Progesterone receptors, their isoforms and progesterone regulated transcription

Molecular and Cellular Endocrinology

Volumn 357, Issue 1-2, 2012, Pages 18-29

  Jacobsen, Britta M ^a   Horwitz, Kathryn B ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Gene regulation; Isoform; Monomer; Progesterone; Progesterone receptor; Transcription

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR; GESTAGEN; ISOPROTEIN; MONOMER; PROGESTERONE; PROGESTERONE RECEPTOR; PROGESTERONE RECEPTOR A; PROGESTERONE RECEPTOR B; TRANSCRIPTION FACTOR;

CHROMATIN; DNA BINDING; GENE CONTROL; GENE EXPRESSION PROFILING; GENE TARGETING; HORMONAL REGULATION; HORMONE ACTION; HORMONE DETERMINATION; HORMONE RESPONSIVE ELEMENT; HUMAN; LONG TERMINAL REPEAT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; TRANSCRIPTION REGULATION;

ANIMALS; GENE EXPRESSION REGULATION; HUMANS; PROGESTERONE; PROGESTINS; PROTEIN ISOFORMS; RECEPTORS, PROGESTERONE; TRANSCRIPTION, GENETIC;

EID: 84860316458     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.09.016     Document Type: Review

References (156)

1. Abdel-Hafiz H., Takimoto G.S., Tung L., Horwitz K.B. The inhibitory function in human progesterone receptor N termini binds SUMO-1 protein to regulate autoinhibition and transrepression. J. Biol. Chem. 2002, 277:33950-33956.
2. Alexander I.E., Clarke C.L., Shine J., Sutherland R.L. Progestin inhibition of progesterone receptor gene expression in human breast cancer cells. Mol. Endocrinol. 1989, 3:1377-1386.
3. Alkhalaf M., Murphy L.C. Regulation of c-jun and jun-B by progestins in T-47D human breast cancer cells. Mol. Endocrinol. 1992, 6:1625-1633.
4. Arnett-Mansfield R.L., Graham J.D., Hanson A.R., Mote P.A., Gompel A., Scurr L.L., Gava N., de Fazio A., Clarke C.L. Focal subnuclear distribution of progesterone receptor is ligand dependent and associated with transcriptional activity. Mol. Endocrinol. 2007, 21:14-29.
5. Aupperlee M.D., Haslam S.Z. Differential hormonal regulation and function of progesterone receptor isoforms in normal adult mouse mammary gland. Endocrinology 2007, 148:2290-2300.
6. Aupperlee M.D., Smith K.T., Kariagina A., Haslam S.Z. Progesterone receptor isoforms A and B: temporal and spatial differences in expression during murine mammary gland development. Endocrinology 2005, 146:3577-3588.
7. Aupperlee M.D., Drolet A.A., Durairaj S., Wang W., Schwartz R.C., Haslam S.Z. Strain-specific differences in the mechanisms of progesterone regulation of murine mammary gland development. Endocrinology 2009, 150:1485-1494.
8. Bailly A., Le Page C., Rauch M., Milgrom E. Sequence-specific DNA binding of the progesterone receptor to the uteroglobin gene: effects of hormone, antihormone and receptor phosphorylation. EMBO J. 1986, 5:3235-3241.
9. Bain D.L., Franden M.A., McManaman J.L., Takimoto G.S., Horwitz K.B. The N-terminal region of the human progesterone A-receptor. Structural analysis and the influence of the DNA binding domain. J. Biol. Chem. 2000, 275:7313-7320.
10. Bain D.L., Franden M.A., McManaman J.L., Takimoto G.S., Horwitz K.B. The N-terminal region of human progesterone B-receptors: biophysical and biochemical comparison to A-receptors. J. Biol. Chem. 2001, 276:23825-23831.
11. Bamberger A.M., Bamberger C.M., Gellersen B., Schulte H.M. Modulation of AP-1 activity by the human progesterone receptor in endometrial adenocarcinoma cells. Proc. Natl. Acad. Sci. USA 1996, 93:6169-6174.
12. Bocquel M.T., Kumar V., Stricker C., Chambon P., Gronemeyer H. The contribution of the N- and C-terminal regions of steroid receptors to activation of transcription is both receptor and cell-specific. Nucleic Acids Res. 1989, 17:2581-2595.
13. Boney-Montoya J., Ziegler Y.S., Curtis C.D., Montoya J.A., Nardulli A.M. Long-range transcriptional control of progesterone receptor gene expression. Mol. Endocrinol. 2010, 24:346-358.
14. Boonyaratanakornkit V., Strong D.D., Mohan S., Baylink D.J., Beck C.A., Linkhart T.A. Progesterone stimulation of human insulin-like growth factor-binding protein-5 gene transcription in human osteoblasts is mediated by a CACCC sequence in the proximal promoter. J. Biol. Chem. 1999, 274:26431-26438.
15. Boonyaratanakornkit V., Scott M.P., Ribon V., Sherman L., Anderson S.M., Maller J.L., Miller W.T., Edwards D.P. Progesterone receptor contains a proline-rich motif that directly interacts with SH3 domains and activates c-Src family tyrosine kinases. Mol. Cell 2001, 8:269-280.
16. Botos J., Xian W., Smith D.F., Smith C.L. Progesterone receptor deficient in chromatin binding has an altered cellular state. J. Biol. Chem. 2004, 279:15231-15239.
