Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone

Cell

Volumn 90, Issue 1, 1997, Pages 65-75

  Prodromou, Chrisostomos ^a   Roe, S Mark ^a   O'Brien, Ronan ^a   Ladbury, John E ^a   Piper, Peter W ^a   Pearl, Laurence H ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; GELDANAMYCIN; STEROID HORMONE;

AMINO TERMINAL SEQUENCE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING SITE; CELL CYCLE; CRYSTAL STRUCTURE; EUKARYOTE; GENE STRUCTURE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EUKARYOTA;

EID: 0031444238     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80314-1     Document Type: Article

References (59)

1. Aligue, R., Akhavannik, A., and Russell, P.A. (1994). A role for Hsp90 in cell-cycle control - Wee1 tyrosine kinase activity requires interaction with Hsp90. EMBO J. 13, 6099-6106.
2. Bergerat, A., de Massy, B. Gadelle, D. Varoutas, P.-C., Nicolas, A., and Forterre, P. (1997). An atypical topoisomerase II from archaea with implications for meotic recombination. Nature 386, 414-417.
3. 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.
4. Brünger, A. (1992). X-PLOR Version 3.1. A System for X-Ray Crystallography and NMR, (New Haven, Connecticut: Yale University Press).
5. CCP4 (1994). Collaborative computational project No. 4. Acta Cryst. D50, 760-763.
6. Chen, C.F., Chen, Y.M., Dai, K., Chen, P.L., Riley, D.J., and Lee, W.H. (1996). A new member of the Hsp90 family of molecular chaperones interacts with the retinoblastoma protein during mitosis and after heat-shock. Mol. Cell. Biol. 16, 4691-4699.
7. Csermely, P., and Kahn, C.R. (1991). The 90 kDa heat-shock protein (Hsp-90) possesses an ATP binding-site and autophosphorylation activity. J. Biol. Chem. 266, 4943-4950.
8. Csermely, P., Kajtár, J., Hollósi, M., Jalsovszky, G., Holly, S., Kahn, C.R., Gergely, P., Jr., Söti, C., Mihály, K., and Somogy, J. (1993). ATP induces a conformational change in the 90-kDa heat shock protein (hsp90). J. Biol. Chem. 268, 1901-1907.
9. Cutforth, T., and Rubin, G. (1994). Mutations in Hsp83 and CDC37 impair signaling by the Sevenless receptor tyrosine kinase in Drosophila. Cell 77, 1027-1036.
10. Czar, M.J., Owens-Grillo, J.K., Dittmar, K.D., Hutchinson, K.A., Zacharek, A.M., Leach, K.L., Deibel, M.R., Jr., and Pratt, W.B. (1994). Characterisation of the protein-protein interactions determining the heat shock protein (hsp90-hsp70-hsp56) heterocomplex. J. Biol. Chem. 269, 11155-11161.
11. Dai, K., Kobayashi, R., and Beach, D. (1996). Physical interaction of mammalian CDC37 with CDK4. J. Biol. Chem. 271, 22030-22034.
12. Dunbrack, R.L., Jr., Gerloff, D.L., Bower, M., Chen, X., Lichtarge, O., and Cohen, F.E. (1997). Meeting review: the second meeting on the critical assessment of techniques for protein structure prediction (CASP2), Asilomar, California, December 13-16, 1966. Folding and Design 1, R27-R42.
13. Flaherty, K.M., Wilbanks, S.M., De Luca-Flaherty, C., and McKay, D.B. (1994). Structural basis of the 70kDa heat shock cognate protein ATP hydrolytic activity. II. Structure of the active site with ATP or ADP bound to wild-type and mutant ATPase fragment. J. Biol. Chem. 269, 12899-12907.
14. Flynn, G.C., Chapell, T.G., and Rothman, J.E.(1991). Peptide binding and release by proteins implicated as catalysts of protein assembly. Science 245, 385-390.
15. 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.
16. Gilbert, E.J., and Maxwell, A. (1994). The 24kDa N-terminal subdomain of the DNA gyrase B protein binds coumarin drugs. Mol. Microbiol. 12, 365-373.
17. Höhfeld, J., Minami, Y., and Hartl, F.-U. (1995). Hip, a novel cochaperone involved in the eukaryotic Hsc70/Hsp40 reaction cycle. Cell 83, 589-598.
