Aberrant expression and localization of deoxyribonucleic acid methyltransferase 3B in endometriotic stromal cells

Fertility and Sterility

Volumn 104, Issue 4, 2015, Pages 953-963.e2

  Dyson, Matthew T ^a   Kakinuma, Toshiyuki ^a   Pavone, Mary Ellen ^a   Monsivais, Diana ^a   Navarro, Antonia ^a   Malpani, Saurabh S ^a   Ono, Masanori ^a   Bulun, Serdar E ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

decidualization; DNA methyltransferase; Endometriosis; estrogen receptor; steroidogenic factor 1

Indexed keywords

8 BROMO CYCLIC AMP; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; MEDROXYPROGESTERONE ACETATE; MESSENGER RNA; STEROIDOGENIC FACTOR 1; DNA (CYTOSINE 5) METHYLTRANSFERASE;

ADULT; ARTICLE; CELL CULTURE; CHROMATIN IMMUNOPRECIPITATION; COMPARATIVE STUDY; CONTROLLED STUDY; DECIDUALIZATION; DNA METHYLATION; ENDOMETRIOSIS; ENDOMETRIOTIC STROMAL CELL; ENDOMETRIUM TUMOR; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IN VITRO STUDY; PREMENOPAUSE; PRIMARY CULTURE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; STROMA CELL; ENDOMETRIUM; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; NIDATION; OVARY DISEASE; PATHOLOGY; TISSUE DISTRIBUTION;

ADULT; CELLS, CULTURED; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; EMBRYO IMPLANTATION; ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MIDDLE AGED; OVARIAN DISEASES; STROMAL CELLS; TISSUE DISTRIBUTION;

EID: 84942819909     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2015.06.046     Document Type: Article

References (73)

