Novel Activation Step Required for Transcriptional Competence of Progesterone Receptor on Chromatin Templates

Molecular Endocrinology

Volumn 17, Issue 12, 2003, Pages 2543-2553

  Thackray, Varykina G ^a,c   Toft, David O ^b   Nordeen, Steven K ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b MAYO CLINIC   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; DNA; GELDANAMYCIN; LIGAND; PROGESTERONE RECEPTOR; PROMEGESTONE; PROTEIN INHIBITOR; RECOMBINANT PROTEIN; STEROID RECEPTOR COACTIVATOR 1;

ANIMAL CELL; ARTICLE; CHROMATIN; CONTROLLED STUDY; DNA SEQUENCE; DNA TEMPLATE; EMBRYO; HORMONE RESPONSIVE ELEMENT; HUMAN; HUMAN CELL; INCUBATION TIME; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DNA BINDING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RABBIT; RETICULOCYTE LYSATE; STEROID BINDING; STIMULATION; TARGET CELL; TRANSCRIPTION INITIATION;

ANIMALS; BASE SEQUENCE; CHROMATIN; DNA; DROSOPHILA; EMBRYO, NONMAMMALIAN; HUMANS; PROGESTERONE; RABBITS; RECEPTORS, PROGESTERONE; RECOMBINANT PROTEINS; RETICULOCYTES; TEMPLATES, GENETIC; TRANSCRIPTION, GENETIC;

ANIMALIA; ORYCTOLAGUS CUNICULUS;

EID: 0346849705     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2003-0200     Document Type: Article

References (59)

