Structure and function of small heat shock/α-crystallin proteins: Established concepts and emerging ideas

Cellular and Molecular Life Sciences

Volumn 57, Issue 6, 2000, Pages 899-913

  MacRae, T H ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Molecular chaperone; Oligomer formation; Protein folding; Small heat shock crystallin protein

Indexed keywords

ALPHA CRYSTALLIN; ARGININE; CHAPERONE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 25; HEAT SHOCK PROTEIN 27; OLIGOMER;

AMINO TERMINAL SEQUENCE; ARTEMIA; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; CRYSTALLOGRAPHY; DROSOPHILA; ESCHERICHIA COLI; MAMMAL; MICROFILAMENT; MOUSE; NONHUMAN; OLIGOMERIZATION; PHOSPHORYLATION; PLASTICITY; REVIEW; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; SOLUBILITY; STRUCTURE ANALYSIS; XENOPUS;

ARTEMIA; CAENORHABDITIS ELEGANS; ESCHERICHIA COLI; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 0033927557     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/PL00000733     Document Type: Review

References (180)

1. 1 Roy S. K., Hiyama T. and Nakamoto H. (1999) Purification and characterization of the 16-kDa heat-shock-responsive protein from the thermophilic cyanobacterium Synechococcus vulcanus, which is an χ-crystallin-related, small heat shock protein. Eur. J. Biochem. 262: 404-416
2. 2 Plesofsky N. and Brambl R. (1999) Glucose metabolism in Neurospora is altered by heat shock and by disruption of HSP30. Biochim. Biophys. Acta 1449: 73-82
3. 3 Shearstone J. R. and Baneyx F. (1999) Biochemical characterization of the small heat shock protein IbpB from Escherichia coli. J. Biol. Chem. 274: 9937-9945
4. 4 IJssel P. van den, Norman D. G. and Quinlan R. A. (1999) Molecular chaperones: small heat shock proteins in the limelight. Curr. Biol. 9: R103-R105
5. 5 Veinger L., Diamant S., Buchner J. and Goloubinoff P. (1998) The small heat-shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J. Biol. Chem. 273: 11032-11037
6. 6 Kim R., Kim K. K., Yokota H. and Kim S.-H. (1998) Small heat shock protein of Methanococcus jannaschii, a hyperthermophile. Proc. Natl. Acad. Sci. USA 95: 9129-9133
7. 7 Kim K. K., Kim R. and Kim S.-H. (1998) Crystal structure of a small heat-shock protein. Nature 394: 595-599
8. 8 Muchowski P. J. and Clark J. I. (1998) ATP-enhanced molecular chaperone functions of the small heat shock protein human χB crystallin. Proc. Natl. Acad. Sci. USA 95: 1004-1009
9. 9 Haley D. A., Horwitz J. and Stewart P. L. (1998) The small heat-shock protein, χB-crystallin, has a variable quaternary structure. J. Mol. Biol. 277: 27-35
10. 10 Jong W. W. de, Caspers G.-J. and Leunissen J. A. M. (1998) Genealogy of the χ-crystalline-small heat-shock protein superfamily. Int. J. Biol. Macromol. 22: 151-162
11. 11 Arrigo A.-P. (1998) Small stress proteins: chaperones that act as regulators of intra-cellular redox state - and programmed cell death. Biol. Chem. 379: 19-26
12. 12 Yuan Y., Crane D. D., Simpson R. M., Zhu Y. Q., Hickey M. J., Sherman D. R. et al. (1998) The 16-kDa χ-crystallin (Acr) protein of Mycobacterium tuberculosis is required for growth in macrophages. Proc. Natl. Acad. Sci. USA 95: 9578-9583
13. 13 Graw J. (1997) The crystallins: genes, proteins and diseases. Biol. Chem. 378: 1331-1348
14. 14 Norris C. E., Brown M. A., Hickey E., Weber L. A. and Hightower L. E. (1997) Low-molecular-weight heat shock proteins in a desert fish (Poeciliopis lucida): homologs of human Hsp27 and Xenopus. Hsp30. Mol. Biol. Evol. 14: 1050-1061
15. 15 Boston R. S., Viitanen P. V. and Vierling E. (1996) Molecular chaperones and protein folding in plants. Plant Mol. Biol. 32: 191-222
16. 16 Waters E. R., Lee G. J. and Vierling E. (1996) Evolution, structure and function of the small heat shock proteins in plants. J. Exp. Bot. 47: 325-338
17. 17 Wotton D., Freeman K. and Shore D. (1996) Multimerization of Hsp42p, a novel heat shock protein of Saccharomyces cerevisiae, is dependent on a conserved carboxyl-terminal sequence. J. Biol. Chem. 271: 2717-2723
18. 18 Caspers G.-J., Leunissen J. A. M. and Jong W. W. de (1995) The expanding small heat-shock protein family, and structure predictions of the conserved "χ-crystallin domain". J. Mol. Evol. 40: 238-248
19. 19 Arrigo A.-P. and Landry J. (1994) Expression and function of the low-molecular-weight heat shock proteins. In: The Biology of Heat Shock Proteins and Molecular Chaperones, pp. 335-373, Morimoto R. I., Tissières A. and Georgopoulos C. (eds.), Cold Spring Harbor Laboratory Press, New York
