Acetylation of lysine 92 improves the chaperone and anti-apoptotic activities of human αb-crystallin

Biochemistry

Volumn 52, Issue 45, 2013, Pages 8126-8138

  Nahomi, Rooban B ^a   Huang, Rong ^b   Nandi, Sandip K ^c   Wang, Benlian ^a   Padmanabha, Smitha ^a   Santhoshkumar, Puttur ^d   Filipek, Slawomir ^e   Biswas, Ashis ^c   Nagaraj, Ram H ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c INDIAN INSTITUTE OF TECHNOLOGY BHUBANESWAR   (India)

^d University of Missouri   (United States)

^e UNIVERSITY OF WARSAW   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-APOPTOTIC PROTEIN; ANTIAPOPTOTIC ACTIVITIES; BINDING AFFINITIES; CHAPERONE ACTIVITY; HYDRODYNAMIC RADIUS; PROTECTIVE FUNCTION; SECONDARY AND TERTIARY STRUCTURES; SURFACE HYDROPHOBICITY;

AMINO ACIDS; BINDING ENERGY; BIOCHEMISTRY; CHEMICAL MODIFICATION; HYDROPHOBICITY; PROTEINS;

ACETYLATION;

ALPHA B CRYSTALLIN; CHAPERONE; CRYSTALLIN; LYSINE; LYSINE 92; N ACETYLPEPTIDE; PROTEIN; UNCLASSIFIED DRUG;

ACETYLATION; APOPTOSIS; ARTICLE; HUMAN; HYDRODYNAMICS; HYDROPHOBICITY; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE;

ACETYLATION; BLOTTING, WESTERN; CRYSTALLINS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LYSINE; MODELS, MOLECULAR; MOLECULAR CHAPERONES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84887577620     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400638s     Document Type: Article

References (59)