17. Bray J.D., Jelinsky S., Ghatge R., Bray J.A., Tunkey C., Saraf K., Jacobsen B.M., Richer J.K., Brown E.L., Winneker R.C., Horwitz K.B., Lyttle C.R. Quantitative analysis of gene regulation by seven clinically relevant progestins suggests a highly similar mechanism of action through progesterone receptors in T47D breast cancer cells. J. Steroid Biochem. Mol. Biol. 2005, 97:328-341.
18. Brayman M.J., Julian J., Mulac-Jericevic B., Conneely O.M., Edwards D.P., Carson D.D. Progesterone receptor isoforms A and B differentially regulate MUC1 expression in uterine epithelial cells. Mol. Endocrinol. 2006, 20:2278-2291.
19. Buser A.C., Gass-Handel E.K., Wyszomierski S.L., Doppler W., Leonhardt S.A., Schaack J., Rosen J.M., Watkin H., Anderson S.M., Edwards D.P. Progesterone receptor repression of prolactin/signal transducer and activator of transcription 5-mediated transcription of the beta-casein gene in mammary epithelial cells. Mol. Endocrinol. 2007, 21:106-125.
20. Carroll J.S., Liu X.S., Brodsky A.S., Li W., Meyer C.A., Szary A.J., Eeckhoute J., Shao W., Hestermann E.V., Geistlinger T.R., Fox E.A., Silver P.A., Brown M. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 2005, 122:33-43.
21. Cato A.C., Miksicek R., Schutz G., Arnemann J., Beato M. The hormone regulatory element of mouse mammary tumour virus mediates progesterone induction. EMBO J. 1986, 5:2237-2240.
22. Chalepakis G., Arnemann J., Slater E., Bruller H.J., Gross B., Beato M. Differential gene activation by glucocorticoids and progestins through the hormone regulatory element of mouse mammary tumor virus. Cell 1988, 53:371-382.
23. Cheng K.W., Cheng C.K., Leung P.C. Differential role of PR-A and -B isoforms in transcription regulation of human GnRH receptor gene. Mol. Endocrinol. 2001, 15:2078-2092.
24. Cho H., Aronica S.M., Katzenellenbogen B.S. Regulation of progesterone receptor gene expression in MCF-7 breast cancer cells: a comparison of the effects of cyclic adenosine 3',5'-monophosphate, estradiol, insulin-like growth factor-I, and serum factors. Endocrinology 1994, 134:658-664.
25. Christian M., Pohnke Y., Kempf R., Gellersen B., Brosens J.J. Functional association of PR and CCAAT/enhancer-binding protein beta isoforms: promoter-dependent cooperation between PR-B and liver-enriched inhibitory protein, or liver-enriched activatory protein and PR-A in human endometrial stromal cells. Mol. Endocrinol. 2002, 16:141-154.
26. Cicatiello L., Addeo R., Sasso A., Altucci L., Petrizzi V.B., Borgo R., Cancemi M., Caporali S., Caristi S., Scafoglio C., Teti D., Bresciani F., Perillo B., Weisz A. Estrogens and progesterone promote persistent CCND1 gene activation during G1 by inducing transcriptional derepression via c-Jun/c-Fos/estrogen receptor (progesterone receptor) complex assembly to a distal regulatory element and recruitment of cyclin D1 to its own gene promoter. Mol. Cell. Biol. 2004, 24:7260-7274.
27. Clarke C.L., Roman S.D., Graham J., Koga M., Sutherland R.L. Progesterone receptor regulation by retinoic acid in the human breast cancer cell line T-47D. J. Biol. Chem. 1990, 265:12694-12700.
28. Clarke C.L., Graham J., Roman S.D., Sutherland R.L. Direct transcriptional regulation of the progesterone receptor by retinoic acid diminishes progestin responsiveness in the breast cancer cell line T-47D. J. Biol. Chem. 1991, 266:18969-18975.
29. Clemens J.W., Robker R.L., Kraus W.L., Katzenellenbogen B.S., Richards J.S. Hormone induction of progesterone receptor (PR) messenger ribonucleic acid and activation of PR promoter regions in ovarian granulosa cells: evidence for a role of cyclic adenosine 3',5'-monophosphate but not estradiol. Mol. Endocrinol. 1998, 12:1201-1214.
30. Condon J.C., Hardy D.B., Kovaric K., Mendelson C.R. Up-regulation of the progesterone receptor (PR)-C isoform in laboring myometrium by activation of nuclear factor-kappaB may contribute to the onset of labor through inhibition of PR function. Mol. Endocrinol. 2006, 20:764-775.
31. Connaghan-Jones K.D., Bain D.L. Using thermodynamics to understand progesterone receptor function: method and theory. Methods Enzymol. 2009, 455:41-70.
32. Connaghan-Jones K.D., Heneghan A.F., Miura M.T., Bain D.L. Thermodynamic dissection of progesterone receptor interactions at the mouse mammary tumor virus promoter: monomer binding and strong cooperativity dominate the assembly reaction. J. Mol. Biol. 2008, 377:1144-1160.
33. Cui X., Lazard Z., Zhang P., Hopp T.A., Lee A.V. Progesterone crosstalks with insulin-like growth factor signaling in breast cancer cells via induction of insulin receptor substrate-2. Oncogene 2003, 22:6937-6941.