20. 20 Groenen P. J. T. A., Merck K. B., Jong W. W. de and Bloemendal H. (1994) Structure and modifications of the junior chaperone χ-crystallin: from lens transparency to molecular pathology. Eur. J. Biochem. 225: 1-19
21. 21 Jong W. W. de, Leunissen J. A. M. and Voorter C. E. M. (1993) Evolution of the χ-crystallin, small heat-shock protein family. Mol. Biol. Evol. 10: 103-126
22. 22 Takemoto L., Emmons T. and Horwitz J. (1993) The C-terminal region of χ-crystallin: involvement in protection against heat-induced denaturation. Biochem. J. 294: 435-438
23. 23 Merck K. B., Haard-Hoekman W. A. de, Essink B. B. O., Bloemendal H. and Jong W. W. de (1992) Expression and aggregation of recombinant χA-crystallin and its two domains. Biochim. Biophys. Acta 1130: 267-276
24. 24 Wistow G. (1985) Domain structure and evolution in χ-crystallins and small heat-shock proteins. FEBS Lett. 181: 1-6
25. 25 Augusteyn R. C. (1998) χ-Crystallin polymers and polymerization: the view from down under. Int. J. Biol. Macromol. 22: 253-262
26. 26 Waters E. R. and Vierling E. (1999) The diversification of plant cytosolic small heat shock proteins preceded the divergence of mosses. Mol. Biol. Evol. 16: 127-139
27. 27 Mornon J.-P., Halaby D., Malfois M., Durand P., Callebaut I. and Tardieu A. (1998) χ-Crystallin C-terminal domain: on the track of an Ig fold. Int. J. Biol. Macromol. 22: 219-227
28. 1H NMR spectroscopy reveals that mouse Hsp25 has a flexible C-terminal extension of 18 amino acids. FEBS Lett. 369: 305-310
29. 29 Carver J. A., Guerreiro N., Nicholls K. A. and Truscott R. J. W. (1995) On the interaction of χ-crystallin with unfolded proteins. Biochim. Biophys. Acta 1252: 251-260
30. 1H NMR spectroscopy of flexible C-terminal extensions in bovine lens χ-crystallin. FEBS Lett. 311: 143-149
31. 31 Farnsworth P. N., Frauwirth H., Groth-Vasselli B. and Singh K. (1998) Refinement of 3D structure of bovine lens χA-crystallin. Int. J. Biol. Macromol. 22: 175-185
32. 32 Smith J. B., Liu Y. and Smith D. L. (1996) Identification of possible regions of chaperone activity in lens χ-crystallin. Exp. Eye Res. 63: 125-128
33. 33 Carver J. A., Aquilina J. A. and Truscott R. J. W. (1994) A possible chaperone-like quaternary structure for χ-crystallin. Exp. Eye Res. 59: 231-234
34. 34 Wistow G. (1993) Possible tetramer-based quaternary structures for χ-crystallins and small heat shock proteins. Exp. Eye Res. 56: 729-732
35. 35 Rao C. M., Raman B., Ramakrishna T., Rajaraman K., Ghosh D., Datta S. et al. (1998) Structural perturbation of χ-crystallin and its chaperone-like activity. Int. J. Biol. Macromol. 22: 271-281
36. 36 Lindner R. A., Kapur A., Mariani M., Titmuss S. J. and Carver J. A. (1998) Structural alterations of χ-crystallin during its chaperone action. Eur. J. Biochem. 258: 170-183
37. 37 Lindner R. A., Kapur A. and Carver J. A. (1997) The interaction of the molecular chaperone, χ-crystallin, with molten globule states of bovine χ-lactalbumin. J. Biol. Chem. 272: 27722-27729
38. 38 Rawat U. and Rao M. (1998) Interactions of chaperone χ-crystallin with the molten globule state of xylose reductasc: implications for reconstitution of the active enzyme. J. Biol. Chem. 273: 9415-9423
39. 39 Rajaraman K., Raman B., Ramakrishna T. and Rao C. M. (1998) The chaperone-like χ-crystallin forms a complex only with the aggregation-prone molten globule state of χ-lactalbumin. Biochem. Biophys. Res. Commun. 249: 917-921
40. 40 Rajaraman K., Raman B. and Rao C. M. (1996) Molten-globule state of carbonic anhydrase binds to the chaperone-like χ-crystallin. J. Biol. Chem. 271: 27595-27600
41. 41 Das K. P., Petrash J. M. and Surewicz W. K. (1996) Conformational properties of substrate proteins bound to a molecular chaperone χ-crystallin. J. Biol. Chem. 271: 10449-10452
42. 42 Das K. P. and Surewicz W. K. (1995) On the substrate specificity of χ-crystallin as a molecular chaperone. Biochem. J. 311: 367-370
43. 43 Rao P. V., Horwitz J. and Zigler J. S. Jr. (1994) Chaperone-like activity of χ-crystallin: the effect of NADPH on its interaction with ζ-crystallin. J. Biol. Chem. 269: 13266-13272
44. 44 Muchowski P. J., Wu G. J. S., Liang J. J. N., Adman E. T. and Clark J. I. (1999) Site-directed mutations within the core "χ-crystallin" domain of the small heat-shock protein, human χB-crystallin, decrease molecular chaperone functions. J. Mol. Biol. 289: 397-411
45. 45 Raman B., Ramakrishna T. and Rao C. M. (1997) Effect of the chaperone-like alpha-crystallin on the refolding of lysozyme and ribonuclease A. FEBS Lett. 416: 369-372
