αA-Crystallin associates with α6 integrin receptor complexes and regulates cellular signaling

Experimental Eye Research

Volumn 91, Issue 5, 2010, Pages 640-651

  Sue Menko, A ^a   Andley, Usha P ^b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Chaperone; ERK; Integrin; JNK; Lens; P38

Indexed keywords

ALPHA CRYSTALLIN; ALPHA6 INTEGRIN; FOCAL ADHESION KINASE; MEMBRANE RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BAD; STRESS ACTIVATED PROTEIN KINASE; UVOMORULIN; CADHERIN; LAMININ RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL MEMBRANE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING; LENS EPITHELIUM; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; QUAIL; ANIMAL; CATARACT; CELL SURVIVAL; CHICK EMBRYO; EPITHELIUM CELL; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSFECTION; GENETICS; LENS; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION;

ALPHA-CRYSTALLIN A CHAIN; ANIMALS; APOPTOSIS; CADHERINS; CATARACT; CELL MEMBRANE; CELL SURVIVAL; CHICK EMBRYO; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INTEGRIN ALPHA6; LENS, CRYSTALLINE; MAP KINASE KINASE 4; MICE; MICE, KNOCKOUT; P38 MITOGEN-ACTIVATED PROTEIN KINASES; QUAIL; RECEPTORS, LAMININ; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 78049490015     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2010.08.006     Document Type: Article

References (74)

