Contribution of N- and C-terminal domains to the function of hsp90 in Saccharomyces cerevisiae

Molecular Microbiology

Volumn 34, Issue 4, 1999, Pages 701-713

  Scheibel, Thomas ^a,c   Weikl, Tina ^a   Rimerman, Ronald ^b   Smith, David ^b   Lindquist, Susan ^c   Buchner, Johannes ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; GLUCOCORTICOID RECEPTOR; HEAT SHOCK PROTEIN 90; PROTEIN KINASE P60;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL VIABILITY; COMPLEX FORMATION; CONTROLLED STUDY; FUNGUS GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SACCHAROMYCES CEREVISIAE; STRUCTURE ACTIVITY RELATION;

EUKARYOTA; FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 0032703419     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01632.x     Document Type: Article

References (75)

1. Alique, R., Akhavan-Niak, H., and Russell, P. (1994) A role for hsp90 in the cell cycle control: Wee1 tyrosine kinase activity requires interaction with Hsp90. EMBO J 13: 6099-6106.
2. Bardwell, J.C.A., and Craig, E.A. (1988) Ancient heat shock protein is dispensible. J Bacteriol 170: 2977-2983.
3. Blachere, N.E., and Srivastava, P.K. (1995) Heat shock protein-based cancer vaccines and related thoughts on immunogenicity of human tumors. Semin Cancer Biol 6: 349-355.
4. Blachere, N.E., Udono, H., Janetzki, S., Li, Z., Heike, M., and Srivastava, P.K. (1993) Heat shock protein vaccines against cancer. J Immunother 14: 352-356.
5. Blachere, N.E., Li, Z., Chandawarkar, R.Y., Suto, R., Jaikaria, N.S., Basu, S., et al. (1997) Heat shock protein-peptide complexes, reconstituted in vitro, elicit peptide-specific cytotoxic T lymphocyte response and tumor immunity. J Exp Med 186: 1315-1322.
6. Bohen, S.P., and Yamamoto, K.R. (1993) Isolation of Hsp90 mutants by screening for decreased steroid receptor function. Proc Natl Acad Sci USA 90: 11424-11428.
7. Bohen, S.P., and Yamamoto, K.R. (1994) Modulation of steroid receptor signal transduction by heat shock proteins. In The Biology of Heat Shock Proteins and Molecular Chaperones. Morimoto R., Tissieres A., and Georgopoulos C. (eds). Cold Spring Harbor NY: Cold Spring Harbor Laboratory Press, pp. 313-334.
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. Brugge, J.S. (1986) Interaction of the Rous sarcoma virus protein pp60src with the cellular proteins pp50 and pp90. Curr Microbiol Immun 123: 1-22.
10. Buchner, J. (1999) Hsp90 and Co: A holding for folding. Trends Biochem Sci 24: 136-141.
11. Carrello, A., Ingley, E., Minchin, R.F., Tsai, S., and Ratajczak, T. (1999) The common tetratricopeptide repeat acceptor site for steroid receptor-associated immunophilins and hop is located in the dimerization domain of Hsp90. J Biol Chem 274: 2682-2689.
12. Chang, H.C.J., and Lindquist, S. (1994) Conservation of Hsp90 macromolecular complexes in Saccharomyces cerevisiae. J Biol Chem 269: 24983-24988.
13. Chen, S., and Smith, D.F. (1998) Hop as an adaptor in the heat shock protein 70 (Hsp70) and hsp90 chaperone machinery. J Biol Chem 273: 35194-35200.
14. Chen, S., Prapapanich, V., Rimerman, R.A., Honoré, B., and Smith, D.F. (1996) Interactions of p60, a mediator of progesterone receptor assembly, with heat shock proteins Hsp90 and Hsp70. Mol Endocrinol 10: 682-693.
15. Chen, S., Sullivan, W.P., Toft, D.O., and Smith, D.F. (1998) Differential interactions of p23 and the TPR-containing proteins Hop, Cyp40, FKBP52 and FKBP51 with Hsp90 mutants. Cell Stress Chaperones 3: 118-129.