34. Cui X., Zhang P., Deng W., Oesterreich S., Lu Y., Mills G.B., Lee A.V. Insulin-like growth factor-I inhibits progesterone receptor expression in breast cancer cells via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin pathway: progesterone receptor as a potential indicator of growth factor activity in breast cancer. Mol. Endocrinol. 2003, 17:575-588.
35. Dai D., Litman E.S., Schonteich E., Leslie K.K. Progesterone regulation of activating protein-1 transcriptional activity: a possible mechanism of progesterone inhibition of endometrial cancer cell growth. J. Steroid Biochem. Mol. Biol. 2003, 87:123-131.
36. Daniel A.R., Knutson T.P., Lange C.A. Signaling inputs to progesterone receptor gene regulation and promoter selectivity. Mol. Cell. Endocrinol. 2009, 308:47-52.
37. Daniel A.R., Gaviglio A.L., Czaplicki L.M., Hillard C.J., Housa D., Lange C.A. The progesterone receptor hinge region regulates the kinetics of transcriptional responses through acetylation, phosphorylation, and nuclear retention. Mol. Endocrinol. 2010, 24:2126-2138.
38. De Amicis F., Zupo S., Panno M.L., Malivindi R., Giordano F., Barone I., Mauro L., Fuqua S.A., Ando S. Progesterone receptor B recruits a repressor complex to a half-PRE site of the estrogen receptor alpha gene promoter. Mol. Endocrinol. 2009, 23:454-465.
39. Dougherty D.C., Sanders M.M. Comparison of the responsiveness of the pGL3 and pGL4 luciferase reporter vectors to steroid hormones. BioTechniques 2005, 39:203-207.
40. Doyle K.M., Russell D.L., Sriraman V., Richards J.S. Coordinate transcription of the ADAMTS-1 gene by luteinizing hormone and progesterone receptor. Mol. Endocrinol. 2004, 18:2463-2478.
41. Eeckhoute J., Keeton E.K., Lupien M., Krum S.A., Carroll J.S., Brown M. Positive cross-regulatory loop ties GATA-3 to estrogen receptor alpha expression in breast cancer. Cancer Res. 2007, 67:6477-6483.
42. Fernandez-Valdivia R., Mukherjee A., Creighton C.J., Buser A.C., DeMayo F.J., Edwards D.P., Lydon J.P. Transcriptional response of the murine mammary gland to acute progesterone exposure. Endocrinology 2008, 149:6236-6250.
43. Gao J., Mazella J., Tang M., Tseng L. Ligand-activated progesterone receptor isoform hPR-A is a stronger transactivator than hPR-B for the expression of IGFBP-1 (insulin-like growth factor binding protein-1) in human endometrial stromal cells. Mol. Endocrinol. 2000, 14:1954-1961.
44. Gao J., Mazella J., Seppala M., Tseng L. Ligand activated hPR modulates the glycodelin promoter activity through the Sp1 sites in human endometrial adenocarcinoma cells. Mol. Cell. Endocrinol. 2001, 176:97-102.
45. Gao J., Mazella J., Tseng L. Hox proteins activate the IGFBP-1 promoter and suppress the function of hPR in human endometrial cells. DNA Cell Biol. 2002, 21:819-825.
46. Ghatge R.P., Jacobsen B.M., Schittone S.A., Horwitz K.B. The progestational and androgenic properties of medroxyprogesterone acetate: gene regulatory overlap with dihydrotestosterone in breast cancer cells. Breast Cancer Res. 2005, 7:R1036-R1050.
47. Giangrande P.H., Kimbrel E.A., Edwards D.P., McDonnell D.P. The opposing transcriptional activities of the two isoforms of the human progesterone receptor are due to differential cofactor binding. Mol. Cell. Biol. 2000, 20:3102-3115.
48. Goldhar A.S., Duan R., Ginsburg E., Vonderhaar B.K. Progesterone induces expression of the prolactin receptor gene through cooperative action of Sp1 and C/EBP. Mol. Cell. Endocrinol. 2011, 335:148-157.
49. Gowland P.L., Buetti E. Mutations in the hormone regulatory element of mouse mammary tumor virus differentially affect the response to progestins, androgens, and glucocorticoids. Mol. Cell. Biol. 1989, 9:3999-4008.
50. Graham J.D., Clarke C.L. Physiological action of progesterone in target tissues. Endocr. Rev. 1997, 18:502-519.
51. Graham J.D., Roman S.D., McGowan E., Sutherland R.L., Clarke C.L. Preferential stimulation of human progesterone receptor B expression by estrogen in T-47D human breast cancer cells. J. Biol. Chem. 1995, 270:30693-30700.
52. Graham J.D., Yeates C., Balleine R.L., Harvey S.S., Milliken J.S., Bilous A.M., Clarke C.L. Characterization of progesterone receptor A and B expression in human breast cancer. Cancer Res. 1995, 55:5063-5068.
53. Graham J.D., Yager M.L., Hill H.D., Byth K., O'Neill G.M., Clarke C.L. Altered progesterone receptor isoform expression remodels progestin responsiveness of breast cancer cells. Mol. Endocrinol. 2005, 19:2713-2735.
54. Graham J.D., Mote P.A., Salagame U., van Dijk J.H., Balleine R.L., Huschtscha L.I., Reddel R.R., Clarke C.L. DNA replication licensing and progenitor numbers are increased by progesterone in normal human breast. Endocrinology 2009, 150:3318-3326.
