantema A, Verlaan-De Vries M, Maasdam D, Bol S, van der EA. Heat shock protein 27 and alpha B-crystallin can form a complex, which dissociates by heat shock. J Biol Chem. 1992; 267(18):12936-12941.
110. Sun X, Welsh MJ, Benndorf R. Conformational changes resulting from pseudophosphorylation of mammalian small heat shock proteins--a two-hybrid study. Cell Stress Chaperones, 2006; 11(1):61-70.
111. Lelj-Garolla B, Mauk AG. Self-association and chaperone activity of Hsp27 are thermally activated. J Biol Chem. 2006; 281(12):8169-8174.
112. Wang X, Klevitsky R, Huang W, Glasford J, Li F, Robbins J. AlphaB-crystallin modulates protein aggregation of abnormal desmin. Circ Res. 2003; 93(10):998-1005.
113. Panasenko OO, Kim MV, Marston SB, Gusev NB. Interaction of the small heat shock protein with molecular mass 25 kDa (hsp25) with actin. Eur J Biochem. 2003; 270(5):892-901.
114. Mounier N, Arrigo AP. Actin cytoskeleton and small heat shock proteins: how do they interact? Cell Stress Chaperones, 2002; 7(2):167-176.
115. Sun Y, MacRae TH. Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci. 2005; 62(21):2460-2476.
116. Brown DD, Christine KS, Showell C, Conlon FL. Small heat shock protein Hsp27 is required for proper heart tube formation. Genesis, 2007; 45(11):667-678.
117. Tessier DJ, Komalavilas P, Panitch A, Joshi L, Brophy CM. The small heat shock protein (HSP) 20 is dynamically associated with the actin cross-linking protein actinin. J Surg Res. 2003; 111(1):152-157.
118. Perng MD, Cairns L, van den IJ, Prescott A, Hutcheson AM, Quinlan RA. Intermediate filament interactions can be altered by HSP27 and alphaB-crystallin. J Cell Sci. 1999; 112 (Pt 13):2099-2112.
119. Bennardini F, Wrzosek A, Chiesi M. Alpha B-crystallin in cardiac tissue. Association with actin and desmin filaments. Circ Res. 1992; 71(2):288-294.
120. Nicholl ID, Quinlan RA. Chaperone activity of alpha-crystallins modulates intermediate filament assembly. EMBO J. 1994; 13(4):945-953.
121. Bova MP, Yaron O, Huang Q, Ding L, Haley DA, Stewart PL et al. 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, 1999; 96(11):6137-6142.
122. Vicart P, Caron A, Guicheney P, Li Z, Prevost MC, Faure A et al. A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat Genet. 1998; 20(1):92-95.
123. Hagemann TL, Boelens WC, Wawrousek EF, Messing A. Suppression of GFAP toxicity by {alpha}B-crystallin in mouse models of Alexander disease. Hum Mol Genet. 2009.
124. Arai H, Atomi Y. Chaperone activity of alpha B-crystallin suppresses tubulin aggregation through complex formation. Cell Struct Funct. 1997; 22(5):539-544.
125. Kato K, Ito H, Inaguma Y, Okamoto K, Saga S. Synthesis and accumulation of alphaB crystallin in C6 glioma cells is induced by agents that promote the disassembly of microtubules. J Biol Chem. 1996; 271(43):26989-26994.
126. Xi JH, Bai F, McGaha R, Andley UP. Alpha-crystallin expression affects microtubule assembly and prevents their aggregation. FASEB J. 2006; 20(7):846-857.
127. Bruey JM, Ducasse C, Bonniaud P, Ravagnan L, Susin SA, Diaz-Latoud C et al. Hsp27 negatively regulates cell death by interacting with cytochrome c. Nat Cell Biol. 2000; 2(9):645-652.
128. Pandey P, Farber R, Nakazawa A, Kumar S, Bharti A, Nalin C et al. Hsp27 functions as a negative regulator of cytochrome c-dependent activation of procaspase-3. Oncogene. 2000; 19(16):1975-1981.
129. Charette SJ, Lavoie JN, Lambert H, Landry J. Inhibition of Daxx-mediated apoptosis by heat shock protein 27. Mol Cell Biol. 2000; 20(20):7602-7612.
130. Mao YW, Liu JP, Xiang H, Li DW. Human alphaA- and alphaB-crystallins bind to Bax and Bcl-X(S) to sequester their translocation during staurosporine-induced apoptosis. Cell Death Differ. 2004; 11(5):512-526.