16. Cufforth, 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.
17. Dittmar, K.D., Demady, D.R., Stancato, L.F., Krishna, P., and Pratt, W.B. (1997) Folding of the glucocorticoid receptor by the heat shock protein (hsp) 90-based chaperone machinery. The role of p23 is to stabilize receptor.hsp90 heterocomplexes formed by hsp90.p60.hsp70. J Biol Chem 272: 21213-21220.
18. Fang, Y., Fliss, A.E., Robins, D.M., and Caplan, A.J. (1996) Hsp90 regulates androgen receptor hormone binding affinity in vivo. J Biol Chem 271: 28697-28702.
19. Gill, S.C., and von Hippel, P.H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal Biochem 182: 319-326.
20. Grenert, J.P., Sullivan, W.P., Fadden, P., Haystead, T.A.J., Clark, J., Mimnaugh, E., et al. (1997) The aminoterminal domain of heat shock protein 90 (hsp90) that binds geldanamycin is an ATP/ADP switch domain that regulates hsp90 conformation. J Biol Chem 272: 23843-23850.
21. Grenert, J.P., Johnson, B.D., and Toft, D.O. (1999) The importance of ATP binding and hydrolysis by hsp90 in formation and function of protein heterocomplexes. J Biol Chem 274: 17525-17533.
22. Hutchison, K.A., de Brott, B.K., Leon, J.H., Perdew, G.H., Jove, R., and Pratt, W.B. (1992a) Reconstitution of the multiprotein complex of pp60src, Hsp90 and p50 in a cell-free system. J Biol Chem 267: 2902-2908.
23. v-src and Hsp90 is stabilized by molybdate, vanadate, tungstate and an endogenous cytosolic metal. J Biol Chem 267: 13952-13957.
24. Jakob, U., and Buchner, J. (1994) Assisting spontaneity: The role of Hsp90 and small Hsps as molecular chaperones. Trends Biochem Sci 19: 205-211.
25. Jakob, U., Meyer, I., Bügl, H., André, S., Bardwell, J.C.A., and Buchner, J. (1995) Structural organization of procaryotic and eucaryotic Hsp90. J Biol Chem 270: 14412-14419.
26. Johnson, J., and Toft, D.O. (1995) Binding of p23 and Hsp90 during assembly with the progesterone receptor. Mol Endocrinol 9: 670-678.
27. Johnson, J.L., and Craig, E.A. (1997) Protein folding in vivo: Unraveling complex pathways. Cell 90: 201-204.
28. Johnson, J., Corbisier, R., Stensgard, B., and Toft, D.O. (1996) The involvement of p23, Hsp90 and immunophilins in the assembly of progesterone receptor complexes. J Steroid Biochem Mol Biol 56: 31-37.
29. Johnston, M., and Davis, R.W. (1984) Sequences that regulate the divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae. Mol Cell Biol 4: 1440-1448.
30. Kang, K.I., Meng, X., Devin-Leclerc, J., Bouhouche, I., Chadli, A., Cadepond, F., et al. (1999) The molecular chaperone Hsp90 can negatively regulate the activity of a glucocorticosteroid-dependent promoter. Proc Natl Acad Sci USA 1999: 96, 1439-1444.
31. Kimura, Y., Rutherford, S.L., Miyata, Y., Yahara, I., Freeman, B.C., Yue, L., et al. (1997) Cdc37 is a molecular chaperone with specific functions in signal transduction. Genes Dev 11: 1775-1785.
32. Kosano, H., Stensgard, B., Charlesworth, M.C., McMahon, N., and Toft, D. (1998) The assembly of progesterone receptor-hsp90 complexes using purified proteins. J Biol Chem 273: 32973-32979.
33. Louvion, J.F., Warth, R., and Picard, D. (1996) Two eukaryote-specific regions of Hsp82 are dispensable for its viability and signal transduction functions in yeast. Proc Natl Acad Sci USA 93: 13937-13942.
34. Louvion, J.F., Abbas-Terki, T., and Picard, D. (1998) Hsp90 is required for pheromone signaling in yeast. Mol Biol Cell 9: 3071-3083.
35. Murphy, S.M., Bergman, M., and Morgan, D.O. (1993) Suppression of c-Src activity by C-terminal Src kinase involves the c-Src SH2 and SH3 domains: Analysis with Saccharomyces cerevisiae. Mol Cell Biol 13: 5290-5300.
