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International Journal of Genomics
Volume 2018 (2018), Article ID 1465348, 13 pages
https://doi.org/10.1155/2018/1465348
Review Article

Endometriosis Malignant Transformation: Epigenetics as a Probable Mechanism in Ovarian Tumorigenesis

The Second Hospital of Jilin University, Jilin, Changchun 130041, China

Correspondence should be addressed to Tianmin Xu; moc.621@nimnaitux

Received 27 December 2017; Accepted 1 March 2018; Published 27 March 2018

Academic Editor: Changwon Park

Copyright © 2018 Jiaxing He et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. Vercellini, P. Viganò, E. Somigliana, and L. Fedele, “Endometriosis: pathogenesis and treatment,” Nature Reviews Endocrinology, vol. 10, no. 5, pp. 261–275, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. P. Viganò, F. Parazzini, E. Somigliana, and P. Vercellini, “Endometriosis: epidemiology and aetiological factors,” Best Practice & Research Clinical Obstetrics & Gynaecology, vol. 18, no. 2, pp. 177–200, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. H. S. Kim, T. H. Kim, H. H. Chung, and Y. S. Song, “Risk and prognosis of ovarian cancer in women with endometriosis: a meta-analysis,” British Journal of Cancer, vol. 110, no. 7, pp. 1878–1890, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. V. H. Eisenberg, C. Weil, G. Chodick, and V. Shalev, “Epidemiology of endometriosis: a large population-based database study from a healthcare provider with 2 million members,” BJOG: An International Journal of Obstetrics & Gynaecology, vol. 125, no. 1, pp. 55–62, 2018. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Siufi Neto, R. M. Kho, D. F. dos Santos Siufi, E. C. Baracat, K. S. Anderson, and M. S. Abrão, “Cellular, histologic, and molecular changes associated with endometriosis and ovarian cancer,” The Journal of Minimally Invasive Gynecology, vol. 21, no. 1, pp. 55–63, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. P. S. Munksgaard and J. Blaakaer, “The association between endometriosis and ovarian cancer: a review of histological, genetic and molecular alterations,” Gynecologic Oncology, vol. 124, no. 1, pp. 164–169, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. J. A. Sampson, “Endometrial carcinoma of the ovary, arising in endometrial tissue in that organ,” Archives of Surgery, vol. 10, no. 1, pp. 1–72, 1925. View at Publisher · View at Google Scholar
  8. A. Melin, P. Sparen, and A. Bergqvist, “The risk of cancer and the role of parity among women with endometriosis,” Human Reproduction, vol. 22, no. 11, pp. 3021–3026, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. C. A. Barton, N. F. Hacker, S. J. Clark, and P. M. O'Brien, “DNA methylation changes in ovarian cancer: implications for early diagnosis, prognosis and treatment,” Gynecologic Oncology, vol. 109, no. 1, pp. 129–139, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. F. W. Grimstad and A. Decherney, “A review of the epigenetic contributions to endometriosis,” Clinical Obstetrics and Gynecology, vol. 60, no. 3, pp. 467–476, 2017. View at Publisher · View at Google Scholar · View at Scopus
  11. B. Borghese, K. T. Zondervan, M. S. Abrao, C. Chapron, and D. Vaiman, “Recent insights on the genetics and epigenetics of endometriosis,” Clinical Genetics, vol. 91, no. 2, pp. 254–264, 2017. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Gordts, P. Koninckx, and I. Brosens, “Pathogenesis of deep endometriosis,” Fertility and Sterility, vol. 108, no. 6, pp. 872–885.e1, 2017. View at Publisher · View at Google Scholar · View at Scopus
  13. H. J. Smith, J. M. Straughn, D. J. Buchsbaum, and R. C. Arend, “Epigenetic therapy for the treatment of epithelial ovarian cancer: a clinical review,” Gynecologic Oncology Reports, vol. 20, pp. 81–86, 2017. View at Publisher · View at Google Scholar · View at Scopus
  14. O. Koukoura, S. Sifakis, and D. A. Spandidos, “DNA methylation in endometriosis (review),” Molecular Medicine Reports, vol. 13, no. 4, pp. 2939–2948, 2016. View at Publisher · View at Google Scholar · View at Scopus
  15. J. Sandoval and M. Esteller, “Cancer epigenomics: beyond genomics,” Current Opinion in Genetics & Development, vol. 22, no. 1, pp. 50–55, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. L. Maldonado and M. O. Hoque, “Epigenomics and ovarian carcinoma,” Biomarkers in Medicine, vol. 4, no. 4, pp. 543–570, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. H. T. Nguyen, G. Tian, and M. M. Murph, “Molecular epigenetics in the management of ovarian cancer: are we investigating a rational clinical promise?” Frontiers in Oncology, vol. 4, p. 71, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Guo, F. Ren, D. Wang et al., “RUNX3 is inactivated by promoter hypermethylation in malignant transformation of ovarian endometriosis,” Oncology Reports, vol. 32, no. 6, pp. 2580–2588, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. F. Ren, D. Wang, Y. Jiang, and F. Ren, “Epigenetic inactivation of hMLH1 in the malignant transformation of ovarian endometriosis,” Archives of Gynecology and Obstetrics, vol. 285, no. 1, pp. 215–221, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. Y. Li, D. An, Y. X. Guan, and S. Kang, “Aberrant methylation of the E-cadherin gene promoter region in endometrium and ovarian endometriotic cysts of patients with ovarian endometriosis,” Gynecologic and Obstetric Investigation, vol. 82, no. 1, pp. 78–85, 2017. View at Publisher · View at Google Scholar · View at Scopus
