Partial agonist activity of the progesterone receptor antagonist RU486 mediated by an amino-terminal domain coactivator and phosphorylation of serine400

Molecular Endocrinology

Volumn 24, Issue 2, 2010, Pages 335-345

  Wardell, Suzanne E ^b,c   Narayanan, Ramesh ^a,d   Weigel, Nancy L ^a   Edwards, Dean P ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d GTx Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN DEPENDENT KINASE 2; JUN DIMERIZATION PROTEIN 2; MIFEPRISTONE; ONAPRISTONE; PROGESTERONE RECEPTOR; PROMEGESTONE; SERINE; STEROID RECEPTOR COACTIVATOR 1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL CULTURE; CELL STRAIN COS1; CONFORMATION; CONTROLLED STUDY; DRUG RECEPTOR BINDING; GENETIC TRANSCRIPTION; HELA CELL; IN VITRO STUDY; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; CYCLIN A; CYCLIN-DEPENDENT KINASE 2; GONANES; HELA CELLS; HORMONE ANTAGONISTS; HUMANS; MIFEPRISTONE; NUCLEAR RECEPTOR COACTIVATOR 1; PHOSPHORYLATION; PROMEGESTONE; PROTEIN INTERACTION DOMAINS AND MOTIFS; RATS; RECEPTORS, PROGESTERONE; REPRESSOR PROTEINS; SERINE; TRANSCRIPTIONAL ACTIVATION;

EID: 75149130096     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2008-0081     Document Type: Article

References (50)

