Effect of cyclic amp and estrogen/progesterone on the transcription of dna methyltransferases during the decidualization of human endometrial stromal cells

Molecular Human Reproduction

Volumn 19, Issue 5, 2013, Pages 302-312

  Logan, Philip C ^a   Ponnampalam, Anna P ^a   Steiner, Michael ^a   Mitchell, Murray D ^a,b,c  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Cyclic AMP; Decidualization; DNA methylation; DNA methyltransferases; Steroid hormone receptors

Indexed keywords

ANDROGEN RECEPTOR; BUCLADESINE; CYCLIC AMP; DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; MEDROXYPROGESTERONE ACETATE; MESSENGER RNA; PROGESTERONE; PROGESTERONE RECEPTOR B;

ARTICLE; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; DECIDUALIZATION; DNA METHYLATION; DOWN REGULATION; ENZYME REGULATION; FEMALE; HORMONAL REGULATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; STROMA CELL;

BUCLADESINE; CELL LINE; DECIDUA; DNA; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 1; MEDROXYPROGESTERONE ACETATE; RECEPTORS, ANDROGEN; RECEPTORS, PROGESTERONE; SIGNAL TRANSDUCTION; STROMAL CELLS; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84877000359     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gas062     Document Type: Article

References (74)

1. Aghajanova L, Horcajadas JA, Weeks JL, Esteban FJ, Nezhat CN, Conti M, Giudice LC. The protein kinase A pathway-regulated transcriptome of endometrial stromal fibroblasts reveals compromised differentiation and persistent proliferative potential in endometriosis. Endocrinology 2010;151:1341-1355.
2. Aghajanova L, Tatsumi K, Horcajadas JA, Zamah AM, Esteban FJ, Herndon CN, Conti M, Giudice LC. Unique transcriptome, pathways, and networks in the human endometrial fibroblast response to progesterone in endometriosis. Biol Reprod 2011;84:801-815.
3. Al-Salihi M, Yu M, Burnett DM, Alexander A, Samlowski WE, Fitzpatrick FA. The depletion of DNA methyltransferase-1 and the epigenetic effects of 5-aza-2′-deoxycytidine (decitabine) are differentially regulated by cell cycle progression. Epigenetics 2011; 6:1021-1028.
4. Asvold BO, Eskild A, Jenum PA, Vatten LJ. Maternal concentrations of insulin-like growth factor I and insulin-like growth factor binding protein 1 during pregnancy and birth weight of offspring. Am J Epidemiol 2011;174:129-135.
5. Bergh PA, Navot D. The impact of embryonic development and endometrial maturity on the timing of implantation. Fertil Steril 1992; 58:537-542.
6. Brosens JJ, Hayashi N, White JO. Progesterone receptor regulates decidual prolactin expression in differentiating human endometrial stromal cells. Endocrinology 1999;140:4809-4820.
7. Chen Z-X, Mann JR, Hsieh C-L, Riggs AD, Chédin F. Physical and functional interactions between the human DNMT3L protein and members of the de novo methyltransferase family. J Cell Biochem 2005;95:902-917.
8. Cho JH, Yoon MS, Koo JB, Kim YS, Lee KS, Lee JH, Han JS. The progesterone receptor as a transcription factor regulates phospholipase D1 expression through independent activation of protein kinase A and Ras during 8-Br-cAMP-induced decidualization in human endometrial stromal cells. Biochem J 2011;436:181-191.