  21. F. Ren, D. B. Wang, T. Li, Y. H. Chen, and Y. Li, “Identification of differentially methylated genes in the malignant transformation of ovarian endometriosis,” Journal of Ovarian Research, vol. 7, no. 1, p. 73, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Martini, M. Ciccarone, G. Garganese et al., “Possible involvement of hMLH1, p16INK4a and PTEN in the malignant transformation of endometriosis,” International Journal of Cancer, vol. 102, no. 4, pp. 398–406, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Senthong, N. Kitkumthorn, P. Rattanatanyong, N. Khemapech, S. Triratanachart, and A. Mutirangura, “Differences in LINE-1 methylation between endometriotic ovarian cyst and endometriosis-associated ovarian cancer,” International Journal of Gynecological Cancer, vol. 24, no. 1, pp. 36–42, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. H. Zhou, J. Li, K. Podratz et al., “Hypomethylation and activation of syncytin-1 gene in endometriotic tissue,” Current Pharmaceutical Design, vol. 20, no. 11, pp. 1786–1795, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. K. C. Wiegand, S. P. Shah, O. M. al-Agha et al., “ARID1A mutations in endometriosis-associated ovarian carcinomas,” The New England Journal of Medicine, vol. 363, no. 16, pp. 1532–1543, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. R. Lakshminarasimhan, C. Andreu-Vieyra, K. Lawrenson et al., “Down-regulation of ARID1A is sufficient to initiate neoplastic transformation along with epigenetic reprogramming in non-tumorigenic endometriotic cells,” Cancer Letters, vol. 401, pp. 11–19, 2017. View at Publisher · View at Google Scholar · View at Scopus
  27. X. Zhang, Q. Sun, M. Shan et al., “Promoter hypermethylation of ARID1A gene is responsible for its low mRNA expression in many invasive breast cancers,” PLoS One, vol. 8, no. 1, article e53931, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. L. C. Giudice and L. C. Kao, “Endometriosis,” The Lancet, vol. 364, no. 9447, pp. 1789–1799, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Jia, K. Dahlman-Wright, and J.-Å. Gustafsson, “Estrogen receptor alpha and beta in health and disease,” Best Practice & Research Clinical Endocrinology & Metabolism, vol. 29, no. 4, pp. 557–568, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Cavallini, L. Resta, A. M. Caringella, E. Dinaro, C. Lippolis, and G. Loverro, “Involvement of estrogen receptor-related receptors in human ovarian endometriosis,” Fertility and Sterility, vol. 96, no. 1, pp. 102–106, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. Q. Xue, Z. Lin, Y. H. Cheng et al., “Promoter methylation regulates estrogen receptor 2 in human endometrium and endometriosis,” Biology of Reproduction, vol. 77, no. 4, pp. 681–687, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. I. Kyriakidis and P. Papaioannidou, “Estrogen receptor beta and ovarian cancer: a key to pathogenesis and response to therapy,” Archives of Gynecology and Obstetrics, vol. 293, no. 6, pp. 1161–1168, 2016. View at Publisher · View at Google Scholar · View at Scopus
  33. J. L. Meyer, D. Zimbardi, S. Podgaec, R. L. Amorim, M. S. Abrão, and C. A. Rainho, “DNA methylation patterns of steroid receptor genes ESR1, ESR2 and PGR in deep endometriosis compromising the rectum,” International Journal of Molecular Medicine, vol. 33, no. 4, pp. 897–904, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. V. Toderow, M. Rahmeh, S. Hofmann et al., “Promotor analysis of ESR1 in endometrial cancer cell lines, endometrial and endometriotic tissue,” Archives of Gynecology and Obstetrics, vol. 296, no. 2, pp. 269–276, 2017. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Bardin, N. Boulle, G. Lazennec, F. Vignon, and P. Pujol, “Loss of ERβ expression as a common step in estrogen-dependent tumor progression,” Endocrine-Related Cancer, vol. 11, no. 3, pp. 537–551, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Y. Jeon, K. A. Hwang, and K. C. Choi, “Effect of steroid hormones, estrogen and progesterone, on epithelial mesenchymal transition in ovarian cancer development,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 158, pp. 1–8, 2016. