Interactive sequences in the stress protein and molecular chaperone human αB crystallin recognize and modulate the assembly of filaments

International Journal of Biochemistry and Cell Biology

Volumn 39, Issue 10, 2007, Pages 1804-1815

  Ghosh, Joy G ^a   Houck, Scott A ^a   Clark, John I ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

crystallin; Actin; Desmin related myopathy (DRM); Glial fibrillary acidic protein; Intermediate filament; Molecular chaperone; Small heat shock protein

Indexed keywords

ACTIN; ALANYLPROLYLSERYLTRYPTOPHYLPHENYLALANYLASPARTYLTHREONYLGLYCINE; ALPHA CRYSTALLIN; ASPARTYLPROLYLLEUCYLTHREONYLISOLEUCYLTHREONYLSERYLSERYLLEUCYLSERYL SERYLASPARTYLGLYCYLVALINE; CHAPERONE; DESMIN; GLIAL FIBRILLARY ACIDIC PROTEIN; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 27; HISTIDYLGLYCYLPHENYLALANYLISOLEUCYLSERYLARGINYLGLUTAMYLPHENYLALANINE; LEUCYLGLUTAMYLSERYLASPARTYLLEUCYLPHENYLALANYLPROLYLTHREONYLSERYL THREONYLSERYLLEUCYLSERYLPROLYLPHENYLALANYLTYROSYLLEUCYLARGINYLPROLYLPROLYL SERYLPHENYLALANYLLEUCYLARGININE; LEUCYLTHREONYLISOLEUCYLTHREONYLSERYLSERYLLEUCYLSERYLSERYLASPARTYL GLYCYLVALINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELLULAR STRESS RESPONSE; CIRCULAR DICHROISM; CONTROLLED STUDY; CYTOSKELETON; DEPOLYMERIZATION; HUMAN; HUMAN CELL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MICROARRAY; PROTEIN STABILITY; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION;

ALPHA-CRYSTALLIN B CHAIN; AMINO ACID SEQUENCE; BINDING SITES; DESMIN; GLIAL FIBRILLARY ACIDIC PROTEIN; HEAT-SHOCK PROTEINS; HUMANS; MICROFILAMENTS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN ARRAY ANALYSIS; PROTEIN FOLDING; PROTEIN INTERACTION MAPPING;

EID: 34548241302     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2007.04.027     Document Type: Article

References (67)

