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

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 8, 2011, Pages 1532-1542

  Adhikari, Amit S ^a   Singh, Bhairab N ^a   Rao, K Sridhar ^a   Rao, Ch Mohan ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

Author keywords

B crystallin; Apoptosis; Differentiation; HSP; NF B; TNF

Indexed keywords

ALPHAB CRYSTALLIN; CRYSTALLIN; HEAT SHOCK PROTEIN; I KAPPA B ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BCL 2; SYNAPTOTAGMIN I; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME ACTIVITY; MOUSE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ALPHA-CRYSTALLIN B CHAIN; ANIMALS; APOPTOSIS; BASE SEQUENCE; BINDING SITES; CELL LINE; DNA, COMPLEMENTARY; HEAT-SHOCK PROTEINS, SMALL; I-KAPPA B KINASE; I-KAPPA B PROTEINS; MICE; MODELS, BIOLOGICAL; MYOBLASTS, SKELETAL; NF-KAPPA B; PHOSPHORYLATION; RNA INTERFERENCE; SERINE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79959362400     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2011.04.009     Document Type: Article

References (52)

1. Parsell D.A., Lindquist S. The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu. Rev. Genet. 1993, 27:437-496.
2. Landry J., Bernier D., Chretien P., Nicole L.M., Tanguay R.M., Marceau N. Synthesis and degradation of heat shock proteins during development and decay of thermotolerance. Cancer Res. 1982, 42:2457-2461.
3. Li G.C., Werb Z. Correlation between synthesis of heat shock proteins and development of thermotolerance in Chinese hamster fibroblasts. Proc. Natl. Acad. Sci. 1982, 79:3218-3222.
4. Horwitz J. Alpha-crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. 1992, 89:10449-10453.
5. Rawat U., Rao M. Interactions of chaperone alpha-crystallin with the molten globule state of xylose reductase. Implications for reconstitution of the active enzyme. J. Biol. Chem. 1998, 273:9415-9423.
6. Goenka S., Raman B., Ramakrishna T., Rao C.M. Unfolding and refolding of a quinone oxidoreductase: alpha-crystallin, a molecular chaperone, assists its reactivation. Biochem. J. 2001, 359:547-556.
7. de Jong W.W., Caspers G.J., Leunissen J.A.M. Genealogy of the α-crystallin- small heat-shock protein superfamily. Int. J. Biol. Macromolecules 1998, 22:151-162.
8. 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, 12:842-846.
9. Klemenz R., Frohli E., Steiger R.H., Schafer R., Aoyama A. AlphaB-crystallin is a small heat shock protein. Proc. Natl. Acad. Sci. 1991, 88:3652-3656.
10. Bhat S.P., Nagineni C.N. alphaB subunit of lens-specific protein alpha- crystallin is present in other ocular and non-ocular tissues. Biochem. Biophys. Res. Commun. 1989, 158:319-325.
11. Kato K., Goto S., Hasegawa K., Inaguma Y. Coinduction of two low-molecular- weight stress proteins, B crystallin and HSP28, by Heat or arsenite stress in human glioma cells. J. Biochem (Tokyo) 1993, 114:640-647.
12. Iwaki T., Kume-Iwaki A., Liem R.K.H., Goldman J.E. αB-crystallin is expressed in non-lenticular tissues and accumulates in Alexander's diseases brain. Cell 1989, 57:71-78.
13. Sun T.-X., Das B.K., Liang J.J.-N. Conformational and functional differences between recombinant human αA- and αB-crystallin. J. Biol. Chem. 1997, 272:6220-6225.
14. Datta S.A., Rao C.M. Differential temperature-dependent chaperone like activity of alpha and alphaB-crystallin homoaggregates. J. Biol. Chem. 1999, 274:34773-34778.
