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Estradiol differentially induces progesterone receptor isoforms expression through alternative promoter regulation in a mouse embryonic hypothalamic cell line

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Abstract

Progesterone receptor (PR) presents two main isoforms (PR-A and PR-B) that are regulated by two specific promoters and transcribed from alternative transcriptional start sites. The molecular regulation of PR isoforms expression in embryonic hypothalamus is poorly understood. The aim of the present study was to assess estradiol regulation of PR isoforms in a mouse embryonic hypothalamic cell line (mHypoE-N42), as well as the transcriptional status of their promoters. MHypoE-N42 cells were treated with estradiol for 6 and 12 h. Then, Western blot, real-time quantitative reverse transcription polymerase chain reaction, and chromatin and DNA immunoprecipitation experiments were performed. PR-B expression was transiently induced by estradiol after 6 h of treatment in an estrogen receptor alpha (ERα)-dependent manner. This induction was associated with an increase in ERα phosphorylation (serine 118) and its recruitment to PR-B promoter. After 12 h of estradiol exposure, a downregulation of this PR isoform was associated with a decrease of specific protein 1, histone 3 lysine 4 trimethylation, and RNA polymerase II occupancy on PR-B promoter, without changes in DNA methylation and hydroxymethylation. In contrast, there were no estradiol-dependent changes in PR-A expression that could be related with the epigenetic marks or the transcription factors evaluated. We demonstrate that PR isoforms are differentially regulated by estradiol and that the induction of PR-B expression is associated to specific transcription factors interactions and epigenetic changes in its promoter in embryonic hypothalamic cells.

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References

  1. B.W. O’Malley, M.R. Sherman, D.O. Toft, Progesterone “receptors” in the cytoplasm and nucleus of chick oviduct target tissue. Proc. Natl. Acad. Sci. U.S.A. 67, 501–508 (1970)

    Article  PubMed  PubMed Central  Google Scholar 

  2. W.L. Kraus, M.M. Montano, B.S. Katzenellenbogen, Cloning of the rat progesterone receptor gene 5′-region and identification of two functionally distinct promoters. Mol. Endocrinol. 7, 1603–1616 (1993)

    CAS  PubMed  Google Scholar 

  3. E. Vegeto, M.M. Shahbaz, D.X. Wen, M.E. Goldman, B.W. O’Malley, D.P. McDonnell, Human progesterone receptor A form is a cell- and promoter-specific repressor of human progesterone receptor B function. Mol. Endocrinol. 7, 1244–1255 (1993)

    CAS  PubMed  Google Scholar 

  4. J.K. Richer, B.M. Jacobsen, N.G. Manning, M.G. Abel, D.M. Wolf, K.B. Horwitz, Differential gene regulation by the two progesterone receptor isoforms in human breast cancer cells. J. Biol. Chem. 277, 5209–5218 (2002)

    Article  CAS  PubMed  Google Scholar 

  5. I. Camacho-Arroyo, A. González-Arenas, G. González-Morán, Ontogenic variations in the content and distribution of progesterone receptor isoforms in the reproductive tract and brain of chicks. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 146, 644–652 (2007)

    Article  Google Scholar 

  6. C. Guerra-Araiza, M.A. Cerbón, S. Morimoto, I. Camacho-Arroyo, Progesterone receptor isoforms expression pattern in the rat brain during the estrous cycle. Life Science 66, 1743–1752 (2000)

    Article  CAS  Google Scholar 

  7. I. Camacho-Arroyo, C. Guerra-Araiza, M.A. Cerbón, Progesterone receptor isoforms are differentially regulated by sex steroids in the rat forebrain. NeuroReport 9, 3993–3996 (1998)

    Article  CAS  PubMed  Google Scholar 

  8. I. Camacho-Arroyo, A. González-Arenas, G. González-Agüero, C. Guerra-Araiza, G. González-Morán, Changes in the content of progesterone receptor isoforms and estrogen receptor alpha in the chick brain during embryonic development. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 136, 447–452 (2003)

    Article  Google Scholar 

  9. M.M. White, I. Sheffer, J. Teeter, E.M. Apostolakis, Hypothalamic progesterone receptor-A mediates gonadotropin surges, self priming and receptivity in estrogen-primed female mice. J. Mol. Endocrinol. 38, 35–50 (2007)