46. 46 Raman B. and Rao C. M. (1997) Chaperone-like activity and temperature-induced structural changes of χ-crystallin. J. Biol. Chem. 272: 23559-23564
47. 47 Liang P. and MacRae T. H. (1999) The synthesis of a small heat shock χ-crystallin protein in Artemia and its relationship to stress tolerance during development. Dev. Biol. 207: 445-456
48. 48 IJssel P. R. L. A. van den, Overkamp P., Knauf U., Gaestel M. and Jong W. W. de (1994) χA-crystallin confers cellular thermoresistance. FEBS Lett. 355: 54-56
49. 49 Lambert H., Charette S. J., Bernier A. F., Guimond A. and Landry J. (1999) Hsp27 multimerization mediated by phosphorylation-sensitive intermolecular interactions at the amino terminus. J. Biol. Chem. 274: 9378-9385
50. 50 Schäfer C., Ross S. E., Bragado M. J., Groblewski G. E., Ernst S. A. and Williams J. A. (1998) A role for the p38 mitogen-activated protein kinase Hsp27 pathway in cholecystokinin-induced changes in the actin cytoskeleton in rat pancreatic acini. J. Biol. Chem. 273: 24173-24180
51. 51 Liang P. and MacRae T. H. (1997) Molecular chaperones and the eytoskeleton. J. Cell Sci. 110: 1431-1440
52. 52 Wagstaff M. J. D., Collaço-Moraes Y., Smith J., Belleroche J. S. de, Coffin R. S. and Latchman D. S. (1999) Protection of neuronal cells from apoptosis by Hsp27 delivered with a herpes simplex virus-based vector. J. Biol. Chem. 274: 5061-5069
53. 53 Mehlen P., Coronas V., Ljubic-Thibal V., Ducasse C., Granger L., Jourdan F. et al. (1999) Small stress protein Hsp27 accumulation during dopamine-mediated differentiation of rat olfactory neurons counteracts apoptosis. Cell Death Differ. 6: 227-233
54. 54 Mehlen P., Mehlen A., Godet J. and Arrigo A.-P. (1997) hsp27 as a switch between differentiation and apoptosis in murine embryonic stem cells. J. Biol. Chem. 272: 31657-31665
55. 55 Mehlen P., Schulze-Osthoff K. and Arrigo A.-P. (1996) Small stress proteins as novel regulators of apoptosis: heat shock protein 27 blocks FAS/APO-1-and staurosporine-induced cell death. J. Biol. Chem. 271: 16510-16514
56. 56 King V. and Tower J. (1999) Aging-specific expression of Drosophila hsp22. Dev. Biol. 207: 107-118
57. 57 Michaud S., Marin R. and Tanguay R. M. (1997) Regulation of heat shock gene induction and expression during Drosophila development. Cell. Mol. Life Sci. 53: 104-113
58. 58 Michaud S., Marin R., Westwood J. T. and Tanguay R. M. (1997) Cell-specific expression and heat-shock induction of lisps during spermatogenesis in Drosophila melanogaster. J. Cell Sci. 110: 1989-1997
59. 59 Carranco R., Almoguera C. and Jordano J. (1997) A plant small heat shock protein gene expressed during zygotic embryogenesis but noninducible by heat stress. J. Biol. Chem. 272: 27470-27475
60. 60 Linder B., Jin Z., Freedman J. H. and Rubin C. S. (1996) Molecular characterization of a novel, developmentally regulated small embryonic chaperone from Caenorhabditis elegans. J. Biol. Chem. 271: 30158-30166
61. 61 Leroux M. R., Ma B. J., Batelier G., Melki R. and Candido E. P. M. (1997) Unique structural features of a novel class of small heat shock proteins. J. Biol. Chem. 272: 12847-12853
62. 62 Stringham E. G., Dixon D. K., Jones D. and Candido E. P. M. (1992) Temporal and spatial expression patterns of the small heat shock (hsp16) genes in transgenic Caenorhabditis elegant Mol. Biol. Cell 3: 221-233
63. 63 Heikkila J. J., Ohan N., Tam Y. and Ali A. (1997) Heat shock protein gene expression during Xenopus development. Cell. Mol. Life Sci. 53: 114-121
64. 64 Chang Z., Primm T. P., Jokana J., Lee I. H., Serysheva I., Chiu W. et al. (1996) Mycobacterium tuberculosis 16-kDa antigen (Hsp16-3) functions as an oligomeric structure in vitro to suppress thermal aggregation. J. Biol. Chem. 271: 7218-7223
65. 65 Yocum G. D., Joplin K. H. and Denlinger D. L. (1998) Upregulation of a 23 kDa small heat shock protein transcript during pupal diapause in the flesh fly, Sarcophaga crassipalpis. Insect Biochem. Mol. Biol. 28: 677-682
66. 66 Allen S. P., Polazzi J. O., Gierse J. K. and Easton A. M. (1992) Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli. J. Bacteriol. 174: 6938-6947
67. 67 Jones D., Russnak R. H., Kay R. J. and Candido E. P. M. (1986) Structure, expression, and evolution of a heat shock gene locus in Caenorhabditis elegans that is flanked by repetitive elements. J. Biol. Chem. 261: 12006-12015
68. 68 Ohan N. W., Tam Y., Fernando P. and Heikkila J. J. (1998) Characterization of a novel group of basic small heat shock proteins in Xenopus laeris A6 kidney epithelial cells. Biochem. Cell Biol. 76: 665-671
