The endometrial epigenome and its response to steroid hormones

Molecular and Cellular Endocrinology

Volumn 358, Issue 2, 2012, Pages 185-196

  Guo, Sun Wei ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

Acetylation; Endometrium; Epigenome; Histone; Methylation; Steroid hormones

Indexed keywords

ANDROGEN RECEPTOR; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; ESTROGEN RECEPTOR; HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE PCAF; HISTONE DEACETYLASE; HISTONE DEMETHYLASE; HISTONE METHYLTRANSFERASE; METHYL CPG BINDING PROTEIN; METHYL CPG BINDING PROTEIN 2; PROGESTERONE RECEPTOR; STEROID HORMONE; STEROID RECEPTOR; STEROID RECEPTOR COACTIVATOR 1; STEROID RECEPTOR COACTIVATOR 3;

CHROMATIN; DISEASE ASSOCIATION; DNA METHYLATION; DNA MODIFICATION; ENDOMETRIUM; ENDOMETRIUM CARCINOMA; EPIGENETICS; EPIGENOME; GENE CONTROL; GENETIC IDENTIFICATION; GENOME; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; MENSTRUAL CYCLE; MOLECULAR INTERACTION; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

ANIMALS; ENDOMETRIUM; EPIGENESIS, GENETIC; FEMALE; GENOME; HORMONES; HUMANS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; STEROIDS;

EID: 84861526077     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.10.025     Document Type: Review

References (150)

1. Ace C.I., Okulicz W.C. Microarray profiling of progesterone-regulated endometrial genes during the rhesus monkey secretory phase. Reprod. Biol. Endocrinol. 2004, 2:54.
2. Amita M., Takahashi T., Tsutsumi S., Ohta T., Takata K., Henmi N., Hara S., Igarashi H., Takahashi K., Kurachi H. Molecular mechanism of the inhibition of estradiol-induced endometrial epithelial cell proliferation by clomiphene citrate. Endocrinology 2010, 151:394-405.
3. An W., Kim J., Roeder R.G. Ordered cooperative functions of PRMT1, p300, and CARM1 in transcriptional activation by p53. Cell 2004, 117:735-748.
4. Bain D.L., Heneghan A.F., Connaghan-Jones K.D., Miura M.T. Nuclear receptor structure: implications for function. Annu. Rev. Physiol. 2007, 69:201-220.
5. Balmer N.N., Richer J.K., Spoelstra N.S., Torkko K.C., Lyle P.L., Singh M. Steroid receptor coactivator AIB1 in endometrial carcinoma, hyperplasia and normal endometrium: Correlation with clinicopathologic parameters and biomarkers. Mod. Pathol. 2006, 19:1593-1605.
6. Bannister A.J., Schneider R., Kouzarides T. Histone methylation: dynamic or static?. Cell 2002, 109:801-806.
7. Barchuk A.R., Cristino A.S., Kucharski R., Costa L.F., Simoes Z.L., Maleszka R. Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Dev. Biol. 2007, 7:70.
8. Bauersachs S., Mitko K., Ulbrich S.E., Blum H., Wolf E. Transcriptome studies of bovine endometrium reveal molecular profiles characteristic for specific stages of estrous cycle and early pregnancy. Exp. Clin. Endocrinol. Diabetes 2008, 116:371-384.
9. Bell S.C., Hales M.W., Patel S., Kirwan P.H., Drife J.O. Protein synthesis and secretion by the human endometrium and decidua during early pregnancy. Br. J. Obstet. Gynaecol. 1985, 92:793-803.
10. Borthwick J.M., Charnock-Jones D.S., Tom B.D., Hull M.L., Teirney R., Phillips S.C., Smith S.K. Determination of the transcript profile of human endometrium. Mol. Hum. Reprod. 2003, 9:19-33.
11. Brackertz M., Boeke J., Zhang R., Renkawitz R. Two highly related p66 proteins comprise a new family of potent transcriptional repressors interacting with MBD2 and MBD3. J. Biol. Chem. 2002, 277:40958-40966.
12. Brosens J.J., Hayashi N., White J.O. Progesterone receptor regulates decidual prolactin expression in differentiating human endometrial stromal cells. Endocrinology 1999, 140:4809-4820.
