Crystal structure of an Hsp90-geldanamycin complex: Targeting of a protein chaperone by an antitumor agent

Cell

Volumn 89, Issue 2, 1997, Pages 239-250

  Stebbins, Charles E ^a   Russo, Alicia A ^b   Schneider, Christine ^c   Rosen, Neal ^b   Hartl, F Ulrich ^c   Pavletich, Nikola P ^b  

^a Weill Cornell Graduate School of Biomedical Sciences   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CHAPERONE; GELDANAMYCIN; HEAT SHOCK PROTEIN 90;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DRUG PROTEIN BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN;

EUKARYOTA;

EID: 0031005361     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80203-2     Document Type: Article

References (61)

1. Aligue, R., Akhavan-Niak, H., and Russell, P. (1994). A role for Hsp90 in cell cycle control: Wee1 tyrosine kinase activity requires interaction with Hsp90. EMBO J. 13, 6099-6106.
2. Barlow, D.J., and Thornton, J.M. (1988). Helix geometry in proteins. J. Mol. Biol. 207, 601-619.
3. Bohen, S.P., and Yamamoto, K.R. (1994). The Biology of Heat Shock Proteins and MolecularChaperones, R.I. Morimoto, A. Tissieres and C. Georgopoulos, eds. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
4. 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.
5. 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.
6. Bose, S., Weikl, T., Bugl, H., and Buchner, J. (1996). Chaperone function of hsp90-associated proteins. Science 274, 1715-1717.
7. Bouchard, L., Lamarre, L., and Tremblay, P.J. (1989). Stochastic appearance of mammary tumors in transgenic mice carrying the MMTV/c-neu oncogene. Cell 57, 931-940.
8. Bresnick, E.H., Dalman, F.C., Sanchez, E.R., and Pratt, W.B. (1989). Evidence that the 90-kDa heat shock protein is necessary for the steroid binding conformation of the L cell glucocorticoid receptor. J. Biol. Chem. 264, 4992-4997.
9. Brunger, A.T. (1991). X-PLOR, a system for X-ray crystallography and NMR, Version 3.1, Yale University. (New Haven, CT: Yale Univ. Press).
10. Chavany, C., Mimnaugh, E., Miller, P., Bitton, R., Nguyen, P., Trepel, J., Whitesell, L., Schnur, R., Moyer, J.D., and Neckers, L. (1996). p185(erbB2) binds to GRP94 in vivo - dissociation of the p185(erbB2γ GRP94 heterocomplex by benzoquinone ansamycins precedes depletion of p185(erbB2). J. Biol. Chem. 271, 4974-4977.
11. Collaborative Computational Project, Number 4. (1994). The CCP4 suite: programs for protein crystallography. Acta Cryst. D50, 760-763.
12. 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.
13. DeBoer, C., Meulman, P.A., Wnuk, R.J., and Peterson, D.H. (1970). Geldanamycin, a new antibiotic. J. Antibiot. (Tokyo) 23, 442-447.
14. Dittmar, K.D., Hutchison, K.A., Owens-Grillo, J.K., and Pratt, W.B. (1996). Reconstitution of the steroid receptor-hsp90 heterocomplex assembly system of rabbit reticulocyte lysate. J. Biol. Chem. 271, 12833-12839.
15. Duina, A.A., Chang, H.J., Marsh, J.A., Lindquist, S., and Gaber, R.F. (1996). A cyclophilin function in hsp90-dependent signal transduction. Science 274, 1713-1715.
16. Flynn, G.C., Pohl, J., Flocco, M.T., and Rothman, J.E. (1991). Peptide-binding specificity of the molecular chaperone BiP. Nature 353, 726-730.
17. Freeman, B.C., and Morimoto, R.I. (1996). The human cytosolic molecular chaperones hsp90, hsp70 (hsc70) and hdj-1 have distinct roles in recognition of a non-native protein and protein refolding. EMBO J. 15, 2969-2979.
18. Freeman, B.C., Toft, D.O., and Morimoto, R.I. (1996). Molecular chaperone machines: chaperone activities of the cyclophilin cyp40 and the steroid aporeceptor-associated protein p23. Science 274, 1718-1720.
19. Furusaki, A., Matsumoto, T., Nakagawa, A., and Omura, S. (1980). Herbimycin A: an ansamycin antibiotic; X-ray crystal structure. J. Antibiot. (Tokyo) 33, 781-782.