    Article  CAS  PubMed  Google Scholar 

  10. L. Mendoza-Garcés, M. Rodríguez-Dorantes, C. Álvarez-Delgado, E.R. Vázquez-Martínez, P. Garcia-Tobilla, M.A. Cerbón, Differential DNA methylation pattern in the A and B promoters of the progesterone receptor is associated with differential mRNA expression in the female rat hypothalamus during proestrus. Brain Res. 1535, 71–77 (2013)

    Article  PubMed  Google Scholar 

  11. L. Mendoza-Garcés, I. Camacho-Arroyo, M.A. Cerbón, Effects of mating on progesterone receptor isoforms in rat hypothalamus. NeuroReport 21, 513–516 (2010)

    Article  PubMed  Google Scholar 

  12. C. Guerra-Araiza, A. Coyoy-Salgado, I. Camacho-Arroyo, Sex differences in the regulation of progesterone receptor isoforms expression in the rat brain. Brain Res. Bull. 59, 105–109 (2002)

    Article  CAS  PubMed  Google Scholar 

  13. S.L. Fitzpatrick, T.J. Berrodin, S.F. Jenkins, D.M. Sindoni, D.C. Deecher, D.E. Frail, Effect of estrogen agonists and antagonists on induction of progesterone receptor in a rat hypothalamic cell line. Endocrinology 140, 3928–3937 (1999)

    Article  CAS  PubMed  Google Scholar 

  14. K.L. Gonzales, P. Quadros-Mennella, M.J. Tetel, C.K. Wagner, Anatomically-specific actions of oestrogen receptor in the developing female rat brain: effects of oestradiol and selective oestrogen receptor modulators on progestin receptor expression. J. Neuroendocrinol. 24, 285–291 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. C.K. Wagner, A.Y. Nakayama, G.J. De Vries, Potential role of maternal progesterone in the sexual differentiation of the brain. Endocrinology 139, 3658–3661 (1998)

    Article  CAS  PubMed  Google Scholar 

  16. P.S. Quadros, C.K. Wagner, Regulation of progesterone receptor expression by estradiol is dependent on age, sex and region in the rat brain. Endocrinology 149, 3054–3061 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. P. Kastner, A. Krust, B. Turcotte, U. Stropp, L. Tora, H. Gronemeyer, P. Chambon, Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO J. 9, 1603–1614 (1990)

    CAS  PubMed  PubMed Central  Google Scholar 

  18. L.N. Petz, Y.S. Ziegler, M.A. Loven, A.M. Nardulli, Estrogen receptor alpha and activating protein-1 mediate estrogen responsiveness of the progesterone receptor gene in MCF-7 breast cancer cells. Endocrinology 143, 4583–4591 (2002)

    Article  CAS  PubMed  Google Scholar 

  19. L.N. Petz, Y.S. Ziegler, J.R. Schultz, H. Kim, J.K. Kemper, A.M. Nardulli, Differential regulation of the human progesterone receptor gene through an estrogen response element half site and Sp1 sites. J. Steroid Biochem. Mol. Biol. 88, 113–122 (2004)

    Article  CAS  PubMed  Google Scholar 

  20. J.K. Won, R. Chodankar, D.J. Purcell, D. Bittencourt, M.R. Stallcup, Gene-specific patterns of coregulator requirements by estrogen receptor-α in breast cancer cells. Mol. Endocrinol. 26, 955–966 (2012)

    Article  Google Scholar 

  21. E.R. Vázquez-Martínez, L. Mendoza-Garcés, E. Vergara-Castañeda, M. Cerbón, Epigenetic regulation of Progesterone Receptor isoforms: from classical models to the sexual brain. Mol. Cell. Endocrinol. 392, 115–124 (2014)

    Article  PubMed  Google Scholar 

  22. L. Fleury, M. Gerus, A.C. Lavigne, H. Richard-Foy, K. Bystricky, Eliminating epigenetic barriers induces transient hormone-regulated gene expression in estrogen receptor negative breast cancer cells. Oncogene 27, 4075–4085 (2008)