13. Cakmak H., Taylor H.S. Molecular mechanisms of treatment resistance in endometriosis: the role of progesterone-hox gene interactions. Semin. Reprod. Med. 2010, 28:69-74.
14. Cao R., Wang L., Wang H., Xia L., Erdjument-Bromage H., Tempst P., Jones R.S., Zhang Y. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 2002, 298:1039-1043.
15. Cao W., Mah K., Carroll R.S., Slayden O.D., Brenner R.M. Progesterone withdrawal up-regulates fibronectin and integrins during menstruation and repair in the rhesus macaque endometrium. Hum. Reprod. 2007, 22:3223-3231.
16. Carninci P., Hayashizaki Y. Noncoding RNA transcription beyond annotated genes. Curr. Opin. Genet. Dev. 2007, 17:139-144.
17. Carson D.D., Lagow E., Thathiah A., Al-Shami R., Farach-Carson M.C., Vernon M., Yuan L., Fritz M.A., Lessey B. Changes in gene expression during the early to mid-luteal (receptive phase) transition in human endometrium detected by high-density microarray screening. Mol. Hum. Reprod. 2002, 8:871-879.
18. Chauchereau A., Amazit L., Quesne M., Guiochon-Mantel A., Milgrom E. Sumoylation of the progesterone receptor and of the steroid receptor coactivator SRC-1. J. Biol. Chem. 2003, 278:12335-12343.
19. Chi P., Allis C.D., Wang G.G. Covalent histone modifications - miswritten, misinterpreted and mis-erased in human cancers. Nat. Rev. Cancer 2010, 10:457-469.
20. Clapier C.R., Cairns B.R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 2009.
21. Couture J.F., Trievel R.C. Histone-modifying enzymes: encrypting an enigmatic epigenetic code. Curr. Opin. Struct. Biol. 2006, 16:753-760.
22. Du W., Sun H., Wang H., Qiang B., Shen Y., Yao Z., Gu J., Xiong M., Huang W., Chen Z., Zuo J., Hua X., Gao W., Sun Q., Fang F. Confirmation of susceptibility gene loci on chromosome 1 in northern China Han families with type 2 diabetes. Chin. Med. J. (Engl.) 2001, 114:876-878.
23. El-Osta A. DNMT cooperativity - the developing links between methylation, chromatin structure and cancer. BioEssays 2003, 25:1071-1084.
24. Erdmann V.A., Barciszewska M.Z., Hochberg A., de Groot N., Barciszewski J. Regulatory RNAs. Cell. Mol. Life Sci. 2001, 58:960-977.
25. Falkenstein E., Tillmann H.C., Christ M., Feuring M., Wehling M. Multiple actions of steroid hormones - a focus on rapid, nongenomic effects. Pharmacol. Rev. 2000, 52:513-556.
26. Featherstone M. Coactivators in transcription initiation: here are your orders. Curr. Opin. Genet. Dev. 2002, 12:149-155.
27. Fraga M.F., Esteller M. Epigenetics and aging: the targets and the marks. Trends Genet. 2007, 23:413-418.
28. Fu M., Wang C., Reutens A.T., Wang J., Angeletti R.H., Siconolfi-Baez L., Ogryzko V., Avantaggiati M.L., Pestell R.G. P300 and p300/cAMP-response element-binding protein-associated factor acetylate the androgen receptor at sites governing hormone-dependent transactivation. J. Biol. Chem. 2000, 275:20853-20860.
29. 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.
30. Ghabreau L., Roux J.P., Niveleau A., Fontaniere B., Mahe C., Mokni M., Frappart L. Correlation between the DNA global methylation status and progesterone receptor expression in normal endometrium, endometrioid adenocarcinoma and precursors. Virchows Arch. 2004, 445:129-134.
31. Ghoshal K., Datta J., Majumder S., Bai S., Kutay H., Motiwala T., Jacob S.T. 5-Aza-deoxycytidine induces selective degradation of DNA methyltransferase 1 by a proteasomal pathway that requires the KEN box, bromo-adjacent homology domain, and nuclear localization signal. Mol. Cell. Biol. 2005, 25:4727-4741.
