GCUNC-45 is a novel regulator for the progesterone receptor/hsp90 chaperoning pathway

Molecular and Cellular Biology

Volumn 26, Issue 5, 2006, Pages 1722-1730

  Chadli, Ahmed ^a   Graham, J Dinny ^b,d   Abel, M Greg ^b   Jackson, Twila A ^b   Gordon, David F ^b   Wood, William M ^b   Felts, Sara J ^a   Horwitz, Kathryn B ^b   Toft, David ^a,c  

^a MAYO GRADUATE SCHOOL   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c MAYO CLINIC   (United States)

^d WESTMEAD HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; FKBP52 PROTEIN; GCUNC 45 PROTEIN; HEAT SHOCK PROTEIN 90; MYOSIN; PROGESTERONE RECEPTOR; PROGESTERONE RECEPTOR A; PROGESTERONE RECEPTOR B; PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELLS, CULTURED; CLONING, MOLECULAR; CYTOPLASM; HETEROTRIMERIC GTP-BINDING PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, PROGESTERONE; SIGNAL TRANSDUCTION; TACROLIMUS BINDING PROTEINS;

EID: 33644524059     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.5.1722-1730.2006     Document Type: Article

References (54)

1. Barral, J. M., A. H. Hutagalung, A. Brinker, F. U. Hartl, and H. F. Epstein. 2002. Role of the myosin assembly protein UNC-45 as a molecular chaperone for myosin. Science 295:669-671.
2. Blatch, G. L., and M. Lassle. 1999. The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. BioEssays 21:932-939.
3. Brinker, A., C. Scheufler, F. von der Mülbe, B. Fleckenstein, C. Herrmann, G. Jung, I. Moarefi, and F. U. Hartl. 2002. Ligand discrimination by TPR domains. J. Biol. Chem. 277:19265-19275.
4. Carrelle, A., E. Ingley, R. F. Minchin, S. Tsai, and T. Ratajczak. 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.
5. Carrigan, P. E., G. M. Nelson, P. J. Roberts, J. N. Stoffer, D. L. Riggs, and D. F. Smith. 2004. Multiple domains of the co-chaperone Hop are important for Hsp70 binding. J. Biol. Chem. 279:16185-16193.
6. Chen, S., W. P. Sullivan, D. O. Toft, and D. F. Smith. 1998. Differential interactions of p23 and the TPR-containing proteins Hop, Cyp40, FKBP52 and FKBP51 with Hsp90 mutants. Cell Stress Chaperones 3:118-129.
7. Collingwood, T. N., F. D. Urnov, and A. P. Wolffe. 1999. Nuclear receptors: coactivators, corepressors and chromatin remodeling in the control of transcription. J. Mol. Endocrinol. 23:255-275.
8. Cornillot, J. D., M. Caron, R. Joubert-Caron, and D. Bladier. 1992. Use of an immobilized human endogenous lectin for the purification of complementary ligands. Int. J. Biochem. 24:1585-1589.
9. Das, A. K., P. T. W. Cohen, and D. Barford. 1998. The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein-protein interactions. EMBO J. 17:1192-1199.
10. Desmond, J., J. Lüders, and J. Höhfeld. 1998. The carboxy-terminal domain of Hsc70 provides binding sites for a distinct set of chaperone cofactors. Mol. Cell. Biol. 18:2023-2028.
11. Elbi, C, D. A. Walker, G. Romero, W. P. Sullivan, D. O. Toft, H. L. Hager, and D. B. DeFranco. 2004. Molecular chaperones function as steroid receptor nuclear mobility factors. Proc. Natl. Acad. Sci. USA 101:2876-2881.
12. Freeman, B. C., and K. R. Yamamoto. 2002. Disassembly of transcriptional regulatory complexes by molecular chaperones. Science 296:2232-2235.
13. Glass, C. K., D. W. Rose, and M. G. Rosenfeld. 1997. Nuclear receptor coactivators. Curr. Opin. Cell Biol. 9:222-232.
14. Grenert, J. P., B. D. Johnson, and D. O. Toft. 1999. The importance of ATP binding and hydrolysis by Hsp90 in formation and function of protein heterocomplexes. J. Biol. Chem. 274:17525-17533.
15. Heery, D. M., E. Kalkhoven, S. Hoare, and M. G. Parker. 1997. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 387:733-736.