9. Cloke B, Huhtinen K, Fusi L, Kajihara T, Yliheikkila M, Ho K-K, Teklenburg G, Lavery S, Jones MC, Trew G et al. The androgen and progesterone receptors regulate distinct gene networks and cellular functions in decidualizing endometrium. Endocrinology 2008; 149:4462-4474.
10. Cloke B, Shah K, Kaneda H, Lavery S, Trew G, Fusi L, Higham J, Dina RE, Ghaem-Maghami S, Ellis P et al. The poly(C)-binding protein-1 regulates expression of the androgen receptor. Endocrinology 2010; 151:3954-3964.
11. Cunha-Filho JSL, Gross JL, Lemos NA, Brandelli A, Castillos M, Passos EP. Hyperprolactinemia and luteal insufficiency in infertile patients with mild and minimal endometriosis. Horm Metab Res 2001;33:216-220.
12. de Ziegler D, Fanchin R, de Moustier B, Bulletti C. The hormonal control of endometrial receptivity: estrogen (E2) and progesterone. J Reprod Immunol 1998;39:149-166.
13. Gao J, Tseng L. Progesterone receptor (PR) inhibits expression of insulin-like growth factor-binding protein-1 (IGFBP-1) in human endometrial cell line HEC-1B: characterization of the inhibitory effect of PR on the distal promoter region of the IGFBP-1 gene. Mol Endocrinol 1997;11:973-979.
14. 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.
15. Garcia E, Bouchard P, De Brux J, Berdah J, Frydman R, Schaison G, Milgrom E, Perrot-Applanat M. Use of immunocytochemistry of progesterone and estrogen receptors for endometrial dating. J Clin Endocrinol Metab 1988;67:80-87.
16. Gellersen B, Brosens J. Cyclic AMP and progesterone receptor cross-talk in human endometrium: a decidualizing affair. J Endocrinol 2003; 178:357-372.
17. Ghoshal K, Datta J, Majumder S, Bai S, Kutay H, Motiwala T, Jacob ST. 5-Aza-deoxycytidine induces selective degradation of DNA methyltransferase 1 by a proteasomal pathway that requires the box KEN, bromo-adjacent homology domain, and nuclear localization signal. Mol Cell Biol 2005;25:4727-4741.
18. Giudice LC, Mark SP, Irwin JC. Paracrine actions of insulin-like growth factors and IGF binding protein-1 in non-pregnant human endometrium and at the decidual-trophoblast interface. J Reprod Immunol 1998;39:133-148.
19. Godbole G, Modi D. Regulation of decidualization, interleukin-11 and interleukin-15 by homeobox A 10 in endometrial stromal cells. J Reprod Immunol 2010;85:130-139.
20. Grimaldi G, Christian M, Steel JH, Henriet P, Poutanen M, Brosens JJ. Down-regulation of the histone methyltransferase EZH2 contributes to the epigenetic programming of decidualizing human endometrial stromal cells. Mol Endocrinol 2011;25:1892-1903.
21. Grimaldi G, Christian M, Quenby S, Brosens JJ. Expression of epigenetic effectors in decidualizing human endometrial stromal cells. Mol Hum Reprod 2012;18:451-458.
22. Guo S. The endometrial epigenome and its response to steroid hormones. Mol Cell Endocrinol 2011;358:185-196.
23. Houserman VL, Todd H, Hertelendy F. Progesterone treatment in vitro enhances prostaglandin E and forskolin-promoted cyclic AMP production in human endometrial stromal cells. J Reprod Fertil 1989; 85:195-202.
24. Hsieh C-L. In vivo activity of murine de novo methyltransferases, Dnmt3a and Dnmt3b. Mol Cell Biol 1999;19:8211-8218.
25. De Caceres II, Dulaimi E, Hoffman AM, Al-Saleem T, Uzzo RG, Cairns P. Identification of novel target genes by an epigenetic reactivation screen of renal cancer. Cancer Res 2006;66:5021-5028.