20. Hartson, S.D., and Matts, R.L. (1994). Association of Hsp90 with cellular Src-family kinases in a cell-free system correlates with altered kinase structure and function. Biochemistry 33, 8912-8920.
21. Hunter, T., and Pines, J. (1994). Cyclins and cancer II: cyclin D and CDK inhibitors come of age. Cell 79, 573-582.
22. Isaacs, J.T., and Coffey, D.S. (1979). Androgenic control of prostatic growth: regulation of steroid levels. UICC Monograph (Prostatic Cancer) 48, 112-122.
23. Jakob, U., and Buchner, J. (1994). Assisting spontaneity: the role of Hsp90 and small Hsps as molecular chaperones. Trends Biochem. Sci. 19, 205-211.
24. Johnson, J., Corbisier, R., Stensgard, B., and Toft, D. (1996). The involvement of p23, hsp90, and immunophilins in the assembly of progesterone receptor complexes. J. Steroid Biochem. Mol. Biol. 56, 31-37.
25. June, C.H., Fletcher, M.C., Ledbetter, J.A., Schieven, G.L., Siegel, J.N., Phillips, A.F., and Samelson, L.E. (1990). Inhibition of tyrosine phosphorylation prevents T-cell receptor-mediated signal transduction. Proc. Natl. Acad. Sci. USA 87, 7722-7726.
26. Kimura, Y., Matsumoto, S., and Yahara, I. (1994). Temperature-sensitive mutants of hsp82 of the budding yeast Saccharomyces cerevisiae. Mol. Gen. Genet. 242, 517-527.
27. Koyasu, S., Nishida, E., Kadowaki, T., Matsuzaki, 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. Natl. Acad. Sci. USA 83, 8054-8058.
28. Kraulis, P.J. (1991). Molscript: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24, 946-950.
29. Merrit, E.A., and Murphy, M.E. (1994). Raster3D Version 2.0: a program for photorealistic molecular graphics. Acta Cryst. D50, 869-873.
30. Miller, P., DiOrio, C., Moyer, M., Schnur, R.C., Bruskin, A., Cullen, W., and Moyer, J.D. (1994). Depletion of the erbB-2 gene product p185 by benzoquinoid ansamycins. Cancer Res. 54, 2724-2730.
31. Miller, S.J. (1995). I. The asymmetric synthesis of the antitumor antibiotic macbecin. Diss. Abstr. Int. [B] 55, 3313.
32. Murakami, Y., Mizuno, S., and Uehara, Y. (1994). Accelerated degradation of 160 kDa epidermal growth factor (EGF) receptor precursor by the tyrosine kinase inhibitor herbimycin A in the endoplasmic reticulum of A431 human epidermoid carcinoma cells. Biochem. J. 301, 63-68.
33. 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 aryl hydrocarbon receptor. Cell Stress and Chaperones 1, 237-250.
34. 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.
35. Nicholls, A., Sharp, K.A., and Honig, B. (1991). Protein Folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins Struct. Funct. Genet. 11, 281-296.
36. Nieland, T.J.F., Tan, M.C.A.A., Monne-van Muijen, M., Koning, F., Kruisbeek, A.M., and Vanbleek, G.M. (1996). Isolation of an immuno-dominant viral peptide that is endogenously bound to the stress protein GP96/GRP94. Proc. Natl. Acad. Sci. USA 93, 6135-6139.
37. Omura, S., Iwai, Y., Takahashi, Y., Sadakane, N., Nakagawa, A., Oiwa, H., Hasegawa, Y., and Ikai, T. (1979). Herbimycin, a new antibiotic produced by a strain of Streptomyces. J. Antibiot. (Tokyo) 32, 255-261.
38. Ono, Y., Kozai, Y., and Ootsu, K. (1982). Antitumor and cytocidal activities of a newly isolated benzenoid ansamycin, macbecin I. Gann. 73, 938-944.
39. Osborne, C.K., Yochmowitz, M.G., Knight, W.A., and McGuire, W.L. (1980). The value of estrogen and progesterone receptors in the treatment of breast cancer. Cancer 46, 2884-2888.
40. Picard, D., Khursheed, B., Garabedian, B., Fortin, M.G., Lindquist, S., and Yamamoto, K.R. (1990). Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature 348, 166-168.
41. Pratt, W.B., and Welsh, M.J. (1994). Chaperone functions of the heat shock proteins associated with steroid receptors. Semin. Cell Biol. 5, 83-93.
