p23/Sba1p protects against Hsp90 inhibitors independently of its intrinsic chaperone activity

Molecular and Cellular Biology

Volumn 28, Issue 10, 2008, Pages 3446-3456

  Forafonov, Fedor ^a   Toogun, Oyetunji A ^b   Grad, Iwona ^a   Suslova, Elena ^a   Freeman, Brian C ^b   Picard, Didier ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; PROTEIN DERIVATIVE; PROTEIN P23; SBA1P PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; ENVIRONMENT; MAMMAL CELL; MICROORGANISM; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; YEAST CELL;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELLS, CULTURED; DNA PRIMERS; DNA, FUNGAL; GENES, FUNGAL; GENETIC COMPLEMENTATION TEST; HSP90 HEAT-SHOCK PROTEINS; INTRAMOLECULAR OXIDOREDUCTASES; MICE; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MUTAGENESIS, SITE-DIRECTED; PHENOTYPE; POINT MUTATION; PROTEIN BINDING; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE DELETION; SEQUENCE HOMOLOGY, AMINO ACID;

EUKARYOTA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 43249105354     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.02246-07     Document Type: Article

References (64)

1. Abbas-Terki, T., O. Donzé, P.-A. Briand, and D. Picard. 2001. Hsp104 interacts with Hsp90 cochaperones in respiring yeast. Mol. Cell. Biol. 21:7569-7575.
2. Ali, M. M., S. M. Roe, C. K. Vaughan, P. Meyer, B. Panaretou, P. W. Piper, C. Prodromou, and L. H. Pearl. 2006. Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 440:1013-1017.
3. Bandhakavi, S., R. O. McCann, D. E. Hanna, and C. V. Glover. 2003. A positive feedback loop between protein kinase CKII and Cdc37 promotes the activity of multiple protein kinases. J. Biol. Chem. 278:2829-2836.
4. Bohen, S. P. 1998. Genetic and biochemical analysis of p23 and ansamycin antibiotics in the function of Hsp90-dependent signaling proteins. Mol. Cell. Biol. 18:3330-3339.
5. Bose, S., T. Weikl, H. Bügl, and J. Buchner. 1996. Chaperone function of Hsp90-associated proteins. Science 274:1715-1717.
6. Brachmann, C. B., A. Davies, G. J. Cost, E. Caputo, J. Li, P. Hieter, and J. D. Boeke. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14:115-132.
7. Cox, M. B., and C. A. Miller III. 2002. The p23 co-chaperone facilitates dioxin receptor signaling in a yeast model system. Toxicol. Lett. 129:13-21.
8. Cox, M. B., and C. A. Miller III. 2003. Pharmacological and genetic analysis of 90-kDa heat shock isoprotein-aryl hydrocarbon receptor complexes. Mol. Pharmacol. 64:1549-1556.
9. Cox, M. B., and C. A. Miller III. 2004. Cooperation of heat shock protein 90 and p23 in aryl hydrocarbon receptor signaling. Cell Stress Chaperones 9:4-20.
10. Cullinan, S. B., and L. Whitesell. 2006. Heat shock protein 90: a unique chemothcrapeutic target. Semin. Oncol. 33:457-465.
11. Dittmar, K. D., D. R. Demady, L. F. Stancato, P. Krishna, and W. B. Pratt. 1997. Folding of the glucocorticoid receptor by the heat shock protein (hsp) 90-based chaperone machinery. J. Biol. Chem. 272:21213- 21220.
12. Dolinski, K. J., M. E. Cardenas, and J. Heitman. 1998. CNS1 encodes an essential p60/Sti1 homolog in Saccharomyces cerevisiae that suppresses cyclophilin 40 mutations and interacts with Hsp90. Mol. Cell. Biol. 18:7344-7352.
13. Donzé, O., T. Abbas-Terki, and D. Picard. 2001. The Hsp90 chaperone complex is both a facilitator and a repressor of the dsRNA-dependent kinase PKR. EMBO J. 20:3771-3780.
14. Donzé, O., and D. Picard. 1999. Hsp90 binds and regulates Gcn2, the ligand-inducible kinase of the α subunit of eukaryotic translation initiation factor kinase Gcn2. Mol. Cell. Biol. 19:8422-8432.