15. Raman B., Ramakrishna T., Rao C.M. Temperature dependent chaperone-like activity of alpha crystallin. FEBS Lett. 1995, 365:133-136.
16. Raman B., Rao C.M. Chaperone-like activity and quaternary structure of alpha-crystallin. J. Biol. Chem. 1994, 269:27264-27268.
17. Bai B., Xi J., Higashikubo R., Andley U.P. A comparative analysis of alphaA- and alphaB-crystallin expression during the cell cycle in primary mouse lens epithelial cultures. Expt. Eye Res. 2004, 79:795-805.
18. Ito H., Kamei K., Iwamoto I., Inaguma Y., Kato K. Regulation of the levels of small heat-shock proteins during differentiation of C2C12 cells. Expt. Cell Res. 2001, 266:213-221.
19. Kamradt M.C., Lu M., Werner M.E., Kwan T., Chen F., Strohecker A., Oshita S., Wilkinson J.C., Yu V., Oliver P.G., Dudkett C.S., Buchsbaum D.J., LoBuglio A.F., Jordan V.C., Cryns V.L. The small heat shock protein AlphaB-crystallin is a novel inhibitor of TRAIL-induced apoptosis that suppresses the activation of caspase-3. J. Biol. Chem. 2005, 280:11059-11066.
20. Singh B.N., Rao K.S., Ramakrishna T., Rangaraj N., Rao C.M. Association of αB-Crystallin, a small heat shock protein, with actin: role in modulating actin filament dynamics in vivo. J. Mol. Biol. 2007, 366:756-767.
21. Adhikari A.S., Rao K.S., Rangaraj N., Parnaik V.K., Rao C.M. Heat stress-induced localization of small heat shock proteins in mouse myoblasts: intranuclear lamin A/C speckles as target for alphaB-crystallin and Hsp25. Expt. Cell Res. 2004, 299:393-403.
22. Vicart P., Caron A., Guicheney P., Li Z., Prévost M.C., Faure A., Chateau D., Chapon F., Tomé F., Dupret J.M., Paulin D., Fardeau M. A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat. Genet. 1998, 20:92-95.
23. Wang X., Osinska H., Klevitsky R., Gerdes A.M., Nieman M., Lorenz J., Hewett T., Robbins J. Expression of R120G-alphaB-crystallin causes aberrant desmin and alphaB-crystallin aggregation and cardiomyopathy in mice. Circulat. Res. 2001, 89:84-91.
24. Kumar L.V., Ramakrishna T., Rao C.M. Structural and functional consequences of the mutation of a conserved arginine residue in alphaA and alphaB crystallins. J. Biol. Chem. 1999, 274:24137-24141.
25. Bova M.P., Yaron O., Huang Q., Ding L., Haley D.A., Stewart P.L., Horwitz J. 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. USA 1999, 96:6137-6142.
26. Perng M.D., Muchowski P.J., van den Ijssel P., Wu G.J.S., Hutcheson A., Clark J.I., Quinlan R.A. The cardiomyopathy and lens cataract mutation in ab-crystallin alters its protein structure, chaperone activity and interaction with intermediate filaments in vitro. J. Biol. Chem. 1999, 274:33235-33243.
27. Brady J.P., Garland D.L., Green D.E., Tamm E.R., Giblin F.J., Wawrousek E.F. AlphaB-crystallin in lens development and muscle integrity: a gene knockout approach. Invest. Ophthalmol. Vis. Sci. 2001, 42:2924-2934.
28. Kamradt M.C., Chen F., Sam S., Cryns V.L. The small heat shock protein AlphaB-crystallin negatively regulates apoptosis during myogenic differentiation by inhibiting caspase-3 activation. J. Biol. Chem. 2002, 277:38731-38736.
29. Mehlen P., Kretz-Remy C., Preville X., Arrigo A.P. Human hsp27, Drosophila hsp27 and human alphaB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNFalpha-induced cell death. EMBO J. 1996, 15:2695-2706.
30. Mao Y.W., Liu J.P., Xiang H., Li D.W. Human alphaA- and alphaB-crystallins bind to Bax and Bcl X(S) to sequester their translocation during staurosporine-induced apoptosis. Cell Death Differ. 2004, 11:512-526.