55. +-dependent 15-hydroxyprostaglandin dehydrogenase gene promoter is controlled by Ets and activating protein-1 transcription factors and progesterone. Endocrinology 2000, 141:581-597.
56. Groshong S.D., Owen G.I., Grimison B., Schauer I.E., Todd M.C., Langan T.A., Sclafani R.A., Lange C.A., Horwitz K.B. Biphasic regulation of breast cancer cell growth by progesterone: role of the cyclin-dependent kinase inhibitors, p21 and p27(Kip1). Mol. Endocrinol. 1997, 11:1593-1607.
57. Hewetson A., Chilton B.S. An Sp1-NF-Y/progesterone receptor DNA binding-dependent mechanism regulates progesterone-induced transcriptional activation of the rabbit RUSH/SMARCA3 gene. J. Biol. Chem. 2003, 278:40177-40185.
58. Hill K.K., Roemer S.C., Jones D.N., Churchill M.E., Edwards D.P. 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. 2009, 284:24415-24424.
59. Hilton H.N., Kalyuga M., Cowley M.J., Alles M.C., Lee H.J., Caldon C.E., Blazek K., Kaplan W., Musgrove E.A., Daly R.J., Naylor M.J., Graham J.D., Clarke C.L., Ormandy C.J. The antiproliferative effects of progestins in T47D breast cancer cells are tempered by progestin induction of the ETS transcription factor Elf5. Mol. Endocrinol. 2010, 24:1380-1392.
60. Hopp T.A., Weiss H.L., Hilsenbeck S.G., Cui Y., Allred D.C., Horwitz K.B., Fuqua S.A. Breast cancer patients with progesterone receptor PR-A-rich tumors have poorer disease-free survival rates. Clin. Cancer Res. 2004, 10:2751-2760.
61. Horwitz K.B., Koseki Y., McGuire W.L. Estrogen control of progesterone receptor in human breast cancer: role of estradiol and antiestrogen. Endocrinology 1978, 103:1742-1751.
62. Hovland A.R., Powell R.L., Takimoto G.S., Tung L., Horwitz K.B. An N-terminal inhibitory function, IF, suppresses transcription by the A-isoform but not the B-isoform of human progesterone receptors. J. Biol. Chem. 1998, 273:5455-5460.
63. Hu Z.Z., Zhuang L., Meng J., Dufau M.L. Transcriptional regulation of the generic promoter III of the rat prolactin receptor gene by C/EBPbeta and Sp1. J. Biol. Chem. 1998, 273:26225-26235.
64. Hubler T.R., Scammell J.G. Intronic hormone response elements mediate regulation of FKBP5 by progestins and glucocorticoids. Cell Stress Chaperon. 2004, 9:243-252.
65. Hubler T.R., Denny W.B., Valentine D.L., Cheung-Flynn J., Smith D.F., Scammell J.G. The FK506-binding immunophilin FKBP51 is transcriptionally regulated by progestin and attenuates progestin responsiveness. Endocrinology 2003, 144:2380-2387.
66. Huggins G.S., Wong J.Y., Hankinson S.E., De Vivo I. GATA5 activation of the progesterone receptor gene promoter in breast cancer cells is influenced by the +331G/A polymorphism. Cancer Res. 2006, 66:1384-1390.
67. Ilenchuk T.T., Walters M.R. Rat uterine progesterone receptor analyzed by [3H]R5020 photoaffinity labeling: evidence that the A and B subunits are not equimolar. Endocrinology 1987, 120:1449-1456.
68. Ismail P.M., Li J., DeMayo F.J., O'Malley B.W., Lydon J.P. A novel LacZ reporter mouse reveals complex regulation of the progesterone receptor promoter during mammary gland development. Mol. Endocrinol. 2002, 16:2475-2489.
69. Jacobsen B.M., Richer J.K., Schittone S.A., Horwitz K.B. New human breast cancer cells to study progesterone receptor isoform ratio effects and ligand-independent gene regulation. J. Biol. Chem. 2002, 277:27793-27800.
70. Jacobsen B.M., Schittone S.A., Richer J.K., Horwitz K.B. Progesterone-independent effects of human progesterone receptors (PRs) in estrogen receptor-positive breast cancer: PR isoform-specific gene regulation and tumor biology. Mol. Endocrinol. 2005, 19:574-587.
71. Jacobsen B.M., Jambal P., Schittone S.A., Horwitz K.B. ALU repeats in promoters are position-dependent co-response elements (coRE) that enhance or repress transcription by dimeric and monomeric progesterone receptors. Mol. Endocrinol. 2009, 23:989-1000.
72. Jaffe R.C., Donnelly K.M., Fazleabas A.T. The induction of baboon glycodelin expression by progesterone is not through Sp1. Mol. Hum. Reprod. 2003, 9:35-40.
73. Jantzen H.M., Strahle U., Gloss B., Stewart F., Schmid W., Boshart M., Miksicek R., Schutz G. Cooperativity of glucocorticoid response elements located far upstream of the tyrosine aminotransferase gene. Cell 1987, 49:29-38.
74. Jantzen K., Fritton H.P., Igo-Kemenes T., Espel E., Janich S., Cato A.C., Mugele K., Beato M. Partial overlapping of binding sequences for steroid hormone receptors and DNaseI hypersensitive sites in the rabbit uteroglobin gene region. Nucleic Acids Res. 1987, 15:4535-4552.