1. Ahmed M., Forsberg J., Bergsten P. Protein profiling of human pancreatic islets by two-dimensional gel electrophoresis and mass spectrometry. J. Proteome Res. 2005, 4:931-940.
2. Andley U.P. Crystallins in the eye: function and pathology. Prog. Retin. Eye Res. 2007, 26:78-98.
3. Andley U.P., Mathur S., Griest T.A., Petrash J.M. Cloning, expression, and chaperone-like activity of human alphaA-crystallin. J. Biol. Chem. 1996, 271:31973-31980.
4. Andley U.P., Patel H.C., Xi J.H. The R116C mutation in alpha A-crystallin diminishes its protective ability against stress-induced lens epithelial cell apoptosis. J. Biol. Chem. 2002, 277:10178-10186.
5. Andley U.P., Rhim J.S., Chylack L.T., Fleming T.P. Propagation and immortalization of human lens epithelial cells in culture. Invest. Ophthalmol. Vis. Sci. 1994, 35:3094-3102.
6. Andley U.P., Song Z., Wawrousek E.F., Bassnett S. The molecular chaperone alphaA-crystallin enhances lens epithelial cell growth and resistance to UVA stress. J. Biol. Chem. 1998, 273:31252-31261.
7. Andley U.P., Song Z., Wawrousek E.F., Brady J.P., Bassnett S., Fleming T.P. Lens epithelial cells derived from alphaB-crystallin knockout mice demonstrate hyperproliferation and genomic instability. FASEB J. 2001, 15:221-229.
8. Andley U.P., Song Z., Wawrousek E.F., Fleming T.P., Bassnett S. Differential protective activity of alpha A- and alphaB-crystallin in lens epithelial cells. J. Biol. Chem. 2000, 275:36823-36831.
9. Aoyagi Y., Fujita N., Tsuruo T. Stabilization of integrin-linked kinase by binding to Hsp90. Biochem. Biophys. Res. Commun. 2005, 331:1061-1068.
10. Arrigo A.P. The cellular " networking" of mammalian Hsp27 and its functions in the control of protein folding, redox state and apoptosis. Adv. Exp. Med. Biol. 2007, 594:14-26.
11. Arrigo A.P., Paul C., Ducasse C., Manero F., Kretz-Remy C., Virot S., Javouhey E., Mounier N., Diaz-Latoud C. Small stress proteins: novel negative modulators of apoptosis induced independently of reactive oxygen species. Prog. Mol. Subcell. Biol. 2002, 28:185-204.
12. Arrigo A.P., Simon S., Gibert B., Kretz-Remy C., Nivon M., Czekalla A., Guillet D., Moulin M., Diaz-Latoud C., Vicart P. Hsp27 (HspB1) and alphaB-crystallin (HspB5) as therapeutic targets. FEBS Lett. 2007, 581:3665-3674.
13. Arya R., Mallik M., Lakhotia S.C. Heat shock genes - integrating cell survival and death. J. Biosci. 2007, 32:595-610.
14. Beebe D.C., Vasiliev O., Guo J., Shui Y.B., Bassnett S. Changes in adhesion complexes define stages in the differentiation of lens fiber cells. Invest. Ophthalmol. Vis. Sci. 2001, 42:727-734.
15. Bhat S.P., Nagineni C.N. Alpha B subunit of lens-specific protein alpha-crystallin is present in other ocular and non-ocular tissues. Biochem. Biophys. Res. Commun. 1989, 158:319-325.
16. Boelens W.C., Croes Y., De Jong W.W. Interaction between alphaB-crystallin and the human 20S proteasomal subunit C8/alpha7. Biochim. Biophys. Acta 2001, 1544:311-319.
17. Brady J.P., Garland D., Duglas-Tabor Y., Robison W.G., Groome A., Wawrousek E.F. Targeted disruption of the mouse alpha A-crystallin gene induces cataract and cytoplasmic inclusion bodies containing the small heat shock protein alpha B-crystallin. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:884-889.
18. Calautti E., Li J., Saoncella S., Brissette J.L., Goetinck P.F. Phosphoinositide 3-kinase signaling to Akt promotes keratinocyte differentiation versus death. J. Biol. Chem. 2005, 280:32856-32865.
19. Chipuk J.E., Kuwana T., Bouchier-Hayes L., Droin N.M., Newmeyer D.D., Schuler M., Green D.R. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004, 303:1010-1014.
20. Cobb B.A., Petrash J.M. Characterization of alpha-crystallin-plasma membrane binding. J. Biol. Chem. 2000, 275:6664-6672.
21. Cobb B.A., Petrash J.M. Alpha-crystallin chaperone-like activity and membrane binding in age-related cataracts. Biochemistry (Moscow) 2002, 41:483-490.
22. Colognato H., Baron W., Avellana-Adalid V., Relvas J.B., Baron-Van Evercooren A., Georges-Labouesse E., Ffrench-Constant C. CNS integrins switch growth factor signalling to promote target-dependent survival. Nat. Cell Biol. 2002, 4:833-841.
23. Cooper H.M., Tamura R.N., Quaranta V. The major laminin receptor of mouse embryonic stem cells is a novel isoform of the alpha 6 beta 1 integrin. J. Cell Biol. 1991, 115:843-850.
24. Den Engelsman J., Keijsers V., De Jong W.W., Boelens W.C. The small heat-shock protein alpha B-crystallin promotes FBX4-dependent ubiquitination. J. Biol. Chem. 2003, 278:4699-4704.