1. Clark, A. R., Lubsen, N. H., and Slingsby, C. (2012) sHSP in the eye lens: Crystallin mutations, cataract and proteostasis Int. J. Biochem. Cell Biol. 44, 1687-1697
2. Horwitz, J. (2003) α-Crystallin Exp. Eye Res. 76, 145-153
3. Basha, E., O'Neill, H., and Vierling, E. (2012) Small heat shock proteins and α-crystallins: Dynamic proteins with flexible functions Trends Biochem. Sci. 37, 106-117
4. Peterson, J., Radke, G., and Takemoto, L. (2005) Interaction of lens α and γ crystallins during aging of the bovine lens Exp. Eye Res. 81, 680-689
5. Acunzo, J., Katsogiannou, M., and Rocchi, P. (2012) Small heat shock proteins HSP27 (HspB1), αB-crystallin (HspB5) and HSP22 (HspB8) as regulators of cell death Int. J. Biochem. Cell Biol. 44, 1622-1631
6. Song, S., Hanson, M. J., Liu, B. F., Chylack, L. T., and Liang, J. J. (2008) Protein-protein interactions between lens vimentin and αB-crystallin using FRET acceptor photobleaching Mol. Vis. 14, 1282-1287
7. Nicholl, I. D. and Quinlan, R. A. (1994) Chaperone activity of α-crystallins modulates intermediate filament assembly EMBO J. 13, 945-953
8. Truscott, R. J., Comte-Walters, S., Ablonczy, Z., Schwacke, J. H., Berry, Y., Korlimbinis, A., Friedrich, M. G., and Schey, K. L. (2011) Tight binding of proteins to membranes from older human cells Age 33, 543-554
9. Xi, J. H., Bai, F., McGaha, R., and Andley, U. P. (2006) α-Crystallin expression affects microtubule assembly and prevents their aggregation FASEB J. 20, 846-857
10. Inaguma, Y., Ito, H., Iwamoto, I., Saga, S., and Kato, K. (2001) αB-Crystallin phosphorylated at Ser-59 is localized in centrosomes and midbodies during mitosis Eur. J. Cell Biol. 80, 741-748
11. Gangalum, R. K., Schibler, M. J., and Bhat, S. P. (2004) Small heat shock protein αB-crystallin is part of cell cycle-dependent Golgi reorganization J. Biol. Chem. 279, 43374-43377
12. Boyle, D. L., Takemoto, L., Brady, J. P., and Wawrousek, E. F. (2003) Morphological characterization of the αA- and αB-crystallin double knockout mouse lens BMC Ophthalmol. 3, 3
13. Brady, J. P., Garland, D., Duglas-Tabor, Y., Robison, W. G., Jr., Groome, A., and Wawrousek, E. F. (1997) Targeted disruption of the mouse αA-crystallin gene induces cataract and cytoplasmic inclusion bodies containing the small heat shock protein αB-crystallin Proc. Natl. Acad. Sci. U.S.A. 94, 884-889
14. Andley, U. P., Hamilton, P. D., Ravi, N., and Weihl, C. C. (2011) A knock-in mouse model for the R120G mutation of αB-crystallin recapitulates human hereditary myopathy and cataracts PLoS One 6, e17671
15. Hsu, C. D., Kymes, S., and Petrash, J. M. (2006) A transgenic mouse model for human autosomal dominant cataract Invest. Ophthalmol. Visual Sci. 47, 2036-2044
16. Rekas, A., Adda, C. G., Andrew Aquilina, J., Barnham, K. J., Sunde, M., Galatis, D., Williamson, N. A., Masters, C. L., Anders, R. F., Robinson, C. V., Cappai, R., and Carver, J. A. (2004) Interaction of the molecular chaperone αB-crystallin with α-synuclein: Effects on amyloid fibril formation and chaperone activity J. Mol. Biol. 340, 1167-1183
17. Ecroyd, H. and Carver, J. A. (2009) Crystallin proteins and amyloid fibrils Cell. Mol. Life Sci. 66, 62-81
18. Wang, X., Osinska, H., Klevitsky, R., Gerdes, A. M., Nieman, M., Lorenz, J., Hewett, T., and Robbins, J. (2001) Expression of R120G-αB-crystallin causes aberrant desmin and αB-crystallin aggregation and cardiomyopathy in mice Circ. Res. 89, 84-91
19. Rothbard, J. B., Kurnellas, M. P., Brownell, S., Adams, C. M., Su, L., Axtell, R. C., Chen, R., Fathman, C. G., Robinson, W. H., and Steinman, L. (2012) Therapeutic effects of systemic administration of chaperone αB-crystallin associated with binding proinflammatory plasma proteins J. Biol. Chem. 287, 9708-9721
20. Ousman, S. S., Tomooka, B. H., van Noort, J. M., Wawrousek, E. F., O'Connor, K. C., Hafler, D. A., Sobel, R. A., Robinson, W. H., and Steinman, L. (2007) Protective and therapeutic role for αB-crystallin in autoimmune demyelination Nature 448, 474-479
21. Kurnellas, M. P., Brownell, S. E., Su, L., Malkovskiy, A. V., Rajadas, J., Dolganov, G., Chopra, S., Schoolnik, G. K., Sobel, R. A., Webster, J., Ousman, S. S., Becker, R. A., Steinman, L., and Rothbard, J. B. (2012) Chaperone activity of small heat shock proteins underlies therapeutic efficacy in experimental autoimmune encephalomyelitis J. Biol. Chem. 287, 36423-36434
