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Cellular and Molecular Life Sciences

, Volume 76, Issue 24, pp 4813–4828 | Cite as

Epigenetic control of embryo–uterine crosstalk at peri-implantation

  • Shuangbo Kong
  • Chan Zhou
  • Haili Bao
  • Zhangli Ni
  • Mengying Liu
  • Bo He
  • Lin Huang
  • Yang Sun
  • Haibin WangEmail author
  • Jinhua LuEmail author
Review

Abstract

Embryo implantation is one of the pivotal steps during mammalian pregnancy, since the quality of embryo implantation determines the outcome of ongoing pregnancy and fetal development. A large number of factors, including transcription factors, signalling transduction components, and lipids, have been shown to be indispensable for embryo implantation. Increasing evidence also suggests the important roles of epigenetic factors in this critical event. This review focuses on recent findings about the involvement of epigenetic regulators during embryo implantation.

Keywords

Implantation Epigenetic regulation Uterine receptivity Blastocyst activation decidualization 

Notes

Acknowledgements

This review article was supported in parts by National Key R&D program of China (2017YFC1001402 to H.W.), and the National Natural Science Foundation (81601285 to S.K., 81830045 and 81490744 to H. W. and 31600945 to J.L.) and Fundamental Research Funds for the Central Universities (20720180039 to S.K., 20720180041 to J.L.).

References

  1. 1.
    Dickmann Z, Noyes RW (1961) The zona pellucida at the time of implantation. Fertil Steril 12:310–318PubMedGoogle Scholar
  2. 2.
    Wang H, Dey SK (2006) Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet 7:185–199PubMedGoogle Scholar
  3. 3.
    Zhang S, Lin H, Kong S, Wang S, Wang H, Wang H, Armant DR (2013) Physiological and molecular determinants of embryo implantation. Mol Aspects Med 34:939–980PubMedPubMedCentralGoogle Scholar
  4. 4.
    Paria BC, Huet-Hudson YM, Dey SK (1993) Blastocyst’s state of activity determines the “window” of implantation in the receptive mouse uterus. Proc Natl Acad Sci USA 90:10159–10162PubMedGoogle Scholar
  5. 5.
    Cha J, Sun X, Dey SK (2012) Mechanisms of implantation: strategies for successful pregnancy. Nat Med 18:1754–1767PubMedPubMedCentralGoogle Scholar
  6. 6.
    Lim HJ, Wang H (2010) Uterine disorders and pregnancy complications: insights from mouse models. J Clin Invest 120:1004–1015PubMedPubMedCentralGoogle Scholar
  7. 7.
    Gellersen B, Brosens JJ (2014) Cyclic decidualization of the human endometrium in reproductive health and failure. Endocr Rev 35:851–905PubMedGoogle Scholar
  8. 8.
    Berger SL, Kouzarides T, Shiekhattar R, Shilatifard A (2009) An operational definition of epigenetics. Genes Dev 23:781–783PubMedPubMedCentralGoogle Scholar
  9. 9.
    Nelissen EC, van Montfoort AP, Dumoulin JC, Evers JL (2011) Epigenetics and the placenta. Hum Reprod Update 17:397–417PubMedGoogle Scholar
  10. 10.
    Herman JG, Baylin SB (2003) Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 349:2042–2054PubMedGoogle Scholar
  11. 11.
    Laird PW (2003) The power and the promise of DNA methylation markers. Nat Rev Cancer 3:253–266PubMedGoogle Scholar
  12. 12.
    Ooi SK, Qiu C, Bernstein E, Li K, Jia D, Yang Z, Erdjument-Bromage H, Tempst P, Lin SP, Allis CD, Cheng X, Bestor TH (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448:714–717PubMedPubMedCentralGoogle Scholar
  13. 13.
    Veland N, Lu Y, Hardikar S, Gaddis S, Zeng Y, Liu B, Estecio MR, Takata Y, Lin K, Tomida MW, Shen J, Saha D, Gowher H, Zhao H, Chen T (2018) DNMT3L facilitates DNA methylation partly by maintaining DNMT3A stability in mouse embryonic stem cells. Nucleic Acids Res 47(1):152–167PubMedCentralGoogle Scholar
  14. 14.
    Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33(Suppl):245–254PubMedGoogle Scholar
  15. 15.
    Kim TH, Barrera LO, Zheng M, Qu C, Singer MA, Richmond TA, Wu Y, Green RD, Ren B (2005) A high-resolution map of active promoters in the human genome. Nature 436:876–880PubMedPubMedCentralGoogle Scholar
  16. 16.
    Weber M, Schubeler D (2007) Genomic patterns of DNA methylation: targets and function of an epigenetic mark. Curr Opin Cell Biol 19:273–280PubMedGoogle Scholar
  17. 17.
    Branco MR, Ficz G, Reik W (2011) Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat Rev Genet 13:7–13PubMedPubMedCentralGoogle Scholar
  18. 18.
    Kouzarides T (2007) SnapShot: histone-modifying enzymes. Cell 131:822PubMedGoogle Scholar
  19. 19.
    Turner BM (2002) Cellular memory and the histone code. Cell 111:285–291PubMedGoogle Scholar
  20. 20.
    Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705PubMedGoogle Scholar
  21. 21.
    Peterson CL, Laniel MA (2004) Histones and histone modifications. Curr Biol 14:R546–R551PubMedGoogle Scholar
  22. 22.
    Sims RJ 3rd, Reinberg D (2006) Histone H3 Lys 4 methylation: caught in a bind? Genes Dev 20:2779–2786PubMedGoogle Scholar
  23. 23.
    Patel DJ, Wang Z (2013) Readout of epigenetic modifications. Annu Rev Biochem 82:81–118PubMedPubMedCentralGoogle Scholar
  24. 24.
    Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, Bell GW, Otte AP, Vidal M, Gifford DK, Young RA, Jaenisch R (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441:349–353PubMedGoogle Scholar
  25. 25.
    Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K, Koseki H, Fuchikami T, Abe K, Murray HL, Zucker JP, Yuan B, Bell GW, Herbolsheimer E, Hannett NM, Sun K, Odom DT, Otte AP, Volkert TL, Bartel DP, Melton DA, Gifford DK, Jaenisch R, Young RA (2006) Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125:301–313PubMedPubMedCentralGoogle Scholar
  26. 26.
    Reik W (2007) Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447:425–432PubMedGoogle Scholar
  27. 27.
    Boon RA, Dimmeler S (2015) MicroRNAs in myocardial infarction. Nat Rev Cardiol 12:135–142PubMedGoogle Scholar
  28. 28.
    Ransohoff JD, Wei Y, Khavari PA (2018) The functions and unique features of long intergenic non-coding RNA. Nat Rev Mol Cell Biol 19:143–157PubMedGoogle Scholar
  29. 29.