    Article  CAS  PubMed  Google Scholar 

  23. J.M. Schwarz, B.M. Nugent, M.M. McCarthy, Developmental and hormone-induced epigenetic changes to estrogen and progesterone receptor genes in brain are dynamic across the life span. Endocrinology 151, 4871–4881 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. K. Gagnidze, Z.M. Weil, L.C. Faustino, S.M. Schaafsma, D.W. Pfaff, Early histone modifications in the ventromedial hypothalamus and preoptic area following oestradiol administration. J. Neuroendocrinol. 25, 939–955 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. P.S. Dalvi, A. Nazarians-Armavil, S. Tung, D.D. Belsham, Immortalized neurons for the study of hypothalamic function. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R1030–R1052 (2011)

    Article  CAS  PubMed  Google Scholar 

  26. M.B. Yilmaz, A. Wolfe, H. Zhao, D.C. Brooks, S.E. Bulun, Aromatase promoter I.f is regulated by progesterone receptor in mouse hypothalamic neuronal cell lines. J. Mol. Endocrinol. 47, 69–80 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. K. Hagihara, X.S. Wu-Peng, T. Funabashi, J. Kato, D.W. Pfaff, Nucleic acid sequence and DNase hypersensitive sites of the 5′ region of the mouse progesterone receptor gene. Biochem. Biophys. Res. Commun. 205, 1093–1101 (1994)

    Article  CAS  PubMed  Google Scholar 

  28. W.J. Kent, C.W. Sugnet, T.S. Furey, K.M. Roskin, T.H. Pringle, A.M. Zahler, D. Haussler, The human genome browser at UCSC. Genome Res. 12, 996–1006 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. B. Lee, A. Morano, A. Porcellini, M.T. Muller, GADD45α inhibition of DNMT1 dependent DNA methylation during homology directed DNA repair. Nucleic Acids Res. 40, 2481–2493 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. C.E. Nestor, R.R. Meehan, Hydroxymethylated DNA immunoprecipitation (hmeDIP). Methods Mol. Biol. 1094, 259–267 (2014)

    Article  CAS  PubMed  Google Scholar 

  31. A. González-Arenas, V. Hansberg-Pastor, O.T. Hernández-Hernández, T.K. González-García, J. Henderson-Villalpando, D. Lemus-Hernández, A. Cruz-Barrios, M. Rivas-Suárez, I. Camacho-Arroyo, Estradiol increases cell growth in human astrocytoma cell lines through ERα activation and its interaction with SRC-1 and SRC-3 coactivators. Biochim. Biophys. Acta 1823, 379–386 (2012)

    Article  PubMed  Google Scholar 

  32. D.P. Gavin, K.A. Chase, R.P. Sharma, Active DNA demethylation in post-mitotic neurons: a reason for optimism. Neuropharmacology 75, 233–245 (2013)

    Article  CAS  PubMed  Google Scholar 

  33. J. Kuo, N. Hamid, G. Bondar, P. Dewing, J. Clarkson, P. Micevych, Sex differences in hypothalamic astrocyte response to estradiol stimulation. Biol. Sex Differ. 1, 7 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. K.L. Gonzales, M.J. Tetel, C.K. Wagner, Estrogen receptor (ER) β modulates ERα responses to estrogens in the developing rat ventromedial nucleus of the hypothalamus. Endocrinology 149, 4615–4621 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. P.S. Quadros, J.L. Pfau, C.K. Wagner, Distribution of progesterone receptor immunoreactivity in the fetal and neonatal rat forebrain. J. Comp. Neurol. 504, 42–56 (2007)

    Article  CAS  PubMed  Google Scholar 

  36. L.N. Petz, A.M. Nardulli, Sp1 binding sites and an estrogen response element half-site are involved in regulation of the human progesterone receptor A promoter. Mol. Endocrinol. 14, 972–985 (2000)

    Article  CAS  PubMed  Google Scholar 

  37. D. Chen, T. Riedl, E. Washbrook, P.E. Pace, R.C. Coombes, J.M. Egly, S. Ali, Activation of estrogen receptor alpha by S118 phosphorylation involves a ligand-dependent interaction with TFIIH and participation of CDK7. Mol. Cell 6, 127–137 (2000)

    Article  CAS  PubMed  Google Scholar 

  38. T.T. Duplessis, C.C. Williams, S.M. Hill, B.G. Rowan, Phosphorylation of estrogen receptor α at serine 118 directs recruitment of promoter complexes and gene-specific transcription. Endocrinology 152, 2517–2526 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. A. Stratmann, B. Haendler, The histone demethylase JARID1A regulates progesterone receptor expression. FEBS J. 278, 1458–1469 (2011)