36. Nair, S.C., Toran, E.J., Rimerman, R.A., Hjermstad, S., Smithgall, T.E., and Smith, D.F. (1996) A pathway of multi-chaperone interactions common to diverse regulatory proteins: Estrogen receptor, Fes tyrosine kinase, heat shock transcription factor HSF1, and the arylhydrocarbon receptor. Cell Stress Chaperones 1: 237-250.
37. 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.
38. Nathan, D.F., Vos, M.H., and Lindquist, S. (1997) In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc Natl Acad Sci USA 94: 12949-12956.
39. Obermann, W.M., Sondermann, H., Russo, A.A., Pavletich, N.P., and Hartl, F.U. (1998) In vivo function of Hsp90 is dependent on ATP binding and ATP hydrolysis. J Cell Biol 143: 901-910.
40. Owens-Grillo, J.K., Hoffmann, K., Hutchison, K.A., Yem, A.W., Deibel, M.R., Handschumacher, R.E., and Pratt, W.B. (1995) The cyclosporin A-binding immunophilin Cyp-40 and the FK506-binding immunophilin Hsp56 bind to a common site on Hsp90 and exist in independent cytosolic heterocomplexes with the untransformed glucocorticold receptor. J Biol Chem 270: 20479-20484.
41. Owens-Grillo, J.K., Czar, M.J., Hutchison, K.A., Hoffmann, K., Perdew, G.H., and Pratt, W.B. (1996) A model of protein targeting mediated by immunophilins and other proteins that bind to Hsp90 via tetratricopeptide repeat domains. J Biol Chem 271: 13468-13475.
42. Palmer, G., Louvion, J.F., Tibbetts, R.S., Engman, D.M., and Picard, D. (1995) Trypanosoma cruzi heat-shock protein 90 can functionally complement yeast. Mol Biochem Parasitol 70: 199-202.
43. Panaretou, B., Prodromou, C., Roe, S.M., O'Brien, R., Ladbury, J.E., Piper, P.W., and Pearl, H. (1998) ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo. EMBO J 17: 4829-4836.
44. Parsell, D.A., and Lindquist, S. (1993) The function of heat shock proteins in stress tolerance: Degradation and reactivation of damaged proteins. Annu Rev Genet 27: 437-496.
45. Picard, D., Khursheed, B., Garabedian, M.J., Fortin, M.G., Lindquist, S., and Yamamoto, K. (1990) Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature 348: 166-168.
46. Prapapanich, V., Chen, S., and Smith, D.F. (1998) Mutation of Hip's carboxy-terminal region inhibits a transitional stage of progesterone receptor assembly. Mol Cell Biol 18: 944-952.
47. 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.
48. Pratt, W.B. (1998) The Hsp90-based chaperone system: Involvement in signal transduction from a variety of hormone and growth factor receptors. Proc Soc Exp Biol Med 217: 420-434.
49. Pratt, W.B., and Toft, D.O. (1997) Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 18: 306-360.
50. Prodromou, C., Roe, S.M., O'Brien, R., Ladbury, J.E., Piper, P.W., and Pearl, L.H. (1997a) Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90: 65-75.
51. Prodromou, C., Roe, S.M., Piper, P.W., and Pearl, L.H. (1997b) A molecular clamp in the crystal structure of the N-terminal domain of the yeast Hsp90 chaperone. Nature Struct Biol 4: 477-482.
52. Prodromou, C., Siligardi, G., O'Brien, R., Woolfson, D.N., Regan, L., Panaretou, B., et al. (1999) Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR) -domain co-chaperones. EMBO J 18: 754-762.
53. Ratajczak, T., and Carrello, A. (1996) Cyclophilin 40 (Cyp-40), mapping of its Hsp90 binding domain and evidence that FKBP52 competes with Cyp-40 for Hsp90 binding. J Biol Chem 271: 2961-2965.
54. Scheibel, T., and Buchner, J. (1997) Hsp90 proteins: the Hsp90 family. In Guidebook to Molecular Chaperones and Protein-Folding Catalysts. Gething M. J. (ed.) Oxford: Oxford University Press, pp. 147-151.
55. Scheibel, T., and Buchner, J. (1998) The Hsp90 complex - A super-chaperone machine as a novel drug target. Biochem Pharmacol 56: 675-682.