22. Fort, P. E. and Lampi, K. J. (2011) New focus on α-crystallins in retinal neurodegenerative diseases Exp. Eye Res. 92, 98-103
23. Pasupuleti, N., Matsuyama, S., Voss, O., Doseff, A. I., Song, K., Danielpour, D., and Nagaraj, R. H. (2010) The anti-apoptotic function of human αA-crystallin is directly related to its chaperone activity Cell Death Dis. 1, e31
24. Kamradt, M. C., Chen, F., and Cryns, V. L. (2001) The small heat shock protein αB-crystallin negatively regulates cytochrome c- and caspase-8-dependent activation of caspase-3 by inhibiting its autoproteolytic maturation J. Biol. Chem. 276, 16059-16063
25. Sreekumar, P. G., Kannan, R., Kitamura, M., Spee, C., Barron, E., Ryan, S. J., and Hinton, D. R. (2010) αB-Crystallin is apically secreted within exosomes by polarized human retinal pigment epithelium and provides neuroprotection to adjacent cells PLoS One 5, e12578
26. Bhat, S. P. and Gangalum, R. K. (2011) Secretion of αB-crystallin via exosomes: New clues to the function of human retinal pigment epithelium Commun. Integr. Biol. 4, 739-741
27. Kannan, R., Sreekumar, P. G., and Hinton, D. R. (2012) Novel roles for α-crystallins in retinal function and disease Prog. Retinal Eye Res. 31, 576-604
28. Losiewicz, M. K. and Fort, P. E. (2011) Diabetes impairs the neuroprotective properties of retinal α-crystallins Invest. Ophthalmol. Visual Sci. 52, 5034-5042
29. Adhikari, A. S., Sridhar Rao, K., Nagaraj, R., Parnaik, V. K., and Mohan Rao, C. (2004) Heat stress-induced localization of small heat shock proteins in mouse myoblasts: Intranuclear lamin A/C speckles as target for αB-crystallin and Hsp25 Exp. Cell Res. 299, 393-403
30. McGreal, R. S., Kantorow, W. L., Chauss, D. C., Wei, J., Brennan, L. A., and Kantorow, M. (2012) αB-Crystallin/sHSP protects cytochrome c and mitochondrial function against oxidative stress in lens and retinal cells Biochim. Biophys. Acta 1820, 921-930
31. Sadoul, K., Wang, J., Diagouraga, B., and Khochbin, S. (2011) The tale of protein lysine acetylation in the cytoplasm J. Biomed. Biotechnol. 2011, 970382
32. Yang, X. J. and Seto, E. (2008) Lysine acetylation: Codified crosstalk with other posttranslational modifications Mol. Cell 31, 449-461
33. Zhao, S., Xu, W., Jiang, W., Yu, W., Lin, Y., Zhang, T., Yao, J., Zhou, L., Zeng, Y., Li, H., Li, Y., Shi, J., An, W., Hancock, S. M., He, F., Qin, L., Chin, J., Yang, P., Chen, X., Lei, Q., Xiong, Y., and Guan, K. L. (2010) Regulation of cellular metabolism by protein lysine acetylation Science 327, 1000-1004
34. Choudhary, C., Kumar, C., Gnad, F., Nielsen, M. L., Rehman, M., Walther, T. C., Olsen, J. V., and Mann, M. (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions Science 325, 834-840
35. Lin, P. P., Barry, R. C., Smith, D. L., and Smith, J. B. (1998) In vivo acetylation identified at lysine 70 of human lens αA-crystallin Protein Sci. 7, 1451-1457
36. Lapko, V. N., Smith, D. L., and Smith, J. B. (2001) In vivo carbamylation and acetylation of water-soluble human lens αB-crystallin lysine 92 Protein Sci. 10, 1130-1136
37. Nagaraj, R. H., Nahomi, R. B., Shanthakumar, S., Linetsky, M., Padmanabha, S., Pasupuleti, N., Wang, B., Santhoshkumar, P., Panda, A. K., and Biswas, A. (2012) Acetylation of αA-crystallin in the human lens: Effects on structure and chaperone function Biochim. Biophys. Acta 1822, 120-129
38. Nahomi, R. B., Oya-Ito, T., and Nagaraj, R. H. (2013) The combined effect of acetylation and glycation on the chaperone and anti-apoptotic functions of human α-crystallin Biochim. Biophys. Acta 1832, 195-203
39. Wang, X. and Hayes, J. J. (2008) Acetylation mimics within individual core histone tail domains indicate distinct roles in regulating the stability of higher-order chromatin structure Mol. Cell. Biol. 28, 227-236
40. Scroggins, B. T., Robzyk, K., Wang, D., Marcu, M. G., Tsutsumi, S., Beebe, K., Cotter, R. J., Felts, S., Toft, D., Karnitz, L., Rosen, N., and Neckers, L. (2007) An acetylation site in the middle domain of Hsp90 regulates chaperone function Mol. Cell 25, 151-159