32. 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.
33. Green J.A., Kim J.G., Whitworth K.M., Agca C., Prather R.S. The use of microarrays to define functionally-related genes that are differentially expressed in the cycling pig uterus. Soc. Reprod. Fertil. Suppl. 2006, 62:163-176.
34. Gregory C.W., Wilson E.M., Apparao K.B., Lininger R.A., Meyer W.R., Kowalik A., Fritz M.A., Lessey B.A. Steroid receptor coactivator expression throughout the menstrual cycle in normal and abnormal endometrium. J. Clin. Endocrinol. Metab. 2002, 87:2960-2966.
35. Grilli S., Ferreri A.M., Gola G., Rocchetta R., Orlandi C., Prodi G. Cytoplasmic receptors for 17 beta-estradiol, 5 alpha-dihydrotestosterone and progesterone in normal and abnormal human uterine tissues. Cancer Lett. 1977, 2:247-258.
36. Gunin A.G., Kapitova I.N., Suslonova N.V. Effects of histone deacetylase inhibitors on estradiol-induced proliferation and hyperplasia formation in the mouse uterus. J. Endocrinol. 2005, 185:539-549.
37. Guo S.W. Epigenetics of endometriosis. Mol. Hum. Reprod. 2009, 15:587-607.
38. Guo J.Z., Gorski J. Estrogen effects on modifications of chromatin proteins in the rat uterus. J. Steroid Biochem. 1989, 32:13-20.
39. Haouzi D., Mahmoud K., Fourar M., Bendhaou K., Dechaud H., De Vos J., Reme T., Dewailly D., Hamamah S. Identification of new biomarkers of human endometrial receptivity in the natural cycle. Hum. Reprod. 2009, 24:198-205.
40. Harvey S.R., Libby P.R. Multiple forms of histone acetyltransferases in the cytosol of calf endometrium. Biochim. Biophys. Acta 1976, 429:742-749.
41. Hendrich B., Bird A. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol. Cell. Biol. 1998, 18:6538-6547.
42. Hendrich B., Abbott C., McQueen H., Chambers D., Cross S., Bird A. Genomic structure and chromosomal mapping of the murine and human Mbd1, Mbd2, Mbd3, and Mbd4 genes. Mamm. Genome 1999, 10:906-912.
43. Hirst M., Marra M.A. Epigenetics and human disease. Int. J. Biochem. Cell Biol. 2009, 41:136-146.
44. Holliday R. Epigenetics: an overview. Dev. Genet. 1994, 15:453-457.
45. Holliday R. Epigenetics: a historical overview. Epigenetics 2006, 1:76-80.
46. Horcajadas J.A., Riesewijk A., Martin J., Cervero A., Mosselman S., Pellicer A., Simon C. Global gene expression profiling of human endometrial receptivity. J. Reprod. Immunol. 2004, 63:41-49.
47. Houshdaran S., Zelenko Z., Tamaresis J., Irwin J.C., Giudice L. Abnormal epigenetic signature in the eutopic endometrium of patients with severe endometriosis. The 58th Annual Meeting of the Society for Gynecologic Investigation 2011, 192A-193A. SAGE, Miami Beach, Florida.
48. Ingrosso D., Cimmino A., Perna A.F., Masella L., De Santo N.G., De Bonis M.L., Vacca M., D'Esposito M., D'Urso M., Galletti P., Zappia V. Folate treatment and unbalanced methylation and changes of allelic expression induced by hyperhomocysteinaemia in patients with uraemia. Lancet 2003, 361:1693-1699.
49. Issa J.P. Age-related epigenetic changes and the immune system. Clin. Immunol. 2003, 109:103-108.
50. Jaenisch R., Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 2003, 33(Suppl.):245-254.
51. 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.
52. Jenuwein T., Allis C.D. Translating the histone code. Science 2001, 293:1074-1080.
53. Jia D., Jurkowska R.Z., Zhang X., Jeltsch A., Cheng X. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 2007, 449:248-251.
54. Kale S., Shuster M., Shangold J. Endometrioma in a cesarean scar: case report and review of the literature. Am. J. Obstet. Gynecol. 1971, 111:596-597.
