Mutational analysis of Hsp9Oα dimerization and subcellular localization: Dimer disruption does not impede 'in vivo' interaction with estrogen receptor

Journal of Cell Science

Volumn 109, Issue 7, 1996, Pages 1677-1687

  Meng, Xia ^a   Devin, Jocelyne ^a   Sullivan, William P ^b   Toft, David ^b   Baulieu, Etienne Emile ^a   Catelli, Maria Grazia ^a  

^a INSERM   (France)

^b MAYO CLINIC   (United States)

Author keywords

Dimerization; Estrogen receptor; Hsp90; Mutagenesis; Subcellular localization; Yeast viability

Indexed keywords

CHAPERONE; ESTROGEN RECEPTOR; HEAT SHOCK PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELLULAR DISTRIBUTION; DELETION MUTANT; DIMERIZATION; GENE MUTATION; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL;

EID: 0029922568     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (70)

1. Aligue, R., Akhavan-Niak, H. and Russell, P. (1994). A role for hsp90 in cell cycle control: Weel tyrosine kinase activity requires interaction with hsp90. EMBO J. 13, 6099-6106.
2. Akner, G., Mossberg, K., Sudquist, K. G., Gustafsson, J. R. and Wikström, A. C. (1992). Evidence for reversible, non-microtube and non-microfilament-dependant nuclear translocation of hsp90 after heat shock in human fibroblasts. Eur. J. Cell Biol. 58, 356-364.
3. Baulieu, E. E. and Catelli, M. G. (1989). Steroid hormone receptors and heat shock protein Mr 90,000 (HSP90): a functional interaction? In Stress-Induced Proteins (ed. M. L. Pardue, J. R. Feramiso and S. Lindquist), pp. 203-219, Alan R. Liss, Inc., New York.
4. Binart, N., Lombes, M. and Baulieu, E. E. (1995). Distinct functions of hsp90 on oestrogen and mineralocoticosteroid receptor activity: effects of hsp90 deletion mutants. Biochem. J. 311, 797-804.
5. Bohen, S. P. and Yamamoto, K. R. (1993). Isolation of hsp90 mutants by screening for decreased steroid receptor function. Proc. Nat. Acad. Sci. USA 90, 11424-11428.
6. Bohen, S. P., Kralli, A. and Yamamoto, K. R. (1995). Hold'em and fold'em: chaperones and signal transduction. Science 268, 1303-1304.
7. Bohen, S. P. (1995). Hsp90 mutants disrupt glucocorticoid receptor ligand binding and destabilize aporeceptor complexes. J. Biol. Chem. 270, 29433-29438.
8. Borkovich, K. A., Farrelly, F. W., Finkelstein, D. B., Taulien, J. and Lindquist, S. (1989). Hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol. Cell Biol. 9, 3919-3930.
9. Braig, K., Otwinowski, Z., Hegde, R., Boisvert, D. C., Joachimiak, A., Horwich, A. L. and Sigler, P. B. (1994). The crystal structure of the bacterial chaperonin GroEL at 2.8 A. Nature 371, 578-586.
10. Bresnick, E. H., Dalman, F. C., Sanchez, E. R. and Pratt, W. B. (1989). Evidence that the 90kDa heat shock protein is necessary for the steroid binding conformation of the L cell glucocorticoid receptor. J. Biol. Chem. 264, 4992-4997.
11. Brugge, J. S. (1986). Interaction of the Rous sarcoma virus protein pp60src with the cellular proteins pp50 and pp90. Curr. Top. Microbiol. Immunol. 123, 1-22.
12. Cadepond, F., Schweizer-Groyer, G., Segard-Maurel, I., Jibard, N., Hollenberg, S. M., Giguère, V., Evans, R. M. and Baulieu, E. E. (1991). Heat shock protein 90 as a critical factor in maintaining glucocorticoid receptor in a nonfunctional state. J. Biol. Chem. 266, 5834-5841.
13. Cadepond, F., Binart, N., Chambraud, B., Jibard, N., Schweizer-Groyer, G., Segard-Maurel, I. and Baulieu, E. E. (1993). Interaction of glucocorticoid receptor and wild-type or mutated 90-kDa heat shock protein coexpressed in baculovirus-infecled Sf9 cells. Proc. Nat. Acad. Sci. USA 90, 10434-10438.
14. Carver, L. A., Jackiw, V. and Bradrield, C. A. (1994). The 90-kDa heat shock protein is essential for Ah receptor signaling in a yeast expression system. J. Biol. Chem. 269, 30109-30112.