31. Kamradt M.C., Chen F., Cryns V.L. The small heat shock protein AlphaB-crystallin negatively regulates cytochrome C- and caspase-8-dependent activation of caspase-3 by inhibiting its autoproteolytic maturation. J. Biol. Chem. 2001, 276:16059-16063.
32. Collins R.A., Grounds M.D. The role of tumor necrosis factor-alpha (TNF-alpha) in skeletal muscle regeneration. Studies in TNF-alpha (-/-) and TNF-alpha (-/-)/LT-alpha (-/-) mice. J. Histochem. Cytochem. 2001, 49:989-1001.
33. Li Y.P., Schwartz R.J. TNF-alpha regulates early differentiation of C2C12 myoblasts in an autocrine fashion. FASEB J. 2001, 8:1413-1415.
34. Mac Lachlan T.K., Giordano A. TRAF2 expression in differentiated muscle. J. Cell. Biochem. 1998, 71:461-466.
35. Li Y.P. TNF- is a mitogen in skeletal muscle. Am. J. Physiol. Cell Physiol. 2003, 285:c370-c376.
36. Pahl H.L. Activators and target genes of Rel/NF-KB transcription factors. Oncogene 1999, 18:6853-6866.
37. Perkins N.D., Gilmore T.D. Good cop, bad cop: the different faces of NF-ΚB. Cell Death Differ. 2006, 13:759-772.
38. Rayet B., Gelinas C. Aberrant rel/nfkb genes and activity in human cancer. Oncogene 1999, 18:6938-6947.
39. Karin M., Lin A. NF-κB at the crossroads of life and death. Nat. Immunol. 2002, 3:221-227.
40. Sun Z., Andersson R. NF-κBB activation and inhibition: a review. Shock 2002, 18:99-106.
41. Wallach D. Cell death induction by TNF: a matter of self control. TIBS 1997, 22:107-109.
42. Zhang S.Q., Kovalenko A., Cantarella G., Wallach D. Recruitment of the IKK signalosome to the p55 TNF receptor: RIP and A20 bind to NEMO (IKKgamma) upon receptor stimulation. Immunity 2000, 12:301-311.
43. Yamamoto Y., Gaynor R.B. IkappaB kinases: key regulators of the NF-kappaB pathway. Trends Biochem. Sci. 2004, 29:72-79.
44. Raingeaud J., Gupta S., Rogers J.S., Dickens M., Han J., Ulevitch R.J., Davis R.J. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem. 1995, 270:7420-7426.
45. 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, 272:29934-29941.
46. Smith J.B., Sun Y., Smith D.L., Green B. Identification of the post-translational modifications of bovine lens aB-crystallins by mass spectrometry. Protein Sci. 1992, 1:601-608.
47. den Engelsman J., Gerrits D., de Jong W.W., Robbins J., Kato K., Boelens W.C. Nuclear import of {alpha}B-crystallin is phosphorylation-dependent and hampered by hyperphosphorylation of the myopathy-related mutant R120G. J. Biol. Chem. 2005, 280:37139-37148.
48. 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, 273:28346-28354.
49. Shishodia S., Aggarwal B.B. Nuclear factor-ΚB activation: a question of life or death. J. Biochem. Mol. Biol. 2002, 35:28-40.
50. Park K.J., Gaynor R.B., Kwak Y.T. Heat shock protein 27 association with the I kappa B kinase complex regulates tumor necrosis factor alpha-induced NF-kappa B activation. J. Biol. Chem. 2003, 278:35272-35278.
51. Dodd S.L., Hain B., Senf S.M., Judge A.R. Hsp27 inhibits IKKβ-induced NF-ΚB activity and skeletal muscle atrophy. FASEB J. 2009, 23:3415-3423.
52. Parcellier A., Schmitt E., Gurbuxani S., Seigneurin-Berny D., Pance A., Chantome A., Plenchette S., Khochbin S., Solary E., Garrido C. HSP27 is a ubiquitin-binding protein involved in I-kappaBalpha proteasomal degradation. Mol. Cell. Biol. 2003, 23:5790-5802.