15. Fang, Y., A. E. Fliss, J. Rao, and A. J. Caplan. 1998. SBA1 encodes a yeast Hsp90 cochaperone that is homologous to vertebrate p23 proteins. Mol. Cell. Biol. 18:3727-3734.
16. Felts, S. J., and D. O. Toft. 2003. p23, a simple protein with complex activities. Cell Stress Chaperones 8:108-113.
17. Freeman, B. C., S. J. Felts, D. O. Toft, and K. R. Yamamoto. 2000. The p23 molecular chaperones act at a late step in intracellular receptor action to differentially affect ligand efficacies. Genes Dev. 14:422-434.
18. Freeman, B. C., M. P. Myers, R. Schumacher, and R. I. Morimoto. 1995. Identification of a regulatory motif in Hsp70 that affects ATPase activity, substrate binding and interaction with HDJ-1. EMBO J. 14:2281-2292.
19. Freeman, B. C., D. O. Toft, and R. I. Morimoto. 1996. Molecular chaperone machines: chaperone activities of the cylophilin Cyp-40 and the steroid aporeceptor-associated protein p23. Science 274:1718-1720.
20. Freeman, B. C., and K. R. Yamamoto. 2002. Disassembly of transcriptional regulatory complexes by molecular chapcrones. Science 296:2232-2235.
21. Gooljarsingh, L. T., C. Fernandes, K. Yan, H. Zhang, M. Grooms, K. Johanson, R. H. Sinnamon, R. B. Kirkpatrick, J. Kerrigan, T. Lewis, M. Arnone, A. J. King, Z. Lai, R. A. Copeland, and P. J. Tummino. 2006. A biochemical rationale for the anticancer effects of Hsp90 inhibitors: slow, tight binding inhibition by geldanamycin and its analogues. Proc. Natl. Acad. Sci. USA 103:7625-7630.
22. Grad, I., T. A. McKee, S. M. Ludwig, G. W. Hoyle, P. Ruiz, W. Wurst, T. Floss, C. A. Miller III, and D. Picard. 2006. The Hsp90 cochaperone p23 is essential for perinatal survival. Mol. Cell. Biol. 26:8976-8983.
23. Grad, I., and D. Picard. 2007. The glucocorticoid responses are shaped by molecular chapcrones. Mol. Cell. Endocrinol. 275:2-12.
24. Johnson, J., R. Corbisier, B. Stensgard, and D. O. Toft. 1996. The involvement of p23, hsp90, and immunophilins in the assembly of progesterone receptor complexes. J. Steroid Biochem. Mol. Biol. 56:31-37.
25. Johnson, J. L., A. Halas, and G. Flom. 2007. Nucleotide-dependent interaction of Saccharomyces cerevisiae Hsp90 with the cochaperone proteins Sti1, Cpr6, and Sba1. Mol. Cell. Biol. 27:768-776.
26. Johnson, J. L., and D. O. Toft. 1995. Binding of p23 and hsp90 during assembly with the progesterone receptor. Mol. Endocrinol. 9:670-678.
27. Kamal, A., L. Thao, J. Sensintaffar, L. Zhang, M. F. Boehm, L. C. Fritz, and F. J. Burrows. 2003. A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425:407-410.
28. Knoblauch, R., and M. J. Garabedian. 1999. Role for Hsp90-associated cochaperone p23 in estrogen receptor signal transduction. Mol. Cell. Biol. 19:3748-3759.
29. 2+-binding modulator protein involved in cell proliferation and in cell death. Biochim. Biophys. Acta 1600:68-73.
30. Louvion, J.-F., R. Warth, and D. Picard. 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.
31. 2 synthesis. Mol. Cell. Biol. 27:4416-4430.
32. McLaughlin, S. H., H. W. Smith, and S. E. Jackson. 2002. Stimulation of the weak ATPase activity of human Hsp90 by a client protein. J. Mol. Biol. 315:787-798.
33. McLaughlin, S. H., F. Sobott, Z. P. Yao, W. Zhang, P. R. Nielsen, J. G. Grossmann, E. D. Laue, C. V. Robinson, and S. E. Jackson. 2006. The co-chaperone p23 arrests the Hsp90 ATPase cycle to trap client proteins. J. Mol. Biol. 356:746-758.