131. Kamradt MC, Chen F, Cryns VL. 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. 2001; 276(19):16059-16063.
132. Stegh AH, Kesari S, Mahoney JE, Jenq HT, Forloney KL, Protopopov A et al. Bcl2L12-mediated inhibition of effector caspase-3 and caspase-7 via distinct mechanisms in glioblastoma. Proc Natl Acad Sci U S A, 2008; 105(31):10703-10708.
133. Nicolaou P, Knoll R, Haghighi K, Fan GC, Dorn GW, Hasenfub G et al. Human mutation in the anti-apoptotic heat shock protein 20 abrogates its cardioprotective effects. J Biol Chem. 2008; 283(48):33465-33471.
134. Shemetov AA, Seit-Nebi AS, Gusev NB. Structure, properties, and functions of the human small heat-shock protein HSP22 (HspB8, H11, E2IG1): a critical review. J Neurosci Res. 2008; 86(2):264-269.
135. Sui X, Li D, Qiu H, Gaussin V, Depre C. Activation of the bone morphogenetic protein receptor by H11kinase/Hsp22 promotes cardiac cell growth and survival. Circ Res. 2009; 104(7):887-895.
136. den Engelsman J, Keijsers V, de Jong WW, Boelens WC. The small heat-shock protein alpha B-crystallin promotes FBX4-dependent ubiquitination. J Biol Chem. 2003; 278(7):4699-4704.
137. Boelens WC, Croes Y, de Jong WW. Interaction between alphaB-crystallin and the human 20S proteasomal subunit C8/alpha7. Biochim Biophys Acta, 2001; 1544(1-2):311-319.
138. Lin DI, Barbash O, Kumar KG, Weber JD, Harper JW, Klein-Szanto AJ et al. Phosphorylation-dependent ubiquitination of cyclin D1 by the SCF(FBX4-alphaB crystallin) complex. Mol Cell, 2006; 24(3):355-366.
139. Parcellier A, Brunet M, Schmitt E, Col E, Didelot C, Hammann A et al. HSP27 favors ubiquitination and proteasomal degradation of p27Kip1 and helps S-phase re-entry in stressed cells. FASEB J. 2006; 20(8):1179-1181.
140. Koteiche HA, McHaourab HS. Mechanism of a hereditary cataract phenotype. Mutations in alphaA-crystallin activate substrate binding. J Biol Chem. 2006; 281(20):14273-14279.
141. Irobi J, Van Impe K, Seeman P, Jordanova A, Dierick I, Verpoorten N et al. Hot-spot residue in small heat-shock protein 22 causes distal motor neuropathy. Nature Genetics, 2004; 36(6):597-601.
142. Kim MV, Kasakov AS, Seit-Nebi AS, Marston SB, Gusev NB. Structure and properties of K141E mutant of small heat shock protein HSP22 (HspB8, H11) that is expressed in human neuromuscular disorders. Archives of Biochemistry and Biophysics, 2006; 454(1):32-41.
143. Perng MD, Wen SF, van den IJ, Prescott AR, Quinlan RA. Desmin aggregate formation by R120G alphaB-crystallin is caused by altered filament interactions and is dependent upon network status in cells. Mol Biol Cell, 2004; 15(5):2335-2346.
144. Sanbe A, Osinska H, Villa C, Gulick J, Klevitsky R, Glabe CG et al. Reversal of amyloid-induced heart disease in desmin-related cardiomyopathy. Proc Natl Acad Sci U S A, 2005; 102(38):13592-13597.
145. Garrido C, Fromentin A, Bonnotte B, Favre N, Moutet M, Arrigo AP et al. Heat shock protein 27 enhances the tumorigenicity of immunogenic rat colon carcinoma cell clones. Cancer Res. 1998; 58(23):5495-5499.
146. Xu L, Chen S, Bergan RC. MAPKAPK2 and HSP27 are downstream effectors of p38 MAP kinase-mediated matrix metalloproteinase type 2 activation and cell invasion in human prostate cancer. Oncogene. 2006; 25(21):2987-2998.
147. Moyano JV, Evans JR, Chen F, Lu M, Werner ME, Yehiely F et al. AlphaB-crystallin is a novel oncoprotein that predicts poor clinical outcome in breast cancer. J Clin Invest. 2006; 116(1):261-270.
148. Sun X, Fontaine JM, Bartl I, Behnam B, Welsh MJ, Benndorf R. Induction of Hsp22 (HspB8) by estrogen and the metalloestrogen cadmium in estrogen receptor-positive breast cancer cells. Cell Stress & Chaperones, 2007; 12(4):307-319.
