Genetic and epigenetic mechanisms of genital endometriosis-associated infertility

1. Адамян Л.В., ред. Эндометриоз: диагностика, лечение и реабилитация. Клинические рекомендации. М.; 2013. 90 с. (ed. by Adamyan L.V. Endometriosis: diagnosis, treatment and rehabilitation. Clinical guidelines. M.: 2013; 90 р. (In Russ.)
2. Баранов В.С. Эндометриоз как проблема системной генетики. Журнал акушерства и женских болезней. 2013; 62(1): 71-8. [Baranov V.S. Endometriosis as a problem of system genetics. Journal of Obstetrics and Women’s Diseases. 2013; 62 (1): 71-78. (In Russ.)]
3. Barnett R., Banks N., Decherney A.H. Endometriosis and fertility preservation. Clin. Obstet. Gynecol. 2017; 60(3): 517-23. https://doi.org/10.1097/GRF.0000000000000311.
4. Saha R., Pettersson H.J., Svedberg P., Olovsson M., Bergqvist A., Marions L. et al. Heritability of endometriosis. Fertil. Steril. 2015; 104(4): 947-52. https://doi.org/10.1016/j.fertnstert.2015.06.035.
5. Borghese B., Zondervan K.T., Abrao M.S., Chapron C., Vaiman D. Recent insights on the genetics and epigenetics of endometriosis. Clin. Genet. 2017; 91(2): 254-64. https://doi.org/ 10.1111/cge.12897.
6. Rahmioglu N., Nyholt D.R., Morris A.P., Missmer S.A., Montgomery G.W., Zondervan K.T. Genetic variants underlying risk of endometriosis: insights from meta‐analysis of eight genome‐wide association and replication datasets. Hum. Reprod. Update. 2014; 20(5): 702-16. https://doi.org/10.1093/humupd/dmu015.
7. Sapkota Y., Fassbender A., Bowdler L., Fung J.N., Peterse D., Montgomery G.W. et al. Independent replication and meta‐analysis for endometriosis risk loci. Twin Res. Hum. Genet. 2015; 18(5): 518-25. https://doi.org/10.1017/thg.2015.61.
8. Zhang L., Xiong W., Xiong Y., Liu H., Liu Y. 17β-Estradiol promotes vascular endothelial growth factor expression via the Wnt/β -catenin pathway during the pathogenesis of endometriosis. Mol. Hum. Reprod. 2016; 22(7): 526-35. https://doi.org/10.1093/molehr/gaw025.
9. Matsuzaki S., Darcha C. Involvement of the Wnt/ β-catenin signaling pathway in the cellular and molecular mechanisms of fibrosis in endometriosis. PLoS One. 2013; 8: e76808. https://doi.org/10.1371/journal.pone.0076808.
10. Dyson M.T., Roqueiro D., Monsivais D., Ercan C.M., Pavone M.E., Brooks D.C. et al. Genome-wide DNA methylation analysis predicts an epigenetic switch for GATA factor expression in endometriosis. PLoS Genet. 2014; 10(3): e1004158. https://doi.org/10.1371/journal.pgen.1004158.
11. Fambrini M., Sorbi F., Bussani C., Cioni R., Sisti G., Andersson K.L. Hypermethylation of HOXA10 gene in mid-luteal endometrium from women with ovarian endometriomas. Acta Obstet. Gynecol. Scand 2013; 92(11): 1331-4. https://doi.org/10.1111/aogs.12236.
12. Andersson K.L., Bussani C., Fambrini M., Polverino V., Taddei G.L., Gemzell-Danielsson K., Scarselli G. DNA methylation of HOXA10 in eutopic and ectopic endometrium. Hum. Reprod 2014; 29(9): 1906-11. https://doi.org/10.1093/humrep/deu161.
13. Özcan C., Özdamar Ö., Gökbayrak M.E., Doğer E., Çakıroğlu Y., Çine N. HOXA-10 gene expression in ectopic and eutopic endometrium tissues: Does it differ between fertile and infertile women with endometriosis? Eur. J. Obstet. Gynecol. Reprod. Biol. 2019; 233: 43-8. https://doi.org/10.1016/j.ejogrb.2018.11.027.
14. Monteiro J.B., Colon‐Diaz M., Garcia M., Gutierrez S., Colón M., Seto E. et al. Endometriosis is characterized by a distinct pattern of histone 3 and histone 4 lysine modifications. Reprod. Sci. 2014; 21(3): 305-18. https://doi.org/10.1177/1933719113497267.
15. Colón-Díaz M., Báez-Vega P., García M., Ruiz A., Monteiro J.B., Fourquet J. et al. HDAC1 and HDAC2 are differentially expressed in endometriosis. Reprod. Sci. 2012; 19(5): 483-92. https://doi.org/10.1177/1933719111432870.
