-Crystallin stabilizes actin filaments and prevents cytochalasin-induced depolymerization in a phosphorylation-dependent manner

European Journal of Biochemistry

Volumn 242, Issue 1, 1996, Pages 56-66

  Wang, Keyang ^a   Spector, Abraham ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Crystallin; Actin; Heat shock protein; Phosphorylation; Stabilization

Indexed keywords

ACTIN; ALPHA CRYSTALLIN; CYTOCHALASIN D; LENS PROTEIN; CRYSTALLIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL TISSUE; ARTICLE; CATTLE; CONTROLLED STUDY; DEPOLYMERIZATION; FLUORESCENCE; LENS EPITHELIUM; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RABBIT; SKELETAL MUSCLE; ANIMAL; CHEMISTRY; METABOLISM; MOLECULAR WEIGHT; PHOSPHORYLATION; SPECTROFLUOROMETRY;

ANIMALIA; BOS TAURUS; ORYCTOLAGUS CUNICULUS;

ACTINS; ANIMALS; CRYSTALLINS; CYTOCHALASIN D; MOLECULAR WEIGHT; MUSCLE, SKELETAL; PHOSPHORYLATION; RABBITS; SPECTROMETRY, FLUORESCENCE;

EID: 0029658123     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1996.0056r.x     Document Type: Article

References (82)