    Article  CAS  PubMed  Google Scholar 

  40. J.R. Schultz, L.N. Petz, A.M. Nardulli, Estrogen receptor α and Sp1 regulate progesterone receptor gene expression. Mol. Cell. Endocrinol. 201, 165–175 (2003)

    Article  CAS  PubMed  Google Scholar 

  41. X. Xu, F.E. Murdoch, E.M. Curran, W.V. Welshons, M.K. Fritsch, 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 328, 143–151 (2004)

    Article  CAS  PubMed  Google Scholar 

  42. M. Tang, J. Mazella, J. Gao, L. Tseng, Progesterone receptor activates its promoter activity in human endometrial stromal cells. Mol. Cell. Endocrinol. 192, 45–53 (2002)

    Article  CAS  PubMed  Google Scholar 

  43. H.-C. Yang, J.-Y. Chuang, W.-Y. Jeng, C.-I. Liu, A.H.J. Wang, P.-J. Lu, W.-C. Chang, J.-J. Hung, Pin1-mediated Sp1 phosphorylation by CDK1 increases Sp1 stability and decreases its DNA-binding activity during mitosis. Nucleic Acids Res. 42, 13573–13587 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. S. Khan, F. Wu, S. Liu, Q. Wu, S. Safe, Role of specificity protein transcription factors in estrogen-induced gene expression in MCF-7 breast cancer cells. J. Mol. Endocrinol. 39, 289–304 (2007)

    Article  CAS  PubMed  Google Scholar 

  45. S. Kangaspeska, B. Stride, R. Métivier, M. Polycarpou-Schwarz, D. Ibberson, R.P. Carmouche, V. Benes, F. Gannon, G. Reid, Transient cyclical methylation of promoter DNA. Nature 452, 112–115 (2008)