69. 69 Liang P., Amons R., Clegg J. S. and MacRae T. H. (1997) Molecular characterization of a small heat shock/χ-crystallin protein in encysted Artemia embryos. J. Biol. Chem. 272: 19051-19058
70. 70 Jaworski C. J. (1995) A reassessment of mammalian χA-crystallin sequences using DNA sequencing: implications for anthropoid affinities of tarsier. J. Mol. Evol. 41: 901-908
71. 71 Plesofsky-Vig N. and Brambl R. (1990) Gene sequence and analysis of hsp30, a small heat shock protein of Neurospora crassa which associates with mitochondria. J. Biol. Chem. 265: 15432-15440
72. 72 Bova M. P., Yaron O., Huang Q., Ding L., Haley D. A., Stewart P. L. et al. (1999) Mutation R120G in χB-crystallin, which is linked to a desmin-related myopathy, results in an irregular structure and defective chaperone-like function. Proc. Natl. Acad. Sci. USA 96: 6137-6142
73. 73 Lee G. J., Roseman A. M., Saibil H. R. and Vierling E. (1997) A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J. 16: 659-671
74. 74 Lee G. J., Pokala N. and Vierling E. (1995) Structure and in vitro molecular chaperone activity of cytosolic small heat shock proteins from pea. J. Biol. Chem. 270: 10432-10438
75. 75 Chen Q., Osteryoung K. and Vierling E. (1994) A 21-kDa chloroplast heat shock protein assembles into high molecular weight complexes in vivo and in organelle. J. Biol. Chem. 269: 13216-13223
76. 76 Bukau B. and Horwich A. L. (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92: 351-366
77. 77 Ranson N. A., White H. E. and Saibil H. R. (1998) Chaperonins. Biochem J. 333: 233-242
78. 78 Kimmins S. and MacRae T. H. (in press) Maturation of steroid receptors: an example of functional cooperation among molecular chaperones and their associated proteins. Cell Stress and Chaperones (in press)
79. 79 Kokke B. P. A., Leroux M. R., Candido E. P. M., Boelens W. C. and Jong W. W. de (1998) Caenorhabditis elegans small heat-shock proteins Hsp12.2 and Hsp12.3 form tetramers and have no chaperone-like activity. FEBS Lett. 433: 228-232
80. 80 Leroux M. R., Melki R., Gordon B., Batelier G. and Candido E. P. M. (1997) Structure-function studies on small heat shock protein oligomeric assembly and interaction with unfolded polypeptides. J. Biol. Chem. 272: 24646-24656
81. 81 Brophy C. M., Dickinson M. and Woodrum D. (1999) Phosphorylation of the small heat shock-related protein, HSP20, in vascular smooth muscles is associated with changes in the macromolecular associations of HSP20. J. Biol. Chem. 274: 6324-6329
82. 82 Shama K. M. A., Suzuki A., Harada K., Fujitani N., Kimura H., Ohno S. et al. (1999) Transient up-regulation of myotonic dystrophy protein kinase-binding protein, MKBP, and HSP27 in the neonatal myocardium. Cell Struct. Funct. 24: 1-4
83. 83 Boelens W. C., Boekel M. A. M. van and Jong W.W. de (1998) HspB3, the most deviating of the six known human small heat shock proteins. Biochim. Biophys. Acta 1388: 513-516
84. 84 Klundert F. A. J. M. van de, Smulders R. H. P. H., Gijsen M. L. J., Lindner R. A., Jaenicke R., Carver J. A. et al. (1998) The mammalian small heat-shock prolein Hsp20 forms dimers and is a poor chaperone. Eur. J. Biochem. 258: 1014-1021
85. 85 Suzuki A., Sugiyama Y., Hayashi Y., Nyu-i N., Yoshida M., Nonaka I. et al. (1998) MKBP, a novel member of the small heat shock protein family, binds and activates the myotonic dystrophy protein kinase. J. Cell Biol. 140: 1113-1124
86. 86 Liao J.-H., Hung C.-C., Lee J.-S., Wu S.-H. and Chiou S.-H. (1998) Characterization, cloning, and expression of porcine χB crystallin. Biochem. Biophys. Res. Commun. 244: 131-137
87. 87 Ehrnsperger M., Gräber S., Gaestel M. and Buchner J. (1997) Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J. 16: 221-229
88. 88 Bova M. P., Ding L.-L., Horwitz J. and Fung B. K.-K. (1997) Subunit exchange of χA-crystallin. J. Biol. Chem. 272: 29511-29517
89. 89 Inaguma Y., Hasegawa K., Kato K. and Nishida Y. (1996) cDNA cloning of a 20-kDa protein (p20) highly homologous 10 small heat shock proteins: developmental and physiological changes in rat hindlimb muscles. Gene 178: 145-150
90. 90 Kato K., Goto S., Inaguma Y., Hasegawa K., Morishita R. and Asano T. (1994) Purification and characterization of a 20-kDa protein that is highly homologous to χB crystallin. J. Biol. Chem. 269: 15302-15309
91. 91 Klundert F. A. J. M. van de, IJssel P. R. L. A. van den. Stege G. J. J. and Jong W. W. de (1999) Rat Hsp20 confers thermoresistance in a clonal survival assay, but fails to protect coexpressed luciferase in Chinese hamster ovary cells. Biochem. Biophys. Res. Commun. 254: 164-168