55. Kangaspeska S., Stride B., Metivier R., Polycarpou-Schwarz M., Ibberson D., Carmouche R.P., Benes V., Gannon F., Reid G. Transient cyclical methylation of promoter DNA. Nature 2008, 452:112-115.
56. Kao L.C., Tulac S., Lobo S., Imani B., Yang J.P., Germeyer A., Osteen K., Taylor R.N., Lessey B.A., Giudice L.C. Global gene profiling in human endometrium during the window of implantation. Endocrinology 2002, 143:2119-2138.
57. Kao L.C., Germeyer A., Tulac S., Lobo S., Yang J.P., Taylor R.N., Osteen K., Lessey B.A., Giudice L.C. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 2003, 144:2870-2881.
58. Keppler B.R., Archer T.K. Chromatin-modifying enzymes as therapeutic targets - part 1. Expert Opin Ther Targets 2008, 12:1301-1312.
59. Kershah S.M., Desouki M.M., Koterba K.L., Rowan B.G. Expression of estrogen receptor coregulators in normal and malignant human endometrium. Gynecol. Oncol. 2004, 92:304-313.
60. Kim M.Y., Woo E.M., Chong Y.T., Homenko D.R., Kraus W.L. Acetylation of estrogen receptor alpha by p300 at lysines 266 and 268 enhances the deoxyribonucleic acid binding and transactivation activities of the receptor. Mol. Endocrinol. 2006, 20:1479-1493.
61. Kim J.J., Taylor H.S., Lu Z., Ladhani O., Hastings J.M., Jackson K.S., Wu Y., Guo S.W., Fazleabas A.T. Altered expression of HOXA10 in endometriosis: potential role in decidualization. Mol. Hum. Reprod. 2007, 13:323-332.
62. Klose R.J., Zhang Y. Regulation of histone methylation by demethylimination and demethylation. Nat. Rev. Mol. Cell Biol. 2007, 8:307-318.
63. Kondo Y. Epigenetic cross-talk between DNA methylation and histone modifications in human cancers. Yonsei Med. J. 2009, 50:455-463.
64. Krikun G., Schatz F., Taylor R., Critchley H.O., Rogers P.A., Huang J., Lockwood C.J. Endometrial endothelial cell steroid receptor expression and steroid effects on gene expression. J. Clin. Endocrinol. Metab. 2005, 90:1812-1818.
65. Krusche C.A., Vloet A.J., Classen-Linke I., von Rango U., Beier H.M., Alfer J. Class I histone deacetylase expression in the human cyclic endometrium and endometrial adenocarcinomas. Hum. Reprod. 2007, 22:2956-2966.
66. Kucharski R., Maleszka J., Foret S., Maleszka R. Nutritional control of reproductive status in honeybees via DNA methylation. Science 2008, 319:1827-1830.
67. Laird P.W., Jaenisch R. The role of DNA methylation in cancer genetic and epigenetics. Annu. Rev. Genet. 1996, 30:441-464.
68. 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.
69. Lee B., Du H., Taylor H.S. Experimental murine endometriosis induces DNA methylation and altered gene expression in eutopic endometrium. Biol. Reprod. 2009, 80:79-85.
70. Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat. Rev. Genet. 2002, 3:662-673.
71. Libby P.R. Histone acetylation and hormone action. Early effects of oestradiol-17beta on histone acetylation in rat uterus. Biochem. J. 1972, 130:663-669.
72. Lindner H.H. Analysis of histones, histone variants, and their post-translationally modified forms. Electrophoresis 2008, 29:2516-2532.
73. Liu Y., Lee K.F., Ng E.H., Yeung W.S., Ho P.C. Gene expression profiling of human peri-implantation endometria between natural and stimulated cycles. Fertil. Steril. 2008, 90:2152-2164.
74. Logan P.C., Ponnampalam A.P., Rahnama F., Lobie P.E., Mitchell M.D. The effect of DNA methylation inhibitor 5-Aza-2'-deoxycytidine on human endometrial stromal cells. Hum. Reprod. 2010, 25:2859-2869.