    Ernst C, Odom DT, Kutter C (2017) The emergence of piRNAs against transposon invasion to preserve mammalian genome integrity. Nat Commun 8:1411PubMedPubMedCentralGoogle Scholar
  30. 30.
    Ferlita A, Battaglia R, Andronico F, Caruso S, Cianci A, Purrello M, Pietro CD (2018) Non-coding RNAs in endometrial physiopathology. Int J Mol Sci 19(7):2120PubMedCentralGoogle Scholar
  31. 31.
    Koerner MV, Pauler FM, Huang R, Barlow DP (2009) The function of non-coding RNAs in genomic imprinting. Development 136:1771–1783PubMedPubMedCentralGoogle Scholar
  32. 32.
    Gendrel AV, Heard E (2014) Noncoding RNAs and epigenetic mechanisms during X-chromosome inactivation. Annu Rev Cell Dev Biol 30:561–580Google Scholar
  33. 33.
    Bagga S, Bracht J, Hunter S, Massirer K, Holtz J, Eachus R, Pasquinelli AE (2005) Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 122:553–563PubMedGoogle Scholar
  34. 34.
    Folco HD, Pidoux AL, Urano T, Allshire RC (2008) Heterochromatin and RNAi are required to establish CENP-A chromatin at centromeres. Science 319:94–97PubMedPubMedCentralGoogle Scholar
  35. 35.
    Varambally S, Cao Q, Mani RS, Shankar S, Wang X, Ateeq B, Laxman B, Cao X, Jing X, Ramnarayanan K, Brenner JC, Yu J, Kim JH, Han B, Tan P, Kumar-Sinha C, Lonigro RJ, Palanisamy N, Maher CA, Chinnaiyan AM (2008) Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science 322:1695–1699PubMedPubMedCentralGoogle Scholar
  36. 36.
    Kopp F, Mendell JT (2018) Functional classification and experimental dissection of long noncoding RNAs. Cell 172:393–407PubMedPubMedCentralGoogle Scholar
  37. 37.
    Sun Q, Hao Q, Prasanth KV (2018) Nuclear long noncoding RNAs: key regulators of gene expression. Trends Genet 34:142–157PubMedPubMedCentralGoogle Scholar
  38. 38.
    Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–655PubMedPubMedCentralGoogle Scholar
  39. 39.
    Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297PubMedPubMedCentralGoogle Scholar
  40. 40.
    Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433:769–773PubMedGoogle Scholar
  41. 41.
    He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5:522–531PubMedPubMedCentralGoogle Scholar
  42. 42.
    Ghildiyal M, Zamore PD (2009) Small silencing RNAs: an expanding universe. Nat Rev Genet 10:94–108PubMedPubMedCentralGoogle Scholar
  43. 43.
    Altmae S, Martinez-Conejero JA, Esteban FJ, Ruiz-Alonso M, Stavreus-Evers A, Horcajadas JA, Salumets A (2013) MicroRNAs miR-30b, miR-30d, and miR-494 regulate human endometrial receptivity. Reprod Sci 20:308–317PubMedPubMedCentralGoogle Scholar
  44. 44.
    Gebert LFR, MacRae IJ (2018) Regulation of microRNA function in animals. Nat Rev Mol Cell Biol 431:350Google Scholar
  45. 45.
    Bartel DP (2018) Metazoan MicroRNAs. Cell 173:20–51PubMedPubMedCentralGoogle Scholar
  46. 46.
    Chen YG, Satpathy AT, Chang HY (2017) Gene regulation in the immune system by long noncoding RNAs. Nat Immunol 18:962–972PubMedGoogle Scholar
  47. 47.
    Fatica A, Bozzoni I (2014) Long non-coding RNAs: new players in cell differentiation and development. Nat Rev Genet 15:7–21PubMedGoogle Scholar
  48. 48.
    Yan P, Luo S, Lu JY, Shen X (2017) Cis- and trans-acting lncRNAs in pluripotency and reprogramming. Curr Opin Genet Dev 46:170–178PubMedGoogle Scholar
  49. 49.
    Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495:384–388PubMedGoogle Scholar
  50. 50.
    Tatomer DC, Wilusz JE (2017) An unchartered journey for ribosomes: circumnavigating circular RNAs to produce proteins. Mol Cell 66:1–2PubMedGoogle Scholar
  51. 51.
    Lee HJ, Hore TA, Reik W (2014) Reprogramming the methylome: erasing memory and creating diversity. Cell Stem Cell 14:710–719PubMedPubMedCentralGoogle Scholar
  52. 52.
    Lepikhov K, Zakhartchenko V, Hao R, Yang F, Wrenzycki C, Niemann H, Wolf E, Walter J (2008) Evidence for conserved DNA and histone H3 methylation reprogramming in mouse, bovine and rabbit zygotes. Epigenetics Chromatin 1:8PubMedPubMedCentralGoogle Scholar
  53. 53.
    Lepikhov K, Walter J (2004) Differential dynamics of histone H3 methylation at positions K4 and K9 in the mouse zygote. BMC Dev Biol 4:12PubMedPubMedCentralGoogle Scholar
  54. 54.
    Zhang B, Zheng H, Huang B, Li W, Xiang Y, Peng X, Ming J, Wu X, Zhang Y, Xu Q, Liu W, Kou X, Zhao Y, He W, Li C, Chen B, Li Y, Wang Q, Ma J, Yin Q, Kee K, Meng A, Gao S, Xu F, Na J, Xie W (2016) Allelic reprogramming of the histone modification H3K4me3 in early mammalian development. Nature 537:553–557PubMedGoogle Scholar
  55. 55.
    Liu X, Wang C, Liu W, Li J, Li C, Kou X, Chen J, Zhao Y, Gao H, Wang H, Zhang Y, Gao Y, Gao S (2016) Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos. Nature 537:558–562PubMedGoogle Scholar
  56. 56.
    Wu J, Huang B, Chen H, Yin Q, Liu Y, Xiang Y, Zhang B, Liu B, Wang Q, Xia W, Li W, Li Y, Ma J, Peng X, Zheng H, Ming J, Zhang W, Zhang J, Tian G, Xu F, Chang Z, Na J, Yang X, Xie W (2016) The landscape of accessible chromatin in mammalian preimplantation embryos. Nature 534:652–657PubMedGoogle Scholar
  57. 57.
    Xu Q, Xie W (2018) Epigenome in early mammalian development: inheritance, reprogramming and establishment. Trends Cell Biol 28:237–253PubMedGoogle Scholar
  58. 58.
    Ladstatter S, Tachibana K (2018) Genomic insights into chromatin reprogramming to totipotency in embryos. J Cell Biol 218:70–82PubMedGoogle Scholar
  59. 59.