92. 92 Klundert F. A. J. M. van de and Jong W. W. de (1999) The small heat shock proteins Hsp20 and χB-crystallin in cultured cardiac myocytes: differences in cellular localization and solubilization afler heat stress. Eur. J. Cell Biol. 78: 567-572
93. 93 Tardieu A. (1998) χ-Crystallin quaternary structure and interactive properties control eye lens transparency. Int. J. Biol. Macromol. 22: 211-217
94. 94 Takemoto L. and Boyle D. (1998) Deamidation of specific glutamine residues from alpha-A crystallin during aging of the human lens. Biochemistry 37: 13681-13685
95. 95 Takemoto L. and Boyle D. (1998) The possible role of χ-crystallins in human senile cataractogenesis. Int. J. Biol. Macromol. 22: 331-337
96. 96 Merck K. B., Groenen P. J. T. A., Voorter C. E. M., Haard-Hoekman W. A. de, Horwitz J., Bloemendal H. et al. (1993) Structural and functional similarities of bovine χ-crystallin and mouse small heat-shock protein: a family of chaperones. J. Biol. Chem. 268: 1046-1052
97. 97 Kaida T., Kozawa O., Ito T., Tanabe K., Ito H., Matsuno H. et al. (1999) Vasopressin stimulates the induction of heat shock protein 27 and χB-crystallin via protein kinase C activation in vascular smooth muscle cells. Exp. Cell Res. 246: 327-337
98. 98 Neufer P. D. and Benjamin I. J. (1996) Differential expression of χB-crystallin and Hsp27 in skeletal muscle during continuous contractile activity: relationship to myogenic regulatory factors. J. Biol. Chem. 271: 24089-24095
99. 99 Inaguma Y., Hasegawa K., Goto S., Ito H. and Kato K. (1995) Induction of the synthesis of hsp27 and χB crystallin in tissues of heat-stressed rats and its suppression by ethanol or an χ1-adrenergic antagonist. J. Biochem. (Tokyo) 117: 1238-1243
100. 100 Head M. W., Corbin E. and Goldman J. E. (1994) Coordinate and independent regulation of χB-crystallin and HSP27 expression in response to physiological stress. J. Cell. Physiol. 159: 41-50
101. 101 Kato K., Goto S., Hasegawa K. and Inaguma Y. (1993) Coinduction of two low-molecular-weight stress proteins, χB crystallin and HSP28, by heat or arsenite stress in human glioma cells. J. Biochem. (Tokyo) 114: 640-647
102. 102 Kato K., Shinohara H., Goto S., Inaguma Y., Morishita R. and Asano T. (1992) Copurification of small heat shock protein with χB crystallin from human skeletal muscle. J. Biol. Chem. 267: 7718-7725
103. 103 Zantema A., Verlaan-De Vries M., Maasdam D., Bol S. and Eb A. van der (1992) Heat shock protein 27 and χB-crystallin can form a complex, which dissociates by heat shock. J. Biol. Chem. 267: 12936-12941
104. 104 Lee J.-S., Samejima T., Liao J.-H., Wu S.-H. and Chiou S.-H. (1998) Physiological role of the association complexes of χ-crystallin and its substrates on the chaperone activity. Biochem. Biophys. Res. Commun. 244: 379-383
105. 105 Muchowski P. J., Bassuk J. A., Lubsen N. H. and Clark J. I. (1997) Human χB-crystallin: small heat shock protein and molecular chaperone. J. Biol. Chem. 272: 2578-2582
106. 106 Farahbakhsh Z. T., Huang Q.-L., Ding L.-L., Altenbach C., Steinhoff H.-J., Horwitz J. et al. (1995) Interaction of χ-cryslallin with spin-labeled peptides. Biochemistry 34: 509-516
107. 107 Horwitz J. (1992) χ-Crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. USA 89: 10449-10453
108. 108 Singh K., Groth-Vasselli B., Kumosinski T. F. and Farnsworth P. N. (1995) χ-Crystallin quaternary structure: molecular basis for its chaperone activity. FEBS Lett. 372: 283-287
109. 109 Palmisano D. V., Groth-Vasselli B., Farnsworth P. N. and Reddy M. C. (1995) Interaction of ATP and lens alpha crystallin characterized by equilibrium binding studies and intrinsic tryptophan fluorescence spectroscopy. Biochim. Biophys. Acta 1246: 91-97
110. 110 Ito H., Hasegawa K., Inaguma Y., Kozawa O. and Kato K. (1996) Enhancement of stress-induced synthesis of hsp27 and χB crystallin by modulators of the arachidonic acid cascade. J. Cell. Physiol. 166: 332-339
111. 111 Kato K., Ito H., Inaguma Y., Okamoto K. and Saga S. (1996) Synthesis and accumulation of χB crystallin in C6 glioma cells is induced by agents that promote the disassembly of microtubules. J. Biol. Chem. 271: 26989-26994
112. 112 Ito H., Okamoto K. and Kato K. (1997) Prostaglandins stimulate the stress-induced synthesis of hsp27 and χB crystallin. J. Cell. Physiol. 170: 255-262
113. 113 Andley U. P., Song Z., Wawrousek E. F. and Bassnett S. (1998) The molecular chaperone χA-crystallin enhances lens epithelial cell growth and resistance to UVA stress. J. Biol. Chem. 273: 31252-31261