26. Irwin JC, Giudice LC. Insulin-like growth factor binding protein-1 binds to placental cytotrophoblast alpha5beta1 integrin and inhibits cytotrophoblast invasion into decidualized endometrial stromal cultures. Growth Horm IGF Res 1998;8:21-31.
27. Juttermann R, Li E, Jaenisch R. Toxicity of 5-aza-2′-deoxycytidine to mammalian cells is mediated primarily by covalent trapping of DNA methyltransferase rather than DNA demethylation. Proc Natl Acad Sci USA 1994;91:11797-11801.
28. Kasahara K, Takakura K, Takebayashi K, Kimura F, Nakanishi K, Noda Y. The role of human chorionic gonadotropin on decidualization of endometrial stromal cells in vitro. J Clin Endocrinol Metab 2001; 86:1281-1286.
29. Kessler CA, Moghadam KK, Schroeder JK, Buckley AR, Brar AK, Handwerger S. Cannabinoid receptor I activation markedly inhibits human decidualization. Mol Cell Endocrinol 2005;229:65-74.
30. Kim JJ, Taylor HS, Lu Z, Ladhani O, Hastings JM, Jackson KS, Wu Y, Guo SW, Fazleabas AT. Altered expression of HOXA10 in endometriosis: potential role in decidualization. Mol Hum Reprod 2007;13:323-332.
31. Klemmt PA, Carver JG, Kennedy SH, Koninckx PR, Mardon HJ. Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity. Fertil Steril 2006; 85:564-572.
32. Krikun G, Mor G, Alvero A, Guller S, Schatz F, Sapi E, Rahman M, Caze R, Qumsiyeh M, Lockwood CJ. A novel immortalized human endometrial stromal cell line with normal progestational response. Endocrinology 2004;145:2291-2296.
33. Latil A, Biéche I, Vidaud D, Lidereau R, Berthon P, Cussenot O, Vidaud M. Evaluation of androgen, estrogen (ERalpha and ERbeta), and progesterone receptor expression in human prostate cancer by real-time quantitative reverse transcription-polymerase chain reaction assays. Cancer Res 2001;61:1919-1926.
34. Lee B, Du H, Taylor HS. Experimental murine endometriosis induces DNA methylation and altered gene expression in eutopic endometrium. Biol Reprod 2009;80:79-85.
35. Liang G, Chan MF, Tomigahara Y, Tsai YC, Gonzales FA, Li E, Laird PW, Jones PA. Cooperativity between DNA methyltransferases in the maintenance methylation of repetitive elements. Mol Cell Biol 2002; 22:480-491.
36. Logan PC, Ponnampalam AP, Rahnama F, Lobie PE, Mitchell MD. The effect of DNA methylation inhibitor 5-Aza-2′-deoxycytidine on human endometrial stromal cells. Hum Reprod 2010;25:2859-2869.
37. Logan PC, Steiner M, Ponnampalam AP, Mitchell MD. Cell cycle regulation of human endometrial stromal cells during decidualization. Reprod Sci 2012;19:883-894.
38. Makrigiannakis A, Margioris AN, Chatzaki E, Zoumakis E, Chrousos GP, Gravanis A. The decidualizing effect of progesterone may involve direct transcriptional activation of corticotrophin-releasing hormone from human endometrial stromal cells. Mol Hum Reprod 1999; 5:789-796.
39. Mertens HJMM, Heineman MJ, Theunissen PHMH, de Jong FH, Evers JLH. Androgen, estrogen and progesterone receptor expression in the human uterus during the menstrual cycle. Eur J Obstet Gynecol Reprod Biol 2001;98:58-65.
40. Minici F, Tiberi F, Tropea A, Orlando M, Gangale MF, Romani F, Campo S, Bompiani A, Lanzone A, Apa R. Endometriosis and human infertility: a new investigation into the role of eutopic endometrium. Hum Reprod 2007;23:530-537.
41. Mote PA, Balleine RL, McGowan EM, Clarke CL. Heterogeneity of progesterone receptors A and B expression in human endometrial glands and stroma. Hum Reprod 2000;15:48-56.