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Ciucci, G. F. Zannoni, M. Buttarelli et al., “Multiple direct and indirect mechanisms drive estrogen-induced tumor growth in high grade serous ovarian cancers,” Oncotarget, vol. 7, no. 7, pp. 8155–8171, 2016. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Yamaguchi, Z. Huang, N. Matsumura et al., “Epigenetic determinants of ovarian clear cell carcinoma biology,” International Journal of Cancer, vol. 135, no. 3, pp. 585–597, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. M. J. Worley Jr., S. Liu, Y. Hua et al., “Molecular changes in endometriosis-associated ovarian clear cell carcinoma,” European Journal of Cancer, vol. 51, no. 13, pp. 1831–1842, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Matsuzaki, M. Canis, C. Darcha, P. J. Déchelotte, J. L. Pouly, and G. Mage, “Expression of WT1 is down-regulated in eutopic endometrium obtained during the midsecretory phase from patients with endometriosis,” Fertility and Sterility, vol. 86, no. 3, pp. 554–558, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Akahane, A. Sekizawa, T. Okuda, M. Kushima, H. Saito, and T. Okai, “Disappearance of steroid hormone dependency during malignant transformation of ovarian clear cell cancer,” International Journal of Gynecological Pathology, vol. 24, no. 4, pp. 369–376, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. J. J. Brosens, M. S. C. Wilson, and E. W.-F. Lam, “FOXO transcription factors: from cell fate decisions to regulation of human female reproduction,” Advances in Experimental Medicine and Biology, vol. 665, pp. 227–241, 2009. View at Publisher · View at Google Scholar
  43. M. Al-Sabbagh, E. W.-F. Lam, and J. J. Brosens, “Mechanisms of endometrial progesterone resistance,” Molecular and Cellular Endocrinology, vol. 358, no. 2, pp. 208–215, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Hayashi, A. Tanabe, S. Kawabe et al., “Dienogest increases the progesterone receptor isoform B/A ratio in patients with ovarian endometriosis,” Journal of Ovarian Research, vol. 5, no. 1, p. 31, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Fazleabas, “Progesterone resistance in a baboon model of endometriosis,” Seminars in Reproductive Medicine, vol. 28, no. 1, pp. 075–080, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Nie, X. Liu, and S.-W. Guo, “Promoter hypermethylation of progesterone receptor isoform B (PR-B) in adenomyosis and its rectification by a histone deacetylase inhibitor and a demethylation agent,” Reproductive Sciences, vol. 17, no. 11, pp. 995–1005, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Li, M. K. Adur, A. Kannan et al., “Progesterone alleviates endometriosis via inhibition of uterine cell proliferation, inflammation and angiogenesis in an immunocompetent mouse model,” PLoS One, vol. 11, no. 10, article e0165347, 2016. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Böhm, W. J. Locke, R. L. Sutherland, J. G. Kench, and S. M. Henshall, “A role for GATA-2 in transition to an aggressive phenotype in prostate cancer through modulation of key androgen-regulated genes,” Oncogene, vol. 28, no. 43, pp. 3847–3856, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. 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 Expression Patterns, vol. 12, no. 5-6, pp. 196–203, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. M. G. del Carmen, A. E. Smith Sehdev, A. N. Fader et al., “Endometriosis-associated ovarian carcinoma: differential expression of vascular endothelial growth factor and estrogen/progesterone receptors,” Cancer, vol. 98, no. 8, pp. 1658–1663, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Pazhohan, F. Amidi, F. Akbari-Asbagh et al., “The Wnt/β-catenin signaling in endometriosis, the expression of total and active forms of β-catenin, total and inactive forms of glycogen synthase kinase-3β, WNT7a and DICKKOPF-1,” European Journal of Obstetrics & Gynecology and Reproductive Biology, vol. 220, pp. 1–5, 2018. View at Publisher · View at Google Scholar · View at Scopus
  52. J. A. MacLean, M. L. King, H. Okuda, and K. Hayashi, “WNT7A regulation by miR-15b in ovarian cancer,” PLoS One, vol. 11, no. 5, article e0156109, 2016. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Yoshioka, M. L. King, S. Ran et al., “WNT7A regulates tumor growth and progression in ovarian cancer through the WNT/β-catenin pathway,” Molecular Cancer Research, vol. 10, no. 3, pp. 469–482, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. M. L. King, M. E. Lindberg, G. R. Stodden et al., “WNT7A/β-catenin signaling induces FGF1 and influences sensitivity to niclosamide in ovarian cancer,” Oncogene, vol. 34, no. 26, pp. 3452–3462, 2015. View at Publisher · View at Google Scholar · View at Scopus
  55. Z. Deng, L. Wang, H. Hou, J. Zhou, and X. Li, “Epigenetic regulation of IQGAP2 promotes ovarian cancer progression via activating Wnt/β-catenin signaling,” International Journal of Oncology, vol. 48, no. 1, pp. 153–160, 2016. View at Publisher · View at Google Scholar · View at Scopus