1. Beato M 1989 Gene regulation by steroid hormones. Cell 56:335-344
2. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schutz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P, Evans RM 1995 The nuclear receptor superfamily: the second decade. Cell 83:835-839
3. Graham JD, Clarke CL 1997 Physiological action of progesterone in target tissues. Endocr Rev 18:502-519
4. Smith DF, Faber LE, Toft DO 1990 Purification of unactivated progesterone receptor and Identification of novel receptor-associated proteins. J Biol Chem 265:3996-4003
5. Bagchi MK, Tsai SY, Tsai MJ, O'Malley BW 1991 Progesterone enhances target gene transcription by receptor free of heat shock proteins hsp90, hsp56, and hsp70. Mol Cell Biol 11:4998-5004
6. DeMarzo AM, Beck CA, Onate SA, Edwards DP 1991 Dimerization of mammalian progesterone receptors occurs in the absence of DNA and is related to the release of the 90-kDa heat shock protein. Proc Natl Acad Sci USA 88:72-76
7. Bagchi MK, Elliston JF, Tsai SY, Edwards DP, Tsai MJ, O'Malley BW 1988 Steroid hormone-dependent interaction of human progesterone receptor with its target enhancer element. Mol Endocrinol 2:1221-1229
8. Tsai MJ, O'Malley BW 1994 Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu Rev Biochem 63:451-486
9. Smith DF, Toft DO 1993 Steroid receptors and their associated proteins. Mol Endocrinol 7:4-11
10. Smith DF 1993 Dynamics of heat shock protein 90-progesterone receptor binding and the disactivation loop model for steroid receptor complexes. Mol Endocrinol 7:1418-1429
11. Pratt WB, Toft DO 1997 Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 18:306-360
12. Kosano H, Stensgard B, Charlesworth MC, McMahon N, Toft D 1998 The assembly of progesterone receptor-hsp90 complexes using purified proteins. J Biol Chem 273:32973-32979
13. Dittmar KD, Hutchison KA, Owens-Grillo JK, Pratt WB 1996 Reconstitution of the steroid receptor. hsp90 heterocomplex assembly system of rabbit reticulocyte lysate. J Biol Chem 271:12833-12839
14. Dittmar KD, Demady DR, Stancato LF, Krishna P, Pratt WB 1997 Folding of the glucocorticoid receptor by the heat shock protein (hsp) 90-based chaperone machinery. The role of p23 is to stabilize receptor. hsp90 heterocomplexes formed by hsp90. p60. hsp70. J Biol Chem 272:21213-21220
15. Dittmar KD, Pratt WB 1997 Folding of the glucocorticoid receptor by the reconstituted Hsp90-based chaperone machinery. The initial hsp90. p60. hsp70-dependent step is sufficient for creating the steroid binding conformation. J Biol Chem 272:13047-13054
16. Dittmar KD, Banach M, Galigniana MD, Pratt WB. 1998 The role of DnaJ-like proteins in glucocorticoid receptor. hsp90 heterocomplex assembly by the reconstituted hsp90. p60. hsp70 foldosome complex. J Biol Chem 273:7358-7366
17. Freeman BC, Felts SJ, Toft DO, Yamamoto KR 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. Murphy PJ, Kanelakis KC, Galigniana MD, Morishima Y, Pratt WB 2001 Stoichiometry, abundance, and functional significance of the hsp90/hsp70-based multiprotein chaperone machinery in reticulocyte lysate. J Biol Chem 276:30092-30098
19. Morishima Y, Kanelakis KC, Silverstein AM, Dittmar KD, Estrada L, Pratt WB 2000 The Hsp organizer protein hop enhances the rate of but is not essential for glucocorticoid receptor folding by the multiprotein Hsp90-based chaperone system. J Biol Chem 275:6894-6900
20. Rajapandi T, Greene LE, Eisenberg E 2000 The molecular chaperones Hsp90 and Hsc70 are both necessary and sufficient to activate hormone binding by glucocorticoid receptor. J Biol Chem 275:22597-22604
21. Cheung J, Smith DF 2000 Molecular chaperone interactions with steroid receptors: an update. Mol Endocrinol 14:939-946
22. Freeman BC, Yamamoto KR 2001 Continuous recycling: a mechanism for modulatory signal transduction. Trends Biochem Sci 26:285-290
23. Freeman BC, Yamamoto KR 2002 Disassembly of transcriptional regulatory complexes by molecular chaperones. Science 296:2232-2235
24. Sabbah M, Radanyi C, Redeuilh G, Baulieu EE 1996 The 90 kDa heat-shock protein (hsp90) modulates the binding of the oestrogen receptor to its cognate DNA. Biochem J 314:205-213
25. Liu J, DeFranco DB 1999 Chromatin recycling of glucocorticoid receptors: implications for multiple roles of heat shock protein 90. Mol Endocrinol 13:355-365
26. Kornberg RD, Lorch Y 1999 Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98:285-294
27. Bruggemeier U, Rogge L, Winnacker EL, Beato M 1990 Nuclear factor I acts as a transcription factor on the MMTV promoter but competes with steroid hormone receptors for DNA binding. EMBO J 9:2233-2239
28. Perlmann T, Wrange O 1988 Specific glucocorticoid receptor binding to DNA reconstituted in a nucleosome. EMBO J 7:3073-3079
29. Perlmann T 1992 Glucocorticoid receptor DNA-binding specificity is increased by the organization of DNA in nucleosomes. Proc Natl Acad Sci USA 89:3884-3888
30. Pina B, Bruggemeier U, Beato M 1990 Nucleosome positioning modulates accessibility of regulatory proteins to the mouse mammary tumor virus promoter. Cell 60:719-731
31. Pham TA, McDonnell DP, Tsai MJ, O'Malley BW 1992 Modulation of progesterone receptor binding to progesterone response elements by positioned nucleosomes. Biochemistry 31:1570-1578