34. McLellan, C. A., T. J. Turbyville, E. M. Wijeratne, A. Kerschen, E. Vierling, C. Queitsch, L. Whitesell, and A. A. Gunatilaka. 2007. A rhizosphere fungus enhances Arabidopsis thermotolerance through production of an HSP90 inhibitor. Plant Physiol. 145:174-182.
35. Mitsiades, C. S., N. S. Mitsiades, C. J. McMullan, V. Poulaki, A. L. Kung, F. E. Davies, G. Morgan, M. Akiyama, R. Shringarpure, N. C. Munshi, P. G. Richardson, T. Hideshima, D. Chauhan, X. Gu, C. Bailey, M. Joseph, T. A. Libermann, N. S. Rosen, and K. C. Anderson. 2006. Antimyeloma activity of heat shock protein-90 inhibition. Blood 107:1092-1100.
36. Mollerup, J., and M. W. Berchtold. 2005. The co-chaperone p23 is degraded by caspases and the proteasome during apoptosis. FEBS Lett. 579:4187-4192.
37. Mollerup, J., T. N. Krogh, P. F. Nielsen, and M. W. Berchtold. 2003. Properties of the co-chaperone protein p23 erroneously attributed to ALG-2 (apoptosis-linked gene 2). FEBS Lett. 555:478-482.
38. Muñoz, M. J., E. R. Bejarano, R. R. Daga, and J. Jimenez. 1999. The identification of Wos2, a p23 homologue that interacts with Wee1 and Cdc2 in the mitotic control of fission yeasts. Genetics 153:1561-1572.
39. Ouspenski, I. I., S. J. Elledge, and B. R. Brinkley. 1999. New yeast genes important for chromosome integrity and segregation identified by dosage effects on genome stability. Nucleic Acids Res. 27:3001-3008.
40. Oxelmark, E., R. Knoblauch, S. Arnal, L. F. Su, M. Schapira, and M. J. Garabedian. 2003. Genetic dissection of p23, an Hsp90 cochaperone, reveals a distinct surface involved in estrogen receptor signaling. J. Biol. Chem. 278:36547-36555.
41. Oxelmark, E., J. M. Roth, P. C. Brooks, S. E. Braunstein, R. J. Sehneider, and M. J. Garabedian. 2006. The cochaperone p23 differentially regulates estrogen receptor target genes and promotes tumor cell adhesion and invasion. Mol. Cell. Biol. 26:5205-5213.
42. Panaretou, B., C. Prodromou, S. M. Roe, R. O'Brien, J. E. Ladbury, P. W. Piper, and L. H. Pearl. 1998. ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo. EMBO J. 17:4829-4836.
43. Parsons, A. B., A. Lopez, I. E. Givoni, D. E. Williams, C. A. Gray, J. Porter, G. Chua, R. Sopko, R. L. Brost, C. H. Ho, J. Wang, T. Ketela, C. Brenner, J. A. Brill, G. E. Fernandez, T. C. Lorenz, G. S. Payne, S. Ishihara, Y. Ohya, B. Andrews, T. R. Hughes, B. J. Frey, T. R. Graham, R. J. Andersen, and C. Boone. 2006. Exploring the mode-of-action of bioactive compounds by chemical-genetic profiling in yeast. Cell 126:611-625.
44. Pearl, L. H., and C. Prodromou. 2006. Structure and mechanism of the hsp90 molecular chaperone machinery. Annu. Rev. Biochem. 75:271-294.
45. Picard, D. 2002. Heat-shock protein 90, a chaperone for folding and regulation. Cell. Mol. Life Sci. 59:1640-1648.
46. Picard, D. 2006. Chaperoning steroid hormone action. Trends Endocrinol. Metab. 17:229-235.
47. Picard, D. 2006. Intracellular dynamics of the Hsp90 co-chaperone p23 is dictated by Hsp90. Exp. Cell Res. 312:198-204.
48. Piper, P. W., S. H. Millson, M. Mollapour, B. Panaretou, G. Siligardi, L. H. Pearl, and C. Prodromou. 2003. Sensitivity to Hsp90-targeting drugs can arise with mutation to the Hsp90 chaperone, cochaperones and plasma membrane ATP binding cassette transporters of yeast. Eur. J. Biochem. 270:4689-4695.