114. 114 Loktionova S. A., Ilyinskaya O. P., Gabai V. L. and Kabakov A. E. (1996) Distinct effects of heat shock and ATP depletion on distribution and isoform patterns of human Hsp27 in endothelial cells. FEBS Lett. 392: 100-104
115. 115 Rogalla T., Ehrnsperger M., Preville X., Kotlyarov A., Lutsch G., Ducasse C. et al. (1999) Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress tumor necrosis factor χ by phosphorylation. J. Biol. Chem. 274: 18947-18956
116. 116 Boelens W. C., Croes Y., Ruwe M. de, Reu L. de and Jong W. W. de (1998) Negative charges in the C-terminal domain stabilize the χB-crystallin complex. J. Biol. Chem. 273: 28085-28090
117. 117 Liu C. and Welsh M. J. (1999) Identification of a site of Hsp27 binding with Hsp27 and χB-crystallin as indicated by the yeast two-hybrid system. Biochem. Biophys. Res. Commun. 255: 256-261
118. 118 Sun T.-X. and Liang J. J.-N. (1998) Intermolecular exchange and stabilization of recombinant human χA-and χB-crystallin. J. Biol. Chem. 273: 286-290
119. 119 Sun T.-X., Akhtar N. J. and Liang J. J.-N. (1998) Subunit exchange of lens χ-crystallin: a fluorescence energy transfer study with the fluorescent labeled χA-crystallin mutant W9F as a probe. FEBS Lett. 430: 401-404
120. 120 Sun T.-X., Das B. K. and Liang J. J.-N. (1997) Conformational and functional differences between recombinant human lens χA-and χB-crystallin. J. Biol. Chem. 272: 6220-6225
121. 121 Mchaourab H. S., Berengian A. R. and Koteiche H. A. (1997) Site-directed spin-labelling study of the structure and subunit interactions along a conserved sequence in the χ-crystallin domain of heat shock protein 27: evidence of a conserved subunit interface. Biochemistry 36: 14627-14634
122. 122 Buchner J. (1999) Hsp90 & Co. a holding for folding. Trends Biochem. Soc. 24: 136-141
123. 123 Jakob U. and Buchner J. (1994) Assisting spontaneity: the role of Hsp90 and small Hsps as molecular chaperones. Trends Biochem. Sci. 19: 205-211
124. 124 Roquemore E. P., Chevrier M. R., Cotter R. J. and Hart G. W. (1996) Dynamic O-GlcNAcylation of the small heat shock protein χB-crystallin. Biochemistry 35: 3578-3586
125. 125 Roquemore E. P., Dell A., Morris H. R., Panico M., Reason A. J., Savoy L.-A. et al. (1992) Vertebrate lens χ-crystallins are modified by O-linked N-acetylglucosamine. J. Biol. Chem. 267: 555-563
126. 126 Cherian M. and Abraham E. C. (1995) Decreased molecular chaperone property of χ-crystallins due to posttranslational modifications. Biochem. Biophys. Res. Commun. 208: 675-679
127. 127 Singh K., Zewge D., Groth-Vasselli B. and Farnsworth P. N. (1996) A comparison of structural relationships among χ-crystallin, human Hsp27, γ-crystallins and βB2-crystallin. Int. J. Biol. Macromol. 19: 227-233
128. 128 Merck K. B., Horwitz J., Kersten M., Overkamp P., Gaestel M., Bloemendal H. et al. (1993) Comparison of the homologous carboxy-terminal domain and tail of χ-crystallin and small heat shock protein. Mol. Biol. Rep. 18: 209-215
129. 129 Koteiche H.-A., Berengian A. R. and Mchaourab H. S. (1998) Identification of protein folding patterns using site-directed spin labeling: structural characterization of a β-sheet and putative substrate binding regions in the conserved domain of χA-crystallin. Biochemistry 37: 12681-12688
130. 130 Berenpian A. R., Parfenova M. and Mchaourab H. S. (1999) Site-directed spin labeling study of subunit interactions in the χ-crystallin domain of small heat-shock proteins: comparison of the oligomer symmetry in χA-crystallin, HSP 27, and HSP 16.3. J. Biol. Chem. 274: 6305-6314
131. 131 Berengian A. R., Bova M. P. and Mchaourab H. S. (1997) Structure and function of the conserved domain in χA-crystallin: site-directed spin labeling identifies a β-strand located near a subunit interface. Biochemistry 36: 9951-9957
132. 132 Crabbe M. J. C. and Goode D. (1994) χ-Crystallin: chaperoning and aggregation. Biochem. J. 297: 653-654
133. 133 Gesierich U. and Pfeil W. (1996) The conformational stability of χ-crystallin is rather low: calorimetric results. FEBS Lett. 393: 151-154
134. 134 Surewicz W. K. and Olesen P. R. (1995) On the thermal stability of χ-crystallin: a new insight from infrared spectroscopy. Biochemistry 34: 9655-9660
135. 135 Raman B., Ramakrishna T. and Rao C. M. (1995) Temperature dependent chaperone-like activity of alpha-crystallin. FEBS Lett. 365: 133-136
136. 136 Raman B. and Rao C. M. (1994) Chaperone-like activity and quaternary structure of χ-crystallin. J. Biol. Chem. 269: 27264-27268