16. Hernández, M. P., A. Chadli, and D. O. Toft. 2002. HSP40 binding is the first step in the HSP90 chaperoning pathway for the progesterone receptor. J. Biol. Chem. 277:11873-11881.
17. Hernández, M. P., W. P. Sullivan, and D. O. Toft. 2002. The assembly and intermolecular properties of the hsp70-Hop-hsp90 molecular chaperone complex. J. Biol. Chem. 277:38294-38304.
18. Horwitz, K. B., and G. R. Freidenberg. 1985. Growth inhibition and increase of insulin receptors in antiestrogen-resistant T47DCO human breast cancer cells by progestins: implications for endocrine therapies. Cancer Res. 45:167-173.
19. Horwitz, K. B., T. A. Jackson, D. L. Bain, J. K. Richer, G. C. Takimoto, and L. Tung. 1996. Nuclear receptor coactivators and corepressors. Mol. Endocrinol. 10:1167-1177.
20. Hutagalung, A. H., M. L. Landsverk, M. G. Price, and H. F. Epstein. 2002. The UCS family of myosin chaperones. J. Cell Sci. 115:3983-3990.
21. Jackson, T. A., J. K. Richer, D. L. Bain, G. S. Takimoto, L. Tung, and K. B. Horwitz. 1997. The partial agonist activity of antagonist-occupied steroid receptors is controlled by a novel hinge domain-binding coactivator L7/SPA and the corepressors N-CoR or SMRT. Mol. Endocrinol. 11:693-705.
22. Jantzen, H.-M., U. Strahle, B. Gloss, F. Stewart, W. Schmid, M. Boshart, R. Miksicek, and G. Schutz. 1987. Cooperaativity of glucocorticoid response elements located far upstream of the tyrosine aminotransferase gene. Cell 49:29-38.
23. King, F. W., A, Wasrzynow, J. Höhfeld, and M. Zylicz. 2001. Co-chaperones Bag-1, Hop and Hsp40 regulate Hsc70 and Hsp90 interactions with wild-type or mutant p53. EMBO J. 20:6297-6305.
24. Kosano, H., B. Stensgard, M. C. Charlesworth, N. McMahon, and D. O. Toft. 1998. The assembly of progesterone receptor-hsp90 complexes using purified proteins. J. Biol. Chem. 273:32973-32979.
25. Lange, C. A., J. K. Richer, and K. B. Horwitz. 1999. Hypothesis: progesterone primes breast cancer cells for cross-talk with proliferative or antiproliferative signals. Mol. Endocrinol. 13:829-836.
26. phox in complex with Rac-GTP. Mol. Cell 6:899-907.
27. McKenna, N. J., and B. W. O'Malley. 2002. Combinatorial control of gene expression by nuclear receptors and coregulators. Cell 108:465-474.
28. Meyer, P., C. Prodromou, C. Liao, B. Hu, S. M. Roe, C. K. Vaughan, I. Vlasic, B. Panaretou, P. W. Piper, and L. H. Pearl. 2004. Structural basis for recruitment of the ATPase activator Aha1 to the hsp90 chaperone machinery. EMBO J. 23:1402-1410.
29. Obermann, W. M. J., H. Sondermann, A. A. Russo, N. P. Pavletich, and F. U. Hartl. 1998. In vivo function of Hsp90 is dependent on ATP binding and ATP hydrolysis. J. Cell Biol. 143:901-910.
30. 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.
31. Panaretou, B., G. Siligardi, P. Meyer, A. Maloney, J. K. Sullivan, S. Singh, S. H. Millson, P. A. Clarke, S. Naaby-Hansen, R. Stein, R., Cramer, M. Mollapour, P. Workman, P. W. Piper, L. H. Pearl, and C. Prodromou. 2002. Activation of the ATPase activity of Hsp90 by the stress-regulated cochaperone Aha1. Mol. Cell 10:307-1318.
32. Owen, B. A. L., W. P. Sullivan, S. J. Felts, and D. O. Toft. 2002. Regulation of heat shock protein 90 ATPase activity by sequences in the carboxyl terminus. J. Biol. Chem. 277:7086-7091.
33. Owens-Grillo, J. K., M. J. Czar, K. A. Huchison, K. Hoffmann, G. H. Perdew, and W. B. Pratt. 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.
34. Prapapanich, V., S. Chen, E. J. Toran, R. A. Rimerman, and D. F. Smith. 1996. Mutational analysis of the hsp70-interacting protein Hip. Mol. Cell. Biol. 16:6200-6207.
