Intermediate filament interactions can be altered by HSP27 and αB-crystallin

Journal of Cell Science

Volumn 112, Issue 13, 1999, Pages 2099-2112

  Der Perng, Ming ^a   Cairns, Lindsay ^a   Van Den IJssel, Paul ^a   Prescott, Alan ^a   Hutcheson, Aileen M ^a   Quinlan, Roy A ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

B crystallin; Aggregate; Chaperone; Disease; GFAP; HSP27; Intermediate filament; Myopathy; Small heat shock protein

Indexed keywords

CHAPERONE; CRYSTALLIN; GLIAL FIBRILLARY ACIDIC PROTEIN; HEAT SHOCK PROTEIN 27; INTERMEDIATE FILAMENT PROTEIN; KERATIN;

ARTICLE; ASTROCYTOMA CELL; CELL STRAIN MCF 7; CONTROLLED STUDY; DNA TRANSFECTION; HUMAN; HUMAN CELL; INTERMEDIATE FILAMENT; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; VISCOMETRY;

CELL COMPARTMENTATION; CELL LINE; CRYSTALLINS; CYTOSKELETON; GLIAL FIBRILLARY ACIDIC PROTEIN; HEAT-SHOCK PROTEINS; HUMANS; INTERMEDIATE FILAMENTS; MICROSCOPY, FLUORESCENCE; NEOPLASM PROTEINS; SOLUBILITY; TRANSFECTION;