1. C.Y. Ramathal, I.C. Bagchi, R.N. Taylor, and M.K. Bagchi Endometrial decidualization: of mice and men Semin Reprod Med 28 2010 17 26
2. B. Gellersen, I.A. Brosens, and J.J. Brosens Decidualization of the human endometrium: mechanisms, functions, and clinical perspectives Semin Reprod Med 25 2007 445 453
3. D. Emera, R. Romero, and G. Wagner The evolution of menstruation: a new model for genetic assimilation: explaining molecular origins of maternal responses to fetal invasiveness Bioessays 34 2012 26 35
4. M.T. Dyson, D. Roqueiro, D. Monsivais, C.M. Ercan, M.E. Pavone, D.C. Brooks, and et al. Genome-wide DNA methylation analysis predicts an epigenetic switch for GATA factor expression in endometriosis PLoS Genet 10 2014 e1004158
5. L.C. Giudice, and L.C. Kao Endometriosis Lancet 364 2004 1789 1799
6. S.E. Bulun Endometriosis N Engl J Med 360 2009 268 279
7. K.G. Osteen, K.L. Bruner-Tran, and E. Eisenberg Endometrial biology and the etiology of endometriosis Fertil Steril 84 2005 33 34 discussion, 8-9
8. B. Gurates, and S.E. Bulun Endometriosis: the ultimate hormonal disease Semin Reprod Med 21 2003 125 134
9. M.T. Dyson, and S.E. Bulun Cutting SRC-1 down to size in endometriosis Nat Med 18 2012 1016 1018
10. R.O. Burney, and L.C. Giudice Pathogenesis and pathophysiology of endometriosis Fertil Steril 98 2012 511 519
11. A. Bricou, R.E. Batt, and C. Chapron Peritoneal fluid flow influences anatomical distribution of endometriotic lesions: why Sampson seems to be right Eur J Obstet Gynecol Reprod Biol 138 2008 127 134
12. P.G. Signorile, F. Baldi, R. Bussani, R. Viceconte, P. Bulzomi, M. D'Armiento, and et al. Embryologic origin of endometriosis: analysis of 101 human female fetuses J Cell Physiol 227 2012 1653 1656
13. J. Halme, M.G. Hammond, J.F. Hulka, S.G. Raj, and L.M. Talbert Retrograde menstruation in healthy women and in patients with endometriosis Obstet Gynecol 64 1984 151 154
14. R.W. Furst, H.H. Meyer, G. Schweizer, and S.E. Ulbrich Is DNA methylation an epigenetic contribution to transcriptional regulation of the bovine endometrium during the estrous cycle and early pregnancy? Mol Cell Endocrinol 348 2012 67 77
15. Q. Xue, Z. Lin, P. Yin, M.P. Milad, Y.H. Cheng, E. Confino, and et al. Transcriptional activation of steroidogenic factor-1 by hypomethylation of the 5' CpG island in endometriosis J Clin Endocrinol Metab 92 2007 3261 3267
16. Q. Xue, Z. Lin, Y.H. Cheng, C.C. Huang, E. Marsh, P. Yin, and et al. Promoter methylation regulates estrogen receptor 2 in human endometrium and endometriosis Biol Reprod 77 2007 681 687
17. Y. Wu, E. Strawn, Z. Basir, G. Halverson, and S.W. Guo Promoter hypermethylation of progesterone receptor isoform B (PR-B) in endometriosis Epigenetics 1 2006 106 111
18. Y. Wu, G. Halverson, Z. Basir, E. Strawn, P. Yan, and S.W. Guo Aberrant methylation at HOXA10 may be responsible for its aberrant expression in the endometrium of patients with endometriosis Am J Obstet Gynecol 193 2005 371 380
19. M. Izawa, T. Harada, F. Taniguchi, Y. Ohama, Y. Takenaka, and N. Terakawa An epigenetic disorder may cause aberrant expression of aromatase gene in endometriotic stromal cells Fertil Steril 89 2008 1390 1396
20. K. Nasu, Y. Kawano, Y. Tsukamoto, M. Takano, N. Takai, H. Li, and et al. Aberrant DNA methylation status of endometriosis: epigenetics as the pathogenesis, biomarker and therapeutic target J Obstet Gynaecol Res 37 2011 683 695
21. D. Wang, Q. Chen, C. Zhang, F. Ren, and T. Li DNA hypomethylation of the COX-2 gene promoter is associated with up-regulation of its mRNA expression in eutopic endometrium of endometriosis Eur J Med Res 17 2012 12
22. Y. Yamagata, K. Nishino, E. Takaki, S. Sato, R. Maekawa, A. Nakai, and et al. Genome-wide DNA methylation profiling in cultured eutopic and ectopic endometrial stromal cells PLoS One 9 2014 e83612
23. H. Naqvi, Y. Ilagan, G. Krikun, and H.S. Taylor Altered genome-wide methylation in endometriosis Reprod Sci 21 2014 1237 1243
24. C.A. Rubel, H.L. Franco, J.W. Jeong, J.P. Lydon, and F.J. DeMayo GATA2 is expressed at critical times in the mouse uterus during pregnancy Gene Expr Patterns 12 2012 196 203
25. F. Gao, X. Ma, A. Rusie, J. Hemingway, A.B. Ostmann, D. Chung, and et al. Epigenetic changes through DNA methylation contribute to uterine stromal cell decidualization Endocrinology 153 2012 6078 6090
26. S.W. Guo The endometrial epigenome and its response to steroid hormones Mol Cell Endocrinol 358 2012 185 196