75. Luger K., Mader A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8A resolution. Nature 1997, 389:251-260.
76. Madauss K.P., Grygielko E.T., Deng S.J., Sulpizio A.C., Stanley T.B., Wu C., Short S.A., Thompson S.K., Stewart E.L., Laping N.J., Williams S.P., Bray J.D. A structural and in vitro characterization of asoprisnil: a selective progesterone receptor modulator. Mol. Endocrinol. 2007, 21:1066-1081.
77. Mattick J.S., Makunin I.V. Small regulatory RNAs in mammals. Hum. Mol. Genet. 2005, 14(Spec No. 1.):R121-R132.
78. Mattick J.S., Makunin I.V. Non-coding RNA. Hum. Mol. Genet. 2006, 15(Spec. No. 1):R17-R29.
79. Metivier R., Gallais R., Tiffoche C., Le Peron C., Jurkowska R.Z., Carmouche R.P., Ibberson D., Barath P., Demay F., Reid G., Benes V., Jeltsch A., Gannon F., Salbert G. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008, 452:45-50.
80. Mirkin S., Arslan M., Churikov D., Corica A., Diaz J.I., Williams S., Bocca S., Oehninger S. In search of candidate genes critically expressed in the human endometrium during the window of implantation. Hum. Reprod. 2005, 20:2104-2117.
81. Mitko K., Ulbrich S.E., Wenigerkind H., Sinowatz F., Blum H., Wolf E., Bauersachs S. Dynamic changes in messenger RNA profiles of bovine endometrium during the oestrous cycle. Reproduction 2008, 135:225-240.
82. Monteiro J.B., Colon-Diaz M., Bello S.A., Baez P.B., Garcia M., Abac S., Bayona M., Alvarez-Garriga C., Seto E., Flores I. Endometriosis is characterized by global histone hypoacetylation and distinct lysine-specific modifications at H3 and H4. Reprod. Biol. 2011, 18:276A.
83. Munro S.K., Farquhar C.M., Mitchell M.D., Ponnampalam A.P. Epigenetic regulation of endometrium during the menstrual cycle. Mol. Hum. Reprod. 2010, 16:297-310.
84. Nan X., Ng H.H., Johnson C.A., Laherty C.D., Turner B.M., Eisenman R.N., Bird A. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998, 393:386-389.
85. Ng H.H., Zhang Y., Hendrich B., Johnson C.A., Turner B.M., Erdjument-Bromage H., Tempst P., Reinberg D., Bird A. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat. Genet. 1999, 23:58-61.
86. Okano M., Bell D.W., Haber D.A., Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999, 99:247-257.
87. Ooi S.K., Qiu C., Bernstein E., Li K., Jia D., Yang Z., Erdjument-Bromage H., Tempst P., Lin S.P., Allis C.D., Cheng X., Bestor T.H. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 2007, 448:714-717.
88. Otsuka A.Y., Andrade P.M., Villanova F.E., Borra R.C., Silva I.D. Human endometrium mRNA profile assessed by oligonucleotide three-dimensional microarray. Gynecol. Endocrinol. 2007, 23:527-534.
89. Pedersen M.T., Helin K. Histone demethylases in development and disease. Trends Cell Biol. 2010, 20:662-671.
90. Peterson C.L., Laniel M.A. Histones and histone modifications. Curr. Biol. 2004, 14:R546-R551.
91. Ponnampalam A.P., Weston G.C., Trajstman A.C., Susil B., Rogers P.A. Molecular classification of human endometrial cycle stages by transcriptional profiling. Mol. Hum. Reprod. 2004, 10:879-893.
92. Punyadeera C., Dassen H., Klomp J., Dunselman G., Kamps R., Dijcks F., Ederveen A., de Goeij A., Groothuis P. Oestrogen-modulated gene expression in the human endometrium. Cell. Mol. Life Sci. 2005, 62:239-250.
93. Quezada S., Avellaira C., Johnson M.C., Gabler F., Fuentes A., Vega M. Evaluation of steroid receptors, coregulators, and molecules associated with uterine receptivity in secretory endometria from untreated women with polycystic ovary syndrome. Fertil. Steril. 2006, 85:1017-1026.