EID: 0032818827     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. Behlke, J., Lutsch, G., Gaestel, M. and Bielka, H. (1991). Supramolecular structure of the recombinant murine small heat shock protein hsp25. FEBS Lett. 288, 119-122.
2. Bennardini, F., Wrzosek, A. and Chiesi, M. (1992). Alpha B-crystallin in cardiac tissue. Association with actin and desmin filaments. Circ. Res. 71, 288-294.
3. Benndorf, R., Hayess, K., Ryazantsev, S., Wieske, M., Behlke, J. and Lutsch, G. (1994). Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J. Biol. Chem. 269, 20780-20784.
4. Carter, J. M., Hutcheson, A. M. and Quinlan, R. A. (1995). In vitro studies on the assembly properties of the lens beaded filament proteins: Co-assembly with α-crystallin but not with vimentin. Exp. Eye Res. 60, 181-192.
5. Caspers, G. J., Leunissen, J. A. M. and de Jong, W. W. (1995). The expanding small heat-shock protein family and structure predictions of the conserved alpha-crystallin domain. J. Mol. Evol. 40, 238-248.
6. de Jong, W. W., Zweers, A., Versteeg, M. and Nuy-Terwindt, E. C. (1984). Primary structures of the alpha-crystallin A chains of twenty-eight mammalian species, chicken and frog. Eur. J. Biochem. 141, 131-140.
7. de Jong, W. W., Caspers, G. J. and Leunissen, J. A. (1998). Genealogy of the alpha-crystallin-small heat-shock protein superfamily. Int. J. Biol. Macromol. 22, 151-162.
8. Debus, E., Weber, K. and Osborn, M. (1983). Monoclonal antibodies specific for glial fibrillary acidic (GFA) protein and for each of the neurofilament triplet polypeptides. Differentiation 25, 193-203.
9. Djabali, K., deNechaud, B., Landon, F. and Portier, M. M. (1997). alpha B-crystallin interacts with intermediate filaments in response to stress. J. Cell Sci. 110, 2759-2769.
10. Dunn, D. K., Whelan, R. D., Hill, B. and King, R. J. (1993). Relationship of HSP27 and oestrogen receptor in hormone sensitive and insensitive cell lines. J. Steroid Biochem. Mol. Biol. 46, 469-479.
11. Ehrnsperger, M., Graber, S., Gaestel, M. and Buchner, J. (1997). Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J. 16, 221-229.
12. Fuchs, E. and Cleveland, D. W. (1998). A structural scaffolding of intermediate filaments in health and disease. Science 279, 514-519.
13. Goldfarb, L. G., Park, K. Y., Cervenakova, L., Gorokhova, S., Lee, H. S., Vasconcelos, O., Nagle, J. W., Semino-Mora, C., Sivakumar, K. and Dalakas, M. C. (1998). Missense mutations in desmin associated with familial cardiac and skeletal myopathy. Nature Genet. 19, 402-403.
14. Goldman, R. D., Khuon, S., Chou, Y. H., Opal, P. and Steinert, P. M. (1996). The function of intermediate filaments in cell shape and cytoskeletal integrity. J. Cell Biol. 134, 971-983.
15. Gopalakrishnan, S. and Takemoto, L. (1992). Binding of actin to lens alpha crystallins. Curr. Eye Res. 11, 929-933.
16. Green, L. A. and Liem, R. K. (1985). Beta-internexin is a microtubule-associated protein identical to the 70-kDa heat-shock cognate protein and the clathrin uncoating ATPase. J. Biol. Chem. 264, 15210-15215.
17. Guay, J., Lambert, H., GingrasBreton, G., Lavoie, J. N., Huot, J. and Landry, J. (1997). Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylalion of heat shock protein 27. J. Cell Sci. 110, 357-368.
18. Haley, D. A., Horwitz, J. and Stewart, P. L. (1998). The small heat-shock protein, alphaB-crystallin, has a variable quaternary structure. J. Mol. Biol. 277, 27-35.
19. Hopwood, D., Moitra, S., Vojtesek, B., Johnston, D. A., Dillon, J. F. and Hupp, T. R. (1997). Biochemical analysis of the stress protein response in human oesophageal epithelium. Gut 41, 156-163.
20. Huot, J., Houle, F., Rousseau, S., Deschesnes, R. G., Shah, G. M. and Landry, J. (1998). SAPK2/p38-dependent F-actin reorganization regulates early membrane blebbing during stress-induced apoptosis. J. Cell Biol. 143, 1361-1373.
21. Iwaki, T., Kume-Iwaki, A., Liem, R. K. H. and Goldman, J. E. (1989). αB-crystallin is expressed in non-lenticular tissues and accumulates in Alexander's disease brain. Cell 57, 71-78.
22. Iwaki, T., Kume, I. A. and Goldman, J. E. (1990). Cellular distribution of alpha B-crystallin in non-lenticular tissues. J. Histochem. Cytochem. 38, 31-39.
23. Iwaki, T., Iwaki, A., Tateishi, J., Sakaki, Y. and Goldman, J. E. (1993). Alpha-B-crystallin and 27-kd heat-shock protein are regulated by stress conditions in the central-nervous-system and accumulate in rosenthal fibers. Am. J. Pathol. 143, 487-495.