    Article  CAS  PubMed  Google Scholar 

  46. E.S. Lander, L.M. Linton, B. Birren, C. Nusbaum, M.C. Zody, J. Baldwin, K. Devon, K. Dewar, M. Doyle, W. FitzHugh, R. Funke, D. Gage, K. Harris, A. Heaford, J. Howland, L. Kann, J. Lehoczky, R. LeVine, P. McEwan, K. McKernan, J. Meldrim, J.P. Mesirov, C. Miranda, W. Morris, J. Naylor, C. Raymond, M. Rosetti, R. Santos, A. Sheridan, C. Sougnez, N. Stange-Thomann, N. Stojanovic, A. Subramanian, D. Wyman, J. Rogers, J. Sulston, R. Ainscough, S. Beck, D. Bentley, J. Burton, C. Clee, N. Carter, A. Coulson, R. Deadman, P. Deloukas, A. Dunham, I. Dunham, R. Durbin, L. French, D. Grafham, S. Gregory, T. Hubbard, S. Humphray, A. Hunt, M. Jones, C. Lloyd, A. McMurray, L. Matthews, S. Mercer, S. Milne, J.C. Mullikin, A. Mungall, R. Plumb, M. Ross, R. Shownkeen, S. Sims, R.H. Waterston, R.K. Wilson, L.W. Hillier, J.D. McPherson, M.A. Marra, E.R. Mardis, L.A. Fulton, A.T. Chinwalla, K.H. Pepin, W.R. Gish, S.L. Chissoe, M.C. Wendl, K.D. Delehaunty, T.L. Miner, A. Delehaunty, J.B. Kramer, L.L. Cook, R.S. Fulton, D.L. Johnson, P.J. Minx, S.W. Clifton, T. Hawkins, E. Branscomb, P. Predki, P. Richardson, S. Wenning, T. Slezak, N. Doggett, J.F. Cheng, A. Olsen, S. Lucas, C. Elkin, E. Uberbacher, M. Frazier, R.A. Gibbs, D.M. Muzny, S.E. Scherer, J.B. Bouck, E.J. Sodergren, K.C. Worley, C.M. Rives, J.H. Gorrell, M.L. Metzker, S.L. Naylor, R.S. Kucherlapati, D.L. Nelson, G.M. Weinstock, Y. Sakaki, A. Fujiyama, M. Hattori, T. Yada, A. Toyoda, T. Itoh, C. Kawagoe, H. Watanabe, Y. Totoki, T. Taylor, J. Weissenbach, R. Heilig, W. Saurin, F. Artiguenave, P. Brottier, T. Bruls, E. Pelletier, C. Robert, P. Wincker, D.R. Smith, L. Doucette-Stamm, M. Rubenfield, K. Weinstock, H.M. Lee, J. Dubois, A. Rosenthal, M. Platzer, G. Nyakatura, S. Taudien, A. Rump, H. Yang, J. Yu, J. Wang, G. Huang, J. Gu, L. Hood, L. Rowen, A. Madan, S. Qin, R.W. Davis, N.A. Federspiel, A.P. Abola, M.J. Proctor, R.M. Myers, J. Schmutz, M. Dickson, J. Grimwood, D.R. Cox, M.V. Olson, R. Kaul, N. Shimizu, K. Kawasaki, S. Minoshima, G.A. Evans, M. Athanasiou, R. Schultz, B.A. Roe, F. Chen, H. Pan, J. Ramser, H. Lehrach, R. Reinhardt, W.R. McCombie, M. de la Bastide, N. Dedhia, H. Blöcker, K. Hornischer, G. Nordsiek, R. Agarwala, L. Aravind, J.A. Bailey, A. Bateman, S. Batzoglou, E. Birney, P. Bork, D.G. Brown, C.B. Burge, L. Cerutti, H.C. Chen, D. Church, M. Clamp, R.R. Copley, T. Doerks, S.R. Eddy, E.E. Eichler, T.S. Furey, J. Galagan, J.G. Gilbert, C. Harmon, Y. Hayashizaki, D. Haussler, H. Hermjakob, K. Hokamp, W. Jang, L.S. Johnson, T.A. Jones, S. Kasif, A. Kaspryzk, S. Kennedy, W.J. Kent, P. Kitts, E.V. Koonin, I. Korf, D. Kulp, D. Lancet, T.M. Lowe, A. McLysaght, T. Mikkelsen, J.V. Moran, N. Mulder, V.J. Pollara, C.P. Ponting, G. Schuler, J. Schultz, G. Slater, A.F. Smit, E. Stupka, J. Szustakowski, D. Thierry-Mieg, J. Thierry-Mieg, L. Wagner, J. Wallis, R. Wheeler, A. Williams, Y.I. Wolf, K.H. Wolfe, S.P. Yang, R.F. Yeh, F. Collins, M.S. Guyer, J. Peterson, A. Felsenfeld, K.A. Wetterstrand, A. Patrinos, M.J. Morgan, P. de Jong, J.J. Catanese, K. Osoegawa, H. Shizuya, S. Choi, Y.J. Chen, J. Szustakowki, Initial sequencing and analysis of the human genome. Nature 409, 860–921 (2001)

    Article  CAS  PubMed  Google Scholar 

  47. S.Y. Chai, R. Smith, T. Zakar, C. Mitchell, G. Madsen, Term myometrium is characterized by increased activating epigenetic modifications at the progesterone receptor-A promoter. Mol. Hum. Reprod. 18, 401–409 (2012)

    Article  CAS  PubMed  Google Scholar 

  48. A. Barski, S. Cuddapah, K. Cui, T.-Y. Roh, D.E. Schones, Z. Wang, G. Wei, I. Chepelev, K. Zhao, High-resolution profiling of histone methylation in the human genome. Cell 129, 823–837 (2007)

    Article  CAS  PubMed  Google Scholar 

  49. I. Garcia-Bassets, Y.S. Kwon, F. Telese, G.G. Prefontaine, K.R. Hutt, C.S. Cheng, B.G. Ju, K.A. Ohgi, J. Wang, L. Escoubet-Lozach, D.W. Rose, C.K. Glass, X.D. Fu, M.G. Rosenfeld, Histone methylation-dependent mechanisms impose ligand dependency for gene activation by nuclear receptors. Cell 128, 505–518 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. M.M. Gaudet, M. Campan, J.D. Figueroa, X.R. Yang, J. Lissowska, B. Peplonska, L.A. Brinton, D.L. Rimm, P.W. Laird, M. Garcia-Closas, M.E. Sherman, DNA hypermethylation of ESR1 and PGR in breast cancer: pathologic and epidemiologic associations. Cancer Epidemiol. Biomarkers Prev. 18, 3036–3043 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. V. Hansberg-Pastor, A. González-Arenas, M.A. Peña-Ortiz, E. García-Gómez, M. Rodríguez-Dorantes, I. Camacho-Arroyo, The role of DNA methylation and histone acetylation in the regulation of progesterone receptor isoforms expression in human astrocytoma cell lines. Steroids 78, 500–507 (2013)