25. Dubin R.A., Wawrousek E.F., Piatigorsky J. Expression of the murine alpha B-crystallin gene is not restricted to the lens. Mol. Cell. Biol. 1989, 9:1083-1091.
26. Ferreira-Cornwell M.C., Veneziale R.W., Grunwald G.B., Menko A.S. N-cadherin function is required for differentiation-dependent cytoskeletal reorganization in lens cells in vitro. Exp. Cell Res. 2000, 256:237-247.
27. Fleming T.P., Song Z., Andley U.P. Expression of growth control and differentiation genes in human lens epithelial cells with extended life span. Invest. Ophthalmol. Vis. Sci. 1998, 39:1387-1398.
28. Friedland J.C., Lakins J.N., Kazanietz M.G., Chernoff J., Boettiger D., Weaver V.M. alpha6beta4 integrin activates Rac-dependent p21-activated kinase 1 to drive NF-kappaB-dependent resistance to apoptosis in 3D mammary acini. J. Cell Sci. 2007, 120:3700-3712.
29. Gaestel M. sHsp-phosphorylation: enzymes, signaling pathways and functional implications. Prog. Mol. Subcell. Biol. 2002, 28:151-169.
30. Garrido C., Bruey J.M., Fromentin A., Hammann A., Arrigo A.P., Solary E. HSP27 inhibits cytochrome c-dependent activation of procaspase-9. FASEB J. 1999, 13:2061-2070.
31. Ghosh J.G., Shenoy A.K., Clark J.I. Interactions between important regulatory proteins and human alphaB crystallin. Biochemistry (Moscw.) 2007, 46:6308-6317.
32. Gumbiner B.M. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 1996, 84:345-357.
33. Gumbiner B.M. Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 2005, 6:622-634.
34. Head M.W., Hurwitz L., Kegel K., Goldman J.E. AlphaB-crystallin regulates intermediate filament organization in situ. Neuroreport 2000, 11:361-365.
35. Horwitz J. Alpha-crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:10449-10453.
36. Horwitz J. The function of alpha-crystallin in vision. Semin. Cell Dev. Biol. 2000, 11:53-60.
37. Ifeanyi F., Takemoto L. Alpha crystallin from human cataractous vs. normal lenses: change in binding to lens membrane. Exp. Eye Res. 1990, 50:113-116.
38. Ifeanyi F., Takemoto L. Specificity of alpha crystallin binding to the lens membrane. Curr. Eye Res. 1990, 9:259-265.
39. Ifeanyi F., Takemoto L. Involvement of the N-terminal region in alpha-crystallin-lens membrane recognition. Exp. Eye Res. 1991, 53:305-308.
40. Kamradt M.C., Chen F., Cryns V.L. 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, 276:16059-16063.
41. 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, 312:3570-3584.
42. Leonard M., Chan Y., Menko A.S. Identification of a novel intermediate filament-linked N-cadherin/gamma-catenin complex involved in the establishment of the cytoarchitecture of differentiated lens fiber cells. Dev. Biol. 2008, 319:298-308.
43. Leong L., Menko A.S., Grunwald G.B. Differential expression of N- and B-cadherin during lens development. Invest. Ophthalmol. Vis. Sci. 2000, 41:3503-3510.
44. Li D.W., Liu J.P., Mao Y.W., Xiang H., Wang J., Ma W.Y., Dong Z., Pike H.M., Brown R.E., Reed J.C. Calcium-activated RAF/MEK/ERK signaling pathway mediates p53-dependent apoptosis and is abrogated by alpha B-crystallin through inhibition of RAS activation. Mol. Biol. Cell 2005, 16:4437-4453.
45. Li W.C., Kuszak J.R., Dunn K., Wang R.R., Ma W., Wang G.M., Spector A., Leib M., Cotliar A.M., Weiss M., et al. Lens epithelial cell apoptosis appears to be a common cellular basis for non-congenital cataract development in humans and animals. J. Cell Biol. 1995, 130:169-181.
46. Litt M., Kramer P., Lamorticella D.M., Murphey W., Lovrien E.W., Weleber R.G. Autosomal dominant congenital cataract associated with a missense mutation in the human alpha crystallin gene CRYAA. Hum. Mol. Genet. 1998, 7:471-474.
47. Liu J.P., Schlosser R., Ma W.Y., Dong Z., Feng H., Lui L., Huang X.Q., Liu Y., Li D.W. Human alphaA- and alphaB-crystallins prevent UVA-induced apoptosis through regulation of PKCalpha, RAF/MEK/ERK and AKT signaling pathways. Exp. Eye Res. 2004, 79:393-403.
48. Mackay D.S., Andley U.P., Shiels A. Cell death triggered by a novel mutation in the alphaA-crystallin gene underlies autosomal dominant cataract linked to chromosome 21q. Eur. J. Hum. Genet. 2003, 11:784-793.
49. Maddala R., Rao V.P. alpha-Crystallin localizes to the leading edges of migrating lens epithelial cells. Exp. Cell Res. 2005, 306:203-215.
50. 2-induced apoptosis through down-regulation of the alpha B-crystallin gene. J. Biol. Chem. 2001, 276:43435-43445.