    Fenelon JC, Banerjee A, Murphy BD (2014) Embryonic diapause: development on hold. Int J Dev Biol 58:163–174PubMedGoogle Scholar
  60. 60.
    Fu Z, Wang B, Wang S, Wu W, Wang Q, Chen Y, Kong S, Lu J, Tang Z, Ran H, Tu Z, He B, Zhang S, Chen Q, Jin W, Duan E, Wang H, Wang YL, Li L, Wang F, Gao S, Wang H (2014) Integral proteomic analysis of blastocysts reveals key molecular machinery governing embryonic diapause and reactivation for implantation in mice. Biol Reprod 90:52PubMedGoogle Scholar
  61. 61.
    Bulut-Karslioglu A, Biechele S, Jin H, Macrae TA, Hejna M, Gertsenstein M, Song JS, Ramalho-Santos M (2016) Inhibition of mTOR induces a paused pluripotent state. Nature 540:119–123PubMedPubMedCentralGoogle Scholar
  62. 62.
    Scognamiglio R, Cabezas-Wallscheid N, Thier MC, Altamura S, Reyes A, Prendergast AM, Baumgartner D, Carnevalli LS, Atzberger A, Haas S, von Paleske L, Boroviak T, Worsdorfer P, Essers MA, Kloz U, Eisenman RN, Edenhofer F, Bertone P, Huber W, van der Hoeven F, Smith A, Trumpp A (2016) Myc depletion induces a pluripotent dormant state mimicking diapause. Cell 164:668–680PubMedPubMedCentralGoogle Scholar
  63. 63.
    Cheong AW, Pang RT, Liu WM, Kottawatta KS, Lee KF, Yeung WS (2014) MicroRNA Let-7a and dicer are important in the activation and implantation of delayed implanting mouse embryos. Hum Reprod 29:750–762PubMedGoogle Scholar
  64. 64.
    Liu WM, Pang RT, Cheong AW, Ng EH, Lao K, Lee KF, Yeung WS (2012) Involvement of microRNA lethal-7a in the regulation of embryo implantation in mice. PLoS One 7:e37039PubMedPubMedCentralGoogle Scholar
  65. 65.
    Capalbo A, Ubaldi FM, Cimadomo D, Noli L, Khalaf Y, Farcomeni A, Ilic D, Rienzi L (2016) MicroRNAs in spent blastocyst culture medium are derived from trophectoderm cells and can be explored for human embryo reproductive competence assessment. Fertil Steril 105(225–235):e221–e223Google Scholar
  66. 66.
    Gao L, Wu K, Liu Z, Yao X, Yuan S, Tao W, Yi L, Yu G, Hou Z, Fan D, Tian Y, Liu J, Chen ZJ, Liu J (2018) Chromatin accessibility landscape in human early embryos and its association with evolution. Cell 173(248–259):e215Google Scholar
  67. 67.
    Munro SK, Farquhar CM, Mitchell MD, Ponnampalam AP (2010) Epigenetic regulation of endometrium during the menstrual cycle. Mol Hum Reprod 16:297–310PubMedGoogle Scholar
  68. 68.
    Sasaki M, Kotcherguina L, Dharia A, Fujimoto S, Dahiya R (2001) Cytosine-phosphoguanine methylation of estrogen receptors in endometrial cancer. Cancer Res 61:3262–3266PubMedGoogle Scholar
  69. 69.
    Hori M, Iwasaki M, Shimazaki J, Inagawa S, Itabashi M (2000) Assessment of hypermethylated DNA in two promoter regions of the estrogen receptor alpha gene in human endometrial diseases. Gynecol Oncol 76:89–96PubMedGoogle Scholar
  70. 70.
    Sasaki M, Dharia A, Oh BR, Tanaka Y, Fujimoto S, Dahiya R (2001) Progesterone receptor B gene inactivation and CpG hypermethylation in human uterine endometrial cancer. Cancer Res 61:97–102PubMedGoogle Scholar
  71. 71.
    Ghabreau L, Roux JP, Niveleau A, Fontaniere B, Mahe C, Mokni M, Frappart L (2004) Correlation between the DNA global methylation status and progesterone receptor expression in normal endometrium, endometrioid adenocarcinoma and precursors. Virchow Arch Int J Pathol 445:129–134Google Scholar
  72. 72.
    Su RW, Strug MR, Jeong JW, Miele L, Fazleabas AT (2016) Aberrant activation of canonical Notch1 signaling in the mouse uterus decreases progesterone receptor by hypermethylation and leads to infertility. Proc Natl Acad Sci USA 113:2300–2305PubMedGoogle Scholar
  73. 73.
    Gao R, Ding Y, Liu X, Chen X, Wang Y, Long C, Li S, Guo L, He J (2012) Effect of folate deficiency on promoter methylation and gene expression of Esr1, Cdh1 and Pgr, and its influence on endometrial receptivity and embryo implantation. Hum Reprod 27:2756–2765PubMedGoogle Scholar
  74. 74.
    Milesi MM, Varayoud J, Ramos JG, Luque EH (2017) Uterine ERalpha epigenetic modifications are induced by the endocrine disruptor endosulfan in female rats with impaired fertility. Mol Cell Endocrinol 454:1–11PubMedGoogle Scholar
  75. 75.
    Taylor HS, Arici A, Olive D, Igarashi P (1998) HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium. J Clin Invest 101:1379–1384PubMedPubMedCentralGoogle Scholar
  76. 76.
    Gui Y, Zhang J, Yuan L, Lessey BA (1999) Regulation of HOXA-10 and its expression in normal and abnormal endometrium. Mol Hum Reprod 5:866–873PubMedGoogle Scholar
  77. 77.
    Satokata I, Benson G, Maas R (1995) Sexually dimorphic sterility phenotypes in Hoxa10-deficient mice. Nature 374:460–463PubMedGoogle Scholar
  78. 78.
    Benson GV, Lim H, Paria BC, Satokata I, Dey SK, Maas RL (1996) Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression. Development 122:2687–2696PubMedGoogle Scholar
  79. 79.
    Yoshida H, Broaddus R, Cheng W, Xie S, Naora H (2006) Deregulation of the HOXA10 homeobox gene in endometrial carcinoma: role in epithelial-mesenchymal transition. Cancer Res 66:889–897PubMedGoogle Scholar
  80. 80.
    Wu Y, Halverson G, Basir Z, Strawn E, Yan P, Guo SW (2005) Aberrant methylation at HOXA10 may be responsible for its aberrant expression in the endometrium of patients with endometriosis. Am J Obstet Gynecol 193:371–380PubMedGoogle Scholar
  81. 81.