94. Rahnama F., Thompson B., Steiner M., Shafiei F., Lobie P.E., Mitchell M.D. Epigenetic regulation of E-cadherin controls endometrial receptivity. Endocrinology 2009, 150:1466-1472.
95. Rea S., Eisenhaber F., O'Carroll D., Strahl B.D., Sun Z.W., Schmid M., Opravil S., Mechtler K., Ponting C.P., Allis C.D., Jenuwein T. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 2000, 406:593-599.
96. Riesewijk A., Martin J., van Os R., Horcajadas J.A., Polman J., Pellicer A., Mosselman S., Simon C. Gene expression profiling of human endometrial receptivity on days LH+2 versus LH+7 by microarray technology. Mol. Hum. Reprod. 2003, 9:253-264.
97. Robertson K.D. DNA methylation, methyltransferases, and cancer. Oncogene 2001, 20:3139-3155.
98. Robertson K.D., Wolffe A.P. DNA methylation in health and disease. Nat. Rev. Genet. 2000, 1:11-19.
99. Rodenhiser D., Mann M. Epigenetics and human disease: translating basic biology into clinical applications. Can. Med. Assoc. J. 2006, 174:341-348.
100. Rosenfeld M.G., Glass C.K. Coregulator codes of transcriptional regulation by nuclear receptors. J. Biol. Chem. 2001, 276:36865-36868.
101. Rossi M., Sharkey A.M., Vigano P., Fiore G., Furlong R., Florio P., Ambrosini G., Smith S.K., Petraglia F. Identification of genes regulated by interleukin-1beta in human endometrial stromal cells. Reproduction 2005, 130:721-729.
102. Saito Y., Kanai Y., Sakamoto M., Saito H., Ishii H., Hirohashi S. Overexpression of a splice variant of DNA methyltransferase 3b, DNMT3b4, associated with DNA hypomethylation on pericentromeric satellite regions during human hepatocarcinogenesis. Proc. Natl. Acad. Sci. USA 2002, 99:10060-10065.
103. 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.
104. Sato N., Tsunoda H., Nishida M., Morishita Y., Takimoto Y., Kubo T., Noguchi M. Loss of heterozygosity on 10q23.3 and mutation of the tumor suppressor gene PTEN in benign endometrial cyst of the ovary: possible sequence progression from benign endometrial cyst to endometrioid carcinoma and clear cell carcinoma of the ovary. Cancer Res. 2000, 60:7052-7056.
105. Schmidt, A., Groth, P., Haendler, B., Hess-Stumpp, H., Kratzschmar, J., Seidel, H., Thaele, M., Weiss, B., 2005. Gene expression during the implantation window: microarray analysis of human endometrial samples. In: Ernst Schering Res Found Workshop, pp. 139-157.
106. Serra M.J., Ledford B.E., Baggett B. Synthesis and modification of the histones during the decidual cell reaction in the mouse uterus. Biol. Reprod. 1979, 20:214-220.
107. Shang Y., Brown M. Molecular determinants for the tissue specificity of SERMs. Science 2002, 295:2465-2468.
108. Shi Y., Lan F., Matson C., Mulligan P., Whetstine J.R., Cole P.A., Casero R.A. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004, 119:941-953.
109. Shimizu T., Krebs S., Bauersachs S., Blum H., Wolf E., Miyamoto A. Actions and interactions of progesterone and estrogen on transcriptome profiles of the bovine endometrium. Physiol. Genomics. 2010, 42A:290-300.
110. Shiozawa T., Shih H.C., Miyamoto T., Feng Y.Z., Uchikawa J., Itoh K., Konishi I. Cyclic changes in the expression of steroid receptor coactivators and corepressors in the normal human endometrium. J. Clin. Endocrinol. Metab. 2003, 88:871-878.
111. Smith C.L., O'Malley B.W. Coregulator function: a key to understanding tissue specificity of selective receptor modulators. Endocr. Rev. 2004, 25:45-71.
112. Spannhoff A., Kim Y.K., Raynal N.J., Gharibyan V., Su M.B., Zhou Y.Y., Li J., Castellano S., Sbardella G., Issa J.P., Bedford M.T. Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Rep. 2011, 12:238-243.
