The co-chaperone Sba1 connects the ATPase reaction of Hsp90 to the progression of the chaperone cycle

Journal of Molecular Biology

Volumn 342, Issue 5, 2004, Pages 1403-1413

  Richter, Klaus ^a   Walter, Stefan ^a   Buchner, Johannes ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

ATP hydrolysis; chaperone; Hsp90; p23; Sba1

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; HEAT SHOCK PROTEIN 90;

ARTICLE; BINDING AFFINITY; CONFORMATION; DIMERIZATION; ENZYME ACTIVITY; HYDROLYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

HUMULUS;

EID: 4444291743     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.07.064     Document Type: Article

References (45)

1. D. Picard Heat-shock protein 90, a chaperone for folding and regulation Cell Mol. Life Sci. 59 2002 1640 1648
2. W.B. Pratt, and D.O. Toft Steroid receptor interactions with heat shock protein and immunophilin chaperones Endocr. Rev. 18 1997 306 360
3. W.B. Pratt, and D.O. Toft Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery Expt. Biol. Med. (Maywood.) 228 2003 111 133
4. J. Brugge, W. Yonemoto, and D. Darrow Interaction between the Rous sarcoma virus transforming protein and two cellular phosphoproteins: analysis of the turnover and distribution of this complex Mol. Cell Biol. 3 1983 9 19
5. J. Hu, and C. Seeger Hsp90 is required for the activity of a hepatitis B virus reverse transcriptase Proc. Natl Acad. Sci. USA 93 1996 1060 1064
6. M.V. Blagosklonny, J. Toretsky, S. Bohen, and L. Neckers Mutant conformation of p53 translated in vitro or in vivo requires functional HSP90 Proc. Natl Acad. Sci. USA 93 1996 8379 8383
7. J.P. Grenert, B.D. Johnson, and D.O. Toft The importance of ATP binding and hydrolysis by hsp90 in formation and function of protein heterocomplexes J. Biol. Chem. 274 1999 17525 17533
8. K. Richter, P. Muschler, O. Hainzl, and J. Buchner Coordinated ATP hydrolysis by the Hsp90 dimer J. Biol. Chem. 276 2001 33689 33696
9. Y. Minami, Y. Kimura, H. Kawasaki, K. Suzuki, and I. Yahara The carboxy-terminal region of mammalian HSP90 is required for its dimerization and function in vivo Mol. Cell Biol. 14 1994 1459 1464
10. C. Prodromou, B. Panaretou, S. Chohan, G. Siligardi, R. O'Brien, J.E. Ladbury, S.M. Roe, P.W. Piper, and L.H. Pearl The ATPase cycle of Hsp90 drives a molecular 'clamp' via transient dimerization of the N-terminal domains EMBO J. 19 2000 4383 4392
11. A. Dehner, J. Furrer, K. Richter, I. Schuster, J. Buchner, and H. Kessler NMR chemical shift perturbation study of the N-terminal domain of Hsp90 upon binding of ADP, AMP-PNP, geldanamycin, and radicicol ChemBiochem. 4 2003 870 877
12. K. Richter, J. Reinstein, and J. Buchner N-terminal residues regulate the catalytic efficiency of the Hsp90 ATPase cycle J. Biol. Chem. 277 2002 44905 44910
13. M.J. Czar, J.K. Owens-Grillo, K.D. Dittmar, K.A. Hutchison, A.M. Zacharek, K.L. Leach, M.R. Deibel Jr, and W.B. Pratt Characterization of the protein-protein interactions determining the heat shock protein (hsp90.hsp70.hsp56) heterocomplex J. Biol. Chem. 269 1994 11155 11161
14. D.F. Smith, W.P. Sullivan, T.N. Marion, K. Zaitsu, B. Madden, D.J. McCormick, and D.O. Toft Identification of a 60-kilodalton stress-related protein, p60, which interacts with hsp90 and hsp70 Mol. Cell Biol. 13 1993 869 876
15. J.L. Johnson, and D.O. Toft A novel chaperone complex for steroid receptors involving heat shock proteins, immunophilins, and p23 J. Biol. Chem. 269 1994 24989 24993
16. B.C. Freeman, S.J. Felts, D.O. Toft, and K.R. Yamamoto The p23 molecular chaperones act at a late step in intracellular receptor action to differentially affect ligand efficacies Genes Dev. 14 2000 422 434
17. J.L. Johnson, and D.O. Toft Binding of p23 and hsp90 during assembly with the progesterone receptor Mol. Endocrinol. 9 1995 670 678
18. D.F. Smith, L. Whitesell, S.C. Nair, S. Chen, V. Prapapanich, and R.A. Rimerman Progesterone receptor structure and function altered by geldanamycin, an hsp90-binding agent Mol. Cell Biol. 15 1995 6804 6812
19. D. Picard, B. Khursheed, M.J. Garabedian, M.G. Fortin, S. Lindquist, and K.R. Yamamoto Reduced levels of hsp90 compromise steroid receptor action in vivo Nature 348 1990 166 168
20. H.C. Chang, and S. Lindquist Conservation of Hsp90 macromolecular complexes in Saccharomyces cerevisiae J. Biol. Chem. 269 1994 24983 24988
21. Y. Fang, A.E. Fliss, J. Rao, and A.J. Caplan SBA1 encodes a yeast hsp90 cochaperone that is homologous to vertebrate p23 proteins Mol. Cell Biol. 18 1998 3727 3734