16. Samartzis E.P., Noske A., Samartzis N., Fink D., Imesch P. The expression of histone deacetylase 1, but not other class I histone deacetylases, is significantly increased in endometriosis. Reprod. Sci. 2013; 20(12): 1416-22. https://doi.org/10.1177/1933719113488450.
17. Xiaomeng X., Ming Z., Jiezhi M., Xiaoling F. Aberrant histone acetylation and methylation levels in woman with endometriosis. Arch. Gynecol. Obstet. 2013; 287(3): 487-94. https://doi.org/10.1007/s00404-012-2591-0.
18. Altucci L., Rots M.G. Epigenetic drugs: from chemistry via biology to medicine and back. Clin. Epigenetics. 2016; 8: 56. https://doi.org/10.1186/s13148-016-0222-5.
19. Kawano Y., Nasu K., Hijiya N., Tsukamoto Y., Amada K., Abe W. et al. CCAAT/enhancer-binding protein α is epigenetically silenced by histone deacetylation in endometriosis and promotes the pathogenesis of endometriosis. J. Clin. Endocrinol. Metab. 2013; 98(9): 1474-82. https://doi.org/10.1210/jc.2013-1608.
20. Monteiro J.B., Colón-Díaz M., García M., Gutierrez S., Colón M., Seto E. et al. Endometriosis is characterized by a distinct pattern of histone 3 and histone 4 lysine modifications. Reprod. Sci. 2014; 21(3): 305-18. https://doi.org/10.1177/1933719113497267.
21. Chen Y., Cai S., Wang J., Xu M. Valproic acid-induced histone acetylation suppresses CYP19 gene expression and inhibits the growth and survival of endometrial stromal cells. Int. J. Mol. Med. 2015; 36(3): 725-32. https://doi.org/10.3892/ijmm.2015.2263.
22. Braza-Boïls A., Marí-Alexandre J., Gilabert J., Sánchez-Izquierdo D., España F., Estellés A. et al. MicroRNA expression profile in endometriosis: its relation to angiogenesis and fibrinolytic factors. Hum. Reprod. 2014; 29(5): 978-88. https://doi.org/ 10.1093/humrep/deu019.
23. Lin S.C., Wang C.C., Wu M.H., Yang S.H., Li Y.H., Tsai S.J. Hypoxia-induced microRNA-20a expression increases ERK phosphorylation and angiogenic gene expression in endometriotic stromal cells. J. Clin. Endocrinol. Metab. 2012; 97(8): 1515-23. https://doi.org/10.1210/jc.2012-1450.
24. Shen L., Yang S., Huang W., Xu W., Wang Q., Song Y. et al. MicroRNA23a and microRNA23b deregulation derepresses SF-1 and upregulates estrogen signaling in ovarian endometriosis. J. Clin. Endocrinol. Metab. 2013; 98(4): 1575-82. https://doi.org/10.1210/jc.2012-3010.
25. Shi X.Y., Gu L., Chen J., Guo X.R., Shi Y.L. Downregulation of miR‐183 inhibits apoptosis and enhances the invasive potential of endometrial stromal cells in endometriosis. Int. J. Mol. Med. 2014; 33: 59-67. https://doi.org/10.3892/ijmm.2013.1536.
26. Hsu C.Y., Hsieh T.H., Tsai C.F., Tsai H.P., Chen H.S., Chang Y. et al. miRNA-199a-5p regulates VEGFA in endometrial mesenchymal stem cells and contributes to the pathogenesis of endometriosis. J. Pathol. 2014; 232(3): 330-43. https://doi.org/10.1002/path.4295.
27. Ghazal S., McKinnon B., Zhou J., Mueller M., Men Y., Yang L. et al. H19 lncRNA alters stromal cell growth via IGF signaling in the endometrium of women with endometriosis. EMBO Mol. Med. 2015; 7(8): 996-1003. https://doi.org/10.15252/emmm.201505245.
28. Scutiero G., Iannone P., Bernardi G., Bonaccorsi G., Spadaro S., Volta C.A. et al. Oxidative stress and endometriosis: a systematic review of the literature. Oxid. Med. Cell. Longev. 2017; 2017: 7265238. https://doi.org/10.1155/2017/7265238.
29. Nasiri N., Moini A., Eftekhari-Yazdi P., Karimian L., Salman-Yazdi R., Arabipoor A. Oxidative stress statues in serum and follicular fluid of women with endometriosis. Cell J. 2017 Winter; 18(4): 582-7. https://doi.org/10.22074/cellj.2016.4724.
30. Bragatto F.B., Barbosa C.P., Christofolini D.M., Peluso C., dos Santos A.A., Mafra F.A. et al. There is no relationship between Paraoxonase serum level activity in women with endometriosis and the stage of the disease: an observational study. Reprod. Health. 2013; 10: 32. https://doi.org/10.1186/1742-4755-10-32.