137. 137 Das K. P. and Surewicz W. K. (1995) Temperature-induced exposure of hydrophobic surfaces and its effect on the chaperone activity of χ-crystallin. FEBS Lett. 369: 321-325
138. 138 Howitz J., Bova M., Huang Q.-L., Ding L., Yaron O. and Lowman S. (1998) Mutation of χB-crystallin: effects on chaperone-like activity. Int. J. Biol. Macromol. 22: 263-269
139. 139 Das B. K. and Liang J. J.-N. (1997) Detection and characterization of χ-crystallin intermediate with maximal chaperone-like activity. Biochem. Biophys. Res. Commun. 236: 370-374
140. 140 Muchowski P. J., Hays L. G., Yates J. R. III and Clark J. I. (1999) ATP and the core "χ-crystallin" domain of the small heat shock protein χB-crystallin. J. Biol. Chem. 274: 30190-30195
141. 141 Sharma K. K., Kumar G. S., Murphy A. S. and Kester K. (1998) Identification of 1,1′ -bi(4-anilino)naphthalene-5,5′-disulfonic acid hinding sequences in χ-crystallin. J. Biol. Chem. 273: 15474-15478
142. 142 Sharma K. K., Kaur H., Kumar G. S. and Kester K. (1998) Interaction of 1,1′-bi(4-anilino)naphthalene-5,5′-disulfonic acid with χ-crystallin. J. Biol. Chem. 273: 8965-8970
143. 143 Smulders R. H. P. H. and Jong W. W. de (1997) The hydrophobic probe 4,4′-bis(1-anilino-8-naphthalene sulfonic acid) is specifically photoincorporated into the N-terminal domain of χB-crystallin. FEBS Lett. 409: 101-104
144. 144 Stevens A. and Augustin R. C. (1997) Binding of 1-anili-nonaphthalene-8-sulfonic acid to χ-crystallin. Eur. J. Biochem. 243: 792-797
145. 145 Smulders R. H. P. H., Carver J. A., Lindner R. A., Boekel M. A. M. van, Bloemendal H. and Jong W. W. de (1996) Immobilization of the C-terminal extension of bovine χA-crystallin reduces chaperone-like activity. J. Biol. Chem. 271: 29060-29066
146. 146 Andley U. P., Mathur S., Griest T. A. and Petrash J. M. (1996) Cloning, expression, and chaperone-like activity of human χA-crystallin. J. Biol. Chem. 271: 31973-31980
147. 147 Smulders R. H. P. H., Merck K. B., Aendekerk J., Horwitz J., Takemoto L., Slingsby C. et al. (1995) The mutation Asp69→Ser affects the chaperone-like activity of χA-crystallin. Eur. J. Biochem. 232: 834-838
148. 148 Plater M. L., Goode D. and Crabbe M. J. C. (1996) Effects of site-directed mutations on the chaperone-like activity of χB-crystallin. J. Biol. Chem. 271: 28558-28566
149. 149 Kumar L. V. S., Ramakrishna T. and Rao C. M. (1999) Structural and functional consequences of the mutation of a conserved arginine residue in χA and χB crystallins. J. Biol. Chem. 274: 24137-24141
150. 150 Vicart P., Caron A., Guicheney P., Li Z., Prévost M.-C., Faure A. et al. (1998) A missense mutation in the χB-crystallin chaperone gene causes a desmin-related myopathy. Nat. Genet. 20: 92-95
151. 151 Litt M., Kramer P., LaMorticella D. M., Murphey W., Lovrien E. W. and Weleber R. G. (1998) Autosomal dominant congenital cataract associated with a missense mutation in the human alpha crystallin gene CRYAA. Hum. Mol. Genet. 7: 471-474
152. 152 Lansbury P. T. Jr (1999) Evolution of amyloid: what normal protein folding may tell us about fibrillogenesis and disease. Proc. Natl. Acad. Sci. USA 96: 3342-3344
153. 153 Radford S. E. and Dobson C. M. (1999) From computer simulations to human disease: emerging themes in protein folding. Cell 97: 291-298
154. 154 Iwaki T., Iwaki A., Tateishi J., Sakaki Y. and Goldman J. E. (1993) χB-Crystallin and 27-kd heat shock protein are regulated by stress conditions in the central nervous system and accumulate in Rosenthal fibers. Am. J. Pathol. 143: 487-495
155. 155 Iwaki T., Kume-Iwaki A., Liem R. K. H. and Goldman J. E. (1989) χB-Crystallin is expressed in non-lenticular tissues and accumulates in Alexander's disease brain. Cell 57: 71-78
156. 156 Lowe J., McDermott H., Pike I., Spendlove I., Langdon M. and Mayer R. J. (1992) Crystallin expression in non-lenticular tissues and selective presence in ubiquitinated inclusion bodies in human disease. J. Pathol. 166: 61-68
157. 157 Noort J. M. van, Sechel A. C. van, Bajramovic J. J., Ouagmirl M. E., Polman C. H., Lassmann H. et al. (1995) The small heat-shock protein χB-crystallin as candidate autoantigen in multiple sclerosis. Nature 375: 798-801
158. 158 Wiesmann K. E. H., Coop A., Goode D., Hepburne-Scott H. W. and Crabbe M. J. C. (1998) Effect of mutations of murine lens χB-crystallin on transfected neural cell viability and cellular translocalion in response to stress. FEBS Lett. 438: 25-31
159. 159 Sharma K. K., Kaur H. and Kester K. (1997) Functional elements in molecular chaperone χ-crystallin: identification of binding sites in χB-crystallin. Biochem. Biophys. Res. Commun. 239: 217-222