22. K. Richter, P. Muschler, O. Hainzl, J. Reinstein, and J. Buchner Sti1 is a non-competitive inhibitor of the Hsp90 ATPase. Binding prevents the N-terminal dimerization reaction during the atpase cycle J. Biol. Chem. 278 2003 10328 10333
23. H. Wegele, M. Haslbeck, J. Reinstein, and J. Buchner Sti1 is a novel activator of the Ssa proteins J. Biol. Chem. 278 2003 25970 25976
24. Y. Morishima, K.C. Kanelakis, P.J. Murphy, D.S. Shewach, and W.B. Pratt Evidence for iterative ratcheting of receptor-bound hsp70 between its ATP and ADP conformations during assembly of glucocorticoid receptor.hsp90 heterocomplexes Biochemistry 40 2001 1109 1116
25. T. Weikl, K. Abelmann, and J. Buchner An unstructured C-terminal region of the Hsp90 co-chaperone p23 is important for its chaperone function J. Mol. Biol. 293 1999 685 691
26. A. Chadli, I. Bouhouche, W. Sullivan, B. Stensgard, N. McMahon, M.G. Catelli, and D.O. Toft Dimerization and N-terminal domain proximity underlie the function of the molecular chaperone heat shock protein 90 Proc. Natl Acad. Sci. USA 97 2000 12524 12529
27. W.P. Sullivan, B.A. Owen, and D.O. Toft The influence of ATP and p23 on the conformation of hsp90 J. Biol. Chem. 277 2002 45942 45948
28. A.J. Weaver, W.P. Sullivan, S.J. Felts, B.A. Owen, and D.O. Toft Crystal structure and activity of human p23, a heat shock protein 90 co-chaperone J. Biol. Chem. 275 2000 23045 23052
29. S.M. Roe, C. Prodromou, R. O'Brien, J.E. Ladbury, P.W. Piper, and L.H. Pearl Structural basis for inhibition of the Hsp90 molecular chaperone by the antitumor antibiotics radicicol and geldanamycin J. Med. Chem. 42 1999 260 266
30. S.H. McLaughlin, H.W. Smith, and S.E. Jackson Stimulation of the weak ATPase activity of human hsp90 by a client protein J. Mol. Biol. 315 2002 787 798
31. B. Panaretou, C. Prodromou, S.M. Roe, R. O'Brien, J.E. Ladbury, P.W. Piper, and L.H. Pearl ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo EMBO J. 17 1998 4829 4836
32. C. Prodromou, G. Siligardi, R. O'Brien, D.N. Woolfson, L. Regan, and B. Panaretou Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain co-chaperones EMBO J. 18 1999 754 762
33. B. Panaretou, G. Siligardi, P. Meyer, A. Maloney, J.K. Sullivan, and S. Singh Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1 Mol. Cell 10 2002 1307 1318
34. J.C. Young, and F.U. Hartl Polypeptide release by Hsp90 involves ATP hydrolysis and is enhanced by the co-chaperone p23 EMBO J. 19 2000 5930 5940
35. Y.W. Xu, S. Morera, J. Janin, and J. Cherfils AlF3 mimics the transition state of protein phosphorylation in the crystal structure of nucleoside diphosphate kinase and MgADP Proc. Natl Acad. Sci. USA 94 1997 3579 3583
36. J. Johnson, R. Corbisier, B. Stensgard, and D. Toft The involvement of p23, hsp90, and immunophilins in the assembly of progesterone receptor complexes J. Steroid Biochem. Mol. Biol. 56 1996 31 37
37. H. Kosano, B. Stensgard, M.C. Charlesworth, N. McMahon, and D. Toft The assembly of progesterone receptor-hsp90 complexes using purified proteins J. Biol. Chem. 273 1998 32973 32979
38. P. Meyer, C. Prodromou, B. Hu, C. Vaughan, S.M. Roe, and B. Panaretou Structural and functional analysis of the middle segment of hsp90: implications for ATP hydrolysis and client protein and cochaperone interactions Mol. Cell 11 2003 647 658
39. L. Brino, A. Urzhumtsev, M. Mousli, C. Bronner, A. Mitschler, P. Oudet, and D. Moras Dimerization of Escherichia coli DNA-gyrase B provides a structural mechanism for activating the ATPase catalytic center J. Biol. Chem. 275 2000 9468 9475
40. D.F. Smith Dynamics of heat shock protein 90-progesterone receptor binding and the disactivation loop model for steroid receptor complexes Mol. Endocrinol. 7 1993 1418 1429
41. C. Mayr, K. Richter, H. Lilie, and J. Buchner Cpr6 and Cpr7, two closely related Hsp90-associated immunophilins from Saccharomyces cerevisiae, differ in their functional properties J. Biol. Chem. 275 2000 34140 34146
42. H. Wegele, P. Muschler, M. Bunck, J. Reinstein, and J. Buchner Dissection of the contribution of individual domains to the ATPase mechanism of Hsp90 J. Biol. Chem. 278 2003 39303 39310
43. S.C. Gill, and P.H. von Hippel Calculation of protein extinction coefficients from amino acid sequence data Anal. Biochem. 182 1989 319 326
44. J.A. Ali, A.P. Jackson, A.J. Howells, and A. Maxwell The 43-kilodalton N-terminal fragment of the DNA gyrase B protein hydrolyzes ATP and binds coumarin drugs Biochemistry 32 1993 2717 2724
45. L. Ditzel, J. Lowe, D. Stock, K.O. Stetter, H. Huber, R. Huber, and S. Steinbacher Crystal structure of the thermosome, the archaeal chaperonin and homolog of CCT Cell 93 1998 125 138