42. Munro SK, Farquhar CM, Mitchell MD, Ponnampalam AP. Epigenetic regulation of endometrium during the menstrual cycle. Mol Hum Reprod 2010;16:297-310.
43. Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999;99:247-257.
44. Pohnke Y, Schneider-Merck T, Fahnenstich J, Kempf R, Christian M, Milde-Langosch K, Brosens JJ, Gellersen B. Wild-type p53 protein is up-regulated upon cyclic adenosine monophosphate-induced differentiation of human endometrial stromal cells. J Clin Endocrinol Metab 2004;89:5233-5244.
45. Ponnampalam AP, Weston GC, Trajstman AC, Susil B, Rogers PAW. Molecular classification of human endometrial cycle stages by transcriptional profiling. Mol Hum Reprod 2004;10:879-893.
46. Psychoyos A. Uterine receptivity for nidation. Ann N Y Acad Sci 1986; 476:36-42.
47. Robertson KD, Keyomarsi K, Gonzales FA, Velicescu M, Jones PA. Differential mRNA expression of the human DNA methyltransferases (DNMTs) 1, 3a and 3b during the G0/G1 to S phase transition in normal and tumor cells. Nucleic Acids Res 2000;28:2108-2113.
48. Sakai N, Maruyama T, Sakurai R, Masuda H, Yamamoto Y, Shimizu A, Kishi I, Asada H, Yamagoe S, Yoshimura Y. Involvement of histone acetylation in ovarian steroid-induced decidualization of human endometrial stromal cells. J Biol Chem 2003;278:16675-16682.
49. Santi DV, Norment A, Garrett CE. Covalent bond formation between a DNA-cytosine methyltransferase and DNA containing 5-azacytosine. Proc Natl Acad Sci USA 1984;81:6993-6997.
50. Schneider-Stock R, Diab-Assef M, Rohrbeck A, Foltzer-Jourdainne C, Boltze C, Hartig R, Schonfeld P, Roessner A, Gali-Muhtasib H. 5-aza-cytidine is a potent inhibitor of DNA methyltransferase 3a and induces apoptosis in HCT-116 colon cancer cells via Gadd45- and p53-dependent mechanisms. J Pharmacol Exp Ther 2005;312: 525-536.
51. Shiota K. DNA methylation profiles of CpG islands for cellular differentiation and development in mammals. Cytogenet Genome Res 2004;105:325-334.
52. Singh RP, Shiue K, Schomberg D, Zhou FC. Cellular epigenetic modifications of neural stem cell differentiation. Cell Transplant 2009; 18:1197-1211.
53. Soultanas P, Andrews PD, Burton DR, Hornby DP. Modulation of human DNA methyltransferase activity and mRNA levels in the monoblast cell line U937 induced to differentiate with dibutyryl cyclic AMP and phorbol ester. J Mol Endocrinol 1993;11:191-200.
54. Takeshima H, Suetake I, Shimahara H, Ura K, Tate S-I, Tajima S. Distinct DNA methylation activity of Dnmt3a and Dnmt3b towards naked and nucleosomal DNA. J Biochem 2006;139:503-515.
55. Tan H, Yi L, Rote NS, Hurd WW, Mesiano S. Progesterone receptor-A and -B have opposite effects on proinflammatory gene expression in human myometrial cells: implications for progesterone actions in human pregnancy and parturition. J Clin Endocrinol Metab 2012; 97:E719-E730.
56. Tang B, Gurpide E. Direct effect of gonadotropins on decidualization of human endometrial stromal cells. J Steroid Biochem Mol Biol 1993; 47:115-121.
57. Tang B, Guller S, Gurpide E. Cyclic adenosine 3′,5′-monophosphate induces prolactin expression in stromal cells isolated from human proliferative endometrium. Endocrinology 1993a;133:2197-2203.
58. Tang B, Guller S, Gurpide E. Mechanisms involved in the decidualization of human endometrial stromal cells. Acta Eur Fertil 1993b;24:221-223.