18. Jackson, A.P., and Maxwell A. (1993). Identifying the catalytic residue of the ATPase reaction of DNA gyrase. Proc. Natl. Acad. Sci. USA 90, 11232-11236.
19. Jakob, U., Scheibel, T., Bose, S., Reinstein, J., and Buchner, J. (1996). Assessment of the ATP binding properties of Hsp90. J. Biol. Chem. 271, 10035-10041.
20. Joab, I., Radanyi, C., Renoir, M., Buchou, T., Catelli, M.-G., Binart, N., and Mester, J. (1984). Common non-hormone binding component in non-transformed chick oviduct receptors of four natural steroids. Nature 308, 850-853.
21. Johnson, J.L., and Toft, D.O. (1994). A novel chaperone complex for steroid-receptors involving heat-shock proteins, immunophilins, and p23. J. Biol. Chem. 269, 24989-24993.
22. Johnson, J.L., and Toft, D.O. (1995). Binding of p23 and Hsp90 during assembly with the progesterone-receptor. Mol. Endocrinol. 9, 670-678.
23. Jones, T.A., Zou, J.-Y., Cowan, S.W., and Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Cryst. A47, 110-119.
24. Kimura, Y., Yahara, I., and Lindquist, S. (1993). The role of the protein chaperone Ydj1 in establishing Hsp90 mediated signal transduction pathways. Science 268, 1362-1365.
25. Kraulis, P.J. (1991). MOLSCRIPT - a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24, 946-950.
26. Ladbury, J.E., and Chowdhry, B.Z. (1996). Sensing the heat: the application of isothermal titration calorimetry to thermodynamic studies of biomolecular interactions. Chem. Biol. 3, 791-801.
27. Lamzin, V.A., and Wilson, K.S. (1993). Automated refinement of proteins. Acta Cryst. D49, 129-147.
28. Lewis, R.J., Singh, O.M.P., Smith, C.V., Skarzynski, T., Maxwell, A., Wonacott, A.J., and Wigley, D.B. (1996). The nature of inhibition of DNA gyrase by the coumarins and the cyclothialidines revealed by X-ray crystallography. EMBO J. 15, 1412-1420.
29. Li, Z., and Srivastava, P.K. (1993). Tumour rejection antigen GP96/GRP94 is an ATPase: implication for antigen presentation and protein folding. EMBO J. 12, 3143-3151.
30. Melnick, J., Aviel, S., and Argon, Y. (1992). The endoplasmic-reticulum stress protein-GRP94, in addition to BiP associates with unassembled immunoglobulin-chains. J. Biol. Chem. 267, 21303-21306.
31. Merrit, E.A., and Murphy, M.E.P. (1994). Raster3D version 2.0 - a program for photorealistic molecular graphics. Acta Cryst. 50, 869-873.
32. Moodie, S.L., and Thornton, J.M. (1993). A study into the effects of protein binding on nucleotide conformation. Nucleic Acids Res. 21, 1369-1380.
33. Nadeau, K., Sullivan, M.A., Bradley, M., Engman, D.M., and Walsh, C.T. (1992). 83-kilodalton heat-shock proteins of Trypanasomes are potent peptide-stimulated ATPases. Prot. Sci. 1, 970-979.
34. Nadeau, K., Das, A., and Walsh, C.T. (1993). Hsp90 chaperonins possess ATPase activity and bind heat-shock transcription factors and peptidyl prolyly isomerases. J. Biol. Chem. 268, 1479-1487.
35. 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.
36. Nicholls, A., Bharadwaj, R., and Honig, B. (1993) GRASP: graphical representation and analysis of surface-properties. Biophys. J. 64, A166.
37. Nieland, T.J.F., Tan, M.C.A.A., Monnee-van Muijen, M., Koning, F., Kruisbeek, A.M., and van Bleek, G.M. (1996). Isolation of an immunodominant viral peptide that is endogenously bound to the stress protein GP96/GRP94. Proc. Natl. Acad. Sci. USA 93, 6135-6139.
38. Opperman, H., Levinson, W., and Bishop, J.M. (1981). A cellular protein that associates with the transforming protein of Rous Sarcoma Virus is also a heat-shock protein. Proc. Natl. Acad. Sci. USA 78, 1067-1071.