113. Storz G. An expanding universe of noncoding RNAs. Science 2002, 296:1260-1263.
114. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature 2000, 403:41-45.
115. Sun L., Zhao H., Xu Z., Liu Q., Liang Y., Wang L., Cai X., Zhang L., Hu L., Wang G., Zha X. Phosphatidylinositol 3-kinase/protein kinase B pathway stabilizes DNA methyltransferase I protein and maintains DNA methylation. Cell. Signal. 2007, 19:2255-2263.
116. Szczepanska M., Wirstlein P., Luczak M., Jagodzinski P.P., Skrzypczak J. Reduced expression of HOXA10 in the midluteal endometrium from infertile women with minimal endometriosis. Biomed. Pharmacother. 2010, 64:697-705.
117. Szymanski M., Barciszewska M.Z., Zywicki M., Barciszewski J. Noncoding RNA transcripts. J. Appl. Genet. 2003, 44:1-19.
118. Talbi S., Hamilton A.E., Vo K.C., Tulac S., Overgaard M.T., Dosiou C., Le Shay N., Nezhat C.N., Kempson R., Lessey B.A., Nayak N.R., Giudice L.C. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology 2006, 147:1097-1121.
119. Tamaya T., Motoyama T., Ohono Y., Ide N., Tsurusaki T., Okada H. Steroid receptor levels and histology of endometriosis and adenomyosis. Fertil. Steril. 1979, 31:396-400.
120. Tamura T., Picciano M.F. Folate and human reproduction. Am. J. Clin. Nutr. 2006, 83:993-1016.
121. Tao M.H., Freudenheim J.L. DNA methylation in endometrial cancer. Epigenetics 2010, 5:491-498.
122. Taylor P.J., Leader A., George R.E., Fick G.H. Correlations between laparoscopic and hysteroscopic findings in 497 women with otherwise unexplained infertility. J. Reprod. Med. 1984, 29:137-140.
123. Taylor H.S., Arici A., Olive D., Igarashi P. HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium. J. Clin. Invest. 1998, 101:1379-1384.
124. Ting A.H., Jair K.W., Suzuki H., Yen R.W., Baylin S.B., Schuebel K.E. Mammalian DNA methyltransferase 1: inspiration for new directions. Cell Cycle 2004, 3:1024-1026.
125. Toloubeydokhti T., Pan Q., Luo X., Bukulmez O., Chegini N. The expression and ovarian steroid regulation of endometrial micro-RNAs. Reprod. Sci. 2008, 15:993-1001.
126. Troiano R.N., Taylor K.J. Sonographically guided therapeutic aspiration of benign-appearing ovarian cysts and endometriomas. AJR Am. J. Roentgenol. 1998, 171:1601-1605.
127. Tseng L. Physiologic changes in binding and metabolism of estradiol and progesterone in human endometrium during the menstrual cycle. Obstet. Gynecol. Annu. 1979, 8:1-17.
128. Uchida H., Maruyama T., Nagashima T., Asada H., Yoshimura Y. Histone deacetylase inhibitors induce differentiation of human endometrial adenocarcinoma cells through up-regulation of glycodelin. Endocrinology 2005, 146:5365-5373.
129. Uchida H., Maruyama T., Nagashima T., Ono M., Masuda H., Arase T., Sugiura I., Onouchi M., Kajitani T., Asada H., Yoshimura Y. Human endometrial cytodifferentiation by histone deacetylase inhibitors. Hum. Cell 2006, 19:38-42.
130. Uchida H., Maruyama T., Ono M., Ohta K., Kajitani T., Masuda H., Nagashima T., Arase T., Asada H., Yoshimura Y. Histone deacetylase inhibitors stimulate cell migration in human endometrial adenocarcinoma cells through up-regulation of glycodelin. Endocrinology 2007, 148:896-902.
131. Uchida H., Maruyama T., Ohta K., Ono M., Arase T., Kagami M., Oda H., Kajitani T., Asada H., Yoshimura Y. Histone deacetylase inhibitor-induced glycodelin enhances the initial step of implantation. Hum. Reprod. 2007, 22:2615-2622.