24. Iwaki, T., Iwaki, A., Tateishi, J. and Goldman, J. E. (1994). Sense and antisense modification of glial alpha B-crystallin production results in alterations of stress fiber formation and thermoresistance. J. Cell Biol. 125, 1385-1393.
25. Kato, K., Shinohara, H., Kurobe, N., Goto, S., Inaguma, Y. and Ohshima, K. (1991a). Immunoreactive alpha A crystallin in rat non-lenticular tissues detected with a sensitive immunoassay method. Biochim. Biophys. Acta 1080, 173-180.
26. Kato, K., Shinohara, H., Kurobe, N., Inaguma, Y., Shimizu, K. and Ohshima, K. (1991b). Tissue distribution and developmental profiles of immunoreactive aB crystallin in the rat non-lenticular tissues determined with a sensitive immunoassay system. Biochim. Biophvs. Acta 1074, 201-208.
27. Kato, S., Hirano, A., Umahara, T., Llena, J. F., Herz, F. and Ohama, E. (1992). Ultrastructural and immunohistochemical studies on ballooned cortical neurons in Creutzfeldt-Jakob disease: expression of alpha B-crystallin. ubiquitin and stress-response protein 27. Acta Neuropathol. Berl. 84, 443-448.
28. Kato, K., Ito, H., Kamei, K., Inaguma, Y., Iwamoto, I. and Saga, S. (1998). Phosphorylation of alphaB-crystallin in mitotic cells and identification of enzymatic activities responsible for phosphorylation. J. Biol. Chem. 273, 28346-28354.
29. Kegel, K. B., Iwaki, A., Iwaki, T. and Goldman, J. E. (1996). Alpha-b-crystallin protects glial-cells from hypertonic stress. Am. J. Physiol.-Cell Physiol. 39, C 903-C 909.
30. King, R. J., Finley, J. R., Coffer, A. I., Millis, R. R. and Rubens, R. D. (1987). Characterization and biological relevance of a 29-kDa, oestrogen receptor-related protein. J. Steroid Biochem. 27, 471-475.
31. Laemmli, U. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277, 680-685.
32. Lavoie, J. N., Hickey, E., Weber, L. A. and Landry, J. (1993). Modulation of actin microfilament dynamics and fluid phase pinocytosis by phospnorylation of heat shock protein 27. J. Biol. Chem. 268, 24210-24214.
33. Liao, J., Lowthert, L. A., Ghori, N. and Omary, M. B. (1995). The 70-kDa heat shock proteins associate with glandular intermediate filaments in an ATP-dependent manner. J. Biol. Chem. 270, 915-922.
34. MacLean-Fletcher, S. and Pollard, T. D. (1980). Identification of a factor in conventional muscle actin preparations which inhibits actin filament self-association. Biochem. Biophys. Res. Commun. 96, 18-27.
35. Magin, T. M., Schroder, R., Leitgeb, S., Wanninger, F., Zatloukal, K., Grund, C. and Melton, D. W. (1998). Lessons from keratin 18 knockout mice: formation of novel keratin filaments, secondary loss of keratin 7 and accumulation of liver- specific keratin 8-positive aggregates. J. Cell Biol. 140, 1441-1451.
36. Mann, E., McDermott, M. J., Goldman, J., Chiesa, R. and Spector, A. (1991). Phosphorylation of alpha-crystallin B in Alexander's disease brain. FEBS Lett. 294, 133-136.
37. Menko, A. S., Croop, J., Toyama, Y., Holtzer, H. and Boettiger, D. (1982) The response of chicken embryo dermal fibroblasts to cytochalasin B is altered by Rous sarcoma virus-induced cell transformation. Mol. Cell Biol. 2, 320-330.
38. Merck, K. B., Groenen, P. J., Voorter, C. E., de Haard Hoekman, W. A., Horwitz, J., Bloemendal, H. and de Jong, W. W. (1993). Structural and functional similarities of bovine alpha-crystallin and mouse small heat-shock protein. A family of chaperones. J. Biol. Chem. 268, 1046-1052.
39. Messing, A., Head, M. W., Galles, K., Galbreath, E. J., Goldman, J. E. and Brenner, M. (1998). Fatal encephalopathy with astrocyte inclusions in GFAP transgenic mice. Am. J. Pathol. 152, 391-398.
40. Miron, T., Wilchek, M. and 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.
41. Miron, T., Vancompernolle, K., Vandekerckhove, J., Wilchek, M. and Geiger, B. (1991). A 25-kd inhibitor of actin polymerization is a low-molecular mass heat-shock protein. J. Cell Biol. 114, 255-261.
42. Muchowski, P. J., Valdez, M. M. and Clark, J. I. (1999). αB-crystallin selectively targets intermediate filament proteins during thermal stress. Invest. Ophthalmol. Vis. Sci. 40, 951-958.
43. Munoz-Marmol, A. M., Strasser, G., Isamat, M., Coulombe, P. A., Yang, Y., Roca, X., Vela, E., Mate, J. L., Coll, J., Fernandez-Figueras, M. T., et al. (1998). A dysfunctional desmin mutation in a patient with severe generalized myopathy. Proc. Nat. Acad. Sci. USA 95, 11312-11327.
44. Napolitano, E. W., Pachter, J. S., Chin, S. S. and Liera, R. K. (1985). beta-Internexin, a ubiquitous intermediate filament-associated protein. J. Cell Biol. 101, 1323-1331.