51. Menko A.S., Philip N.J. Beta 1 integrins in epithelial tissues: a unique distribution in the lens. Exp. Cell Res. 1995, 218:516-521.
52. Morozov V., Wawrousek E.F. Caspase-dependent secondary lens fiber cell disintegration in alphaA-/alphaB-crystallin double-knockout mice. Development 2006, 133:813-821.
53. Mosser D.D., Morimoto R.I. Molecular chaperones and the stress of oncogenesis. Oncogene 2004, 23:2907-2918.
54. Muchowski P.J., Valdez M.M., Clark J.I. AlphaB-crystallin selectively targets intermediate filament proteins during thermal stress. Invest. Ophthalmol. Vis. Sci. 1999, 40:951-958.
55. Nicholl I.D., Quinlan R.A. Chaperone activity of alpha-crystallins modulates intermediate filament assembly. EMBO J. 1994, 13:945-953.
56. Nollen E.A., Morimoto R.I. Chaperoning signaling pathways: molecular chaperones as stress-sensing 'heat shock' proteins. J. Cell Sci. 2002, 115:2809-2816.
57. Piatigorsky J. Lens differentiation in vertebrates. A review of cellular and molecular features. Differentiation 1981, 19:134-153.
58. Pontoriero G.F., Smith A.N., Miller L.A., Radice G.L., West-Mays J.A., Lang R.A. Co-operative roles for E-cadherin and N-cadherin during lens vesicle separation and lens epithelial cell survival. Dev. Biol. 2009, 326:403-417.
59. Sax C.M., Piatigorsky J. Expression of the alpha-crystallin/small heat-shock protein/molecular chaperone genes in the lens and other tissues. Adv. Enzymol. Relat. Areas Mol. Biol. 1994, 69:155-201.
60. Shaw L.M., Mercurio A.M. Regulation of alpha 6 beta 1 integrin laminin receptor function by the cytoplasmic domain of the alpha 6 subunit. J. Cell Biol. 1993, 123:1017-1025.
61. Shin J.H., Kim S.W., Lim C.M., Jeong J.Y., Piao C.S., Lee J.K. alphaB-crystallin suppresses oxidative stress-induced astrocyte apoptosis by inhibiting caspase-3 activation. Neurosci. Res. 2009, 64:355-361.
62. Stegh A.H., Kesari S., Mahoney J.E., Jenq H.T., Forloney K.L., Protopopov A., Louis D.N., Chin L., Depinho R.A. Bcl2L12-mediated inhibition of effector caspase-3 and caspase-7 via distinct mechanisms in glioblastoma. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:10703-10708.
63. Straub B.K., Boda J., Kuhn C., Schnoelzer M., Korf U., Kempf T., Spring H., Hatzfeld M., Franke W.W. A novel cell-cell junction system: the cortex adhaerens mosaic of lens fiber cells. J. Cell Sci. 2003, 116:4985-4995.
64. Walker J.L., Menko A.S. alpha6 Integrin is regulated with lens cell differentiation by linkage to the cytoskeleton and isoform switching. Dev. Biol. 1999, 210:497-511.
65. Walker J.L., Zhang L., Menko A.S. A signaling role for the uncleaved form of alpha 6 integrin in differentiating lens fiber cells. Dev. Biol. 2002, 251:195-205.
66. Walker J.L., Zhang L., Menko A.S. Transition between proliferation and differentiation for lens epithelial cells is regulated by Src family kinases. Dev. Dyn. 2002, 224:361-372.
67. Walker J.L., Zhang L., Zhou J., Woolkalis M.J., Menko A.S. Role for alpha 6 integrin during lens development: evidence for signaling through IGF-1R and ERK. Dev. Dyn. 2002, 223:273-284.
68. Wang X., Garcia C.M., Shui Y.B., Beebe D.C. Expression and regulation of alpha-, beta-, and gamma-crystallins in mammalian lens epithelial cells. Invest. Ophthalmol. Vis. Sci. 2004, 45:3608-3619.
69. Weber G.F., Menko A.S. The canonical intrinsic mitochondrial death pathway has a non-apoptotic role in signaling lens cell differentiation. J. Biol. Chem. 2005, 280:22135-22145.
70. Xi J.H., Bai F., Andley U.P. Reduced survival of lens epithelial cells in the alphaA-crystallin-knockout mouse. J. Cell Sci. 2003, 116:1073-1085.
71. Xi J.H., Bai F., Gross J., Townsend R.R., Menko A.S., Andley U.P. Mechanism of small heat shock protein function in vivo: a knock-in mouse model demonstrates that the R49C mutation in alpha A-crystallin enhances protein insolubility and cell death. J. Biol. Chem. 2008, 283:5801-5814.
72. Xi J.H., Bai F., Mcgaha R., Andley U.P. Alpha-crystallin expression affects microtubule assembly and prevents their aggregation. FASEB J. 2006, 20:846-857.
73. Xu L., Overbeek P.A., Reneker L.W. Systematic analysis of E-, N- and P-cadherin expression in mouse eye development. Exp. Eye Res. 2002, 74:753-760.
74. Zhou J., Leonard M., Van Bockstaele E., Menko A.S. Mechanism of Src kinase induction of cortical cataract following exposure to stress: destabilization of cell-cell junctions. Mol. Vis. 2007, 13:1298-1310.