    Leu YW, Yan PS, Fan M, Jin VX, Liu JC, Curran EM, Welshons WV, Wei SH, Davuluri RV, Plass C, Nephew KP, Huang TH (2004) Loss of estrogen receptor signaling triggers epigenetic silencing of downstream targets in breast cancer. Cancer Res 64:8184–8192PubMedGoogle Scholar
  82. 82.
    Metivier R, Gallais R, Tiffoche C, Le Peron C, Jurkowska RZ, Carmouche RP, Ibberson D, Barath P, Demay F, Reid G, Benes V, Jeltsch A, Gannon F, Salbert G (2008) Cyclical DNA methylation of a transcriptionally active promoter. Nature 452:45–50PubMedGoogle Scholar
  83. 83.
    Houshdaran S, Zelenko Z, Irwin JC, Giudice LC (2014) Human endometrial DNA methylome is cycle-dependent and is associated with gene expression regulation. Mol Endocrinol 28:1118–1135PubMedPubMedCentralGoogle Scholar
  84. 84.
    Horne AW, Lalani EN, Margara RA, White JO (2006) The effects of sex steroid hormones and interleukin-1-beta on MUC1 expression in endometrial epithelial cell lines. Reproduction 131:733–742PubMedGoogle Scholar
  85. 85.
    Meseguer M, Aplin JD, Caballero-Campo P, O’Connor JE, Martin JC, Remohi J, Pellicer A, Simon C (2001) Human endometrial mucin MUC1 is up-regulated by progesterone and down-regulated in vitro by the human blastocyst. Biol Reprod 64:590–601PubMedGoogle Scholar
  86. 86.
    Rahnama F, Thompson B, Steiner M, Shafiei F, Lobie PE, Mitchell MD (2009) Epigenetic regulation of E-cadherin controls endometrial receptivity. Endocrinology 150:1466–1472PubMedGoogle Scholar
  87. 87.
    Vincent ZL, Farquhar CM, Mitchell MD, Ponnampalam AP (2011) Expression and regulation of DNA methyltransferases in human endometrium. Fertil Steril 95(1522–1525):e1521Google Scholar
  88. 88.
    Yamagata Y, Asada H, Tamura I, Lee L, Maekawa R, Taniguchi K, Taketani T, Matsuoka A, Tamura H, Sugino N (2009) DNA methyltransferase expression in the human endometrium: down-regulation by progesterone and estrogen. Hum Reprod 24:1126–1132PubMedGoogle Scholar
  89. 89.
    van Kaam KJ, Delvoux B, Romano A, D’Hooghe T, Dunselman GA, Groothuis PG (2011) Deoxyribonucleic acid methyltransferases and methyl-CpG-binding domain proteins in human endometrium and endometriosis. Fertil Steril 95:1421–1427PubMedGoogle Scholar
  90. 90.
    Kukushkina V, Modhukur V, Suhorutsenko M, Peters M, Magi R, Rahmioglu N, Velthut-Meikas A, Altmae S, Esteban FJ, Vilo J, Zondervan K, Salumets A, Laisk-Podar T (2017) DNA methylation changes in endometrium and correlation with gene expression during the transition from pre-receptive to receptive phase. Sci Rep 7:3916PubMedPubMedCentralGoogle Scholar
  91. 91.
    Maekawa R, Tamura I, Shinagawa M, Mihara Y, Sato S, Okada M, Taketani T, Tamura H, Sugino N (2019) Genome-wide DNA methylation analysis revealed stable DNA methylation status during decidualization in human endometrial stromal cells. BMC Genomics 20:324PubMedPubMedCentralGoogle Scholar
  92. 92.
    Serra MJ, Ledford BE, Baggett B (1979) Synthesis and modification of the histones during the decidual cell reaction in the mouse uterus. Biol Reprod 20:214–220PubMedGoogle Scholar
  93. 93.
    Libby PR (1972) Histone acetylation and hormone action. Early effects of oestradiol-17beta on histone acetylation in rat uterus. Biochem J 130:663–669PubMedPubMedCentralGoogle Scholar
  94. 94.
    Guo JZ, Gorski J (1989) Estrogen effects on modifications of chromatin proteins in the rat uterus. J Steroid Biochem 32:13–20PubMedGoogle Scholar
  95. 95.
    Sakai N, Maruyama T, Sakurai R, Masuda H, Yamamoto Y, Shimizu A, Kishi I, Asada H, Yamagoe S, Yoshimura Y (2003) Involvement of histone acetylation in ovarian steroid-induced decidualization of human endometrial stromal cells. J Biol Chem 278:16675–16682PubMedGoogle Scholar
  96. 96.
    Gunin AG, Kapitova IN, Suslonova NV (2005) Effects of histone deacetylase inhibitors on estradiol-induced proliferation and hyperplasia formation in the mouse uterus. J Endocrinol 185:539–549PubMedGoogle Scholar
  97. 97.
    Uchida H, Maruyama T, Nagashima T, Asada H, Yoshimura Y (2005) Histone deacetylase inhibitors induce differentiation of human endometrial adenocarcinoma cells through up-regulation of glycodelin. Endocrinology 146:5365–5373PubMedGoogle Scholar
  98. 98.
    Grimaldi G, Christian M, Quenby S, Brosens JJ (2012) Expression of epigenetic effectors in decidualizing human endometrial stromal cells. Mol Hum Reprod 18:451–458PubMedGoogle Scholar
  99. 99.
    Uchida H, Maruyama T, Ohta K, Ono M, Arase T, Kagami M, Oda H, Kajitani T, Asada H, Yoshimura Y (2007) Histone deacetylase inhibitor-induced glycodelin enhances the initial step of implantation. Hum Reprod 22:2615–2622PubMedGoogle Scholar
  100. 100.
    Zhu LH, Sun LH, Hu YL, Jiang Y, Liu HY, Shen XY, Jin XY, Zhen X, Sun HX, Yan GJ (2013) PCAF impairs endometrial receptivity and embryo implantation by down-regulating beta3-integrin expression via HOXA10 acetylation. J Clin Endocrinol Metab 98:4417–4428Google Scholar
  101. 101.
    Xin Q, Kong S, Yan J, Qiu J, He B, Zhou C, Ni Z, Bao H, Huang L, Lu J, Xia G, Liu X, Chen ZJ, Wang C, Wang H (2018) Polycomb subunit BMI1 determines uterine progesterone responsiveness essential for normal embryo implantation. J Clin Invest 128:175–189PubMedGoogle Scholar
  102. 102.
    Filant J, Spencer TE (2014) Uterine glands: biological roles in conceptus implantation, uterine receptivity and decidualization. Int J Dev Biol 58:107–116PubMedPubMedCentralGoogle Scholar
  103. 103.