160. ms-crystallin, an alternative splicing product containing a large insert peplide. J. Biol. Chem. 270: 13916-13924
161. 161 Iho H., Iida K., Kamei K., Iwamoto I., Inaguma Y. and Kato K. (1999) χB-Crystallin in the rat lens is phosphorylated at an early post-natal age. FEBS Lett. 446: 269-272
162. 162 Kozawa O., Tanabe K., Ito H., Matsuno H., Niwa M., Kato K. et al. (1999) Sphingosine 1-phosphate regulates heat shock protein 27 induction by a p38 MAP kinase-dependent mechanism in aortic smooth muscle cells. Exp. Cell Res. 250: 376-380
163. 163 Kato K., Ito H., Kamei K. and Iwamoto I. (1999) Selective stimulation of Hsp27 and χB-crystallin but not Hsp70 expression by p38 MAP kinase activation. Cell Stress Chaperone. 4: 94-101
164. 164 Kato K., Ito H., Kamei K., Inaguma Y., Iwamoto I. and Saga S. (1998) Phosphorylation of χβ-crystallin in mitotic cells and identification of enzymatic activities responsible for phosphorylation. J. Biol. Chem. 273: 28346-28354
165. 165 Kato K., Hasegawa K., Goto S. and Inaguma Y. (1994) Dissociation as a result of phosphorylation of an aggregated form of the small stress protein. hsp27. J. Biol. Chem. 269: 11274-11278
166. 166 Nakatsue T., Katoh I., Nakamura S., Takahashi Y., Ikawa Y. and Yoshinaka Y. (1998) Acute infection of Sindbis virus induces phosphorylation and intracellular translocation of small heat shock protein HSP27 and activation of p38 MAP kinase signaling pathway. Biochem. Biophys. Res. Commun. 253: 59-64
167. 167 Clerk A., Michael A. and Sugden P. H. (1998) Stimulation of multiple mitogen-activated protein kinase sub-families by oxidative stress and phosphorylation of the small heat shock protein, HSP25/27 in neonatal ventricular myocytes. Biochem. J. 333: 581-589
168. 168 Guay J., Lambert H., Gingras-Breton G., Lavoie J. N., Huot J. and Landry J. (1997) Regulation of actin filament dynamics by p38 Map kinase-mediated phosphorylation of heat shock protein 27. J. Cell Sci. 110: 357-368
169. 169 Huot J., Lambert H., Lavoie J. N., Guimond A., Houle F. and Landry J. (1995) Characterization of 45-kDa 54-kDa HSP27 kinase, a stress-sensitive kinase which may activate the phosphorylation-dependent protective function of mammalian 27-kDa heat-shock protein HSP27. Eur. J. Biochem. 227: 416-427
170. 170 Ito H., Okamoto K., Nakayama H., Isobe T. and Kato K. (1997) Phosphorylation of χB-crystallin in response to various types of stress. J. Biol. Chem. 272: 29934-29941
171. 171 Beall A., Bagwell D., Woodrum D., Stoming T. A., Kato K., Suzuki A. et al. (1999) The small heat shock-related protein, HSP20, is phosphorylated on serine 16 during cyclic nucleotide-dependent relaxation. J. Biol. Chem. 274: 11344-11351
172. 172 Loktionova S. A. and Kabakov A. E. (1998) Protein phosphatase inhibitors and heat preconditioning prevent Hsp27 dephosphorylation, F-actin disruption and deterioration of morphology in ATP-depleted endothelial cells. FEBS Lett. 433: 294-300
173. 173 Hout J., Houle F., Spitz D. R. and Landry J. (1996) HSP27 phosphorylation-mediated resistance against actin fragmentation and cell death induced by oxidative stress. Cancer Res. 56: 273-279
174. 174 Wang K. and Spector A. (1996) χ-Crystallin stabilizes actin filaments and prevents cytochalasin-induced depolymerization in a phosphorylation-dependent manner. Eur. J. Biochem. 242: 56-66
175. 175 Benndorf R., Hayeß K., Ryazantse S., Wieske M., Behlke J. and Lutsch G. (1994) Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J. Biol. Chem. 269: 20780-20784
176. 176 Perng M. D., Cairns L., IJssel P. van den, Prescott A., Hutcheson A. M. and Quinlan R. A. (1999) Intermediate filament interactions can be altered by HSP27 and χB-crystallin. J. Cell Sci. 112: 2099-2112
177. 177 Quinlan R. A., Sandilands A., Procter J. E., Prescott A. R., Hutcheson A. M., Dahm R. et al. (1999) The eye lens cytoskeleton. Eye 13: 409-416
178. 178 Clark J. I., Matsushima H., David L. L. and Clark J. M. (1999) Lens cytoskeleton and transparency: a model. Eye 13: 417-424
179. 179 Mehlen P., Hickey E., Weber L. A. and Arrigo A.-P. (1997) Large unphosphorylated aggregates as the active form of hsp27 which controls intracellular reactive oxygen species and glutathione levels and generates a protection against TNFχ in NIH-3T3-ras cells. Biochem. Biophys. Res. Commun. 241: 187-192
180. 180 Suzuki T. C., Krawitz D. C. and Vierling E. (1998) The chloroplast small heat-shock protein oligomer is not phosphorylated and does not dissociate during heat stress in vivo. Plant Physiol. 116: 1151-1161