59. Tang B, Guller S, Gurpide E. Mechanism of human endometrial stromal cells decidualization. Ann N Y Acad Sci 1994;734:19-25.
60. Telgmann R, Gellersen B. Marker genes of decidualization: activation of the decidual prolactin gene. Hum Reprod Update 1998;4:472-479.
61. van Kaam KJAF, Delvoux B, Romano A, D'Hooghe T, Dunselman GAJ, Groothuis PG. Deoxyribonucleic acid methyltransferases and methyl-CpG-binding domain proteins in human endometrium and endometriosis. Fertil Steril 2011;95:1421-1427.
62. Vegeto E, Shahbaz MM, Wen DX, Goldman ME, O'Malley BW, McDonnell DP. Human progesterone receptor A form is a cell- and promoter-specific repressor of human progesterone receptor B function. Mol Endocrinol 1993;7:1244-1255.
63. Vincent ZL, Farquhar CM, Mitchell MD, Ponnampalam AP. Expression and regulation of DNA methyltransferases in human endometrium. Fertil Steril 2011;95:1522-1525.e1.
64. Walton EL, Francastel C, Velasco G. Maintenance of DNA methylation: Dnmt3b joins the dance. Epigenetics 2011;6:1373-1377. Wang X, Seed B. A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res 2003;31:1-8.
65. Wang H, Critchley HO, Kelly RW, Shen D, Baird DT. Progesterone receptor subtype B is differentially regulated in human endometrial stroma. Mol Hum Reprod 1998;4:407-412.
66. Wu Y, Halverson G, Basir Z, Strawn E, Yan P, Guo S-W. Aberrant methylation at HOXA10 may be responsible for its aberrant expression in the endometrium of patients with endometriosis. Am J Obstet Gynecol 2005;193:371-380.
67. Wu Y, Strawn E, Basir Z, Halverson G, Guo S. Promoter hypermethylation of progesterone receptor isoform B (PR-B) in endometriosis. Epigenetics 2006;1:106-111.
68. Wu Y, Strawn E, Basir Z, Halverson G, Guo S-W. Aberrant expression of deoxyribonucleic acid methyltransferases DNMT1, DNMT3A, and DNMT3B in women with endometriosis. Fertil Steril 2007;87:24-32.
69. Xue Q, Lin Z, Cheng Y-H, Huang C-C, Marsh E, Yin P, Milad MP, Confino E, Reierstad S, Innes J et al. Promoter methylation regulates estrogen receptor 2 in endometrium and endometriosis. Biol Reprod 2007;77:681-687.
70. Yamagata Y, Asada H, Tamura I, Lee L, Maekawa R, Taniguchi K, Taketani T, Matsuoka A, Tamura H, Sugino N. DNA methyltransferase expression in the human endometrium: down-regulation by progesterone and estrogen. Hum Reprod 2009;24:1126-1132.
71. Yoshie M, Kashima H, Bessho T, Takeichi M, Isaka K, Tamura K. Expression of stathmin, a microtubule regulatory protein, is associated with the migration and differentiation of cultured early trophoblasts. Hum Reprod 2008;23:2766-2774.
72. Yudt MR, Berrodin TJ, Jelinsky SA, Hanna LA, Brown EL, Chippari S, Bhat RA, Winneker RC, Zhang Z. Selective and opposing actions of progesterone receptor isoforms in human endometrial stromal cells. Mol Cell Endocrinol 2006;247:116-126.
73. Zelenko Z, Aghajanova L, Irwin JC, Giudice LC. Nuclear receptor, coregulator signaling, and chromatin remodeling pathways suggest involvement of the epigenome in the steroid hormone response of endometrium and abnormalities in endometriosis. Reprod Sci 2012;19:152-162.
74. Zhang Y, Andrews GK, Wang L. Zinc-induced Dnmt1 expression involves antagonism between MTF-1 and nuclear receptor SHP. Nucleic Acids Res 2012;40:4850-4860.