1. Bagchi M., Katar M., and Maisel H. Heat shock proteins of adult and embryonic human ocular lenses. J. Cell. Biochem. 84 2 (2002) 278-284
2. Bennardini F., Wrzosek A., and Chiesi M. Alpha B-crystallin in cardiac tissue. Association with actin and desmin filaments. Circ. Res. 71 2 (1992) 288-294
3. Benndorf R., Hayess K., Ryazantsev S., Wieske M., Behlke J., and Lutsch G. Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J. Biol. Chem. 269 32 (1994) 20780-20784
4. Bertazzon A., Tian G.H., Lamblin A., and Tsong T.Y. Enthalpic and entropic contributions to actin stability: Calorimetry, circular dichroism, and fluorescence study and effects of calcium. Biochemistry 29 1 (1990) 291-298
5. Bertazzon A., and Tsong T.Y. Effects of ions and pH on the thermal stability of thin and thick filaments of skeletal muscle: High-sensitivity differential scanning calorimetric study. Biochemistry 29 21 (1990) 6447-6452
6. Bloemendal H., de Jong W., Jaenicke R., Lubsen N.H., Slingsby C., and Tardieu A. Ageing and vision: Structure, stability and function of lens crystallins. Prog. Biophys. MolBiol. 86 3 (2004) 407-485
7. Bova M.P., Yaron O., Huang Q., Ding L., Haley D.A., Stewart P.L., 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. 96 11 (1999) 6137-6142
8. Carter J.M., Hutcheson A.M., and Quinlan R.A. In vitro studies on the assembly properties of the lens proteins CP49, CP115: Coassembly with alpha-crystallin but not with vimentin. Exp. Eye Res. 60 2 (1995) 181-192
9. Chou R.G., Stromer M.H., Robson R.M., and Huiatt T.W. Determination of the critical concentration required for desmin assembly. Biochem. J. 272 1 (1990) 139-145
10. Djabali K., Piron G., de Nechaud B., and Portier M.M. AlphaB-crystallin interacts with cytoplasmic intermediate filament bundles during mitosis. Exp. Cell Res. 253 2 (1999) 649-662
11. Ecroyd H., Meehan S., Horwitz J., Aquilina J.A., Benesch J.L., Robinson C.V., et al. Mimicking phosphorylation of alphaB-crystallin affects its chaperone activity. Biochem. J. 401 1 (2006) 129-141
12. FitzGerald P.G., and Graham D. Ultrastructural localization of alpha A-crystallin to the bovine lens fiber cell cytoskeleton. Curr. Eye Res. 10 5 (1991) 417-436
13. Fu L., and Liang J.J. Alteration of protein-protein interactions of congenital cataract crystallin mutants. Invest. Ophthalmol. Vis. Sci. 44 3 (2003) 1155-1159
14. Fuchs E., and Weber K. Intermediate filaments: Structure, dynamics, function, and disease. Annu. Rev. Biochem. 63 (1994) 345-382
15. Geysen H.M. Molecular technology: Peptide epitope mapping and the pin technology. Southeast Asian J. Trop. Med. Public Health 21 4 (1990) 523-533
16. Ghosh J.G., and Clark J.I. Insights into the domains required for dimerization and assembly of human alphaB crystallin. Protein Sci. 14 3 (2005) 684-695
17. Ghosh J.G., Estrada M.R., and Clark J.I. Interactive domains for chaperone activity in the small heat shock protein. Human alphaB crystallin. Biochemistry 44 45 (2005) 14854-14869
18. Ghosh J.G., Estrada M.R., and Clark J.I. Structure-based analysis of the beta8 interactive sequence of human alphaB crystallin. Biochemistry 45 32 (2006) 9878-9886
19. Ghosh J.G., Estrada M.R., Houck S.A., and Clark J.I. The function of the beta3 interactive domain in the small heat shock protein and molecular chaperone, human alphaB crystallin. Cell Stress Chaperones 11 2 (2006) 187-197
20. Ghosh J.G., Shenoy Jr. A.K., and Clark J.I. N- and C-terminal motifs in human alphaB crystallin play an important role in the recognition, selection, and solubilization of substrates. Biochemistry 45 46 (2006) 13847-13854
21. Gopalakrishnan S., Boyle D., and Takemoto L. Association of actin with alpha crystallins. Trans. Kans. Acad. Sci. 96 1/2 (1993) 7-12
22. Gopalakrishnan S., and Takemoto L. Binding of actin to lens alpha crystallins. Curr. Eye Res. 11 9 (1992) 929-933
23. Head M.W., Hurwitz L., Kegel K., and Goldman J.E. AlphaB-crystallin regulates intermediate filament organization in situ. Neuroreport 11 2 (2000) 361-365