1. Li X, O'Malley BW 2003 Unfolding the action of progesterone receptors. J Biol Chem 278:39261-39264
2. Kastner P, Krust A, Turcotte B, Stropp U, Tora L, Gronemeyer H, Chambon P 1990 Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO J 9:1603-1614
3. Tora L, White J, Brou C, Tasset D, Webster N, Scheer E, Chambon P 1989 The human estrogen receptor has two independent non-acidic transcriptional activation functions. Cell 59:477-487
4. Meyer ME, Quirin-Stricker C, Lerouge T, Bocquel MT, Gronemeyer H 1992 A limiting factor mediates the differential activation of promoters by the human progesterone receptor isoforms. J Biol Chem 267:10882-10887
5. Giangrande PH, McDonnel DP 1999 The A and B isoforms of the human progesterone receptor: two functionally different transcription factors encoded by a single gene. Recent Prog Horm Res 45: 291-313
6. Mulac-Jericevic B, Mullinax RA, DeMayo FJ, Lydon JP, Conneely OM 2000 Subgroup of reproductive functions of progesterone mediated by progesterone receptor-B isoform. Science 289:1751-1754
7. Mulac-Jericevic B, Lydon JP, DeMayo FJ, Conneely OM 2003 Defective mammary gland morphogenesis in mice lacking the progesterone receptor B isoform. Proc Natl Acad Sci USA 100:9744-9749
8. Wardell SE, Edwards DP 2005 Mechanisms controlling agonist and antagonist potential of selective progesterone receptor modulators (SPRMs). Semin Reprod Med 23:9-21
9. Hovland AR, Powell RL, Takimoto GS, Tung L, Horwitz KB 1998 An N-terminal inhibitory function, IF, suppresses transcription by the A-isoform but not the B-isoform of human progesterone receptors. J Biol Chem 273:5455-5460
10. Giangrande PH, Pollio G, McDonnell DP 1997 Mapping and characterization of the functional domains responsible for the differential activity of the A and B isoforms of the human progesterone receptor. J Biol Chem 272:32889-32900
11. Weigel NL, Moore NL 2007 Steroid receptor phosphorylation: a key modulator of multiple receptor functions. Mol Endocrinol 21: 2311-2319
12. Clemm DL, Sherman L, Boonyaratanakornkit V, Schrader WT, Weigel NL, Edwards DP 2000 Differential hormone-dependent phosphorylation of progesterone receptor A and B forms revealed by a phosphoserine site-specific monoclonal antibody. Mol Endocrinol 14:52-65
13. Knotts TA, Orkiszewski RS, Cook RG, Edwards DP, Weigel NL 2001 Identification of a phosphorylation site in the hinge region of the human progesterone receptor and additional amino-terminal phosphorylation sites. J Biol Chem 276:8475-8383
14. Takimoto GS, Hovland AR, Tasset DM, Melville MY, Tung L, Horwitz KB 1996 Role of phosphorylation on DNA binding and transcriptional functions of human progesterone receptors. J Biol Chem 271:13308-13316
15. Lange CA, Shen T, Horwitz KB 2000 Phosphorylation of human progesterone receptors at serine-294 by mitogen-activated protein kinase signals their degration by the 26S proteasome. Proc Natl Acad Sci USA 97:1032-1037
16. Qiu M, Olsen A, Faivre E, Horwitz KB, Lange CA 2003 Mitogen-activated protein kinase regulates nuclear association of human progesterone receptors. Mol Endocrinol 17:628-642
17. Pierson-Mullany LK, Lange CA 2004 Phosphorylation of progesterone receptor serine 400 mediates ligand-independent transcriptional activity in response to activation of cyclin-dependent protein kinase 2. Mol Cell Biol 24:10542-10557
18. Shen T, Horwitz KB, Lange CA 2001 Transcriptional hyperactivity of human progesterone receptors is coupled to their ligand-dependent down-regulation by mitogen-activated protein kinase-dependent phosphorylation of serine 294. Mol Cell Biol 21:6122-6131
19. Daniel AR, Faivre EJ, Lange CA 2007 Phosphorylation-dependent antagonism of sumoylation derepresses progesterone receptor action in breast cancer cells. Mol Endocrinol 21:2890-2906
20. Daniel AR, Knutson TP, Lange CA 2009 Review: signaling inputs to progesterone receptor gene regulation promoter selectivity. Mol Cell Endocrinol 308:47-52
21. Narayanan R, Edwards DP, Weigel NL 2005 Human progesterone receptor displays cell cycle-dependent changes in transcriptional activity. Mol Cell Biol 25:2885-2898
22. Labriola L, Salatino M, Proietti CJ, Pecci A, Coso OA, Kornblihtt AR, Charreau EH, Elizalde PV 2003 Heregulin induces transcriptional activation of the progesterone receptor by a mechanism that requires functional ErbB-2 and mitogen-activated protein kinase activation in breast cancer cells. Mol Cell Biol 23:1095-1111
23. Faivre EJ, Daniel AR, Hillard CJ, Lange CA 2008 Progesterone receptor rapid signaling mediates serine 345 phosphorylation and tethering to specificity protein 1 transcription factors. Mol Endocrinol 22:823-837
24. Daniel AR, Lange CA 2009 Protein kinases mediate ligand-independent derepression of sumoylated progesterone receptors in breast cancer cells. Proc Natl Acad Sci USA 106:14287-14292
25. Chen W, Dang T, Blind RD, Wang Z, Cavasotto CN, Hittelman AB, Rogatsky I, Logan SK, Garabedian MJ 2008 Glucocorticoid receptor phosphorylation differentially affects target gene expression. Mol Endocrinol 22:1754-1766