  56. H. Y. Su, H. C. Lai, Y. W. Lin et al., “Epigenetic silencing of SFRP5 is related to malignant phenotype and chemoresistance of ovarian cancer through Wnt signaling pathway,” International Journal of Cancer, vol. 127, no. 3, pp. 555–567, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Alizadeh, S. Mahjoub, S. Esmaelzadeh, K. Hajian, Z. Basirat, and M. Ghasemi, “Evaluation of oxidative stress in endometriosis: a case-control study,” Caspian Journal of Internal Medicine, vol. 6, no. 1, pp. 25–29, 2015. View at Google Scholar
  58. J. Donnez, M. M. Binda, O. Donnez, and M. M. Dolmans, “Oxidative stress in the pelvic cavity and its role in the pathogenesis of endometriosis,” Fertility and Sterility, vol. 106, no. 5, pp. 1011–1017, 2016. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Van Langendonckt, F. Casanas-Roux, and J. Donnez, “Oxidative stress and peritoneal endometriosis,” Fertility and Sterility, vol. 77, no. 5, pp. 861–870, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. F. Ito, Y. Yamada, A. Shigemitsu et al., “Role of oxidative stress in epigenetic modification in endometriosis,” Reproductive Sciences, vol. 24, no. 11, pp. 1493–1502, 2017. View at Publisher · View at Google Scholar · View at Scopus
  61. H. Xie, P. Chen, H. W. Huang, L. P. Liu, and F. Zhao, “Reactive oxygen species downregulate ARID1A expression via its promoter methylation during the pathogenesis of endometriosis,” European Review for Medical and Pharmacological Sciences, vol. 21, no. 20, pp. 4509–4515, 2017. View at Google Scholar
  62. F. J. Roca, H. A. Loomans, A. T. Wittman, C. J. Creighton, and S. M. Hawkins, “Ten-eleven translocation genes are downregulated in endometriosis,” Current Molecular Medicine, vol. 16, no. 3, pp. 288–298, 2016. View at Publisher · View at Google Scholar · View at Scopus
  63. A. V. Bhat, S. Hora, A. Pal, S. Jha, and R. Taneja, “Stressing the (epi)genome: dealing with reactive oxygen species in cancer,” Antioxidants & Redox Signaling, 2017. View at Publisher · View at Google Scholar
  64. J. Zhong, L. Ji, H. Chen et al., “Acetylation of hMOF modulates H4K16ac to regulate DNA repair genes in response to oxidative stress,” International Journal of Biological Sciences, vol. 13, no. 7, pp. 923–934, 2017. View at Publisher · View at Google Scholar · View at Scopus
  65. X. Gao, X. Gào, Y. Zhang, L. P. Breitling, B. Schöttker, and H. Brenner, “Associations of self-reported smoking, cotinine levels and epigenetic smoking indicators with oxidative stress among older adults: a population-based study,” European Journal of Epidemiology, vol. 32, no. 5, pp. 443–456, 2017. View at Publisher · View at Google Scholar · View at Scopus
  66. T. Maser, M. Rich, D. Hayes et al., “Tolcapone induces oxidative stress leading to apoptosis and inhibition of tumor growth in neuroblastoma,” Cancer Medicine, vol. 6, no. 6, pp. 1341–1352, 2017. View at Publisher · View at Google Scholar · View at Scopus
  67. W. Li, Y. Guo, C. Zhang et al., “Dietary phytochemicals and cancer chemoprevention: a perspective on oxidative stress, inflammation, and epigenetics,” Chemical Research in Toxicology, vol. 29, no. 12, pp. 2071–2095, 2016. View at Publisher · View at Google Scholar · View at Scopus
  68. R. Zhang, K. A. Kang, K. C. Kim et al., “Oxidative stress causes epigenetic alteration of CDX1 expression in colorectal cancer cells,” Gene, vol. 524, no. 2, pp. 214–219, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. M. Hou, X. Zuo, C. Li, Y. Zhang, and Y. Teng, “miR-29b regulates oxidative stress by targeting SIRT1 in ovarian cancer cells,” Cellular Physiology and Biochemistry, vol. 43, no. 5, pp. 1767–1776, 2017. View at Publisher · View at Google Scholar · View at Scopus
  70. P. K. Mahalingaiah, L. Ponnusamy, and K. P. Singh, “Oxidative stress-induced epigenetic changes associated with malignant transformation of human kidney epithelial cells,” Oncotarget, vol. 8, no. 7, pp. 11127–11143, 2017. View at Publisher · View at Google Scholar · View at Scopus
  71. M. A. Dawson and T. Kouzarides, “Cancer epigenetics: from mechanism to therapy,” Cell, vol. 150, no. 1, pp. 12–27, 2012. View at Publisher · View at Google Scholar · View at Scopus
  72. M. Esteller, “Cancer epigenomics: DNA methylomes and histone-modification maps,” Nature Reviews Genetics, vol. 8, no. 4, pp. 286–298, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. D. Schübeler, D. M. MacAlpine, D. Scalzo et al., “The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote,” Genes & Development, vol. 18, no. 11, pp. 1263–1271, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. C. Martin and Y. Zhang, “The diverse functions of histone lysine methylation,” Nature Reviews Molecular Cell Biology, vol. 6, no. 11, pp. 838–849, 2005. View at Publisher · View at Google Scholar · View at Scopus