41. Huang, R., Holbert, M. A., Tarrant, M. K., Curtet, S., Colquhoun, D. R., Dancy, B. M., Dancy, B. C., Hwang, Y., Tang, Y., Meeth, K., Marmorstein, R., Cole, R. N., Khochbin, S., and Cole, P. A. (2010) Site-specific introduction of an acetyl-lysine mimic into peptides and proteins by cysteine alkylation J. Am. Chem. Soc. 132, 9986-9987
42. Biswas, A. and Das, K. P. (2007) Differential recognition of natural and nonnatural substrate by molecular chaperone α-crystallin-A subunit exchange study Biopolymers 85, 189-197
43. Nagaraj, R. H., Panda, A. K., Shanthakumar, S., Santhoshkumar, P., Pasupuleti, N., Wang, B., and Biswas, A. (2012) Hydroimidazolone modification of the conserved Arg12 in small heat shock proteins: Studies on the structure and chaperone function using mutant mimics PLoS One 7, e30257
44. Pasupuleti, N., Gangadhariah, M., Padmanabha, S., Santhoshkumar, P., and Nagaraj, R. H. (2010) The role of the cysteine residue in the chaperone and anti-apoptotic functions of human Hsp27 J. Cell. Biochem. 110, 408-419
45. Biswas, A., Goshe, J., Miller, A., Santhoshkumar, P., Luckey, C., Bhat, M. B., and Nagaraj, R. H. (2007) Paradoxical effects of substitution and deletion mutation of Arg56 on the structure and chaperone function of human αB-crystallin Biochemistry 46, 1117-1127
46. Biswas, A. and Das, K. P. (2004) Role of ATP on the interaction of α-crystallin with its substrates and its implications for the molecular chaperone function J. Biol. Chem. 279, 42648-42657
47. Bagneris, C., Bateman, O. A., Naylor, C. E., Cronin, N., Boelens, W. C., Keep, N. H., and Slingsby, C. (2009) Crystal structures of α-crystallin domain dimers of αB-crystallin and Hsp20 J. Mol. Biol. 392, 1242-1252
48. Ghosh, J. G. and Clark, J. I. (2005) Insights into the domains required for dimerization and assembly of human αB-crystallin Protein Sci. 14, 684-695
49. Liu, Y., Zhang, X., Luo, L., Wu, M., Zeng, R., Cheng, G., Hu, B., Liu, B., Liang, J. J., and Shang, F. (2006) A novel αB-crystallin mutation associated with autosomal dominant congenital lamellar cataract Invest. Ophthalmol. Visual Sci. 47, 1069-1075
50. Berengian, A. R., Parfenova, M., and McHaourab, H. S. (1999) Site-directed spin labeling study of subunit interactions in the α-crystallin domain of small heat-shock proteins. Comparison of the oligomer symmetry in αA-crystallin, HSP 27, and HSP 16.3 J. Biol. Chem. 274, 6305-6314
51. Delbecq, S. P. and Klevit, R. E. (2013) One size does not fit all: The oligomeric states of αB-crystallin FEBS Lett. 587, 1073-1080
52. Sreelakshmi, Y. and Sharma, K. K. (2005) Recognition sequence 2 (residues 60-71) plays a role in oligomerization and exchange dynamics of αB-crystallin Biochemistry 44, 12245-12252
53. Santhoshkumar, P., Murugesan, R., and Sharma, K. K. (2009) Deletion of (54)FLRAPSWF(61) residues decreases the oligomeric size and enhances the chaperone function of αB-crystallin Biochemistry 48, 5066-5073
54. Pasta, S. Y., Raman, B., Ramakrishna, T., and Rao, Ch. M. (2003) Role of the conserved SRLFDQFFG region of α-crystallin, a small heat shock protein. Effect on oligomeric size, subunit exchange, and chaperone-like activity J. Biol. Chem. 278, 51159-51166
55. Kumar, L. V. and Rao, C. M. (2000) Domain swapping in human αA- and αB-crystallins affects oligomerization and enhances chaperone-like activity J. Biol. Chem. 275, 22009-22013
56. Saha, S. and Das, K. P. (2007) Unfolding and refolding of bovine α-crystallin in urea and its chaperone activity Protein J. 26, 315-326
57. Wettstein, G., Bellaye, P. S., Micheau, O., and Bonniaud, P. (2012) Small heat shock proteins and the cytoskeleton: An essential interplay for cell integrity? Int. J. Biochem. Cell Biol. 44, 1680-1686
58. Li, W. C., Kuszak, J. R., Dunn, K., Wang, R. R., Ma, W., Wang, G. M., Spector, A., Leib, M., Cotliar, A. M., and Weiss, M. 1995, Lens epithelial cell apoptosis appears to be a common cellular basis for non-congenital cataract development in humans and animals J. Cell Biol. 130, 169-181
59. Takamura, Y., Kubo, E., Tsuzuki, S., and Akagi, Y. (2003) Apoptotic cell death in the lens epithelium of rat sugar cataract Exp. Eye Res. 77, 51-57