149. de Wit NJ, Verschuure P, Kappe G, King SM, de Jong WW, van Muijen GN et al. Testis-specific human small heat shock protein HSPB9 is a cancer/testis antigen, and potentially interacts with the dynein subunit TCTEL1. Eur J Cell Biol. 2004; 83(7):337-345.
150. Pozsgai E, Gomori E, Szigeti A, Boronkai A, Gallyas F, Jr., Sumegi B et al. Correlation between the progressive cytoplasmic expression of a novel small heat shock protein (Hsp16.2) and malignancy in brain tumors. BMC Cancer, 2007; 7:233.
151. Rocchi P, So A, Kojima S, Signaevsky M, Beraldi E, Fazli L et al. Heat shock protein 27 increases after androgen ablation and plays a cytoprotective role in hormone-refractory prostate cancer. Cancer Res. 2004; 64(18):6595-6602.
152. Oesterreich S, Weng CN, Qiu M, Hilsenbeck SG, Osborne CK, Fuqua SA. The small heat shock protein hsp27 is correlated with growth and drug resistance in human breast cancer cell lines. Cancer Res. 1993; 53(19):4443-4448.
153. Oesterreich S, Schunck H, Benndorf R, Bielka H. Cisplatin induces the small heat shock protein hsp25 and thermotolerance in Ehrlich ascites tumor cells. Biochem Biophys Res Commun. 1991; 180(1):243-248.
154. Sanbe A, Daicho T, Mizutani R, Endo T, Miyauchi N, Yamauchi J et al. Protective effect of geranylgeranylacetone via enhancement of HSPB8 induction in desmin-related cardiomyopathy. PLoS ONE, 2009; 4(4):e5351.
155. Hu Z, Chen L, Zhang J, Li T, Tang J, Xu N et al. Structure, function, property, and role in neurologic diseases and other diseases of the sHsp22. J Neurosci Res. 2007; 85(10):2071-2079.
156. Ackerley S, James PA, Kalli A, French S, Davies KE, Talbot K. A mutation in the small heat-shock protein HSPB1 leading to distal hereditary motor neuronopathy disrupts neurofilament assembly and the axonal transport of specific cellular cargoes. Hum Mol Genet. 2006; 15(2):347-354.
157. An JJ, Lee YP, Kim SY, Lee SH, Lee MJ, Jeong MS et al. Transduced human PEP-1-heat shock protein 27 efficiently protects against brain ischemic insult. FEBS J. 2008.
158. Sakamoto K, Urushidani T, Nagao T. Translocation of HSP27 to sarcomere induced by ischemic preconditioning in isolated rat hearts. Biochem Biophys Res Commun. 2000; 269(1):137-142.
159. Bluhm WF, Martin JL, Mestril R, Dillmann WH. Specific heat shock proteins protect microtubules during simulated ischemia in cardiac myocytes. Am J Physiol. 1998; 275(6 Pt 2):H2243-H2249.
160. Schober A, Burger-Kentischer A, Muller E, Beck FX. Effect of ischemia on localization of heat shock protein 25 in kidney. Kidney Int Suppl. 1998; 67:S174-S176.
161. Uozaki H, Horiuchi H, Ishida T, Iijima T, Imamura T, Machinami R. Overexpression of resistance-related proteins (metallothioneins, glutathione-S-transferase pi, heat shock protein 27, and lung resistance-related protein) in osteosarcoma. Relationship with poor prognosis. Cancer, 1997; 79(12):2336-2344.
162. Benjamin IJ, Guo Y, Srinivasan S, Boudina S, Taylor RP, Rajasekaran NS et al. CRYAB and HSPB2 deficiency alters cardiac metabolism and paradoxically confers protection against myocardial ischemia in aging mice. Am J Physiol Heart Circ Physiol. 2007; 293(5):H3201-H3209.
163. Morrison LE, Whittaker RJ, Klepper RE, Wawrousek EF, Glembotski CC. 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. 2004; 286(3):H847-H855.
164. Suzuki A, Sugiyama Y, Hayashi Y, Nyu-i N, Yoshida M, Nonaka I et al. MKBP, a novel member of the small heat shock protein family, binds and activates the myotonic dystrophy protein kinase. J Cell Biol. 1998; 140(5):1113-1124.
165. Yoshida K, Aki T, Harada K, Shama KM, Kamoda Y, Suzuki A et al. Translocation of HSP27 and MKBP in ischemic heart. Cell Struct Funct. 1999; 24(4):181-185.