24. Herrmann H., and Aebi U. Intermediate filaments: Molecular structure, assembly mechanism, and integration into functionally distinct intracellular Scaffolds. Annu. Rev. Biochem. 73 (2004) 749-789
25. Inagaki N., Hayashi T., Arimura T., Koga Y., Takahashi M., Shibata H., et al. AlphaB-crystallin mutation in dilated cardiomyopathy. Biochem. Biophys. Res. Commun. 342 2 (2006) 379-386
26. Ireland M., and Maisel H. A family of lens fiber cell specific proteins. Lens Eye Toxicol. Res. 6 4 (1989) 623-638
27. Iwaki T., Kume-Iwaki A., Liem R.K., and Goldman J.E. Alpha B-crystallin is expressed in non-lenticular tissues and accumulates in Alexander's disease brain. Cell 57 1 (1989) 71-78
28. Kato S., Hirano A., Umahara T., Kato M., Herz F., and Ohama E. Comparative immunohistochemical study on the expression of alpha B crystallin, ubiquitin and stress-response protein 27 in ballooned neurons in various disorders. Neuropathol. Appl. Neurobiol. 18 4 (1992) 335-340
29. Kato K., Inaguma Y., Ito H., Iida K., Iwamoto I., Kamei K., et al. Ser-59 is the major phosphorylation site in alphaB-crystallin accumulated in the brains of patients with Alexander's disease. J. Neurochem. 76 3 (2001) 730-736
30. Kumar N., Tomar A., Parrill A.L., and Khurana S. Functional dissection and molecular characterization of calcium-sensitive actin-capping and actin-depolymerizing sites in villin. J. Biol. Chem. 279 43 (2004) 45036-45046
31. Launay N., Goudeau B., Kato K., Vicart P., and Lilienbaum A. Cell signaling pathways to alphaB-crystallin following stresses of the cytoskeleton. Exp. Cell Res. 312 18 (2006) 3570-3584
32. Liang P., and MacRae T.H. Molecular chaperones and the cytoskeleton. J. Cell Sci. 110 Pt 13 (1997) 1431-1440
33. Lieska N., Chen J., Maisel H., and Romero-Herrera A.E. Subunit characterization of lens intermediate filaments. Biochim. Biophys. Acta 626 1 (1980) 136-153
34. Litt M., Kramer P., LaMorticella D.M., Murphey W., Lovrien E.W., and Weleber R.G. Autosomal dominant congenital cataract associated with a missense mutation in the human alpha crystallin gene CRYAA. Hum. Mol. Genet. 7 3 (1998) 471-474
35. Liu L., Ghosh J.G., Clark J.I., and Jiang S. Studies of alphaB crystalline subunit dynamics by surface plasmon resonance. Anal. Biochem. 350 2 (2006) 186-195
36. Lobley A., Whitmore L., and Wallace B.A. DICHROWEB: An interactive website for the analysis of protein secondary structure from circular dichroism spectra. Bioinformatics 18 1 (2002) 211-212
37. Longoni S., Lattonen S., Bullock G., and Chiesi M. Cardiac alpha-crystallin. II. Intracellular localization. Mol. Cell Biochem. 97 2 (1990) 121-128
38. MacRae T.H. Structure and function of small heat shock/alpha-crystallin proteins: Established concepts and emerging ideas. Cell Mol. Life Sci. 57 6 (2000) 899-913
39. Maglara A.A., Vasilaki A., Jackson M.J., and McArdle A. Damage to developing mouse skeletal muscle myotubes in culture: Protective effect of heat shock proteins. J. Physiol. 548 Pt 3 (2003) 837-846
40. Melkani G.C., Cammarato A., and Bernstein S.I. AlphaB-crystallin maintains skeletal muscle myosin enzymatic activity and prevents its aggregation under heat-shock stress. J. Mol. Biol. 358 3 (2006) 635-645
41. Morrison L.E., Hoover H.E., Thuerauf D.J., and Glembotski C.C. Mimicking phosphorylation of alphaB-crystallin on serine-59 is necessary and sufficient to provide maximal protection of cardiac myocytes from apoptosis. Circ. Res. 92 2 (2003) 203-211
42. Mounier N., and Arrigo A.P. Actin cytoskeleton and small heat shock proteins: How do they interact?. Cell Stress Chaperones 7 2 (2002) 167-176
43. Muchowski P.J., Valdez M.M., and Clark J.I. AlphaB-crystallin selectively targets intermediate filament proteins during thermal stress. Invest. Ophthalmol. Vis. Sci. 40 5 (1999) 951-958
44. Nicholl I.D., and Quinlan R.A. Chaperone activity of alpha-crystallins modulates intermediate filament assembly. EMBO J. 13 4 (1994) 945-953
45. Orban J., Halasi S., Papp G., Barko S., and Bugyi B. Thermodynamic characterization of different actin isoforms. J. Therm. Anal. Calorimetry 82 1 (2005) 287-290