56. Scheibel, T., Neuhofen, S., Weikl, T., Mayr, C., Reinstein, J., Vogel, P.D., and Buchner, J. (1997) ATP-binding properties of human Hsp90. J Biol Chem 272: 18608-18613.
57. Scheibel, T., Weikl, T., and Buchner, J. (1998) Two chaperone sites in Hsp90 differing in substrate specificity and ATP dependence. Proc Natl Acad Sci USA 95: 1495-1499.
58. Scheibel, T., Siegmund, H.I., Jaenicke, R., Ganz, P., Lilie, H., and Buchner, J. (1999) The charged region of Hsp90 modulates the function of the N-terminal domain. Proc Natl Acad Sci USA 96: 1297-1302.
59. Sherman, F. (1991) Getting started with yeast. Methods Enzymol 194: 3-21.
60. Sikorski, R.S., and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in S. Cerevisiae. Genetics 122: 19-27.
61. Smith, D.F. (1993) Dynamics of heat shock protein 90-progesterone receptor binding and the disactivation loop model for steroid receptor complexes. Mol Endocrinol 7: 1418-1429.
62. Smith, D.F. (1995) Steroid receptors and molecular chaperones. Sci Med 2: 38-47.
63. Smith, D.F., Sullivan, W.P., Marion, T.N., Zaitsu, K., Madden, B., McCormick, D.J., and Toft, D.O. (1993) Identification of a 60-kilodalton stress-related protein, p60, which interacts with hsp90 and hsp70. Mol Cell Biol 13: 869-876.
64. Smith, D.F., Whitesell, L., Nair, S.C., Chen, S., Prapapanich, V., and Rimerman, R. (1995) Progesterone receptor structure and function altered by geldanamycin, an Hsp90-binding agent. Mol Cell Biol 15: 6804-6812.
65. Srivastava, P.K. (1997) Purification of heat shock protein-peptide complexes for use in vaccination against cancers and intracellular pathogens. Methods 12: 165-171.
66. Stebbins, C.E., Russo, A.A., Schneider, C., Rosen, N., Hartl, F.U., and Pavletich, N.P. (1997) Crystal structure of an Hsp90-geldanamycin complex: Targeting of a protein chaperone by an antitumor agent. Cell 89: 239-250.
67. Sullivan, W.P., Beito, T.G., Proper, J., Krco, C.J., and Toft, D.O. (1986) Preparation of monoclonal antibodies to the avian progesterone receptor. Endocrinology 119: 1549-1557.
68. Sullivan, W., Stensgard, B., Caucutt, G., Bartha, B., McMahon, N., Alnemri, E.S., et al. (1997) Nucleotides and two functional states of Hsp90. J Biol Chem 272: 8007-8012.
69. Wearsch, P.A., and Nicchitta, C.V. (1997) Interaction of endoplasmic reticulum chaperone Grp94 with peptide substrates is adenine nucleotide-independent. J Biol Chem 272: 5152-5156.
70. Wearsch, P.A., Voglino, L., and Nicchitta, C.V. (1998) Structural transitions accompanying the activation of peptide binding to the endoplasmic reticulum Hsp90 chaperone GRP94. Biochemistry 37: 5709-5719.
71. Whitelaw, M.L., Hutchison, K., and Perdew, G.H. (1991) A 50 kDa cytosolic protein complexed with the 90 kDa heat shock protein (Hsp90) is the same protein complexed with v-Src in cells transformed by the Rous sarcoma virus. J Biol Chem 266: 16436-16440.
72. Xu, Y., and Lindquist, S. (1993) Heat shock protein Hsp90 governs the activity of v-Src kinase. Proc Natl Acad Sci USA 90: 7074-7078.
73. Xu, Y., Singer, M., and Lindquist, S. (1999) Maturation of the tyrosine kinase c-src as a kinase and as a substrate depends on the molecular chaperone Hsp90. Proc Natl Acad Sci USA 96: 109-114.
74. Young, J.C., Schneider, C., and Hartl, F.U. (1997) In vitro evidence that hsp90 contains two independent chaperone sites. FEBS Lett 418: 139-143.
75. Young, J.C., Obermann, W.M., and Hartl, F.U. (1998) Specific binding of tetratricopeptide repeat proteins to the C-terminal 12 kDa domain of hsp90. J Biol Chem 273: 18007-18010.