75. John S., Sabo P.J., Thurman R.E., Sung M.H., Biddie S.C., Johnson T.A., Hager G.L., Stamatoyannopoulos J.A. Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat. Genet. 2011, 43:264-268.
76. Kang H.Y., Lin H.K., Hu Y.C., Yeh S., Huang K.E., Chang C. From transforming growth factor-beta signaling to androgen action: identification of Smad3 as an androgen receptor coregulator in prostate cancer cells. Proc. Natl. Acad. Sci. USA 2001, 98:3018-3023.
77. Kariagina A., Aupperlee M.D., Haslam S.Z. Progesterone receptor isoforms and proliferation in the rat mammary gland during development. Endocrinology 2007, 148:2723-2736.
78. Kastner P., Krust A., Turcotte B., Stropp U., Tora L., Gronemeyer H., Chambon P. Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO J. 1990, 9:1603-1614.
79. Katiyar P., Ma Y., Riegel A., Fan S., Rosen E.M. Mechanism of BRCA1-mediated inhibition of progesterone receptor transcriptional activity. Mol. Endocrinol. 2009, 23:1135-1146.
80. Kepa J.K., Jacobsen B.M., Boen E.A., Prendergast P., Edwards D.P., Takimoto G., Wierman M.E. Direct binding of progesterone receptor to nonconsensus DNA sequences represses rat GnRH. Mol. Cell. Endocrinol. 1996, 117:27-39.
81. Kim J.J., Buzzio O.L., Li S., Lu Z. Role of FOXO1A in the regulation of insulin-like growth factor-binding protein-1 in human endometrial cells: interaction with progesterone receptor. Biol. Reprod. 2005, 73:833-839.
82. Kraus W.L., Montano M.M., Katzenellenbogen B.S. Cloning of the rat progesterone receptor gene 5'-region and identification of two functionally distinct promoters. Mol. Endocrinol. 1993, 7:1603-1616.
83. Kraus W.L., Montano M.M., Katzenellenbogen B.S. Identification of multiple, widely spaced estrogen-responsive regions in the rat progesterone receptor gene. Mol. Endocrinol. 1994, 8:952-969.
84. Krikun G., Schatz F., Mackman N., Guller S., Demopoulos R., Lockwood C.J. Regulation of tissue factor gene expression in human endometrium by transcription factors Sp1 and Sp3. Mol. Endocrinol. 2000, 14:393-400.
85. Lamian V., Gonzalez B.Y., Michel F.J., Simmen R.C. Non-consensus progesterone response elements mediate the progesterone-regulated endometrial expression of the uteroferrin gene. J. Steroid Biochem. Mol. Biol. 1993, 46:439-450.
86. Lange C.A., Richer J.K., Shen T., Horwitz K.B. Convergence of progesterone and epidermal growth factor signaling in breast cancer. Potentiation of mitogen-activated protein kinase pathways. J. Biol. Chem. 1998, 273:31308-31316.
87. Lange C.A., Shen T., Horwitz K.B. Phosphorylation of human progesterone receptors at serine-294 by mitogen-activated protein kinase signals their degradation by the 26S proteasome. Proc. Natl. Acad. Sci. USA 2000, 97:1032-1037.
88. Leo J.C., Wang S.M., Guo C.H., Aw S.E., Zhao Y., Li J.M., Hui K.M., Lin V.C. Gene regulation profile reveals consistent anticancer properties of progesterone in hormone-independent breast cancer cells transfected with progesterone receptor. Int. J. Cancer 2005, 117:561-568.
89. Lieberman B.A., Bona B.J., Edwards D.P., Nordeen S.K. The constitution of a progesterone response element. Mol. Endocrinol. 1993, 7:515-527.
90. Lin B., Wang J., Hong X., Yan X., Hwang D., Cho J.H., Yi D., Utleg A.G., Fang X., Schones D.E., Zhao K., Omenn G.S., Hood L. Integrated expression profiling and ChIP-seq analyses of the growth inhibition response program of the androgen receptor. PLoS One 2009, 4:e6589.
91. Maccarrone M., Bari M., Di Rienzo M., Finazzi-Agro A., Rossi A. Progesterone activates fatty acid amide hydrolase (FAAH) promoter in human T lymphocytes through the transcription factor Ikaros. Evidence for a synergistic effect of leptin. J. Biol. Chem. 2003, 278:32726-32732.
92. Magklara A., Smith C.L. A composite intronic element directs dynamic binding of the progesterone receptor and GATA-2. Mol. Endocrinol. 2009, 23:61-73.
93. Mallick S., Horwitz S.B. Transcriptional regulation of the murine multidrug resistance gene mdr1b by progesterone occurs via an indirect mechanism. DNA Cell Biol. 1997, 16:807-818.
94. Maston G.A., Evans S.K., Green M.R. Transcriptional regulatory elements in the human genome. Annu. Rev. Genomics Hum. Genet. 2006, 7:29-59.
95. McGowan E.M., Clarke C.L. Effect of overexpression of progesterone receptor A on endogenous progestin-sensitive endpoints in breast cancer cells. Mol. Endocrinol. 1999, 13:1657-1671.
96. Mohamed M.K., Tung L., Takimoto G.S., Horwitz K.B. The leucine zippers of c-fos and c-jun for progesterone receptor dimerization: A-dominance in the A/B heterodimer. J. Steroid Biochem. Mol. Biol. 1994, 51:241-250.