42. Rinehart, K.L., Jr., and Shield, L.S. (1976). Chemistry of the ansamycin antibiotics. Fortschr. Chem. Org. Naturst. 33, 231-307.
43. Sasaki, K., Yasuda, H., and Onodera, K. (1979). Growth inhibition of virus transformed cells in vitro and antitumor activity in vivo of geldanamycin and its derivatives. J. Antibiot. (Tokyo) 32, 849-851.
44. Schneider, C., Sepp-Lorenzino, L., Nimmesgern, E., Ouerfelli, O., Danishefsky, S., Rosen, N., and Hartl, F.U. (1996). Pharmacologic shifting of a balance between protein refolding and degradation mediated by Hsp90. Proc. Natl. Acad. Sci. USA 93, 14536-14541.
45. Schnur, R.C., Corman, R.J., Gallaschum, R.J., Cooper, B.A., Dee, J.L., Doty, J.L., Muzzi, M.L., DiOrio, C.I., Barbacci, E.G., et al. (1995a). erbB-2 oncogene inhibition by geldanamycin derivatives: synthesis, mechanism of action, and structure-activity relationships. J. Med. Chem. 38, 3813-3820.
46. Schnur, R.C., Corman, R.J., Gallaschum, R.J., Cooper, B.A., Dee, J.L., Doty, J.L., Muzzi, M.L., Moyer, J.D., DiOrio, C.I., Barbacci, E.G., et al. (1995b). Inhibition of the oncogene product p185(erbB-2) in vitro and in vivo by geldanamycin and dihydrogeldanamycin derivatives. J. Med. Chem. 38, 3806-3812.
47. Schulte, T.W., Blagosklonny, M.V., Ingui, C., and Neckers, L. (1995). Disruption of the Raf-1-Hsp90 molecularcomplex results in destabilization of Raf-1 and loss of Raf-1-Ras association. J. Biol. Chem. 270, 24585-24588.
48. Schumacher, R.J., Hurst, R., Sullivan, W.P., McMahon, N.J., Toft, D.O., and Matts, R.L. (1994). ATP-dependent chaperoning activity of reticulocyte lysate. J. Biol. Chem. 269, 9493-9499.
49. 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.
50. Smith, D.F., Whitesell, L., Nair, S.C., Chen, S.Y., Prapapanich, V., and Rimerman, R.A. (1995). Progesterone receptor structure and function altered by geldanamycin, an hsp90-binding agent. Mol. Cell Biol. 15, 6804-6812.
51. 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.
52. Stepanova, L., Leng, X., Parker, S.B., and Harper, J.W. (1996). Mammalian p50Cdc37 is a protein kinase-targeting subunit of Hsp90 that binds and stabilizes Cdk4. Genes Dev. 10, 1491-1502.
53. Sullivan, W.P., and Toft, D.O. (1993). Mutational analysis of hsp90 binding to the progesterone receptor. J. Biol. Chem. 268, 20373-20379.
54. Supko, J.G., Hickman, R.L., Grever, M.R., and Malspeis, L. (1995). Preclinical pharmacologic evaluation of geldanamycin as an antitumor agent. Cancer Chemother. Pharmacol. 36, 305-315.
55. Tronick, S.R., and Aaronson, S.A. (1995). Growth factors and signal transduction. In The Molecular Basis of Cancer, J. Mendelsohn, P. Howley, M. Israel and L. Liotta, eds., pp. 117-140.
56. Wearsch, P.A., and Nicchitta, C.V. (1996). Endoplasmic reticulum chaperone GRP94 subunit assembly is regulated through a defined oligomerization domain. Biochemistry 35, 16760-16769.
57. 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 pp60v-src hsp90 in cells transformed by the Rous sarcoma virus. J. Biol. Chem. 266, 16436-16440.
58. Whitesell, L., and Cook, P. (1996). Stable and specific binding of heat shock protein 90 by geldanamycin disrupts glucocorticoid receptor function in intact cells. Mol. Endocrinol. 10, 705-712.
59. Whitesell, L., Mimnaugh, E.G., De Costa, B., Myers, C.E., and Neckers, L.M. (1994). Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc. Natl. Acad. Sci. USA 91, 8324-8328.
60. Xu, Y., and Lindquist, S. (1993). Heat-shock protein hsp90 governs the activity of pp60v-src kinase. Proc. Natl. Acad. Sci. USA 90, 7074-7078.
61. Zhu, X., Zhao, X., Burkholder, W.F., Gragerov, A., Ogata, C.M., Gottesman, M.E., and Hendrickson, W.A. (1996). Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272, 1606-1614.