49. Piper, P. W., B. Panaretou, S. H. Millson, A. Truman, M. Mollapour, L. H. Pearl, and C. Prodromou. 2003. Yeast is selectively hypersensitised to heat shock protein 90 (Hsp90)-targeting drugs with heterologous expression of the human Hsp90β, a property that can be exploited in screens for new Hsp90 chaperone inhibitors. Gene 302:165-170.
50. Prodromou, C., B. Panaretou, S. Chohan, G. Siligardi, R. O'Brien, J. E. Ladbury, S. M. Roe, P. W. Piper, and L. H. Pearl. 2000. The ATPase cycle of Hsp90 drives a molecular 'clamp' via transient dimerization of the N-terminal domains. EMBO J. 19:4383-4392.
51. Richter, K., P. Muschler, O. Hainzl, and J. Buchner. 2001. Coordinated ATP hydrolysis by the Hsp90 dimer. J. Biol. Chem. 276:33689-33696.
52. Richter, K., S. Walter, and J. Buchner. 2004. The co-chaperone Sba1 connects the ATPase reaction of Hsp90 to the progression of the chaperone cycle. J. Mol. Biol. 342:1403-1413.
53. Scheibel, T., T. Weikl, R. Rimerman, D. Smith, S. Lindquist, and J. Buchner. 1999. Contribution of N- and C-terminal domains to the function of Hsp90 in Saccharomyces cerevisiae. Mol. Microbiol. 34:701-713.
54. Schulte, T. W., M. V. Blagosklonny, C. Ingui, and L. Neckers. 1995. Disruption of the Raf-1-Hsp90 molecular complex results in destabilization of Raf-1 and loss of Raf-1-Ras association. J. Biol. Chem. 270:24585- 24588.
55. Schwede, T., J. Kopp, N. Guex, and M. C. Peitsch. 2003. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31:3381-3385.
56. Siligardi, G., B. Hu, B. Panaretou, P. W. Piper, L. H. Pearl, and C. Prodromou. 2004. Co-chaperone regulation of conformational switching in the Hsp90 ATPase cycle. J. Biol. Chem. 279:51989-51998.
57. Song, Y., and D. C. Masison. 2005. Independent regulation of Hsp70 and Hsp90 chaperones by Hsp70/Hsp90-organizing protein Sti1 (Hop1). J. Biol. Chem. 280:34178-34185.
58. Sullivan, W. P., B. A. Owen, and D. O. Toft. 2002. The influence of ATP and p23 on the conformation of hsp90. J. Biol. Chem. 277:45942- 45948.
59. Toogun, O. A., W. Zeiger, and B. C. Freeman. 2007. The p23 molecular chaperone promotes functional telomerase complexes through DNA dissociation. Proc. Natl. Acad. Sci. USA 104:5765-5770.
60. Weaver, A. J., W. P. Sullivan, S. J. Felts, B. A. Owen, and D. O. Toft. 2000. Crystal structure and activity of human p23, a heat shock protein 90 co-chaperone. J. Biol. Chem. 275:23045-23052.
61. Weikl, T., K. Abelmann, and J. Buchner. 1999. An unstructured C-terminal region of the Hsp90 co-chaperone p23 is important for its chaperone function. J. Mol. Biol. 293:685-691.
62. Whitesell, L., and S. L. Lindquist. 2005. HSP90 and the chaperoning of cancer. Nat. Rev. Cancer 5:761-772.
63. Wochnik, G. M., J. C. Young, U. Schmidt, F. Holsboer, F. U. Hartl, and T. Rein. 2004. Inhibition of GR-mediated transcription by p23 requires interaction with Hsp90. FEBS Lett. 560:35-38.
64. Zhao, R., M. Davey, Y. C. Hsu, P. Kaplanek, A. Tong, A. B. Parsons, N. Krogan, G. Cagney, D. Mai, J. Greenblatt, C. Boone, A. Emili, and W. A. Houry. 2005. Navigating the chaperone network: integrative map of physical and genetic interactions mediated by the Hsp90 chaperone. Cell 120:715-727.