166. Agius MA, Kirvan CA, Schafer AL, Gudipati E, Zhu S. High prevalence of anti-alpha-crystallin antibodies in multiple sclerosis: correlation with severity and activity of disease. Acta Neurol Scand. 1999; 100(3):139-147.
167. Bullard B, Ferguson C, Minajeva A, Leake MC, Gautel M, Labeit D et al. Association of the chaperone alphaB-crystallin with titin in heart muscle. J Biol Chem. 2004; 279(9):7917-7924.
168. Berry V, Francis P, Reddy MA, Collyer D, Vithana E, MacKay I et al. Alpha-B crystallin gene (CRYAB) mutation causes dominant congenital posterior polar cataract in humans. Am J Hum Genet. 2001; 69(5):1141-1145.
169. Graw J. Genetics of crystallins: Cataract and beyond. Exp Eye Res 2008.
170. Lee S, Carson K, Rice-Ficht A, Good T. Hsp20, a novel alpha-crystallin, prevents Abeta fibril formation and toxicity. Protein Sci. 2005; 14(3):593-601.
171. Islamovic E, Duncan A, Bers DM, Gerthoffer WT, Mestril R. Importance of small heat shock protein 20 (hsp20) C-terminal extension in cardioprotection. J Mol Cell Cardiol. 2007; 42(4):862-869.
172. Zhu YH, Ma TM, Wang X. Gene transfer of heat-shock protein 20 protects against ischemia/reperfusion injury in rat hearts. Acta Pharmacol Sin. 2005; 26(10):1193-1200.
173. Houlden H, Laura M, Wavrant-De Vrieze F, Blake J, Wood N, Reilly MM. Mutations in the HSP27 (HSPB1) gene cause dominant, recessive, and sporadic distal HMN/CMT type 2. Neurology, 2008; 71(21):1660-1668.
174. Wilhelmus MMM, Boelens WC, Otte-Holler I, Kamps B, Kusters B, Maat-Schieman MLC et al. 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 Neuropathologica, 2006; 111(2):139-149.
175. Yu YX, Heller A, Liehr T, Smith CC, Aurelian L. Expression analysis and chromosome location of a novel gene (H11) associated with the growth of human melanoma cells. Int J Oncol. 2001; 18(5):905-911.
176. Depre C, Wang L, Sui X, Qiu H, Hong C, Hedhli N et al. H11 kinase prevents myocardial infarction by preemptive preconditioning of the heart. Circ Res. 2006; 98(2):280-288.
177. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994; 22(22):4673-4680.
178. Nicholas KB. GeneDoc: Analysis and Visualization of Genetic Variation. Nicholas H.B., Deerfield DW, editors. EMBNEW.NEWS, 4(14): 1997.
179. Baumgartner S, Hofmann K, Chiquet-Ehrismann R, Bucher P. The discoidin domain family revisited: new members from prokaryotes and a homology-based fold prediction. Protein Sci. 1998; 7(7):1626-1631.
180. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003; 52(5):696-704.
181. Haslbeck M. sHsps and their role in the chaperone network. Cell Mol Life Sci. 2002; 59(10):1649-1657.
182. Fu L, Liang JJ. Detection of protein-protein interactions among lens crystallins in a mammalian two-hybrid system assay. J Biol Chem. 2002; 277(6):4255-4260.
183. Pipkin W, Johnson JA, Creazzo TL, Burch J, Komalavilas P, Brophy C. Localization, macromolecular associations, and function of the small heat shock-related protein HSP20 in rat heart. Circulation, 2003; 107(3):469-476.
184. Fontaine JM, Sun X, Benndorf R, Welsh MJ. Interactions of HSP22 (HSPB8) with HSP20, alphaB-crystallin, and HSPB3. Biochem Biophys Res Commun. 2005; 337(3):1006-1011.
185. Sun X, Fontaine JM, Rest JS, Shelden EA, Welsh MJ, Benndorf R. Interaction of human HSP22 (HSPB8) with other small heat shock proteins. J Biol Chem 2004; 279(4):2394-2402.
186. Kato K, Shinohara H, Goto S, Inaguma Y, Morishita R, Asano T. Copurification of small heat shock protein with alpha B crystallin from human skeletal muscle. J Biol Chem. 1992; 267(11):7718-7725.
187. Benndorf R, Sun X, Gilmont RR, Biederman KJ, Molloy MP, Goodmurphy CW et al. HSP22, a new member of the small heat shock protein superfamily, interacts with mimic of phosphorylated HSP27 ((3D)HSP27). J Biol Chem. 2001; 276(29):26753-26761.