    Kelleher AM, Milano-Foster J, Behura SK, Spencer TE (2018) Uterine glands coordinate on-time embryo implantation and impact endometrial decidualization for pregnancy success. Nat Commun 9:2435PubMedCentralGoogle Scholar
  104. 104.
    Cui T, He B, Kong S, Zhou C, Zhang H, Ni Z, Bao H, Qiu J, Xin Q, Reinberg D, Lydon JP, Lu J, Wang H (2017) PR-Set7 deficiency limits uterine epithelial population growth hampering postnatal gland formation in mice. Cell Death Differ 24:2013–2021PubMedPubMedCentralGoogle Scholar
  105. 105.
    Li Q, Kannan A, DeMayo FJ, Lydon JP, Cooke PS, Yamagishi H, Srivastava D, Bagchi MK, Bagchi IC (2011) The antiproliferative action of progesterone in uterine epithelium is mediated by Hand2. Science 331:912–916PubMedPubMedCentralGoogle Scholar
  106. 106.
    Barron F, Woods C, Kuhn K, Bishop J, Howard MJ, Clouthier DE (2011) Downregulation of Dlx5 and Dlx6 expression by Hand2 is essential for initiation of tongue morphogenesis. Development 138:2249–2259PubMedPubMedCentralGoogle Scholar
  107. 107.
    Daikoku T, Cha J, Sun X, Tranguch S, Xie H, Fujita T, Hirota Y, Lydon J, DeMayo F, Maxson R, Dey SK (2011) Conditional deletion of Msx homeobox genes in the uterus inhibits blastocyst implantation by altering uterine receptivity. Dev Cell 21:1014–1025PubMedPubMedCentralGoogle Scholar
  108. 108.
    Wang J, Kumar RM, Biggs VJ, Lee H, Chen Y, Kagey MH, Young RA, Abate-Shen C (2011) The Msx1 homeoprotein recruits polycomb to the nuclear periphery during development. Dev Cell 21:575–588PubMedPubMedCentralGoogle Scholar
  109. 109.
    Creighton CJ, Benham AL, Zhu H, Khan MF, Reid JG, Nagaraja AK, Fountain MD, Dziadek O, Han D, Ma L, Kim J, Hawkins SM, Anderson ML, Matzuk MM, Gunaratne PH (2010) Discovery of novel microRNAs in female reproductive tract using next generation sequencing. PLoS One 5:e9637PubMedPubMedCentralGoogle Scholar
  110. 110.
    Kuokkanen S, Chen B, Ojalvo L, Benard L, Santoro N, Pollard JW (2010) Genomic profiling of microRNAs and messenger RNAs reveals hormonal regulation in microRNA expression in human endometrium. Biol Reprod 82:791–801PubMedGoogle Scholar
  111. 111.
    Hu SJ, Ren G, Liu JL, Zhao ZA, Yu YS, Su RW, Ma XH, Ni H, Lei W, Yang ZM (2008) MicroRNA expression and regulation in mouse uterus during embryo implantation. J Biol Chem 283:23473–23484PubMedGoogle Scholar
  112. 112.
    Chakrabarty A, Tranguch S, Daikoku T, Jensen K, Furneaux H, Dey SK (2007) MicroRNA regulation of cyclooxygenase-2 during embryo implantation. Proc Natl Acad Sci USA 104:15144–15149PubMedGoogle Scholar
  113. 113.
    Revel A, Achache H, Stevens J, Smith Y, Reich R (2011) MicroRNAs are associated with human embryo implantation defects. Hum Reprod 26:2830–2840PubMedGoogle Scholar
  114. 114.
    Moreno-Moya JM, Vilella F, Martinez S, Pellicer A, Simon C (2014) The transcriptomic and proteomic effects of ectopic overexpression of miR-30d in human endometrial epithelial cells. Mol Hum Reprod 20:550–566PubMedGoogle Scholar
  115. 115.
    Ponsuksili S, Tesfaye D, Schellander K, Hoelker M, Hadlich F, Schwerin M, Wimmers K (2014) Differential expression of miRNAs and their target mRNAs in endometria prior to maternal recognition of pregnancy associates with endometrial receptivity for in vivo- and in vitro-produced bovine embryos. Biol Reprod 91:135PubMedGoogle Scholar
  116. 116.
    Kresowik JD, Devor EJ, Van Voorhis BJ, Leslie KK (2014) MicroRNA-31 is significantly elevated in both human endometrium and serum during the window of implantation: a potential biomarker for optimum receptivity. Biol Reprod 91:17PubMedPubMedCentralGoogle Scholar
  117. 117.
    Liu JL, Liang XH, Su RW, Lei W, Jia B, Feng XH, Li ZX, Yang ZM (2012) Combined analysis of microRNome and 3′-UTRome reveals a species-specific regulation of progesterone receptor expression in the endometrium of rhesus monkey. J Biol Chem 287:13899–13910PubMedPubMedCentralGoogle Scholar
  118. 118.
    Vilella F, Moreno-Moya JM, Balaguer N, Grasso A, Herrero M, Martinez S, Marcilla A, Simon C (2015) Hsa-miR-30d, secreted by the human endometrium, is taken up by the pre-implantation embryo and might modify its transcriptome. Development 142:3210–3221PubMedGoogle Scholar
  119. 119.
    Desrochers LM, Bordeleau F, Reinhart-King CA, Cerione RA, Antonyak MA (2016) Microvesicles provide a mechanism for intercellular communication by embryonic stem cells during embryo implantation. Nat Commun 7:11958PubMedPubMedCentralGoogle Scholar
  120. 120.
    Galliano D, Pellicer A (2014) MicroRNA and implantation. Fertil Steril 101:1531–1544PubMedGoogle Scholar
  121. 121.
    Liu W, Niu Z, Li Q, Pang RT, Chiu PC, Yeung WS (2016) MicroRNA and Embryo Implantation. Am J Reprod Immunol 75:263–271PubMedGoogle Scholar
  122. 122.
    Liang J, Wang S, Wang Z (2017) Role of microRNAs in embryo implantation. Reprod Biol Endocrinol 15:90PubMedPubMedCentralGoogle Scholar
  123. 123.
    Haraguchi H, Saito-Fujita T, Hirota Y, Egashira M, Matsumoto L, Matsuo M, Hiraoka T, Koga K, Yamauchi N, Fukayama M, Bartos A, Cha J, Dey SK, Fujii T, Osuga Y (2014) MicroRNA-200a locally attenuates progesterone signaling in the cervix, preventing embryo implantation. Mol Endocrinol 28:1108–1117PubMedPubMedCentralGoogle Scholar
  124. 124.