32. Onate SA, Tsai SY, Tsai MJ, O'Malley BW 1995 Sequence and characterization of a coactlvator for the steroid hormone receptor superfamily. Science 270:1354-1357
33. Spencer TE, Jenster G, Burcin MM, Allis CD, Zhou J, Mizzen CA, McKenna NJ, Onate SA, Tsai SY, Tsai MJ, O'Malley BW 1997 Steroid receptor coactivator-1 is a histone acetyltransferase. Nature 389:194-198
34. Ogryzko VV, Schiltz RL, Russanova V, Howard BH, Nakatani Y 1996 The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 87:953-959
35. Chen D, Ma H, Hong H, Koh SS, Huang SM, Schurter BT, Aswad DW, Stallcup MR 1999 Regulation of transcription by a protein methyltransferase. Science 284:2174-2177
36. McKenna NJ, O'Malley BW 2002 Combinatorial control of gene expression by nuclear receptors and coregulators. Cell 108:465-474
37. Vignali M, Hassan AH, Neely KE, Workman JL 2000 ATP-dependent chromatin-remodeling complexes. Mol Cell Biol 20:1899-1910
38. Narlikar GJ, Fan HY, Kingston RE 2002 Cooperation between complexes that regulate chromatin structure and transcription. Cell 108:475-487
39. Liu Z, Wong J, Tsai SY, Tsai MJ, O'Malley BW 2001 Sequential recruitment of steroid receptor coactivator-1 (SRC-1) and p300 enhances progesterone receptor-dependent initiation and reinitiation of transcription from chromatin. Proc Natl Acad Sci USA 98:12426-12431
40. Liu Z, Wong J, Tsai SY, Tsai MJ, O'Malley BW 1999 Steroid receptor coactivator-1 (SRC-1) enhances ligand-dependent and receptor-dependent cell-free transcription of chromatin. Proc Natl Acad Sci USA 96:9485-9490
41. Di Croce L, Koop R, Venditti P, Westphal HM, Nightingale KP, Corona DF, Becker PB, Beato M 1999 Two-step synergism between the progesterone receptor and the DNA-binding domain of nuclear factor 1 on MMTV minichromosomes. Mol Cell 4:45-54
42. Gee AC, Carlson KE, Martini PG, Katzenellenbogen BS, Katzenellenbogen JA 1999 Coactivator peptides have a differential stabilizing effect on the binding of estrogens and antiestrogens with the estrogen receptor. Mol Endocrinol 13:1912-1923
43. Kraus WL, Kadonaga JT 1998 p300 and estrogen receptor cooperatively activate transcription via differential enhancement of initiation and reinitiation. Genes Dev 12:331-342
44. Mohandas N, Groner W 1989 Cell membrane and volume changes during red cell development and aging. Ann NY Acad Sci 554:217-224
45. Smith DF, Whitesell L, Nair SC, Chen S, Prapapanich V, Rlmerman RA 1995 Progesterone receptor structure and function altered by geldanamycin, an hsp90-binding agent. Mol Cell Biol 15:6804-6812
46. Arbeitman MN, Hogness DS 2000 Molecular chaperones activate the Drosophila ecdysone receptor, an RXR heterodimer. Cell 101:67-77
47. Smith DF, Stensgard BA, Welch WJ, Toft DO 1992 Assembly of progesterone receptor with heat shock proteins and receptor activation are ATP mediated events. J Biol Chem 267:1350-1356
48. Prapapanich V, Chen S, Nair SC, Rimerman RA, Smith DF 1996 Molecular cloning of human p48, a transient component of progesterone receptor complexes and an Hsp70-binding protein. Mol Endocrinol 10:420-431
49. Smith DF 1998 Sequence motifs shared between chaperone components participating in the assembly of progesterone receptor complexes. Biol Chem 379:283-288
50. Thackray VG, Nordeen SK 2002 High-yield purification of functional, full-length steroid receptor coactivator 1 expressed in insect cells. Biotechniques 32:260, 262-263
51. Chasman DI, Leatherwood J, Carey M, Ptashne M, Kornberg RD 1989 Activation of yeast polymerase II transcription by herpesvirus VP16 and GAL4 derivatives in vitro. Mol Cell Biol 9:4746-4749
52. Schumacher RJ, Hansen WJ, Freeman BC, Alnemri E, Litwack G, Toft DO 1996 Cooperative action of Hsp70, Hsp90, and DnaJ proteins in protein renaturation. Biochemistry 35:14889-14898
53. Grenert JP, Johnson BD, Toft DO 1999 The importance of ATP binding and hydrolysis by hsp90 in formation and function of protein heterocomplexes. J Biol Chem 274:17525-17533
54. Kraus WL, Manning ET, Kadonaga JT 1999 Biochemical analysis of distinct activation functions in p300 that enhance transcription initiation with chromatin templates. Mol Cell Biol 19:8123-8135
55. Kraus WL, Kadonaga JT 1999 Ligand- and cofactor-regulated transcription by nuclear hormone receptors with chromatin templates. In: Picard D, ed. Nuclear receptors: a practical approach. Oxford, UK: Oxford University Press; 167-189
56. Pazin MJ, Kamakaka RT, Kadonaga JT 1994 ATP-dependent nucleosome reconfiguration and transcriptional activation from preassembled chromatin templates. Science 266:2007-2011
57. Boonyaratanakornkit V, Melvin V, Prendergast P, Altmann M, Ronfani L, Bianchi ME, Taraseviciene L, Nordeen SK, Allegretto EA, Edwards DP 1998 High-mobility group chromatin proteins 1 and 2 functionally interact with steroid hormone receptors to enhance their DNA binding in vitro and transcriptional activity in mammalian cells. Mol Cell Biol 18:4471-4487
58. Kundu TK, Palhan VB, Wang Z, An W, Cole PA, Roeder RG 2000 Activator-dependent transcription from chromatin in vitro involving targeted histone acetylation by p300. Mol Cell 6:551-561
59. Lambert JR, Nordeen SK 2001 Analysis of steroid hormone-induced histone acetylation by chromatin immunoprecipitation assay. In: Lieberman B, ed. Steroid receptor methods, protocols and assays. Totowa, NJ: Humana Press; 273-282