46. Pan X.X., and Ware B.R. Actin assembly by lithium ions. Biophys. J. 53 1 (1988) 11-16
47. Papp G., Bugyi B., Ujfalusi Z., Halasi S., and Orban J. The effect of pH on the thermal stability of a-actin isoforms. J. Therm. Anal. Calorimetry 82 1 (2005) 281-285
48. Perng M.D., Cairns L., van den I.P., Prescott A., Hutcheson A.M., and Quinlan R.A. Intermediate filament interactions can be altered by HSP27 and alphaB-crystallin. J. Cell Sci. 112 Pt 13 (1999) 2099-2112
49. Perng M.D., Muchowski P.J., van Den I.P., Wu G.J., Hutcheson A.M., Clark J.I., et al. The cardiomyopathy and lens cataract mutation in alphaB-crystallin alters its protein structure, chaperone activity, and interaction with intermediate filaments in vitro. J. Biol. Chem. 274 41 (1999) 33235-33243
50. Perng M.D., Wen S.F., van den I.P., Prescott A.R., and Quinlan R.A. Desmin aggregate formation by R120G alphaB-crystallin is caused by altered filament interactions and is dependent upon network status in cells. Mol. Biol. Cell 15 5 (2004) 2335-2346
51. Prescott A.R., Sandilands A., Hutcheson A.M., Carter J.M., and Quinlan R.A. The intermediate filament cytoskeleton of the lens: An ever changing network through development and differentiation. A minireview. Ophthal. Res. 28 Suppl. 1 (1996) 58-61
52. Quinlan R. Cytoskeletal competence requires protein chaperones. Prog. Mol. Subcell Biol. 28 (2002) 219-233
53. Quinlan R.A., Carte J.M., Sandilands A., and Prescott A.R. The beaded filament of the eye lens: An unexpected key to intermediate filament structure and function. Trends Cell Biol. 6 4 (1996) 123-126
54. Sandilands A., Prescott A.R., Carter J.M., Hutcheson A.M., Quinlan R.A., Richards J., et al. Vimentin and CP49/filensin form distinct networks in the lens which are independently modulated during lens fibre cell differentiation. J. Cell Sci. 108 Pt 4 (1995) 1397-1406
55. Selcen D., and Engel A.G. Myofibrillar myopathy caused by novel dominant negative alpha B-crystallin mutations. Ann. Neurol. 54 6 (2003) 804-810
56. Shu E., Matsuno H., Akamastu S., Kanno Y., Suga H., Nakajima K., et al. alphaB-crystallin is phosphorylated during myocardial infarction: Involvement of platelet-derived growth factor-BB. Arch. Biochem. Biophys. 438 2 (2005) 111-118
57. Singh B.N., Rao K.S., Ramakrishna T., Rangaraj N., and Rao C.M. Association of alphaB-crystallin, a small heat shock protein, with actin: Role in modulating actin filament dynamics in vivo. J. Mol. Biol. 366 3 (2006) 756-767
58. Sun Y., and Macrae T.H. The small heat shock proteins and their role in human disease. FEBS J. 272 11 (2005) 2613-2627
59. Tomokane N., Iwaki T., Tateishi J., Iwaki A., and Goldman J.E. Rosenthal fibers share epitopes with alpha B-crystallin, glial fibrillary acidic protein, and ubiquitin, but not with vimentin. Immunoelectron microscopy with colloidal gold. Am. J. Pathol. 138 4 (1991) 875-885
60. van Rijk A.F., and Bloemendal H. Alpha-B-crystallin in neuropathology. Ophthalmologica 214 1 (2000) 7-12
61. Vicart P., Caron A., Guicheney P., Li Z., Prevost M.C., Faure A., et al. A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat. Genet. 20 1 (1998) 92-95
62. Wang F., Sampogna R.V., and Ware B.R. pH dependence of actin self-assembly. Biophys. J. 55 2 (1989) 293-298
63. Wang K., and Spector A. Alpha-crystallin stabilizes actin filaments and prevents cytochalasin-induced depolymerization in a phosphorylation-dependent manner. Eur. J. Biochem. 242 1 (1996) 56-66
64. Webster K.A. Serine phosphorylation and suppression of apoptosis by the small heat shock protein alphaB-crystallin. Circ. Res. 92 2 (2003) 130-132
65. Whitmore L., and Wallace B.A. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucl. Acids Res. 32 Web Server issue (2004) W668-W673
66. Wisniewski T., and Goldman J.E. Alpha B-crystallin is associated with intermediate filaments in astrocytoma cells. Neurochem. Res. 23 3 (1998) 385-392
67. Yang Z.W., and Babitch J.A. Factors modulating filament formation by bovine glial fibrillary acidic protein, the intermediate filament component of astroglial cells. Biochemistry 27 18 (1988) 7038-7045