97. Moore M.R., Zhou J.L., Blankenship K.A., Strobl J.S., Edwards D.P., Gentry R.N. A sequence in the 5' flanking region confers progestin responsiveness on the human c-myc gene. J. Steroid Biochem. Mol. Biol. 1997, 62:243-252.
98. Mote P.A., Bartow S., Tran N., Clarke C.L. Loss of co-ordinate expression of progesterone receptors A and B is an early event in breast carcinogenesis. Breast Cancer Res. Treat. 2002, 72:163-172.
99. Mote P.A., Graham J.D., Clarke C.L. Progesterone receptor isoforms in normal and malignant breast. Ernst Schering Found. Symp. Proc. 2007, 77:107.
100. Musgrove E.A., Lee C.S., Sutherland R.L. Progestins both stimulate and inhibit breast cancer cell cycle progression while increasing expression of transforming growth factor alpha, epidermal growth factor receptor, c-fos, and c-myc genes. Mol. Cell. Biol. 1991, 11:5032-5043.
101. Ni X., Hou Y., Yang R., Tang X., Smith R., Nicholson R.C. Progesterone receptors A and B differentially modulate corticotropin-releasing hormone gene expression through a cAMP regulatory element. Cell. Mol. Life Sci. 2004, 61:1114-1122.
102. Nishida K., Kitazawa R., Mizuno K., Maeda S., Kitazawa S. Identification of regulatory elements of human alpha 6 integrin subunit gene. Biochem. Biophys. Res. Commun. 1997, 241:258-263.
103. Nordeen S.K., Ogden C.A., Taraseviciene L., Lieberman B.A. Extreme position dependence of a canonical hormone response element. Mol. Endocrinol. 1998, 12:891-898.
104. O'Conner J.L., Wade M.F., Prendergast P., Edwards D.P., Boonyaratanakornkit V., Mahesh V.B. A 361 base pair region of the rat FSH-beta promoter contains multiple progesterone receptor-binding sequences and confers progesterone responsiveness. Mol. Cell. Endocrinol. 1997, 136:67-78.
105. Owen G.I., Richer J.K., Tung L., Takimoto G., Horwitz K.B. Progesterone regulates transcription of the p21(WAF1) cyclin-dependent kinase inhibitor gene through Sp1 and CBP/p300. J. Biol. Chem. 1998, 273:10696-10701.
106. Park-Sarge O.K., Mayo K.E. Regulation of the progesterone receptor gene by gonadotropins and cyclic adenosine 3',5'-monophosphate in rat granulosa cells. Endocrinology 1994, 134:709-718.
107. Petz L.N., Ziegler Y.S., Loven M.A., Nardulli A.M. Estrogen receptor alpha and activating protein-1 mediate estrogen responsiveness of the progesterone receptor gene in MCF-7 breast cancer cells. Endocrinology 2002, 143:4583-4591.
108. Petz L.N., Ziegler Y.S., Schultz J.R., Kim H., Kemper J.K., Nardulli A.M. Differential regulation of the human progesterone receptor gene through an estrogen response element half site and Sp1 sites. J. Steroid Biochem. Mol. Biol. 2004, 88:113-122.
109. Petz L.N., Ziegler Y.S., Schultz J.R., Nardulli A.M. Fos and Jun inhibit estrogen-induced transcription of the human progesterone receptor gene through an activator protein-1 site. Mol. Endocrinol. 2004, 18:521-532.
110. Piekarz R.L., Cohen D., Horwitz S.B. Progesterone regulates the murine multidrug resistance mdr1b gene. J. Biol. Chem. 1993, 268:7613-7616.
111. Proietti C.J., Beguelin W., Flaque M.C., Cayrol F., Rivas M.A., Tkach M., Charreau E.H., Schillaci R., Elizalde P.V. Novel role of signal transducer and activator of transcription 3 as a progesterone receptor coactivator in breast cancer. Steroids 2011, 76:381-392.
112. Purmonen S., Manninen T., Pennanen P., Ylikomi T. Progestins regulate genes that can elicit both proliferative and antiproliferative effects in breast cancer cells. Oncol. Rep. 2008, 19:1627-1634.
113. Reichardt H.M., Kaestner K.H., Tuckermann J., Kretz O., Wessely O., Bock R., Gass P., Schmid W., Herrlich P., Angel P., Schutz G. DNA binding of the glucocorticoid receptor is not essential for survival. Cell 1998, 93:531-541.
114. Renkawitz R., Schutz G., von der Ahe D., Beato M. Sequences in the promoter region of the chicken lysozyme gene required for steroid regulation and receptor binding. Cell 1984, 37:503-510.
115. Richer J.K., Lange C.A., Manning N.G., Owen G., Powell R., Horwitz K.B. Convergence of progesterone with growth factor and cytokine signaling in breast cancer. Progesterone receptors regulate signal transducers and activators of transcription expression and activity. J. Biol. Chem. 1998, 273:31317-31326.
116. Richer J.K., Jacobsen B.M., Manning N.G., Abel M.G., Wolf D.M., Horwitz K.B. Differential gene regulation by the two progesterone receptor isoforms in human breast cancer cells. J. Biol. Chem. 2002, 277:5209-5218.
117. Roemer S.C., Donham D.C., Sherman L., Pon V.H., Edwards D.P., Churchill M.E. Structure of the progesterone receptor-deoxyribonucleic acid complex: novel interactions required for binding to half-site response elements. Mol. Endocrinol. 2006, 20:3042-3052.