  75. H. A. LaVoie, “Epigenetic control of ovarian function: the emerging role of histone modifications,” Molecular and Cellular Endocrinology, vol. 243, no. 1-2, pp. 12–18, 2005. View at Publisher · View at Google Scholar · View at Scopus
  76. D. J. Marsh, J. S. Shah, and A. J. Cole, “Histones and their modifications in ovarian cancer—drivers of disease and therapeutic targets,” Frontiers in Oncology, vol. 4, p. 144, 2014. View at Publisher · View at Google Scholar · View at Scopus
  77. A. Hayashi, A. Horiuchi, N. Kikuchi et al., “Type-specific roles of histone deacetylase (HDAC) overexpression in ovarian carcinoma: HDAC1 enhances cell proliferation and HDAC3 stimulates cell migration with downregulation of e-cadherin,” International Journal of Cancer, vol. 127, no. 6, pp. 1332–1346, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. W. Weichert, “HDAC expression and clinical prognosis in human malignancies,” Cancer Letters, vol. 280, no. 2, pp. 168–176, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. S. Ropero and M. Esteller, “The role of histone deacetylases (HDACs) in human cancer,” Molecular Oncology, vol. 1, no. 1, pp. 19–25, 2007. View at Publisher · View at Google Scholar · View at Scopus
  80. K. Y. Jang, K. S. Kim, S. H. Hwang et al., “Expression and prognostic significance of SIRT1 in ovarian epithelial tumours,” Pathology, vol. 41, no. 4, pp. 366–371, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. X. Xiaomeng, Z. Ming, M. Jiezhi, and F. Xiaoling, “Aberrant histone acetylation and methylation levels in woman with endometriosis,” Archives of Gynecology and Obstetrics, vol. 287, no. 3, pp. 487–494, 2013. View at Publisher · View at Google Scholar · View at Scopus
  82. M. Colón-Díaz, P. Báez-Vega, M. García et al., “HDAC1 and HDAC2 are differentially expressed in endometriosis,” Reproductive Sciences, vol. 19, no. 5, pp. 483–492, 2012. View at Publisher · View at Google Scholar · View at Scopus
  83. J. Guo, J. Cai, L. Yu, H. Tang, C. Chen, and Z. Wang, “EZH2 regulates expression of p57 and contributes to progression of ovarian cancer in vitro and in vivo,” Cancer Science, vol. 102, no. 3, pp. 530–539, 2011. View at Publisher · View at Google Scholar · View at Scopus
  84. Y. Kuang, F. Lu, J. Guo et al., “Histone demethylase KDM2B upregulates histone methyltransferase EZH2 expression and contributes to the progression of ovarian cancer in vitro and in vivo,” OncoTargets and Therapy, vol. 10, pp. 3131–3144, 2017. View at Publisher · View at Google Scholar · View at Scopus
  85. P. H. Abbosh, J. S. Montgomery, J. A. Starkey et al., “Dominant-negative histone H3 lysine 27 mutant derepresses silenced tumor suppressor genes and reverses the drug-resistant phenotype in cancer cells,” Cancer Research, vol. 66, no. 11, pp. 5582–5591, 2006. View at Publisher · View at Google Scholar · View at Scopus
  86. J. H. Hurst, N. Mendpara, and S. B. Hooks, “Regulator of G-protein signalling expression and function in ovarian cancer cell lines,” Cellular and Molecular Biology Letters, vol. 14, no. 1, pp. 153–174, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. E. Cacan, “Epigenetic regulation of RGS2 (regulator of G-protein signaling 2) in chemoresistant ovarian cancer cells,” Journal of Chemotherapy, vol. 29, no. 3, pp. 173–178, 2017. View at Publisher · View at Google Scholar · View at Scopus
  88. L. Schulke, M. Berbic, F. Manconi, N. Tokushige, R. Markham, and I. S. Fraser, “Dendritic cell populations in the eutopic and ectopic endometrium of women with endometriosis,” Human Reproduction, vol. 24, no. 7, pp. 1695–1703, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. I. Jeung, K. Cheon, and M. R. Kim, “Decreased cytotoxicity of peripheral and peritoneal natural killer cell in endometriosis,” BioMed Research International, vol. 2016, Article ID 2916070, 6 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  90. E. Oral, D. L. Olive, and A. Arici, “The peritoneal environment in endometriosis,” Human Reproduction Update, vol. 2, no. 5, pp. 385–398, 1996. View at Publisher · View at Google Scholar · View at Scopus
  91. S. Mahdian, R. Aflatoonian, R. S. Yazdi et al., “Macrophage migration inhibitory factor as a potential biomarker of endometriosis,” Fertility and Sterility, vol. 103, no. 1, pp. 153–159.e3, 2015. View at Publisher · View at Google Scholar · View at Scopus
  92. C. M. Kyama, L. Overbergh, A. Mihalyi et al., “Endometrial and peritoneal expression of aromatase, cytokines, and adhesion factors in women with endometriosis,” Fertility and Sterility, vol. 89, no. 2, pp. 301–310, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. D. Hornung, I. P. Ryan, V. A. Chao, J. L. Vigne, E. D. Schriock, and R. N. Taylor, “Immunolocalization and regulation of the chemokine RANTES in human endometrial and endometriosis tissues and cells,” The Journal of Clinical Endocrinology & Metabolism, vol. 82, no. 5, pp. 1621–1628, 1997. View at Publisher · View at Google Scholar