27. B. Borghese, S. Barbaux, F. Mondon, P. Santulli, G. Pierre, G. Vinci, and et al. Research resource: genome-wide profiling of methylated promoters in endometriosis reveals a subtelomeric location of hypermethylation Mol Endocrinol 24 2010 1872 1885
28. X. Liao, M.K. Siu, K.Y. Chan, E.S. Wong, H.Y. Ngan, Q.K. Chan, and et al. Hypermethylation of RAS effector-related genes and DNA methyltransferase 1 expression in endometrial carcinogenesis Int J Cancer 123 2008 296 302
29. Y. Yamagata, H. Asada, I. Tamura, L. Lee, R. Maekawa, K. Taniguchi, and et al. DNA methyltransferase expression in the human endometrium: down-regulation by progesterone and estrogen Hum Reprod 24 2009 1126 1132
30. K.J. van Kaam, B. Delvoux, A. Romano, T. D'Hooghe, G.A. Dunselman, and P.G. Groothuis Deoxyribonucleic acid methyltransferases and methyl-CpG-binding domain proteins in human endometrium and endometriosis Fertil Steril 95 2011 1421 1427
31. Z.L. Vincent, C.M. Farquhar, M.D. Mitchell, and A.P. Ponnampalam Expression and regulation of DNA methyltransferases in human endometrium Fertil Steril 95 2011 1522 1525.e1
32. G. Grimaldi, M. Christian, S. Quenby, and J.J. Brosens Expression of epigenetic effectors in decidualizing human endometrial stromal cells Mol Hum Reprod 18 2012 451 458
33. Y. Wu, E. Strawn, Z. Basir, G. Halverson, and S.W. Guo Aberrant expression of deoxyribonucleic acid methyltransferases DNMT1, DNMT3A, and DNMT3B in women with endometriosis Fertil Steril 87 2007 24 32
34. I.P. Ryan, E.D. Schriock, and R.N. Taylor Isolation, characterization, and comparison of human endometrial and endometriosis cells in vitro J Clin Endocrinol Metab 78 1994 642 649
35. L.S. Noble, K. Takayama, K.M. Zeitoun, J.M. Putman, D.A. Johns, M.M. Hinshelwood, and et al. Prostaglandin E2 stimulates aromatase expression in endometriosis-derived stromal cells J Clin Endocrinol Metab 82 1997 600 606
36. J.J. Kim, H.S. Taylor, Z. Lu, O. Ladhani, J.M. Hastings, K.S. Jackson, and et al. Altered expression of HOXA10 in endometriosis: potential role in decidualization Mol Hum Reprod 13 2007 323 332
37. S.C. Schutte, and R.N. Taylor A tissue-engineered human endometrial stroma that responds to cues for secretory differentiation, decidualization, and menstruation Fertil Steril 97 2012 997 1003
38. A. Navarro, P. Yin, D. Monsivais, S.M. Lin, P. Du, J.J. Wei, and et al. Genome-wide DNA methylation indicates silencing of tumor suppressor genes in uterine leiomyoma PLoS One 7 2012 e33284
39. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 25 2001 402 408
40. M.E. Pavone, M. Dyson, S. Reirstad, E. Pearson, H. Ishikawa, Y.H. Cheng, and et al. Endometriosis expresses a molecular pattern consistent with decreased retinoid uptake, metabolism and action Hum Reprod 26 2011 2157 2164
41. T.I. Lee, S.E. Johnstone, and R.A. Young Chromatin immunoprecipitation and microarray-based analysis of protein location Nat Protoc 1 2006 729 748
42. P.A. Fujita, B. Rhead, A.S. Zweig, A.S. Hinrichs, D. Karolchik, M.S. Cline, and et al. The UCSC Genome Browser database: update 2011 Nucleic Acids Res 39 2011 D876 D882
43. E. Trukhacheva, Z. Lin, S. Reierstad, Y.H. Cheng, M. Milad, and S.E. Bulun Estrogen receptor (ER) beta regulates ERalpha expression in stromal cells derived from ovarian endometriosis J Clin Endocrinol Metab 94 2009 615 622
44. P.A. Klemmt, J.G. Carver, S.H. Kennedy, P.R. Koninckx, and H.J. Mardon Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity Fertil Steril 85 2006 564 572
45. Q. Xue, Y.F. Zhou, S.N. Zhu, and S.E. Bulun Hypermethylation of the CpG island spanning from exon II to intron III is associated with steroidogenic factor 1 expression in stromal cells of endometriosis Reprod Sci 18 2011 1080 1084
46. E.A. Hoivik, T.E. Bjanesoy, O. Mai, S. Okamoto, Y. Minokoshi, Y. Shima, and et al. DNA methylation of intronic enhancers directs tissue-specific expression of steroidogenic factor 1/adrenal 4 binding protein (SF-1/Ad4BP) Endocrinology 152 2011 2100 2112
47. S.E. Bulun, D. Monsavais, M.E. Pavone, M. Dyson, Q. Xue, E. Attar, and et al. Role of estrogen receptor-beta in endometriosis Semin Reprod Med 30 2012 39 45
48. R.W. Furst, H. Kliem, H.H. Meyer, and S.E. Ulbrich A differentially methylated single CpG-site is correlated with estrogen receptor alpha transcription J Steroid Biochem Mol Biol 130 2012 96 104
49. Y.L. Ottaviano, J.P. Issa, F.F. Parl, H.S. Smith, S.B. Baylin, and N.E. Davidson Methylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cells Cancer Res 54 1994 2552 2555