    Chau YM, Pando S, Taylor HS (2002) HOXA11 silencing and endogenous HOXA11 antisense ribonucleic acid in the uterine endometrium. J Clin Endocrinol Metab 87:2674–2680PubMedGoogle Scholar
  125. 125.
    Arao Y, Carpenter K, Hewitt S, Korach KS (2010) Estrogen down-regulation of the Scx gene is mediated by the opposing strand-overlapping gene Bop1. J Biol Chem 285:4806–4814PubMedGoogle Scholar
  126. 126.
    Mihalich A, Reina M, Mangioni S, Ponti E, Alberti L, Vigano P, Vignali M, Di Blasio AM (2003) Different basic fibroblast growth factor and fibroblast growth factor-antisense expression in eutopic endometrial stromal cells derived from women with and without endometriosis. J Clin Endocrinol Metab 88:2853–2859PubMedGoogle Scholar
  127. 127.
    Noonan FC, Goodfellow PJ, Staloch LJ, Mutch DG, Simon TC (2003) Antisense transcripts at the EMX2 locus in human and mouse. Genomics 81:58–66PubMedGoogle Scholar
  128. 128.
    Lanz RB, Chua SS, Barron N, Soder BM, DeMayo F, O’Malley BW (2003) Steroid receptor RNA activator stimulates proliferation as well as apoptosis in vivo. Mol Cell Biol 23:7163–7176PubMedPubMedCentralGoogle Scholar
  129. 129.
    Sigurgeirsson B, Amark H, Jemt A, Ujvari D, Westgren M, Lundeberg J, Gidlof S (2017) Comprehensive RNA sequencing of healthy human endometrium at two time points of the menstrual cycle. Biol Reprod 96:24–33PubMedGoogle Scholar
  130. 130.
    Hu S, Yao G, Wang Y, Xu H, Ji X, He Y, Zhu Q, Chen Z, Sun Y (2014) Transcriptomic changes during the pre-receptive to receptive transition in human endometrium detected by RNA-Seq. J Clin Endocrinol Metab 99:E2744–E2753PubMedGoogle Scholar
  131. 131.
    Wang Q, Wang N, Cai R, Zhao F, Xiong Y, Li X, Wang A, Lin P, Jin Y (2017) Genome-wide analysis and functional prediction of long non-coding RNAs in mouse uterus during the implantation window. Oncotarget 8:84360–84372PubMedPubMedCentralGoogle Scholar
  132. 132.
    Wang Y, Hu T, Wu L, Liu X, Xue S, Lei M (2017) Identification of non-coding and coding RNAs in porcine endometrium. Genomics 109:43–50PubMedGoogle Scholar
  133. 133.
    Zeng H, Fan X, Liu N (2017) Expression of H19 imprinted gene in patients with repeated implantation failure during the window of implantation. Arch Gynecol Obstet 296:835–839PubMedGoogle Scholar
  134. 134.
    Feng C, Shen JM, Lv PP, Jin M, Wang LQ, Rao JP, Feng L (2018) Construction of implantation failure related lncRNA-mRNA network and identification of lncRNA biomarkers for predicting endometrial receptivity. Int J Biol Sci 14:1361–1377PubMedPubMedCentralGoogle Scholar
  135. 135.
    Zhang L, Liu X, Che S, Cui J, Liu Y, An X, Cao B, Song Y (2018) CircRNA-9119 regulates the expression of prostaglandin-endoperoxide synthase 2 (PTGS2) by sponging miR-26a in the endometrial epithelial cells of dairy goat. Reprod Fertil Dev 30(12):1759–1769PubMedGoogle Scholar
  136. 136.
    Liu L, Li L, Ma X, Yue F, Wang Y, Wang L, Jin P, Zhang X (2017) Altered circular RNA expression in patients with repeated implantation failure. Cell Physiol Biochem 44:303–313PubMedGoogle Scholar
  137. 137.
    Logan PC, Ponnampalam AP, Rahnama F, Lobie PE, Mitchell MD (2010) The effect of DNA methylation inhibitor 5-Aza-2′-deoxycytidine on human endometrial stromal cells. Hum Reprod 25:2859–2869PubMedGoogle Scholar
  138. 138.
    Gao F, Ma X, Rusie A, Hemingway J, Ostmann AB, Chung D, Das SK (2012) Epigenetic changes through DNA methylation contribute to uterine stromal cell decidualization. Endocrinology 153:6078–6090PubMedPubMedCentralGoogle Scholar
  139. 139.
    Ding YB, Long CL, Liu XQ, Chen XM, Guo LR, Xia YY, He JL, Wang YX (2012) 5-aza-2′-deoxycytidine leads to reduced embryo implantation and reduced expression of DNA methyltransferases and essential endometrial genes. PLoS One 7:e45364PubMedPubMedCentralGoogle Scholar
  140. 140.
    Logan PC, Ponnampalam AP, Steiner M, Mitchell MD (2013) Effect of cyclic AMP and estrogen/progesterone on the transcription of DNA methyltransferases during the decidualization of human endometrial stromal cells. Mol Hum Reprod 19:302–312PubMedGoogle Scholar
  141. 141.
    Brown LY, Bonney EA, Raj RS, Nielsen B, Brown S (2013) Generalized disturbance of DNA methylation in the uterine decidua in the CBA/J x DBA/2 mouse model of pregnancy failure. Biol Reprod 89:120PubMedPubMedCentralGoogle Scholar
  142. 142.
    Yu M, Du G, Xu Q, Huang Z, Huang X, Qin Y, Han L, Fan Y, Zhang Y, Han X, Jiang Z, Xia Y, Wang X, Lu C (2018) Integrated analysis of DNA methylome and transcriptome identified CREB5 as a novel risk gene contributing to recurrent pregnancy loss. EBioMedicine 35:334–344PubMedPubMedCentralGoogle Scholar
  143. 143.
    Hou W, Li Z, Li Y, Fang L, Li J, Huang J, Li X, You Z (2016) Correlation between protein expression of FOXP3 and level of FOXP3 promoter methylation in recurrent spontaneous abortion. J Obstet Gynaecol Res 42:1439–1444PubMedGoogle Scholar
  144. 144.
    Jones A, Teschendorff AE, Li Q, Hayward JD, Kannan A, Mould T, West J, Zikan M, Cibula D, Fiegl H, Lee SH, Wik E, Hadwin R, Arora R, Lemech C, Turunen H, Pakarinen P, Jacobs IJ, Salvesen HB, Bagchi MK, Bagchi IC, Widschwendter M (2013) Role of DNA methylation and epigenetic silencing of HAND2 in endometrial cancer development. PLoS Med 10:e1001551PubMedCentralGoogle Scholar
  145. 145.