15. Catelli, M. G., Binart, N., Jung-Testas, I., Renoir, J. M., Baulieu, E. E., Feramisco, J. R. and Welch, W. J. (1985). The common 90-kd protein component of non-transformed '8S' steroid receptors is a heat-shock protein. EMBOJ. 4, 3131-3135.
16. Chambraud, B., Berry, M., Redeuilh, G., Chambon, P. and Baulieu, E. E. (1990). Several regions of human estrogen receptor are involved in the formation of receptor-heat shock protein 90 complexes. J. Biol. Chem. 265, 20686-20691.
17. Chang, H.-C. J. and Lindquist, S. (1994). Conservation of hsp90 macromolecular complexes in Saccharomyces cerevisiae. J. Biol. Chem. 269, 24983-24988.
18. Collier, N. C. and Schlessinger, M. J. (1986). The dynamic state of heat shock proteins in chicken embryo fibroblastes. J. Cell Biol. 103, 1495-1507.
19. Coumailleau, P., Billoud, B., Sourrouille, P., Moreau, N. and Angelier, N. (1995). Evidence for a 90 kDa heat-shock protein gene expression in the amphibian oocyte. Dev. Biol. 168, 247-258.
20. Cutforth, T. and Rubin, G. M. (1994). Mutations in hsp83 and cdc37 impair signaling by the sevenless receptor tyrosine kinase in Drosophila. Cell 77, 1027-1036.
21. Denis, M., Cuthill, S., Wikström, A.-C., Poellinger, L. and Gustafsson, J.-A. (1988). Association of the dioxin receptor with the Mr 90,000 heat shock protein: a structural kinship with the glucocorticoid receptor. Biochem. Biophys. Res. Commun. 155, 801-807.
22. Dingwall, C. and Laskey, R. A. (1991). Nuclear targeting sequences - a consensus? Trends Biochem. Sci. 16, 478-481.
23. Flaherty, K. M., DeLuca-Flaberty, C. and McKay, D. B. (1990). Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature 346, 623-628.
24. Gasc, J. M., Renoir, J. M., Radanyi, C., Joab, I., Tuohimaa, P. and Baulieu, E. E. (1984). Progesterone receptor in the chick oviduct: an immunohistochemical study with antibodies to distinct receptor components. J. Cell Biol. 99, 1193-1201.
25. Greene, G. L., Sobel, N. B., King, W. J. and Jensen, E. V. (1984). Immunochemical studies of estrogen receptors. J. Steroid Biochem. 20, 51-56.
26. Guiochon-Mantel, A., Loosfelt, H., Lescop, P., Sar, S., Atger, M., Perrot-Applanat, M. and Milgrom, E. (1989). Mechanisms of nuclear localization of the progesterone receptor: evidence for interaction between monomers. Cell 57, 1147-1154.
27. Inanobe, A., Takahashi, K. and Katada, T. (1994). Association of the beta gamma subunits of trimeric GTP-binding proteins with 90-kDa heat shock protein, hsp90. J. Biochem. (Tokyo) 115, 486-492.
28. Jakob, U. and Buchner, J. (1994). Assisting spontaneity: the role of hsp90 and small hsps as molecular chaperones. Trends Biochem. Sci. 19, 205-211.
29. Jakob, U., Meyer, I., Bügl, H., André, S., Bardwell, J. C. A. and Buchner, J. (1995). Structure organization of procaryotic and eucaryotic Hsp90 - Influence of divalent cations on structure and function. J. Biol. Chem. 270, 1-8.
30. Johnson, J. L. and Toft, D. (1995). Binding of p23 and hsp90 during assembly with the progesterone receptor. Mol. Endocrinol. 9, 670-678.
31. Kang, K. I., Devin, J., Cadepond, F., Jibard, N., Guiochon-Mantel, A., Baulieu, E. E. and Catelli, M. G. (1994). In vivo functional protein-protein interaction: nuclear targeted hsp90 shifts cytoplasmic steroid receptor mutants into the nucleus. Proc. Nat. Acad. Sci. USA 91, 340-344.
32. Kimura, Y., Yahara, I. and Lindquist, S. (1995). Role of the protein chaperone YDJI in establishing hsp90-mediated signal transduction pathways. Science 268, 1362-1365.
33. Kolodziej, P. A. and Young, R. A. (1991). Epitope tagging and protein surveillance. Meth. Enzymol. 194, 308-519.