  94. X. J. Yang, J. Yang, Z. Liu, G. Yang, and Z. J. Shen, “Telocytes damage in endometriosis-affected rat oviduct and potential impact on fertility,” Journal of Cellular and Molecular Medicine, vol. 19, no. 2, pp. 452–462, 2015. View at Publisher · View at Google Scholar · View at Scopus
  95. S. Yoshida, T. Harada, T. Iwabe et al., “A combination of interleukin-6 and its soluble receptor impairs sperm motility: implications in infertility associated with endometriosis,” Human Reproduction, vol. 19, no. 8, pp. 1821–1825, 2004. View at Publisher · View at Google Scholar · View at Scopus
  96. E. Hosseini, F. Mehraein, M. Shahhoseini et al., “Epigenetic alterations of CYP19A1 gene in Cumulus cells and its relevance to infertility in endometriosis,” Journal of Assisted Reproduction and Genetics, vol. 33, no. 8, pp. 1105–1113, 2016. View at Publisher · View at Google Scholar · View at Scopus
  97. Y. Tao, Q. Zhang, W. Huang, H. L. Zhu, D. Zhang, and W. Luo, “The peritoneal leptin, MCP-1 and TNF-α in the pathogenesis of endometriosis-associated infertility,” American Journal of Reproductive Immunology, vol. 65, no. 4, pp. 403–406, 2011. View at Publisher · View at Google Scholar · View at Scopus
  98. N. Rathore, A. Kriplani, R. K. Yadav, U. Jaiswal, and R. Netam, “Distinct peritoneal fluid ghrelin and leptin in infertile women with endometriosis and their correlation with interleukin-6 and vascular endothelial growth factor,” Gynecological Endocrinology, vol. 30, no. 9, pp. 671–675, 2014. View at Publisher · View at Google Scholar · View at Scopus
  99. H. Kobayashi, Y. Higashiura, H. Shigetomi, and H. Kajihara, “Pathogenesis of endometriosis: the role of initial infection and subsequent sterile inflammation (review),” Molecular Medicine Reports, vol. 9, no. 1, pp. 9–15, 2014. View at Publisher · View at Google Scholar · View at Scopus
  100. B. D. McKinnon, D. Bertschi, N. A. Bersinger, and M. D. Mueller, “Inflammation and nerve fiber interaction in endometriotic pain,” Trends in Endocrinology & Metabolism, vol. 26, no. 1, pp. 1–10, 2015. View at Publisher · View at Google Scholar · View at Scopus
  101. J. Sikora, M. Smycz-Kubańska, A. Mielczarek-Palacz, and Z. Kondera-Anasz, “Abnormal peritoneal regulation of chemokine activation—the role of IL-8 in pathogenesis of endometriosis,” American Journal of Reproductive Immunology, vol. 77, no. 4, 2017. View at Publisher · View at Google Scholar · View at Scopus
  102. N. Malhotra, D. Karmakar, V. Tripathi, K. Luthra, and S. Kumar, “Correlation of angiogenic cytokines-leptin and IL-8 in stage, type and presentation of endometriosis,” Gynecological Endocrinology, vol. 28, no. 3, pp. 224–227, 2012. View at Publisher · View at Google Scholar · View at Scopus
  103. M. Ulukus, E. C. Ulukus, E. N. Tavmergen Goker, E. Tavmergen, W. Zheng, and A. Arici, “Expression of interleukin-8 and monocyte chemotactic protein 1 in women with endometriosis,” Fertility and Sterility, vol. 91, no. 3, pp. 687–693, 2009. View at Publisher · View at Google Scholar · View at Scopus
  104. J. L. Herington, K. L. Bruner-Tran, J. A. Lucas, and K. G. Osteen, “Immune interactions in endometriosis,” Expert Review of Clinical Immunology, vol. 7, no. 5, pp. 611–626, 2011. View at Publisher · View at Google Scholar · View at Scopus
  105. H. Cakmak, O. Guzeloglu-Kayisli, U. A. Kayisli, and A. Arici, “Immune-endocrine interactions in endometriosis,” Frontiers in Bioscience (Elite Edition), vol. 1, pp. 429–443, 2009. View at Google Scholar
  106. H. R. Gatla, Y. Zou, M. M. Uddin, and I. Vancurova, “Epigenetic regulation of interleukin-8 expression by class I HDAC and CBP in ovarian cancer cells,” Oncotarget, vol. 8, no. 41, pp. 70798–70810, 2017. View at Publisher · View at Google Scholar · View at Scopus
  107. H. R. Gatla, Y. Zou, M. M. Uddin et al., “Histone deacetylase (HDAC) inhibition induces IκB kinase (IKK)-dependent interleukin-8/CXCL8 expression in ovarian cancer cells,” Journal of Biological Chemistry, vol. 292, no. 12, pp. 5043–5054, 2017. View at Publisher · View at Google Scholar · View at Scopus
  108. R. Schickel, B. Boyerinas, S. M. Park, and M. E. Peter, “MicroRNAs: key players in the immune system, differentiation, tumorigenesis and cell death,” Oncogene, vol. 27, no. 45, pp. 5959–5974, 2008. View at Publisher · View at Google Scholar · View at Scopus
  109. J. D. Kuhlmann, J. Rasch, P. Wimberger, and S. Kasimir-Bauer, “MicroRNA and the pathogenesis of ovarian cancer—a new horizon for molecular diagnostics and treatment?” Clinical Chemistry and Laboratory Medicine, vol. 50, no. 4, pp. 601–615, 2012. View at Publisher · View at Google Scholar · View at Scopus