1. Bloemendal, H. (1981) The lens proteins, in Molecular and cellular biology of the eye lens (Bloemendal, H., ed.) pp. 1-47, John Wiley & Sons, Inc., New York.
2. Spector, A., Li, L., Augusteyn, R. C., Schneider, A. & Freund, T. (1971) The isolation and characterization of distinct macromolecular fractions, Biochem. J. 124, 337-343.
3. Bloemendal, H. & de Jong, W. W. (1991) Lens proteins and their genes, Progr. Nucleic Acid Res. Mol. Biol. 41, 259-281.
4. 2 but phosphorylation has no effect on chaperone activity, Exp. Eye Res. 61, 115-124.
5. Augusteyn, R. C., Koretz, J. F. & Schurtenberger, P. (1989) The effect of phosphorylation on the structure of α-crystallin, Biochim. Biophys. Acta 999, 293-299.
6. B-crystallin is present in other ocular and non-ocular tissues, Biochem. Biophys. Res. Commun. 158, 319-325.
7. B-crystallin is expressed in non-lenticular tissues and accumulates in Alexander's disease brain, Cell 57, 71-78.
8. Longoni, S., Lattonen, S., Bullock, G. & Chiesi, M. (1990) Cardiac α-crystallin, Mol. Cell. Biochem. 97, 113-128.
9. B-crystallin in the absence of stress, J. Cell Biol. 120, 639-645.
10. A-crystallin in rat non-lenticular tissues detected with a sensitive immunoassay method, Biochim. Biophys. Acta 1080, 173-180.
11. A-crystallin is expressed in non-ocular tissues, J. Biol. Chem. 267, 23337-23341.
12. B-crystallin in the retina, J. Biol. Chem. 269, 16853-16861.
13. Ingolia, T. D. & Craig, E. A. (1982) Four small Drosophila heat-shock proteins are related to each other and to mammalian α-crystallin, Proc. Natl Acad. Sci. USA 79, 2360-2364.
14. B-crystallin is a small heat-shock protein, Proc. Natl Acad. Sci. USA 88, 3652-3656.
15. Merck, K. B., Groenen, P. J. T. A., Voorter, C. E. M., de Haard-Hoekman, A., Horwitz, J., Bloemendal, H. & de Jong, W. W. (1993) Structural and functional similarities of bovine α-crystallin and mouse small heat-shock protein, J. Biol. Chem. 268, 1046-1052.
16. B-crystallin by heat-shock in rat glioma GA-1 cells, Biochem. Biophys. Res. Commun. 182, 844-850.
17. B-crystallin expression, Exp. Eye Res. 54, 461-470.
18. Horwitz, J. (1992) α-Crystallin can function as a molecular chaperone, Proc. Natl Acad. Sci. USA 89, 10449-10453.
19. Horwitz, J. (1993) The function of α-crystallin, Invest. Ophthalmol. Visual Sci. 34, 10-22.
20. Jakob, U., Gaestel, M., Engel, K. & Buchner, J. (1993) Small heat-shock proteins are molecular chaperones, J. Biol. Chem. 268, 1517-1520.
21. Rao, P. V., Horwitz, J. & Zigler, J. S. Jr (1993) α-Crystallin, a molecular chaperone, forms a stable complex with carbonic anhydrase upon heat denaturation, Biochem. Biophys. Res. Commun. 190, 786-793.
22. Horwitz, J., Emmons, T. & Takemoto, L. (1993) The ability of lens α-crystallin to protect against heat-induced aggregation is age-dependent, Curr. Eye Res. 11, 817-822.
23. Wang, K. & Spector, A. (1994) The chaperone activity of bovine α-crystallin: interaction with other lens crystallins in native and denatured states, J. Biol. Chem. 269, 13601-13608.
24. Wang, K. & Spector, A. (1995) α-Crystallin can act as a chaperone under conditions of oxidative stress, Invest. Ophthalmol. Visual Sci. 36, 311-321.
25. Borkman, R. F., Knight, G. & Obi, B. (1996) The molecular chaperone α-crystallin inhibits UV-induced protein aggregation, Exp. Eye Res. 62, 141-148.
26. Ganea, E. & Harding, J. J. (1995) Molecular chaperones protect against glycation-induced inactivation of glucose-6-phosphate dehydrogenase, Eur. J. Biochem. 231, 181-185.
27. Chiesa, R., McDermott, M. J. & Spector, A. (1989) Differential synthesis and phosphorylation of the α-crystallin A and B chains during bovine lens fiber cell differentiation, Curr. Eye Res. 8, 151-158.
28. Spector, A., Chiesa, R., Sredy, J. & Garner, W. (1985) cAMP-dependent phosphorylation of bovine lens alphα-crystallin, Proc. Natl Acad. Sci. USA 82, 4712-4716.
29. Voorter, C. E. M., Mulders, J. W. M., Bloemendal, H. & de Jong, W. W. (1986) Some aspects of the phosphorylation of α-crystallin A, Eur. J. Biochem. 160, 203-210.
30. Chiesa, R., Gawinowicz-Kolks, M. A. & Spector, A. (1987) The phosphorylation of the primary gene products of α-crystallin, J. Biol. Chem. 262, 1438-1441.