34. Koyasu, S., Nishida, E., Kadowaki, T., Matsuzami, F., Iida, K., Harada, F., Kasuga, M., Sakai, H. and Yahara, I. (1986). Two mammalian heat shock proteins, hsp90 and hsp100, are actin-binding proteins. Proc. Nat. Acad. Sci. USA 83, 8054-8058.
35. Lebeau, M. C., Massol, N., Herrick, J., Faber, L. E., Renoir, J. M., Radanyi, C. and Baulieu, E. E. (1992). P59, an hsp90-binding protein. J. Biol. Chem. 267, 4281-4284.
36. Le Douarin, B., Zechel, C., Gamier, J. M., Lutz, Y., Tora, L., Pierrat, B., Heery, D., Gronemeyer, H., Chambon, P. and Losson, R. (1995). The N-terminal part of TIF1, a putative mediator of the ligand-dependent activation function (AF-2) of nuclear receptors, is fused to B-raf in the oncogenic protein T18. EMBO J. 14, 2020-2033.
37. Meng, X., Jérôme, V., Devin, J., Baulieu, E. E. and Catelli, M. G. (1993). Cloning of chicken hsp90β: the only vertebrate hsp90 insensitive to heat shock. Biochem. Biophys. Res. Commun. 2, 630-636.
38. Michael, S. F. (1994). Mutagenesis by incorporation of a phosphorylated oligo during PCR amplification. Biotechniques 16, 410-412.
39. Minami, Y., Kawasaki, H., Miyata, Y., Suzuki, K. and Yahara, I. (1991). Analysis of native forms and isoforms composition of mouse 90-kDa heat shock protein, hsp90. J. Biol. Chem. 266, 10099-10103.
40. Minami, Y., Kawasaki, H., Suzuki, K. and Yahara, I. (1993). The calmodulin-binding domain of mouse 90-kDa heat shock protein. J. Biol. Chem. 268, 9604-9610.
41. Minami, Y., Kimura, Y., Kawasaki, H., Suzuki, K. and Yahara, I. (1994). The carboxy-terminal region of mammalian hsp90 is required for its dimerization and function in vivo. Mol. Cell Biol. 14, 1459-1464.
42. Miyata, Y. and Yahara, I. (1992). The 90-kDa heat shock protein, hsp90, binds and protects casein kinase II from self-aggregation and enhances its kinase activity. J. Biol. Chem. 267, 7042-7047.
43. Moncharmont, B., Su, J.-L. and Parikh, I. (1982). Monoclonal antibodies against estrogen receptor: interaction with different molecular forms and functions of the receptor. Biochemistry 21, 6916-6921.
44. Nadeau, K., Das, A. and Walsh, C. T. (1993). Hsp90 chaperonins possess ATPase activity and bind heat shock transcription factors and peptidyl prolyl isomerases. J. Biol. Chem. 268, 1479-1487.
45. Nathan, D. F. and Lindquist, S. (1995). Mutational analysis of hsp90 function: interactions with a steroid receptor and a protein kinase. Mol. Cell. Biol. 15, 3917-3925.
46. Nemoto, T., Ohara-Nemoto, Y., Ota, M., Takagi, T. and Yokoyama, K. (1995). Mechanism of dimer formation of the 90-kDa heat-shock protein. Eur. J. Biochem. 233, 1-8.
47. Perdew, G. H., Hord, N., Hollenback, C. E. and Welsh, M. J. (1993). Localization and characterization of the 86- and 84- kDa heat shock proteins in hepa 1c1cV cells. Exp. Cell Res. 209, 350-356.
48. Picard, D., Khursheed, B., Garabedian, M. J., Fortin, M. G., Lindquist, S. and Yamamoto, K. R. (1990a). Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature 348, 166-168.
49. Picard, D., Kumar, V., Chambon, P. and Yamamoto, K. R. (1990b). Signal transduction by steroid hormones: nuclear localization is differentially regulated in estrogen and glucocorticoid receptors. Cell Regul. 1, 291-299.
50. Pratt, W. B. (1993). The role of heat shock proteins in regulating the function, folding, and trafficking of the glucocorticoid receptor. J. Biol. Chem. 268, 21455-21458.
51. Radanyi, C., Renoir, J. M., Sabbah, M. and Baulieu, E. E. (1989). Chick heat-shock protein of Mr=90, 000. free or released from progesterone receptor, is in a dimeric form. J. Biol. Chem. 264, 2568-2573.