    Estella C, Herrer I, Atkinson SP, Quinonero A, Martinez S, Pellicer A, Simon C (2012) Inhibition of histone deacetylase activity in human endometrial stromal cells promotes extracellular matrix remodelling and limits embryo invasion. PLoS One 7:e30508PubMedPubMedCentralGoogle Scholar
  146. 146.
    He H, Kong S, Liu F, Zhang S, Jiang Y, Liao Y, Jiang Y, Li Q, Wang B, Zhou Z, Wang H, Huo R (2015) Rbbp7 Is required for uterine stromal decidualization in mice. Biol Reprod 93:13PubMedGoogle Scholar
  147. 147.
    Tamura I, Sato S, Okada M, Tanabe M, Lee L, Maekawa R, Asada H, Yamagata Y, Tamura H, Sugino N (2014) Importance of C/EBPbeta binding and histone acetylation status in the promoter regions for induction of IGFBP-1, PRL, and Mn-SOD by cAMP in human endometrial stromal cells. Endocrinology 155:275–286Google Scholar
  148. 148.
    Tamura I, Ohkawa Y, Sato T, Suyama M, Jozaki K, Okada M, Lee L, Maekawa R, Asada H, Sato S, Yamagata Y, Tamura H, Sugino N (2014) Genome-wide analysis of histone modifications in human endometrial stromal cells. Mol Endocrinol 28:1656–1669PubMedPubMedCentralGoogle Scholar
  149. 149.
    Tamura I, Jozaki K, Sato S, Shirafuta Y, Shinagawa M, Maekawa R, Taketani T, Asada H, Tamura H, Sugino N (2018) The distal upstream region of insulin-like growth factor-binding protein-1 enhances its expression in endometrial stromal cells during decidualization. J Biol Chem 293:5270–5280PubMedPubMedCentralGoogle Scholar
  150. 150.
    Grimaldi G, Christian M, Steel JH, Henriet P, Poutanen M, Brosens JJ (2011) Down-regulation of the histone methyltransferase EZH2 contributes to the epigenetic programming of decidualizing human endometrial stromal cells. Mol Endocrinol 25:1892–1903PubMedPubMedCentralGoogle Scholar
  151. 151.
    Nancy P, Tagliani E, Tay CS, Asp P, Levy DE, Erlebacher A (2012) Chemokine gene silencing in decidual stromal cells limits T cell access to the maternal-fetal interface. Science 336:1317–1321PubMedPubMedCentralGoogle Scholar
  152. 152.
    Nancy P, Siewiera J, Rizzuto G, Tagliani E, Osokine I, Manandhar P, Dolgalev I, Clementi C, Tsirigos A, Erlebacher A (2018) H3K27me3 dynamics dictate evolving uterine states in pregnancy and parturition. J Clin Invest 128:233–247PubMedGoogle Scholar
  153. 153.
    Fang X, Ni N, Lydon JP, Ivanov I, Bayless KJ, Rijnkels M, Li Q (2019) Enhancer of Zeste 2 polycomb repressive complex 2 subunit is required for uterine epithelial integrity. Am J Pathol 189:1212–1225PubMedGoogle Scholar
  154. 154.
    Bian F, Gao F, Kartashov AV, Jegga AG, Barski A, Das SK (2016) Polycomb repressive complex 1 controls uterine decidualization. Sci Rep 6:26061PubMedPubMedCentralGoogle Scholar
  155. 155.
    Estella C, Herrer I, Moreno-Moya JM, Quinonero A, Martinez S, Pellicer A, Simon C (2012) miRNA signature and Dicer requirement during human endometrial stromal decidualization in vitro. PLoS One 7:e41080PubMedPubMedCentralGoogle Scholar
  156. 156.
    Shah KM, Webber J, Carzaniga R, Taylor DM, Fusi L, Clayton A, Brosens JJ, Hartshorne G, Christian M (2013) Induction of microRNA resistance and secretion in differentiating human endometrial stromal cells. J Mol Cell Biol 5:67–70PubMedGoogle Scholar
  157. 157.
    Zhang Q, Zhang H, Jiang Y, Xue B, Diao Z, Ding L, Zhen X, Sun H, Yan G, Hu Y (2015) MicroRNA-181a is involved in the regulation of human endometrial stromal cell decidualization by inhibiting Kruppel-like factor 12. Reprod Biol Endocrinol 13:23PubMedPubMedCentralGoogle Scholar
  158. 158.
    Tochigi H, Kajihara T, Mizuno Y, Mizuno Y, Tamaru S, Kamei Y, Okazaki Y, Brosens JJ, Ishihara O (2017) Loss of miR-542-3p enhances IGFBP-1 expression in decidualizing human endometrial stromal cells. Sci Rep 7:40001PubMedPubMedCentralGoogle Scholar
  159. 159.
    Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386–389PubMedGoogle Scholar
  160. 160.
    Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, Landsberger N, Strouboulis J, Wolffe AP (1998) Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 19:187–191PubMedGoogle Scholar
  161. 161.
    Lehnertz B, Ueda Y, Derijck AA, Braunschweig U, Perez-Burgos L, Kubicek S, Chen T, Li E, Jenuwein T, Peters AH (2003) Suv39 h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 13:1192–1200PubMedGoogle Scholar
  162. 162.
    Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, Morey L, Van Eynde A, Bernard D, Vanderwinden JM, Bollen M, Esteller M, Di Croce L, de Launoit Y, Fuks F (2006) The polycomb group protein EZH2 directly controls DNA methylation. Nature 439:871–874PubMedGoogle Scholar
  163. 163.
    Delcuve GP, Rastegar M, Davie JR (2009) Epigenetic control. J Cell Physiol 219:243–250PubMedGoogle Scholar
  164. 164.
    Januchowski R, Dabrowski M, Ofori H, Jagodzinski PP (2007) Trichostatin A down-regulate DNA methyltransferase 1 in Jurkat T cells. Cancer Lett 246:313–317PubMedGoogle Scholar
  165. 165.
    Barnhart K, Dunsmoor-Su R, Coutifaris C (2002) Effect of endometriosis on in vitro fertilization. Fertil Steril 77:1148–1155PubMedGoogle Scholar
  166. 166.
    Olive DL, Schwartz LB (1993) Endometriosis. N Engl J Med 328:1759–1769PubMedGoogle Scholar
  167. 167.
    Matsuzaki S, Canis M, Darcha C, Pouly JL, Mage G (2009) HOXA-10 expression in the mid-secretory endometrium of infertile patients with either endometriosis, uterine fibromas or unexplained infertility. Hum Reprod 24:3180–3187PubMedGoogle Scholar
  168. 168.
    Taylor HS, Bagot C, Kardana A, Olive D, Arici A (1999) HOX gene expression is altered in the endometrium of women with endometriosis. Hum Reprod 14:1328–1331PubMedGoogle Scholar
  169. 169.