132. Uchikawa J., Shiozawa T., Shih H.C., Miyamoto T., Feng Y.Z., Kashima H., Oka K., Konishi I. Expression of steroid receptor coactivators and corepressors in human endometrial hyperplasia and carcinoma with relevance to steroid receptors and Ki-67 expression. Cancer 2003, 98:2207-2213.
133. Vaisse C., Atger M., Potier B., Milgrom E. Human placental protein 14 gene: sequence and characterization of a short duplication. DNA Cell Biol. 1990, 9:401-413.
134. Vaissiere T., Sawan C., Herceg Z. Epigenetic interplay between histone modifications and DNA methylation in gene silencing. Mutat. Res. 2008, 659:40-48.
135. van Kaam K.J., Delvoux B., Romano A., D'Hooghe T., Dunselman G.A., Groothuis P.G. Deoxyribonucleic acid methyltransferases and methyl-CpG-binding domain proteins in human endometrium and endometriosis. Fertil. Steril. 2011, 95:1421-1427.
136. Vienonen A., Miettinen S., Blauer M., Martikainen P.M., Tomas E., Heinonen P.K., Ylikomi T. Expression of nuclear receptors and cofactors in human endometrium and myometrium. J. Soc. Gynecol. Invest. 2004, 11:104-112.
137. Vincent Z.L., Farquhar C.M., Mitchell M.D., Ponnampalam A.P. Expression and regulation of DNA methyltransferases in human endometrium. Fertil. Steril. 2011, 95:1522-1525.e1.
138. Wang C., Fu M., Angeletti R.H., Siconolfi-Baez L., Reutens A.T., Albanese C., Lisanti M.P., Katzenellenbogen B.S., Kato S., Hopp T., Fuqua S.A., Lopez G.N., Kushner P.J., Pestell R.G. Direct acetylation of the estrogen receptor alpha hinge region by p300 regulates transactivation and hormone sensitivity. J. Biol. Chem. 2001, 276:18375-18383.
139. Wang G.G., Allis C.D., Chi P. Chromatin remodeling and cancer, part I: covalent histone modifications. Trends Mol. Med. 2007, 13:363-372.
140. White C.A., Robb L., Salamonsen L.A. Uterine extracellular matrix components are altered during defective decidualization in interleukin-11 receptor alpha deficient mice. Reprod. Biol. Endocrinol. 2004, 2:76.
141. Wieser F., Schneeberger C., Hudelist G., Singer C., Kurz C., Nagele F., Gruber C., Huber J.C., Tschugguel W. Endometrial nuclear receptor co-factors SRC-1 and N-CoR are increased in human endometrium during menstruation. Mol. Hum. Reprod. 2002, 8:644-650.
142. Wolf M., Klug J., Hackenberg R., Gessler M., Grzeschik K.H., Beato M., Suske G. Human CC10, the homologue of rabbit uteroglobin: genomic cloning, chromosomal localization and expression in endometrial cell lines. Hum. Mol. Genet. 1992, 1:371-378.
143. 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.
144. 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.
145. Xie S., Wang Z., Okano M., Nogami M., Li Y., He W.W., Okumura K., Li E. Cloning, expression and chromosome locations of the human DNMT3 gene family. Gene 1999, 236:87-95.
146. Xiong Y., Dowdy S.C., Eberhardt N.L., Podratz K.C., Jiang S.W. HMLH1 promoter methylation and silencing in primary endometrial cancers are associated with specific alterations in MBDs occupancy and histone modifications. Gynecol. Oncol. 2006, 103:321-328.
147. 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.
148. Yanaihara A., Otsuka Y., Iwasaki S., Aida T., Tachikawa T., Irie T., Okai T. Differences in gene expression in the proliferative human endometrium. Fertil. Steril. 2005, 83(Suppl. 1):1206-1215.
149. Zhang Y., Ng H.H., Erdjument-Bromage H., Tempst P., Bird A., Reinberg D. Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev. 1999, 13:1924-1935.
150. Zhou X.C., Dowdy S.C., Podratz K.C., Jiang S.W. Epigenetic considerations for endometrial cancer prevention, diagnosis and treatment. Gynecol. Oncol. 2007, 107:143-153.