52. Radanyi, C., Chambraud, B. and Baulieu, E. E. (1994). The ability of immunophilin FKBP59-HBI to interact with the 90-kDa heat shock protein is encoded by its tetratricoptide repeat domain. Proc. Nat. Acad. Sci. USA 90, 11197-11201.
53. Rafestin-Oblin, M. E., Couette, B., Radanyi, C., Lombes, M. and Baulieu, E. E. (1989). Mineralocorticosteroid receptor of chick intestine: oligomeric structure and transformation. J. Biol. Chem. 264, 9304-9309.
54. Ratajczak, T., Carrello, A., Mark, P. J., Warner, B. J., Simpson, R. J., Moritz, R. L. and House, A. K. (1993). The cyclophilin component of the unactivated estrogen receptor contains a tetratricopeptide repeat domain and shares identity with p59 (FKBP59). J. Biol. Chem. 268, 13187-13192.
55. Renoir, J. M., Radanyi, C., Jung-Testas, I., Faber, L. E. and Baulieu, E. E. (1990). The non-activated progesterone receptor is a nuclear heterooligomer. J. Biol. Chem. 265, 14402-14406.
56. Rose, D. W., Welch, W. J., Kramer, G. and Hardesty, B. (1989) Possible involvement of the 90-kDa heat shock protein in the regulation of protein synthesis. J. Biol. Chem. 264, 6239-6244.
57. Sabbah, H., Redeuilh, G. and Baulieu, E. E. (1989). Subunit composition of the estrogen receptor. Involvement of the hormone-binding domain in the dimeric state. J. Biol. Chem. 264, 2397-2400.
58. Sanchez, E. R., Toft, D. O., Schlesinger, M. J. and Pratt, W. B. (1985). Evidence that the 90-kDa phosphoprotein associated with the untransformed L-cell glucocortcoid receptor is a murine heat shock protein. J. Biol. Chem. 260, 12398-13401.
59. Sanchez, E. R., Redmond, T., Scherrer, L. C., Bresnick, E. H., Welsh, M. J. and Pratt, W. B. (1988). Evidence that the 90-kilodalton heat shock protein is associated with tubulin containing complexes in L cell cytosol and in intact PtK Cell. Mol. Endocrinol. 2, 756-760.
60. Shaknovich, R., Shue, G. and Kohtz, D. S. (1992). Conformational activation of a basic helix-loop-helix protein (MyoD1) by the C-terminal region of murine hsp90 (hsp84). Mol. Cell. Biol. 12, 5059-5068.
61. Siegel, L. M. and Monty, K. J. (1966). Determination of molecular weights and frictional ratios of proteins in impure systems by use of gel filtration and density gradient centrifugation. Application to crude preparations of sulfate and hydroxylamine reductases. Biochim. Biophys. Acta 112, 346-362.
62. Sikorski, R. S. and Boeke, J. D. (1991). In vitro mutagenesis and plasmid shuffling: from cloned gene to mutant yeast. Meth. Enzymol. 194, 302-318.
63. Smith, D. F., Stensgard, B. A., Welch, W. J. and Toft, D. O. (1992) Assembly of progesterone receptor with heat shock proteins and receptor activation are ATP mediated events. J. Biol. Chem. 267, 1350-1356.
64. Smith, D. F. and Toft, D. (1993). Steroid receptors and their associated proteins. MoI. Endocrinol. 7, 4-11.
65. Spence, J. and Georgopoulos, C. (1989). Purification and properties of the Escherichia coli heat shock protein, HtpG. J. Biol. Chem. 264, 4398-4403.
66. Stancato, L. F., Chow, Y.-H., Hutchison, K. A., Perdew, G. H., Jove, R. and Pratt, W. B. (1993). Raf exists in a native heterocomplex with hsp90 and p50 that can be reconstituted in a cell-free system. J. Biol. Chem. 268, 21711-21716.
67. Sullivan, W. P. and Toft, D. (1993). Mutational analysis of hsp90 binding to the progesterone receptor. J. Biol. Chem. 268, 20373-20379.
68. Welch, W. J. and Feramisco, J. R. (1982). Purification of the major mammalian heat shock proteins. J. Biol. Chem. 257, 14949-14959.
69. v-src kinase. Proc. Nat. Acad. Sci. USA 90, 7074-7078.
70. Ylikomi, T., Bocquel, M. T., Berry, M., Gronemeyer, H. and Chambon, P. (1992). Cooperation of proto-signals for nuclear accumulation of estrogen and progesterone receptors. EMBO J. 11, 3681-3694.