31. Chiesa, R., Gawinowicz-Kolks, M. A., Kleiman, N. J. & Spector, A. (1987) Identification of the specific phosphorylated serine in the bovine alphα crystallin A1 chain, Curr. Eye Res. 6, 539-542.
32. Chiesa, R., Gawinowicz-Kolks, M. A., Kleiman, N. J. & Spector, A. (1987) The phosphorylation sites of the B2 chain of bovine α-crystallin, Biochem. Biophys. Res. Commun. 144, 1340-1347.
33. B-crystallin, FEBS Lett. 259, 50-52.
34. Kantorow, M. & Piatigorsky, J. (1994) α-Crystallin/small heat-shock protein has autokinase activity, Proc. Natl Acad. Sci. USA 91, 3112-3116.
35. Kantorow, M., Horwitz, J., van Boekel, M. A. M., de Jong, W. W. & Piatigorsky, J. (1995) Conversion from oligomers to tetramers enhances autophosphorylation by lens αA-crystallin, J. Biol. Chem. 270, 17215-17220.
36. Arrigo, A.-P. & Landry, J. (1994) Expression and function of the low-molecular-weight heat-shock proteins, in The biology of heat-shock proteins and molecular chaperones (Morimoto, R. I., Tissieres, A. & Georgopoulos, C., eds) pp. 335-373, Cold Spring Harbor Laboratory Press, Plainview, New York.
37. Nicholl, I. D. & Quinlan, R. A. (1994) Chaperone activity of α-crystallins modulates intermediate filament assembly, EMBO J. 13, 945-953.
38. Del Vecchio, P., MacElroy, K., Rosser, M. & Church, R. (1984) Association of alpha-crystallin with actin in cultured lens cells, Curr. Eye Res. 3, 1213-1219.
39. Benedetti, L., Dunia, I., Ramaekers, F. C. S. & Kibbelaar, M. A. (1981) Lenticular plasma membranes and cytoskeleton, in Molecular and cellular biology of the eye lens (Bloemendal, H., ed.) pp. 137, John Wiley and Sons, New York.
40. Bennardini, F., Wrzosek, A. & Chiesi, M. (1992) αB-Crystallin in cardiac tissue. Association with actin and desmin filaments, Circ. Res. 71, 288-294.
41. Gopalakrishnan, S. & Takemoto, L. (1992) Binding of actin to lens alpha crystallins, Curr. Eye Res. 11, 929-933.
42. Kabsch, W. & Vandekerckhove, J. (1992) Structure and function of actin, Annu. Rev. Biophys. Biomol. Struct. 21, 49-76.
43. Janmey, P. A. (1991) Mechanical properties of cytoskeletal polymers, Curr. Opin. Cell Biol. 3, 4-11.
44. Pollard, T. D. & Cooper, J. A. (1986) Actin and actin-binding proteins. A critical evaluation of mechanisms and functions, Annu. Rev. Biochem. 55, 987-1035.
45. Cooper, J. A. (1992) Actin filament assembly and organization in vitro, in The cytoskeleton (Carraway, K. L. & Carraway, G. A. C., eds) pp. 47-72, Oxford University Press, New York.
46. Korn, E. D., Carlier, M. F. & Pantaloni, D. (1987) Actin polymerization and ATP hydrolysis, Science 238, 638-644.
47. 2+-induced process at pH 8 and 20 degrees C, Proc. Natl Acad. Sci. USA 80, 6513-6517.
48. Cooper, J. A., Buhle, E. L. Jr, Walker, S. B., Tsong, T. Y. & Pollard, T. D. (1983) Kinetic evidence for a monomer activation step in actin polymerization, Biochemistry 22, 2193-2202.
49. Vandekerckhove, J. (1990) Actin-binding proteins, Curr. Opin. Cell Biol. 2, 41-50.
50. Sun, H.-Q., Kwiatkowska, K. & Yin, H. L. (1995) Actin monomer binding proteins, Curr. Opin. Cell Biol. 7, 102-110.
51. Otto, J. J. (1994) Actin-bundling proteins, Curr. Opin. Cell Biol. 6, 105-109.
52. Kouyama, T. & Mihashi, K. (1981) Fluorimetry study of N-(1-pyrenyl)iodoacetamide-labelled F-actin, Eur. J. Biochem. 114, 33-38.
53. Cooper, J. A., Walker, S. B. & Pollard, T. D. (1983) Pyrene actin: documentation of the validity of a sensitive assay for actin polymerization, J. Muscle Res. Cell Motil. 4, 253-262.
54. Rafferty, N. S. (1985) Lens morphology, in The ocular lens: structure, function & pathology (Maisel, H., ed.) pp. 1-60, Marcel Dekker, Inc., New York.
55. Mousa, G. Y. & Trevithick, J. R. (1977) Differentiation of rat lens epithelial cells in tissue culture. II. Effects of cytochalasins B and D on actin organization and differentiation, Dev. Biol. 60, 14-25.
56. Mousa, G. Y., Creighton, M. O. & Trevithick, J. R. (1979) Eye lens opacity in cortical cataracts associated with actin-related globular degeneration, Exp. Eye Res. 29, 379-391.
57. Zigman, S., Rafferty, N. S., Scholz, D. L. & Lowe, K. (1992) The effects of near-UV radiation on elasmobranch lens cytoskeletal actin, Exp. Eye Res. 55, 193-201.