39. Orengo, C.A., and Taylor, W.R. (1996). SSAP - sequential structure alignment program for protein-structure comparison. Meth. Enzymol. 266, 617-635.
40. Owens-Grillo, J.K., Czar, M.J., Hutchinson, K.A., Hoffman, K., Perdew, G.H., and Pratt, W.B. (1996). A model of protein targetting mediated by immunophilins and other proteins that bind to hsp90 via tetratricopeptide repeat domains. J. Biol. Chem. 271, 13468-13475.
41. Prodromou, C., Piper, P.W., and Pearl, L.H. (1996). Expression and crystallisation of the yeast Hsp82 chaperone, and preliminary X-ray diffraction studies of the amino-terminal domain. Prot. Struct. Funct. Genet. 25, 517-522.
42. Prodromou, C., Roe, S.M., Piper, P.W., and Pearl, L.H. (1997). A molecular clamp in the crystal structure of the N-terminal domain of the yeast Hsp90 chaperone. Nature Struct. Biol. 4, 477-482.
43. Roseman, A.M., Chen, S., White, H., Braig, K., and Saibil, H.R. (1996). The chaperonin ATPase cycle: mechanism of allosteric switching and movements of substrate-binding domains in GroEL. Cell 87, 241-251.
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 folding and degradation mediated by Hsp90. Proc. Natl. Acad. Sci. USA 93, 14536-14541.
45. Sepehrnia, B., Paz, I.B., Dasgupta, G., and Momand, J. (1996). Heat-shock protein 84 forms a complex with mutant p53 protein predominantly within a cytoplasmic compartment of the cell. J. Biol. Chem. 271, 15084-15090.
46. Smith, D.F., and Toft, D.O. (1993). Steroid receptors and their associated proteins. Mol. Endocrinol. 7, 4-11.
47. Smith, D.F., Sullivan, W.P., Marion, T.N., Zaitsu, K., Madden, B., McCormick, D.J., and Toft, D.O. (1993). Identification of a 60kDa stress related protein, p60, which interacts with hsp90 and hsp70. Mol. Cell. Biol. 13, 869-876.
48. Stancato, L.F., Chow, Y.-H., Hutchinson, 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.
49. 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: targetting of a protein chaperone by an antitumor agent. Cell 89, 239-250.
50. Stepanova, L., Leng, X.H., Parker, S.B., and Harper, J.W. (1996). Mammalian p50 (CDC37) is a protein kinase targetting subunit of Hsp90 that binds and stabilises CDK4. Genes Dev. 10, 1491-1502.
51. Sullivan, W., Stensgard, B., Caucutt, G., Bartha, B., McMahon, N., Alnemri, E.S., Litwack, G., and Toft, D.O. (1997). Nucleotides and two functional states of Hsp90. J. Biol. Chem. 272, 8007-8012.
52. Wallace, A.C., Laskowski, R.A.,and Thornton, J.M. (1995). LIPGLOT: a program to generate schematic diagrams of protein-ligand interactions. Prot. Eng. 8, 127-134.
53. Weich, H., Buchner, J., Zimmermann, R., and Jakob, U. (1992). HSP90 chaperones protein folding in vitro. Nature 358, 169-170.
54. Weich, H., Buchner, J., Zimmermann, M., Zimmermann, R., and Jakob, U. (1993). Hsc70, immunoglobulin heavy-chain binding-protein, and Hsp90 differ in their ability to stimulate transport of precursor proteins into mammalian microsomes. J. Biol. Chem. 268, 7414-7421.
55. 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.
56. Wigley, D.B., Davies, G.J., Dodson, E.J., Maxwell, A., and Dodson, G. (1991). Crystal structure of an N-terminal fragment of the DNA gyrase B protein. Nature 351, 624-629.
57. Wilhelmson, A., Cuthill, S., Denis, M., Wikström, A.-C., Gustafsson, J.-Å., and Poellinger, L. (1990). The specific DNA binding activity of the dioxin receptor is modulated by the 90 kDa heat-shock protein. EMBO J. 9, 69-76.
58. Wiseman, T., Williston, S., Brandtas, J.F., and Lin, L.N. (1989). Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem. 179, 131-137.
59. Zhu, X.T., 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.