45. Nicholl, I. D. and Quinlan, R. A. (1994). Chaperone activity of α-crystallins modulates intermediate filament assembly. EMBO J. 13, 945-953.
46. Okabe, S., Miyasaka, H. and Hirokawa, N. (1993). Dynamics of the neuronal intermediate filaments. J. Cell Biol. 121, 375-386.
47. Porter, R. M., Hutcheson, A. M., Rugg, E. L., Quinlan, R. A. and Lane, E. B. (1998). cDNA cloning, expression and assembly characteristics of mouse keratin 16. J. Biol. Chem. 273, 32265-32272.
48. Prescott, A. R., Dowrick, P. G. and Warn, R. M. (1992). Stable and slow-turning-over microtubules characterize the processes of motile epithelial cells treated with scatter factor. J. Cell Sci. 102, 103-112.
49. Quinlan, R. A., Carter, J. M., Sandilands, A. and Prescott, A. R. (1996). The beaded filament of the eye lens: an unexpected key to intermediate filament structure and function. Trends Cell Biol. 6, 123-126.
50. Quinlan, R. and van den IJssel, P. (1999). Fatal attraction: when chaperone turns harlot. Nature Med. 5, 25-26.
51. Ralton, J. E., Lu, X., Hutcheson, A. M. and Quinlan, R. A. (1994). Identification of two N-terminal non-alpha-helical domain motifs important in the assembly of glial fibrillary acidic protein. J. Cell Sci. 107, 1935-1948.
52. Rouse, J., Cohen, P., Trigon, S., Morange, M., Alonso Llamazares, A., Zamanillo, D., Hunt, T. and Nebreda, A. R. (1994). A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell 78, 1027-1037.
53. Sawada, K., Agata, K., Yoshiki, A. and Eguchi, G. (1993). A set of anti-crystallin monoclonal-antibodies for detecting lens specificities - beta-crystallin as a specific marker for detecting lentoidogenesis in cultures of chicken lens epithelial-cells. Jpn J. Ophthalmol. 37, 355-368.
54. Söllner, P., Quinlan, R. A. and Franke, W. W. (1985) Identification of a distinct soluble subunit of an intermediate filament protein: tetrameric vimentin from living cells. Proc. Nat. Acad. Sci. USA 82, 7929-7933.
55. Srinivasan, A. N., Nagineni, C. N. and Bhat, S. P. (1992). alpha A-crystallin is expressed in non-ocular tissues. J. Biol. Chem. 267, 23337-23341.
56. Studier, F. W., Rosenberg, A. H., Dunn, J. J. and Dubendorff, J. W. (1990). Use of T7 RNA polymerase to direct expression of cloned genes. Meth. Enzymol. 185, 60-89.
57. Sun, T. X., Das, B. K. and Liang, J. J. N. (1997). Conformational and functional differences between recombinant human lens alpha A- and alpha B-crystallin. J. Biol. Chem. 272, 6220-6225.
58. Tabor, S. and Richardson, C. C. (1985). A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive epression of specific genes. Proc. Nat. Acad. Sci. USA 82, 1074-1078.
59. van de Klundert, F. A. J. M., Gijsen, M. L. J., van den IJssel, P. R. L. A., Snoeckx, L. H. E. H. and de Jong, W. W. (1998). alpha B-crystallin and hsp25 in neonatal cardiac cells - differences in cellular localization under stress conditions. Eur. J. Cell Biol. 75, 38-45.
60. Vicart, P., Caron, A., Guicheney, P., Li, Z., Prevost, M. C., Faure, A., Chateau, D., Chapon, F., Tome, F., Dupret, J. M., et al. (1998). A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nature Genet. 20, 92-95.
61. Vikstrom, K. L., Lim, S. S., Goldman, R. D. and Borisy, G. G. (1992). Steady state dynamics of intermediate filament networks. J. Cell Biol. 118, 121-129.
62. Wang, K. and Spector, A. (1996). α-crystallin stabilises actin filaments and prevents cytochalasin-induced depolymerisation in a phosphorylation-dependent manner. Eur. J. Biochem. 242, 56-66.
63. Welch, W. J. and Feramisco, J. R. (1985). Rapid purification of mammalian 70,000-dalton stress proteins: affinity of the proteins for nucleotides. Mol. Cell Biol. 5, 1229-1237.
64. Welch, W. J. and Suhan, J. P. (1985). Morphological study of the mammalian stress response: characterization of changes in cytoplasmic organelles, cytoskeleton and nucleoli and appearance of intranuclear actin filaments in rat fibroblasts after heat-shock treatment. J. Cell Biol. 101, 1198-1211.
65. Wessel, D. and Flügge, U. I. (1984). A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141-143.
66. Wisniewski, T. and Goldman, J. E. (1998). alpha B-crystallin is associated with intermediate filaments in astrocytoma cells. Neurochem. Res. 23, 385-392.
67. Zantema, A., M., V.-D. V., Maasdam, D., Bol, S. and Van der Eb, A. (1992). Heat shock protein 27 and alpha B-crystallin can form a complex, which dissociates by heat shock. J. Biol. Chem. 267, 12936-12941.