  110. R. C. Lee, R. L. Feinbaum, and V. Ambros, “The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14,” Cell, vol. 75, no. 5, pp. 843–854, 1993. View at Publisher · View at Google Scholar · View at Scopus
  111. Y. Wang and R. Blelloch, “Cell cycle regulation by microRNAs in stem cells,” Results and Problems in Cell Differentiation, vol. 53, pp. 459–472, 2011. View at Publisher · View at Google Scholar · View at Scopus
  112. M. Carleton, M. A. Cleary, and P. S. Linsley, “MicroRNAs and cell cycle regulation,” Cell Cycle, vol. 6, no. 17, pp. 2127–2132, 2007. View at Publisher · View at Google Scholar · View at Scopus
  113. S. Oliveto, M. Mancino, N. Manfrini, and S. Biffo, “Role of microRNAs in translation regulation and cancer,” World Journal of Biological Chemistry, vol. 8, no. 1, pp. 45–56, 2017. View at Publisher · View at Google Scholar
  114. N. Li, B. Long, W. Han, S. Yuan, and K. Wang, “MicroRNAs: important regulators of stem cells,” Stem Cell Research & Therapy, vol. 8, no. 1, p. 110, 2017. View at Publisher · View at Google Scholar · View at Scopus
  115. Y. Lee, M. Kim, J. Han et al., “MicroRNA genes are transcribed by RNA polymerase II,” The EMBO Journal, vol. 23, no. 20, pp. 4051–4060, 2004. View at Publisher · View at Google Scholar · View at Scopus
  116. S. M. Hammond, “An overview of microRNAs,” Advanced Drug Delivery Reviews, vol. 87, pp. 3–14, 2015. View at Publisher · View at Google Scholar · View at Scopus
  117. M. Ha and V. N. Kim, “Regulation of microRNA biogenesis,” Nature Reviews Molecular Cell Biology, vol. 15, no. 8, pp. 509–524, 2014. View at Publisher · View at Google Scholar · View at Scopus
  118. G. Pampalakis, E. P. Diamandis, D. Katsaros, and G. Sotiropoulou, “Down-regulation of dicer expression in ovarian cancer tissues,” Clinical Biochemistry, vol. 43, no. 3, pp. 324–327, 2010. View at Publisher · View at Google Scholar · View at Scopus
  119. W. M. Merritt, Y. G. Lin, L. Y. Han et al., “Dicer, Drosha, and outcomes in patients with ovarian cancer,” The New England Journal of Medicine, vol. 359, no. 25, pp. 2641–2650, 2008. View at Publisher · View at Google Scholar · View at Scopus
  120. M. V. Iorio, R. Visone, G. di Leva et al., “MicroRNA signatures in human ovarian cancer,” Cancer Research, vol. 67, no. 18, pp. 8699–8707, 2007. View at Publisher · View at Google Scholar · View at Scopus
  121. A. E. Pasquinelli, B. J. Reinhart, F. Slack et al., “Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA,” Nature, vol. 408, no. 6808, pp. 86–89, 2000. View at Publisher · View at Google Scholar · View at Scopus
  122. S. Shell, S. M. Park, A. R. Radjabi et al., “Let-7 expression defines two differentiation stages of cancer,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 27, pp. 11400–11405, 2007. View at Publisher · View at Google Scholar · View at Scopus
  123. N. Yang, S. Kaur, S. Volinia et al., “MicroRNA microarray identifies Let-7i as a novel biomarker and therapeutic target in human epithelial ovarian cancer,” Cancer Research, vol. 68, no. 24, pp. 10307–10314, 2008. View at Publisher · View at Google Scholar · View at Scopus
  124. H. Lee, C. Park, G. Deftereos et al., “MicroRNA expression in ovarian carcinoma and its correlation with clinicopathological features,” World Journal of Surgical Oncology, vol. 10, no. 1, p. 174, 2012. View at Publisher · View at Google Scholar · View at Scopus
  125. T. H. Kim, Y. K. Kim, Y. Kwon et al., “Deregulation of miR-519a, 153, and 485-5p and its clinicopathological relevance in ovarian epithelial tumours,” Histopathology, vol. 57, no. 5, pp. 734–743, 2010. View at Publisher · View at Google Scholar · View at Scopus
  126. A. Mahdian-shakib, R. Dorostkar, M. Tat, M. S. Hashemzadeh, and N. Saidi, “Differential role of microRNAs in prognosis, diagnosis, and therapy of ovarian cancer,” Biomedicine & Pharmacotherapy, vol. 84, pp. 592–600, 2016. View at Publisher · View at Google Scholar · View at Scopus
  127. B. Shen, Y. Jiang, Y.-R. Chen et al., “Expression and inhibitory role of TIMP-3 in hepatocellular carcinoma,” Oncology Reports, vol. 36, no. 1, pp. 494–502, 2016. View at Publisher · View at Google Scholar · View at Scopus
  128. S. Qin, Y. Zhu, F. Ai et al., “MicroRNA-191 correlates with poor prognosis of colorectal carcinoma and plays multiple roles by targeting tissue inhibitor of metalloprotease 3,” Neoplasma, vol. 61, no. 1, pp. 27–34, 2014. View at Publisher · View at Google Scholar · View at Scopus
  129. M. Dong, P. Yang, and F. Hua, “miR-191 modulates malignant transformation of endometriosis through regulating TIMP3,” Medical Science Monitor, vol. 21, pp. 915–920, 2015. View at Publisher · View at Google Scholar · View at Scopus
  130. C. Y. Chang, M. T. Lai, Y. Chen et al., “Up-regulation of ribosome biogenesis by MIR196A2 genetic variation promotes endometriosis development and progression,” Oncotarget, vol. 7, no. 47, pp. 76713–76725, 2016. View at Publisher · View at Google Scholar · View at Scopus