35. Pratt, W. P., M. D. Galigniana, J. M. Harrell, and D. B. DeFranco. 2004. Role of hsp90 and the hsp90-binding immunophilins in signalling protein movements. Cell. Signal. 16:857-872.
36. Pratt, W. P., and D. O. Toft. 2003. Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp. Biol. Med. 228:111-133.
37. Price, M. G., M. L. Landsverk, J. M. Barral, and H. F. Epstein. 2002. Two mammalian UNC-45 isoforms are related to distinct cytoskeletal and muscle-specific functions. J. Cell Sci. 115:4013-4023.
38. Prodromou, C., G. Siligardi, R. O'Brien, D. N. Woolfson, L. Regan, B. Panaretou, J. E. Ladbury, P. W. Piper, and L. H. Pearl. 1999. Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain co-chaperones. EMBO J. 18:754-762.
39. Richter, K., and J. Buchner. 2001. Hsp90: chaperoning signal transduction. J. Cell Physiol. 188:281-290.
40. Russell, L. C., S. R. Whitt, M.-S. Chen, and M. Chinkers. 1999. Identification of conserved residues required for the binding of a tetracopeptide repeat domain to heat shock protein 90. J. Biol. Chem. 174:20060-20063.
41. Sartorius, C. A., S. D. Groshong, L. A. Miller, R. L. Powell, L. Tung, G. S. Takimoto, and K. B. Horwitz. 1994. New T47D breast cancer cell lines for the independent study of progesterone B- and A-receptors: only antiprogestin- occupied B-receptors are switched to transcriptional agonists by cAMP. Cancer Res. 54:868-3877.
42. Sartorius, C. A., M. Y. Melville, A. R. Hovland, L. Tung, G. S. Takimoto, and K. B. Horwitz. 1994. A third transactivation function (AF3) of human progesterone receptors located in the unique N-terminal segment of the B-isoform. Mol. Endocrinol. 8:1347-1360.
43. Scheufler, C., A. Brinker, G. Bourenkov, S. Pegoraro, L. Moroder, H. Bartunik, F. U. Hartl, and I. Moarefi. 2000. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101:99-210.
44. Shibata, H., T. E. Spencer, S. A. Onate, G. Jenster, S. Y. Tsai, M. J. Tsai, and B. W. O'Malley. 1997. Role of co-activators and co-repressors in the mechanism of steroid/thyroid receptor action. Recent Prog. Horm. Res. 52:141-164.
45. cdc37. J. Biol. Chem. 277:20151-20159.
46. Smith, D. F. 2004. Tetratricopeptide repeat cochaperones in steroid receptor complexes. Cell Stress Chaperones 9:109-121.
47. Sullivan, W. P., T. G. Beito, J. Proper, C. J. Krco, and D. O. Toft. 1986. Preparation of monoclonal antibodies to the avian progesterone receptor. Endocrinology 119:1549-15557.
48. Sullivan, W. P., B. Stensgard, G. Caucutt, B. Bartha, N. McMahon, E. S. Alnemri, G. Litwack, and D. O. Toft. 1997. Nucleotides and two functional states of hsp90. J. Biol. Chem. 272:8007-8012.
49. Tranguch, S., J. Cheung-Flynn, T. Daikoku, V. Prapapanich, M. B. Cox, H. Xie, H. Wang, S. K. Das, D. F. Smith, and S. K. Dey. 2005. Cochaperone immunophilin FKBP52 is critical to uterine receptivity for embryo implantation. Proc. Natl. Acad. Sci. USA 102:14326-14331.
50. Tsai, M.-J., and B. W. O'Malley. 1994. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem. 63:451-486.
51. Wood, W. M., M. Y. Kao, D. F. Gordon, and E. C. Ridgway. 1989. Thyroid hormone regulates the mouse thyrotropin beta subunit gene promoter in transfected primary thyrotropes. J. Biol. Chem. 264:14840-14847.
52. Young, J. C., I. Moarefi, and F. U. Hartl. 2001. Hsp90: a specialized but essential protein-folding tool. J. Cell Biol. 154:267-273.
53. Young, J. C., M. J. Obermann, and F. U. Hartl. 1998. Specific binding of tetratricopeptide repeat proteins to the C-terminal 12-kDa domain of hsp90. J. Biol. Chem. 273:18007-18010.
54. Yu, Q., and S. I. Bernstein. 2003. UCS proteins: managing the myosin motor. Curr. Biol. 13:R525-R527.