    Lee B, Du H, Taylor HS (2009) Experimental murine endometriosis induces DNA methylation and altered gene expression in eutopic endometrium. Biol Reprod 80:79–85PubMedPubMedCentralGoogle Scholar
  170. 170.
    Kim JJ, Taylor HS, Lu Z, Ladhani O, Hastings JM, Jackson KS, Wu Y, Guo SW, Fazleabas AT (2007) Altered expression of HOXA10 in endometriosis: potential role in decidualization. Mol Hum Reprod 13:323–332PubMedGoogle Scholar
  171. 171.
    Szczepanska M, Wirstlein P, Luczak M, Jagodzinski PP, Skrzypczak J (2010) Reduced expression of HOXA10 in the midluteal endometrium from infertile women with minimal endometriosis. Biomed Pharmacother 64:697–705PubMedGoogle Scholar
  172. 172.
    Wu Y, Strawn E, Basir Z, Halverson G, Guo SW (2007) Aberrant expression of deoxyribonucleic acid methyltransferases DNMT1, DNMT3A, and DNMT3B in women with endometriosis. Fertil Steril 87:24–32PubMedGoogle Scholar
  173. 173.
    Wu Y, Strawn E, Basir Z, Halverson G, Guo SW (2006) Promoter hypermethylation of progesterone receptor isoform B (PR-B) in endometriosis. Epigenetics 1:106–111PubMedGoogle Scholar
  174. 174.
    Izawa M, Harada T, Taniguchi F, Ohama Y, Takenaka Y, Terakawa N (2008) An epigenetic disorder may cause aberrant expression of aromatase gene in endometriotic stromal cells. Fertil Steril 89:1390–1396PubMedGoogle Scholar
  175. 175.
    Xue Q, Lin Z, Cheng YH, Huang CC, Marsh E, Yin P, Milad MP, Confino E, Reierstad S, Innes J, Bulun SE (2007) Promoter methylation regulates estrogen receptor 2 in human endometrium and endometriosis. Biol Reprod 77:681–687PubMedGoogle Scholar
  176. 176.
    Colon-Diaz M, Baez-Vega P, Garcia M, Ruiz A, Monteiro JB, Fourquet J, Bayona M, Alvarez-Garriga C, Achille A, Seto E, Flores I (2012) HDAC1 and HDAC2 are differentially expressed in endometriosis. Reprod Sci 19:483–492PubMedPubMedCentralGoogle Scholar
  177. 177.
    Monteiro JB, Colon-Diaz M, Garcia M, Gutierrez S, Colon M, Seto E, Laboy J, Flores I (2014) Endometriosis is characterized by a distinct pattern of histone 3 and histone 4 lysine modifications. Reprod Sci 21:305–318PubMedPubMedCentralGoogle Scholar
  178. 178.
    Colon-Caraballo M, Monteiro JB, Flores I (2015) H3K27me3 is an epigenetic mark of relevance in endometriosis. Reprod Sci 22:1134–1142PubMedPubMedCentralGoogle Scholar
  179. 179.
    Rackow BW, Jorgensen E, Taylor HS (2011) Endometrial polyps affect uterine receptivity. Fertil Steril 95:2690–2692PubMedPubMedCentralGoogle Scholar
  180. 180.
    Kulp JL, Mamillapalli R, Taylor HS (2016) Aberrant HOXA10 methylation in patients with common gynecologic disorders: implications for reproductive outcomes. Reprod Sci 23:455–463PubMedPubMedCentralGoogle Scholar
  181. 181.
    Daftary GS, Taylor HS (2002) Hydrosalpinx fluid diminishes endometrial cell HOXA10 expression. Fertil Steril 78:577–580PubMedGoogle Scholar
  182. 182.
    Saito T, Nishimura M, Yamasaki H, Kudo R (2003) Hypermethylation in promoter region of E-cadherin gene is associated with tumor dedifferention and myometrial invasion in endometrial carcinoma. Cancer 97:1002–1009PubMedGoogle Scholar
  183. 183.
    Memczak S, Papavasileiou P, Peters O, Rajewsky N (2015) Identification and characterization of circular RNAs as a new class of putative biomarkers in human blood. PLoS One 10:e0141214PubMedPubMedCentralGoogle Scholar
  184. 184.
    Li MQ, Yao MN, Yan JQ, Li ZL, Gu XW, Lin S, Hu W, Yang ZM (2017) The decline of pregnancy rate and abnormal uterine responsiveness of steroid hormones in aging mice. Reprod Biol 17:305–311PubMedGoogle Scholar
  185. 185.
    Woods L, Perez-Garcia V, Kieckbusch J, Wang X, DeMayo F, Colucci F, Hemberger M (2017) Decidualisation and placentation defects are a major cause of age-related reproductive decline. Nat Commun 8:352PubMedPubMedCentralGoogle Scholar
  186. 186.
    Jefferson WN, Chevalier DM, Phelps JY, Cantor AM, Padilla-Banks E, Newbold RR, Archer TK, Kinyamu HK, Williams CJ (2013) Persistently altered epigenetic marks in the mouse uterus after neonatal estrogen exposure. Mol Endocrinol 27:1666–1677PubMedPubMedCentralGoogle Scholar
  187. 187.
    Franczak A, Zglejc K, Waszkiewicz E, Wojciechowicz B, Martyniak M, Sobotka W, Okrasa S, Kotwica G (2017) Periconceptional undernutrition affects in utero methyltransferase expression and steroid hormone concentrations in uterine flushings and blood plasma during the peri-implantation period in domestic pigs. Reprod Fertil Dev 29:1499–1508PubMedGoogle Scholar
  188. 188.
    Zglejc K, Franczak A (2017) Peri-conceptional under-nutrition alters the expression of TRIM28 and ZFP57 in the endometrium and embryos during peri-implantation period in domestic pigs. Reprod Domest Anim 52:542–550PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Shuangbo Kong
    • 1
    • 2
  • Chan Zhou
    • 2
  • Haili Bao
    • 2
  • Zhangli Ni
    • 2
  • Mengying Liu
    • 2
  • Bo He
    • 2
  • Lin Huang
    • 1
    • 2
  • Yang Sun
    • 1
    • 2
  • Haibin Wang
    • 1
    • 2
    Email author
  • Jinhua Lu
    • 1
    • 2
    Email author
  1. 1.Reproductive Medical CenterThe First Affiliated Hospital of Xiamen UniversityXiamenPeople’s Republic of China
  2. 2.Fujian Provincial Key Laboratory of Reproductive Health Research, School of MedicineXiamen UniversityXiamenPeople’s Republic of China

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