50. H. Zhou, J. Li, K.C. Podratz, T. Tipton, S. Marzolf, H.B. Chen, and et al. Hypomethylation and activation of syncytin-1 gene in endometriotic tissue Curr Pharm Des 20 2014 1786 1795
51. M. Szczepanska, A. Mostowska, P. Wirstlein, J. Malejczyk, R. Ploski, J. Skrzypczak, and et al. Polymorphic variants of DNMT3A and the risk of endometriosis Eur J Obstet Gynecol Reprod Biol 166 2013 81 85
52. B. Borghese, P. Santulli, D. Hequet, G. Pierre, D. de Ziegler, D. Vaiman, and et al. Genetic polymorphisms of DNMT3L involved in hypermethylation of chromosomal ends are associated with greater risk of developing ovarian endometriosis Am J Pathol 180 2012 1781 1786
53. P.C. Logan, A.P. Ponnampalam, M. Steiner, and M.D. Mitchell Effect of cyclic AMP and estrogen/progesterone on the transcription of DNA methyltransferases during the decidualization of human endometrial stromal cells Mol Hum Reprod 19 2013 302 312
54. Y. Liu, E.J. Oakeley, L. Sun, and J.P. Jost Multiple domains are involved in the targeting of the mouse DNA methyltransferase to the DNA replication foci Nucleic Acids Res 26 1998 1038 1045
55. C.L. Hsieh In vivo activity of murine de novo methyltransferases, Dnmt3a and Dnmt3b Mol Cell Biol 19 1999 8211 8218
56. M. Szczepanska, P. Wirstlein, J. Skrzypczak, and P.P. Jagodzinski Expression of HOXA11 in the mid-luteal endometrium from women with endometriosis-associated infertility Reprod Biol Endocrinol 10 2012 1
57. D. Repsilber, S. Kern, A. Telaar, G. Walzl, G.F. Black, J. Selbig, and et al. Biomarker discovery in heterogeneous tissue samples - taking the in-silico deconfounding approach BMC Bioinformatics 11 2010 27
58. S.K. Munro, C.M. Farquhar, M.D. Mitchell, and A.P. Ponnampalam Epigenetic regulation of endometrium during the menstrual cycle Mol Hum Reprod 16 2010 297 310
59. K.D. Robertson DNA methylation and human disease Nat Rev Genet 6 2005 597 610
60. M.T. McCabe, J.C. Brandes, and P.M. Vertino Cancer DNA methylation: molecular mechanisms and clinical implications Clin Cancer Res 15 2009 3927 3937
61. C. Plass, and D.J. Smiraglia Genome-wide analysis of DNA methylation changes in human malignancies Curr Top Microbiol Immunol 310 2006 179 198
62. K.D. Robertson, E. Uzvolgyi, G. Liang, C. Talmadge, J. Sumegi, F.A. Gonzales, and et al. The human DNA methyltransferases (DNMTs) 1, 3a and 3b: coordinate mRNA expression in normal tissues and overexpression in tumors Nucleic Acids Res 27 1999 2291 2298
63. K. Ghoshal, T. Motiwala, R. Claus, P. Yan, H. Kutay, J. Datta, and et al. HOXB13, a target of DNMT3B, is methylated at an upstream CpG island, and functions as a tumor suppressor in primary colorectal tumors PLoS One 5 2010 e10338
64. S. Bai, K. Ghoshal, and S.T. Jacob Identification of T-cadherin as a novel target of DNA methyltransferase 3B and its role in the suppression of nerve growth factor-mediated neurite outgrowth in PC12 cells J Biol Chem 281 2006 13604 13611
65. Q. Xue, Y. Xu, H. Yang, L. Zhang, J. Shang, C. Zeng, and et al. Methylation of a novel CpG island of intron 1 is associated with steroidogenic factor 1 expression in endometriotic stromal cells Reprod Sci 21 2014 395 400
66. H. Cedar, and Y. Bergman Linking DNA methylation and histone modification: patterns and paradigms Nat Rev Genet 10 2009 295 304
67. P.A. Jones Functions of DNA methylation: islands, start sites, gene bodies and beyond Nat Rev Genet 13 2012 484 492
68. Z.D. Smith, and A. Meissner DNA methylation: roles in mammalian development Nat Rev Genet 14 2013 204 220
69. E. Vire, C. Brenner, R. Deplus, L. Blanchon, M. Fraga, C. Didelot, and et al. The Polycomb group protein EZH2 directly controls DNA methylation Nature 439 2006 871 874
70. X. Yang, D.L. Phillips, A.T. Ferguson, W.G. Nelson, J.G. Herman, and N.E. Davidson Synergistic activation of functional estrogen receptor (ER)-alpha by DNA methyltransferase and histone deacetylase inhibition in human ER-alpha-negative breast cancer cells Cancer Res 61 2001 7025 7029
71. T.M. D'Hooghe, C.M. Kyama, D. Chai, A. Fassbender, A. Vodolazkaia, A. Bokor, and et al. Nonhuman primate models for translational research in endometriosis Reprod Sci 16 2009 152 161
72. J.A. Deane, R.C. Gualano, and C.E. Gargett Regenerating endometrium from stem/progenitor cells: Is it abnormal in endometriosis, Asherman's syndrome and infertility? Curr Opin Obstet Gynecol 25 2013 193 200
73. Y. Afshar, J. Hastings, D. Roqueiro, J.W. Jeong, L.C. Giudice, and A.T. Fazleabas Changes in eutopic endometrial gene expression during the progression of experimental endometriosis in the baboon, Papio anubis Biol Reprod 88 2013 44