118. Rudd M.D., Gonzalez-Robayna I., Hernandez-Gonzalez I., Weigel N.L., Bingman W.E., Richards J.S. Constitutively active FOXO1a and a DNA-binding domain mutant exhibit distinct co-regulatory functions to enhance progesterone receptor A activity. J. Mol. Endocrinol. 2007, 38:673-690.
119. Salama S.A., Jamaluddin M., Kumar R., Hassan M.H., Al-Hendy A. Progesterone regulates catechol-O-methyl transferase gene expression in breast cancer cells: distinct effect of progesterone receptor isoforms. J. Steroid Biochem. Mol. Biol. 2007, 107:253-261.
120. Salih S.M., Salama S.A., Jamaluddin M., Fadl A.A., Blok L.J., Burger C.W., Nagamani M., Al-Hendy A. Progesterone-mediated regulation of catechol-O-methyl transferase expression in endometrial cancer cells. Reprod. Sci. 2008, 15:210-220.
121. Santos S.J., Aupperlee M.D., Xie J., Durairaj S., Miksicek R., Conrad S.E., Leipprandt J.R., Tan Y.S., Schwartz R.C., Haslam S.Z. Progesterone receptor A-regulated gene expression in mammary organoid cultures. J. Steroid Biochem. Mol. Biol. 2009, 115:161-172.
122. Sartorius C.A., Groshong S.D., Miller L.A., Powell R.L., Tung L., Takimoto G.S., Horwitz K.B. 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. 1994, 54:3868-3877.
123. Sartorius C.A., Melville M.Y., Hovland A.R., Tung L., Takimoto G.S., Horwitz K.B. A third transactivation function (AF3) of human progesterone receptors located in the unique N-terminal segment of the B-isoform. Mol. Endocrinol. 1994, 8:1347-1360.
124. Savouret J.F., Bailly A., Misrahi M., Rauch C., Redeuilh G., Chauchereau A., Milgrom E. Characterization of the hormone responsive element involved in the regulation of the progesterone receptor gene. EMBO J. 1991, 10:1875-1883.
125. Scheidereit C., Krauter P., von der Ahe D., Janich S., Rabenau O., Cato A.C., Suske G., Westphal H.M., Beato M. Mechanism of gene regulation by steroid hormones. J. Steroid Biochem. 1986, 24:19-24.
126. Schneider W., Ramachandran C., Satyaswaroop P.G., Shyamala G. Murine progesterone receptor exists predominantly as the 83-kD 'A' form. J. Steroid Biochem. Mol. Biol. 1991, 38:285-291.
127. Schule R., Muller M., Kaltschmidt C., Renkawitz R. Many transcription factors interact synergistically with steroid receptors. Science 1988, 242:1418-1420.
128. Schultz J.R., Petz L.N., Nardulli A.M. Estrogen receptor alpha and Sp1 regulate progesterone receptor gene expression. Mol. Cell. Endocrinol. 2003, 201:165-175.
129. Seagroves T.N., Lydon J.P., Hovey R.C., Vonderhaar B.K., Rosen J.M. C/EBPbeta (CCAAT/enhancer binding protein) controls cell fate determination during mammary gland development. Mol. Endocrinol. 2000, 14:359-368.
130. Shen T., Horwitz K.B., Lange C.A. 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. 2001, 21:6122-6131.
131. Slater E.P., Cato A.C., Karin M., Baxter J.D., Beato M. Progesterone induction of metallothionein-IIA gene expression. Mol. Endocrinol. 1988, 2:485-491.
132. So A.Y., Chaivorapol C., Bolton E.C., Li H., Yamamoto K.R. Determinants of cell- and gene-specific transcriptional regulation by the glucocorticoid receptor. PLoS Genet. 2007, 3:e94.
133. Sriraman V., Sharma S.C., Richards J.S. Transactivation of the progesterone receptor gene in granulosa cells: evidence that Sp1/Sp3 binding sites in the proximal promoter play a key role in luteinizing hormone inducibility. Mol. Endocrinol. 2003, 17:436-449.
134. Strahle U., Klock G., Schutz G. A DNA sequence of 15 base pairs is sufficient to mediate both glucocorticoid and progesterone induction of gene expression. Proc. Natl. Acad. Sci. USA 1987, 84:7871-7875.
135. Subtil-Rodriguez A., Millan-Arino L., Quiles I., Ballare C., Beato M., Jordan A. Progesterone induction of the 11beta-hydroxysteroid dehydrogenase type 2 promoter in breast cancer cells involves coordinated recruitment of STAT5A and progesterone receptor to a distal enhancer and polymerase tracking. Mol. Cell. Biol. 2008, 28:3830-3849.
136. Takano M., Lu Z., Goto T., Fusi L., Higham J., Francis J., Withey A., Hardt J., Cloke B., Stavropoulou A.V., Ishihara O., Lam E.W., Unterman T.G., Brosens J.J., Kim J.J. Transcriptional cross talk between the forkhead transcription factor forkhead box O1A and the progesterone receptor coordinates cell cycle regulation and differentiation in human endometrial stromal cells. Mol. Endocrinol. 2007, 21:2334-2349.