  131. M. A. Nieto, R. Y.-J. Huang, R. A. Jackson, and J. P. Thiery, “EMT: 2016,” Cell, vol. 166, no. 1, pp. 21–45, 2016. View at Publisher · View at Google Scholar · View at Scopus
  132. J. Bartley, A. Jülicher, B. Hotz, S. Mechsner, and H. Hotz, “Epithelial to mesenchymal transition (EMT) seems to be regulated differently in endometriosis and the endometrium,” Archives of Gynecology and Obstetrics, vol. 289, no. 4, pp. 871–881, 2014. View at Publisher · View at Google Scholar · View at Scopus
  133. S. Matsuzaki and C. Darcha, “Epithelial to mesenchymal transition-like and mesenchymal to epithelial transition-like processes might be involved in the pathogenesis of pelvic endometriosis,” Human Reproduction, vol. 27, no. 3, pp. 712–721, 2012. View at Publisher · View at Google Scholar · View at Scopus
  134. N. Filigheddu, I. Gregnanin, P. E. Porporato et al., “Differential expression of microRNAs between eutopic and ectopic endometrium in ovarian endometriosis,” Journal of Biomedicine and Biotechnology, vol. 2010, Article ID 369549, 29 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  135. J. C. Eggers, V. Martino, R. Reinbold et al., “MicroRNA miR-200b affects proliferation, invasiveness and stemness of endometriotic cells by targeting ZEB1, ZEB2 and KLF4,” Reproductive Biomedicine Online, vol. 32, no. 4, pp. 434–445, 2016. View at Publisher · View at Google Scholar · View at Scopus
  136. T. Brabletz, A. Jung, S. Reu et al., “Variable β-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 18, pp. 10356–10361, 2001. View at Publisher · View at Google Scholar · View at Scopus
  137. Y. Lou, H. Jiang, Z. Cui, L. Wang, X. Wang, and T. Tian, “Linc-ROR induces epithelial-to-mesenchymal transition in ovarian cancer by increasing Wnt/β-catenin signaling,” Oncotarget, vol. 8, no. 41, pp. 69983–69994, 2017. View at Publisher · View at Google Scholar · View at Scopus
  138. F. Ma, W. Li, C. Liu et al., “miR-23a promotes TGF-β1-induced EMT and tumor metastasis in breast cancer cells by directly targeting CDH1 and activating Wnt/β-catenin signaling,” Oncotarget, vol. 8, no. 41, pp. 69538–69550, 2017. View at Publisher · View at Google Scholar · View at Scopus
  139. J.-J. Qiu, L.-C. Ye, J.-X. Ding et al., “Expression and clinical significance of estrogen‑regulated long non-coding RNAs in estrogen receptor α-positive ovarian cancer progression,” Oncology Reports, vol. 31, no. 4, pp. 1613–1622, 2014. View at Publisher · View at Google Scholar · View at Scopus
  140. Y. Wang, Y. Chen, and J. Fang, “Post-transcriptional and post-translational regulation of central carbon metabolic enzymes in cancer,” Anti-Cancer Agents in Medicinal Chemistry, vol. 17, no. 11, pp. 1456–1465, 2017. View at Publisher · View at Google Scholar · View at Scopus
  141. R. Asadollahi, C. A. C. Hyde, and X. Y. Zhong, “Epigenetics of ovarian cancer: from the lab to the clinic,” Gynecologic Oncology, vol. 118, no. 1, pp. 81–87, 2010. View at Publisher · View at Google Scholar · View at Scopus
  142. P.-R. Sun, S.-Z. Jia, H. Lin, J.-H. Leng, and J.-H. Lang, “Genome-wide profiling of long noncoding ribonucleic acid expression patterns in ovarian endometriosis by microarray,” Fertility and Sterility, vol. 101, no. 4, pp. 1038–1046.e7, 2014. View at Publisher · View at Google Scholar · View at Scopus
  143. C. Zhou, T. Zhang, F. Liu et al., “The differential expression of mRNAs and long noncoding RNAs between ectopic and eutopic endometria provides new insights into adenomyosis,” Molecular BioSystems, vol. 12, no. 2, pp. 362–370, 2016. View at Publisher · View at Google Scholar · View at Scopus
  144. H. Liu and J. H. Lang, “Is abnormal eutopic endometrium the cause of endometriosis? The role of eutopic endometrium in pathogenesis of endometriosis,” Medical Science Monitor, vol. 17, no. 4, pp. RA92–RA99, 2011. View at Publisher · View at Google Scholar
  145. M. Zhou, J. Fu, L. Xiao et al., “miR-196a overexpression activates the MEK/ERK signal and represses the progesterone receptor and decidualization in eutopic endometrium from women with endometriosis,” Human Reproduction, vol. 31, no. 11, pp. 2598–2608, 2016. View at Publisher · View at Google Scholar · View at Scopus
  146. H. Jørgensen, A. S. Hill, M. T. Beste et al., “Peritoneal fluid cytokines related to endometriosis in patients evaluated for infertility,” Fertility and Sterility, vol. 107, no. 5, pp. 1191–1199.e2, 2017. View at Publisher · View at Google Scholar · View at Scopus
  147. S. Vicente-Muñoz, I. Morcillo, L. Puchades-Carrasco, V. Payá, A. Pellicer, and A. Pineda-Lucena, “Pathophysiologic processes have an impact on the plasma metabolomic signature of endometriosis patients,” Fertility and Sterility, vol. 106, no. 7, pp. 1733–1741.e1, 2016. View at Publisher · View at Google Scholar · View at Scopus