    Article  CAS  PubMed  Google Scholar 

  52. X. Li, C. Chen, H. Luo, J.C. van Velkinburgh, B. Ni, Q. Chang, Decreased DNA methylations at the progesterone receptor promoter a induce functional progesterone withdrawal in human parturition. Reprod. Sci. 21, 898–905 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. J.L. Meyer, D. Zimbardi, S. Podgaec, R.L. Amorim, M.S. Abrão, C.A. Rainho, DNA methylation patterns of steroid receptor genes ESR1, ESR2 and PGR in deep endometriosis compromising the rectum. Int. J. Mol. Med. 33, 897–904 (2014)

    CAS  PubMed  Google Scholar 

  54. T.N. Pathiraja, P.B. Shetty, J. Jelinek, R. He, R. Hartmaier, A.L. Margossian, S.G. Hilsenbeck, J.P.J. Issa, S. Oesterreich, Progesterone receptor isoform-specific promoter methylation: association of PRA promoter methylation with worse outcome in breast cancer patients. Clin. Cancer Res. 17, 4177–4186 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Y.W. Leu, P.S. Yan, M. Fan, V.X. Jin, J.C. Liu, E.M. Curran, W.V. Welshons, S.H. Wei, R.V. Davuluri, C. Plass, K.P. Nephew, T.H.M. Huang, Loss of estrogen receptor signaling triggers epigenetic silencing of downstream targets in breast cancer. Cancer Res. 64, 8184–8192 (2004)

    Article  CAS  PubMed  Google Scholar 

  56. P.S. Quadros, J.L. Pfau, A.Y.N. Goldstein, G.J. De Vries, C.K. Wagner, Sex differences in progesterone receptor expression: a potential mechanism for estradiol-mediated sexual differentiation. Endocrinology 143, 3727–3739 (2002)

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We acknowledge the technical support of Lucía Flores Peredo (Departamento de Bioquímica, Facultad de Medicina, Universidad Nacional Autónoma de México, Mexico) regarding ChIP technique and Patricia Mendoza-Lorenzo (División Académica de Ciencias Básicas, Unidad Chontalpa, Universidad Juárez Autónoma de Tabasco, Mexico) for her assistance in real-time PCR experiments. This work was supported by the Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT) No. IN210412 and IA202814, and Programa de Apoyo a la Investigación para Estudiantes de Posgrado (PAIP) No. 5000-9108 and 5000-9141, from the Universidad Nacional Autónoma de México (UNAM, México). E.R.V-M. is recipient of a Ph.D. scholarship from CONACYT (CVU 288806).

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Authors and Affiliations

  1. Unidad de Investigación en Reproducción Humana, Instituto Nacional de Perinatología-Facultad de Química, Universidad Nacional Autónoma de México (UNAM), Ciudad Universitaria, Av. Universidad 3000, Coyoacán, 04510, Mexico, DF, Mexico

    Edgar Ricardo Vázquez-Martínez, Ignacio Camacho-Arroyo & Marco Cerbón

  2. Departamento de Bioquímica, Facultad de Medicina, UNAM, Mexico, Mexico

    Angel Zarain-Herzberg

  3. Instituto Nacional de Salud Pública, SSA, Cuernavaca, Mexico

    María Carmen Rodríguez

  4. Instituto Nacional de Geriatría, SSA, Cuernavaca, DF, Mexico

    Luciano Mendoza-Garcés

  5. Departamento de Medicina Genómica y Toxicología Ambiental, Instituto de Investigaciones Biomédicas, UNAM, Mexico, Mexico

    Patricia Ostrosky-Wegman

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  1. Edgar Ricardo Vázquez-Martínez
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Vázquez-Martínez, E.R., Camacho-Arroyo, I., Zarain-Herzberg, A. et al. Estradiol differentially induces progesterone receptor isoforms expression through alternative promoter regulation in a mouse embryonic hypothalamic cell line. Endocrine 52, 618–631 (2016). https://doi.org/10.1007/s12020-015-0825-1

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