137. Takimoto G.S., Tung L., Abdel-Hafiz H., Abel M.G., Sartorius C.A., Richer J.K., Jacobsen B.M., Bain D.L., Horwitz K.B. Functional properties of the N-terminal region of progesterone receptors and their mechanistic relationship to structure. J. Steroid Biochem. Mol. Biol. 2003, 85:209-219.
138. Tetel M.J., Jung S., Carbajo P., Ladtkow T., Skafar D.F., Edwards D.P. Hinge and amino-terminal sequences contribute to solution dimerization of human progesterone receptor. Mol. Endocrinol. 1997, 11:1114-1128.
139. Tora L., Gronemeyer H., Turcotte B., Gaub M.P., Chambon P. The N-terminal region of the chicken progesterone receptor specifies target gene activation. Nature 1988, 333:185-188.
140. Tseng L., Zhu H.H. Progestin, estrogen, and insulin-like growth factor-I stimulate the prolactin receptor mRNA in human endometrial stromal cells. J. Soc. Gynecol. Invest. 1998, 5:149-155.
141. Tseng L., Tang M., Wang Z., Mazella J. Progesterone receptor (hPR) upregulates the fibronectin promoter activity in human decidual fibroblasts. DNA Cell Biol. 2003, 22:633-640.
142. Tsuchiya S., Tanaka S., Sugimoto Y., Katsuyama M., Ikegami R., Ichikawa A. Identification and characterization of a novel progesterone receptor-binding element in the mouse prostaglandin E receptor subtype EP2 gene. Genes Cells 2003, 8:747-758.
143. Tung L., Abdel-Hafiz H., Shen T., Harvell D.M., Nitao L.K., Richer J.K., Sartorius C.A., Takimoto G.S., Horwitz K.B. Progesterone receptors (PR)-B and -A regulate transcription by different mechanisms: AF-3 exerts regulatory control over coactivator binding to PR-B. Mol. Endocrinol. 2006, 20:2656-2670.
144. Vegeto E., Shahbaz M.M., Wen D.X., Goldman M.E., O'Malley B.W., McDonnell D.P. Human progesterone receptor A form is a cell- and promoter-specific repressor of human progesterone receptor B function. Mol. Endocrinol. 1993, 7:1244-1255.
145. Viegas L.R., Vicent G.P., Baranao J.L., Beato M., Pecci A. Steroid hormones induce bcl-X gene expression through direct activation of distal promoter P4. J. Biol. Chem. 2004, 279:9831-9839.
146. Vienonen A., Syvala H., Miettinen S., Tuohimaa P., Ylikomi T. Expression of progesterone receptor isoforms A and B is differentially regulated by estrogen in different breast cancer cell lines. J. Steroid Biochem. Mol. Biol. 2002, 80:307-313.
147. von der Ahe D., Janich S., Scheidereit C., Renkawitz R., Schutz G., Beato M. Glucocorticoid and progesterone receptors bind to the same sites in two hormonally regulated promoters. Nature 1985, 313:706-709.
148. Wan Y., Nordeen S.K. Overlapping but distinct gene regulation profiles by glucocorticoids and progestins in human breast cancer cells. Mol. Endocrinol. 2002, 16:1204-1214.
149. Wang H., Lee E.W., Zhou L., Leung P.C., Ross D.D., Unadkat J.D., Mao Q. Progesterone receptor (PR) isoforms PRA and PRB differentially regulate expression of the breast cancer resistance protein in human placental choriocarcinoma BeWo cells. Mol. Pharmacol. 2008, 73:845-854.
150. Wei L.L., Krett N.L., Francis M.D., Gordon D.F., Wood W.M., O'Malley B.W., Horwitz K.B. Multiple human progesterone receptor messenger ribonucleic acids and their autoregulation by progestin agonists and antagonists in breast cancer cells. Mol. Endocrinol. 1988, 2:62-72.
151. Wei L.L., Gonzalez-Aller C., Wood W.M., Miller L.A., Horwitz K.B. 5'-Heterogeneity in human progesterone receptor transcripts predicts a new amino-terminal truncated " C" -receptor and unique A-receptor messages. Mol. Endocrinol. 1990, 4:1833-1840.
152. Xie Y., Wang Y.L., Yu L., Hu Q., Ji L., Zhang Y., Liao Q.P. Metformin promotes progesterone receptor expression via inhibition of mammalian target of rapamycin (mTOR) in endometrial cancer cells. J. Steroid Biochem. Mol. Biol. 2010.
153. Xu X., Murdoch F.E., Curran E.M., Welshons W.V., Fritsch M.K. Transcription factor accessibility and histone acetylation of the progesterone receptor gene differs between parental MCF-7 cells and a subline that has lost progesterone receptor expression. Gene 2004, 328:143-151.
154. Yang C., Chen L., Li C., Lynch M.C., Brisken C., Schmidt E.V. Cyclin D1 enhances the response to estrogen and progesterone by regulating progesterone receptor expression. Mol. Cell. Biol. 2010, 30:3111-3125.
155. Yie S.M., Xiao R., Librach C.L. Progesterone regulates HLA-G gene expression through a novel progesterone response element. Hum. Reprod. 2006, 21:2538-2544.
156. Zhang X.L., Zhang D., Michel F.J., Blum J.L., Simmen F.A., Simmen R.C. Selective interactions of Kruppel-like factor 9/basic transcription element-binding protein with progesterone receptor isoforms A and B determine transcriptional activity of progesterone-responsive genes in endometrial epithelial cells. J. Biol. Chem. 2003, 278:21474-21482.