26. Zhang Y, Beck CA, Poletti A, Clement 4th JP, Prendergast P, Yip TT, Hutchens TW, Edwards DP, Weigel NL 1997 Phosphorylation of human progesterone receptor by cyclin-dependent kinase 2 on three sites that are authentic basal phosphorylation sites in vivo. Mol Endocrinol 11:823-832
27. Spitz IM, Croxatto HB, Robbins A 1996 Antiprogestins: mechanism of action and contraceptive potential. Annu Rev Pharmacol Toxicol 36:47-81
28. Meyer ME, Pronon A, Ji JW, Bocquel MT, Chambon P, Gronemeyer H 1990 Agonistic and antagonistic activities of RU486 on the functions of the human progesterone receptor. EMBO J 9:3923-3932
29. Klein-Hitpass L, Cato AC, Henderson D, Ryffel GU 1991 Two types of antiprogestins identified by their differential action in transcriptionally active extracts from T47D cells. Nucleic Acids Res 19:1227-12234
30. Gass EK, Leonhardt SA, Nordeen SK, Edwards DP 1998 The antagonists RU486 and ZK98299 stimulate progesterone receptor binding to deoxyribonucleic acid in vitro and in vivo, but have distinct effects on receptor conformation. Endocrinology 139:1905-1919
31. Vegeto E, Allan GF, Schrader WT, Tsai MJ, McDonnell DP, O'Malley BW 1992 The mechanism of RU486 antagonism in dependent on the conformation of the carboxyl-terminal tail of the human progesterone receptor. Cell 69:703-713
32. Leonhardt S, Edwards D 2002 Mechanism of action of progesterone antagonists. Exp Biol Med 227:969-980
33. Wagner BL, Norris JD, Knotts TA, Weigel NL, McDonnell DP 1998 The nuclear corepressors NCoR and SMRT are key regulators of both ligand- and 8-bromo-cyclic AMP-dependent transcriptional activity of the human progesterone receptor. Mol Cell Biol 18:1369-1378
34. Jackson TA, Richer JK, Bain DL, Takimoto GS, Tung L, Horwitz KB 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 and SMRT. Mol Endocrinol 11:693-705
35. Liu Z, Auboeuf D, Wong J, Chen JD, Tsai SY, Tsai MJ, O'Malley BW 2002 Coactivator/corepressor ratios modulate PR-mediated transcription by the selective receptor modulator RU486. Proc Natl Acad Sci USA 99:7940-7944
36. Beck CA, Weigel NL, Moyer ML, Nordeen SK, Edwards DP 1993 The progesterone antagonist RU486 acquires agonist activity upon stimulation of cAMP signaling pathways. Proc Natl Acad Sci USA 90:4441-4445
37. Sartorius CA, Tung L, Takimoto GS, Horwitz KB 1993 Antagonist-occupied human progesterone receptors bound to DNA are functionally switched to transcriptional agonists by cAMP. J Biol Chem 268:9262-9266
38. Wardell SE, Boonyaratanakornkit V, Adelman JS, Aronheim A, Edwards DP 2002 Jun dimerization protein 2 functions as a progesterone receptor N-terminal domain coactivator. Mol Cell Biol 22:5451-5466
39. Wardell SE, Kwok SC, Sherman L, Hodges RS, Edwards DP 2005 Regulation of the amino-terminal transcription activation domain of progesterone receptor by a cofactor-induced protein folding mechanism. Mol Cell Biol 25:8792-8808
40. Kumar R, Thompson EB 2003 Transactivation functions of the N-terminal domains of nuclear hormone receptors: protein folding and coactivator interactions. Mol Endocrinol 17:1-10
41. Bain DL, Franden MA, McManaman JL, Takimoto GS, Horwitz KB 2001 The N-terminal region of human progesterone B-receptors. J Biol Chem 276:23825-23831
42. Kumar R, Volk DE, Li J, Lee JC, Gorenstein DG, Thompson EB 2004 TATA box binding protein induces structure in the recombinant glucocorticoid receptor AF1 domain. Proc Natl Acad Sci USA 101:16425-16430
43. Wärnmark A, Wikström A, Wright AP, Gustafsson JA, Härd T 2001 The N-terminal regions of estrogen receptor α and β are unstructured and show different TBP binding properties. J Biol Chem 276:45939-45944
44. McEwan IJ, Lavery D, Fischer K, Watt K 2007 Natural disordered sequences in the amino terminal domain of nuclear receptors: lessons from the androgen and glucocorticoid receptors. Nucl Recept Signal 5:e001
45. Hill KK, Roemer SC, Jones DN, Churchill ME, Edwards DP 2009 A progesterone receptor co-activator (JDP2) mediates activity through interaction with residues in the carboxyl-terminal extension of the DNA binding domain. J Biol Chem 284:24415-24424
46. Takimoto GS, Tasset DM, Eppert AC, Horwitz KB 1992 Hormone-induced progesterone receptor phosphorylation consists of sequential DNA-independent and DNA-dependent stages: analysis with zinc finger mutants and the progesterone antagonist ZK98299. Proc Natl Acad Sci USA 89:3050-3054
47. Narayanan R, Adigun AA, Edwards DP, Weigel NL 2005 Cyclin-dependent kinase activity is required for progesterone receptor function: novel role for cyclin A/Cdk2 as a progesterone receptor coactivator. Mol Cell Biol 25:264-277
48. McInerney EM, Katzenellenbogen BS 1996 Different regions in activation function-1 of the human estrogen receptor required for antiestrogen- and estradiol-dependent transcriptional activation. J Biol Chem 271:24172-24178
49. Xu J, Nawaz Z, Tsai SY, Tsai MJ, O'Malley BW 1996 The extreme C terminus of progesterone receptor contains a transcriptional repressor domain that functions through a putative corepressor. Proc Natl Acad Sci USA 93:12195-12199
50. Boonyaratanakornkit V, Melvin V, Prendergast P, Altmann M, Ronfani L, Bianchi M, 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