58. Rafferty, N. S., Zigman, S., McDaniel, T. & Scholz, D. L. (1993) Near-UV radiation disrupts filamentous actin in lens epithelial cells, Cell Motil. Cytoskel. 26, 40-48.
59. Lavoie, J. N., Hickey, E., Weber, L. A. & Landry, J. (1993) Modulation of actin microfilament dynamics and fluid phase pinocytosis by phosphorylation of heat-shock protein 27, J. Biol. Chem. 268, 24210-24214.
60. Lavoie, J. N., Gingras-Breton, G., Tanguay, R. M. & Landry, J. (1993) Induction of Chinese hamster HSP27 gene expression in mouse cells confers resistance to heat-shock, J. Biol. Chem. 268, 3420-3429.
61. Iwaki, T., Iwaki, A., Tateishi, J. & Goldman, J. E. (1994) Sense and antisense modification of glial αB-crystallin production results in alterations of stress fiber formation and thermoresistance, J. Cell Biol. 125, 1385-1393.
62. Roy, D. & Spector, A. (1976) Human alphα-crystallin, characterization of the protein isolated from the periphery of cataractous lenses, Biochemistry 15, 1180-1188.
63. Stoscheck, C. M. (1990) Quantitation of protein, Methods Enzymol. 182, 50-68.
64. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem. 72, 248-254.
65. Spudich, J. A. & Watt, S. (1971) The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin, J. Biol Chem. 246, 4866-4871.
66. Houk, T. W. Jr & Ue, K. (1974) The measurement of actin concentration in solution: a comparison of methods, Anal. Biochem. 62, 66-74.
67. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
68. Chiesa, R., McDermott, M. J. & Spector, A. (1989) Differential synthesis and phosphorylation of the α-crystallin A and B chains during bovine lens fiber cell differentiation, Curr. Eye Res. 8, 151-158.
69. Chiesa, R. & Spector, A. (1989) The dephosphorylation of the lens α-crystallin A chain, Biochem. Biophys. Res. Commun. 162, 1495-1501.
70. Rahman, D. R. J., Bentley, N. J. & Tuite, M. F. (1995) The Saccharomyces cerevisiae small heat-shock protein Hsp26 inhibits actin polymerisation, Biochem. Soc. Trans. 23, 775S.
71. Vanderkerchove, J. & Weber, K. (1978) Actin amino-acid sequences. Comparison of actins from calf thymus, bovine brain, and SV40-transformed mouse 3T3 cells with rabbit skeletal, Eur. J. Biochem. 90, 451-462.
72. van der Ouderaa, F. J., de Jong, W. W., Hiderink, A. & Bloemendal, H. (1974) The amino-acids sequence of the alphaB2 chain of bovine alpha-crystallin, Eur. J. Biochem. 49, 157-168.
73. Kibbelaur, M. A., Seten-Versteegan, A. M., Dunia, I., Benedetti, E. I. & Bloemendal, H. (1979) Actin in mammalian lens, Eur. J. Biochem. 95, 543-549.
74. Fitzgerald, P. & Graham, D. (1991) Ultrastructural localization of αA-crystallin to the bovine lens fiber cell cytoskeleton, Curr. Eye Res. 10, 417-436.
75. Bloemendal, H., Berbera, G., de Jong, W., Ramaekers, R., Vermorken, A., Dunia, E. & Benedetti, L. (1984) Interaction of crystallins with the cytoskeletal-plasma membrane complex of the bovine lens, Ciba Found. Symp. 106, 177-190.
76. Miron, T., Vancompernolle, K., Vandekerckhove, J., Wilchek, M. & Geiger, B. (1991) A 25-kD inhibitor of actin polymerization is a low molecular mass heat-shock protein, J. Cell Biol. 114, 255-261.
77. Miron, T., Wilchek, M. & Geiger, B. (1988) Characterization of an inhibitor of actin polymerization in vinculin-rich fraction of turkey gizzard smooth muscle, Eur. J. Biochem. 178, 543-553.
78. Benndorf, R., Hayess, K., Ryazantsev, S., Wieske, M., Behlke, J. & Lutsch, G. (1994) Phosphorylation and supramolecular organization of murine sHSP25 abolish its actin polymerization-inhibiting activity, J. Biol. Chem. 269, 20780-20784.
79. Knauf, U., Jakob, U., Engel, K., Buchner, J. & Gaestel, M. (1994) Stress- and mitogen-induced phosphorylation of small heat-shock protein HSP25 by MAPKAP kinase 2 is not essential for chaperone properties and cellular thermoresistance, EMBO J. 13, 54-60.
80. 2+-dependent processes during heat-shock: role in cell thermoresistance, Radiat. Res. 113, 426-436.
81. Crete, P. & Landry, J. (1990) Induction of HSP27 phosphorylation and thermoresistance in Chinese hamster cells by arsenite, cycloheximide, A23187, and EGTA, Radiat. Res. 121, 320-327.
82. Lavoie, J. N., Lambert, H., Hickey, E., Weber, L. A. & Landry, J. (1995) Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat-shock protein 27, Mol. Cell. Biol. 15, 505-516.