31. Prieto L., Quesada J.F., Cambero O., Pacheco A., Pellicer A., Codoceo R., Garcia-Velasco J.A. et al. Analysis of follicular fluid and serum markers of oxidative stress in women with infertility related to endometriosis. Fertil. Steril. 2012; 98(1): 126-30. https://doi.org/10.1016/j.fertnstert.2012.03.052.
32. Turkyilmaz E., Yildirim M., Cendek B.D., Baran P., Alisik M., Dalgaci F., Yavuz A.F. Evaluation of oxidative stress markers and intra-extracellular antioxidant activities in patients with endometriosis. Eur. J. Obstet. Gynecol. Reprod. Biol. 2016; 199: 164-8. https://doi.org/10.1016/j.ejogrb.2016.02.027.
33. Santulli P., Chouzenoux S., Fiorese M., Marcellin L., Lemarechal H., Millischer A.E. et al. Protein oxidative stress markers in peritoneal fluids of women with deep infiltrating endometriosis are increased. Hum. Reprod. 2015; 30(1): 49-60. https://doi.org/10.1093/humrep/deu290.
34. Nakagawa K., Hisano M., Sugiyama R., Yamaguchi K. Measurement of oxidative stress in the follicular fluid of infertility patients with an endometrioma. Arch. Gynecol. Obstet. 2016; 293(1): 197-202. https://doi.org/10.1007/s00404-015-3834-7.
35. Da Broi M.G., Jordão A.A. Jr., Ferriani R.A., Navarro P.A. Oocyte oxidative DNA damage may be involved in minimal/mild endometriosis-related infertility. Mol. Reprod. Dev. 2018; 85(2): 128-36. https://doi.org/10.1002/mrd.22943.
36. Goud P.T., Goud A.P., Joshi N., Puscheck E., Diamond M.P., Abu-Soud H.M. Dynamics of nitric oxide, altered follicular microenvironment, and oocyte quality in women with endometriosis. Fertil. Steril. 2014; 102(1): 151-9. https://doi.org/ 10.1016/j.fertnstert.2014.03.053.
37. Máté G., Bernstein L.R., Török A.L. Endometriosis is a +cause of infertility. Does reactive oxygen damage to gametes and embryos play a key role in the pathogenesis of infertility caused by endometriosis? Front. Endocrinol. (Lausanne). 2018; 9: 725. https://doi.org/10.3389/fendo.2018.00725.
38. Qiao J., Wang Z.B., Feng H.L., Miao Y.L., Wang Q., Yu Y. The root of reduced fertility in aged women and possible therapentic options: current status and future perspects. Mol. Aspects Med. 2014; 38: 54-85. https://doi.org/10.1016/j.mam.2013.06.001.
39. Sharma R.K., Azeem A., Agarwal A. Spindle and chromosomal alterations in metaphase II oocytes. Reprod. Sci. 2013; 20(11): 1293-301. https://doi.org/10.1177/1933719113483018.
40. Perkins A.T., Das T.M., Panzera L.C., Bickel S.E. Oxidative stress in oocytes during midprophase induces premature loss of cohesion and chromosome segregation errors. Proc. Natl. Acad. Sci. USA. 2016; 113(44): E6823-30. https://doi.org/ 10.1073/pnas.1612047113.
41. Li Y.J., Han Z., Ge L., Zhou C.J., Zhao Y.F., Wang D.H. et al. C-phycocyanin protects against low fertility by inhibiting reactive oxygen species in aging mice. Oncotarget. 2016; 7(14): 17393-409. https://doi.org/10.18632/oncotarget.8165.
42. Liu J., Liu M., Ye X., Liu K., Huang J., Wang L. et al. Delay in oocyte aging in mice by the antioxidant N-acetyl-L-cysteine (NAC). Hum. Reprod. 2012; 27(5): 1411-20. https://doi.org/10.1093/humrep/des019.
43. Mihalas B.P., De Iuiis G.N., Redgrove K.A., McLaughlin E.A., Nixon B. The lipid peroxidation product 4-hydroxynonenal contributes to oxidative stress-mediated deterioration of the ageing oocyte. Sci. Rep. 2017; 7(1): 6247. https://doi.org/10.1038/s41598-017-06372-z.
44. Liu M., Yin Y., Ye X., Zeng M., Zhao Q., Keefe D.L. Resveratrol protects against age-associated infertility in mice. Hum. Reprod. 2013; 28(3): 707-17. https://doi.org/ 10.1093/humrep/des437.
45. Liang L.F., Qi S.T., Xian Y.X., Huang L., Sun X.F., Wang W.H. Protective effect of antioxidants on the pre-maturation aging of mouse oocytes. Sci. Rep. 2017; 7: 1434. https://doi.org/10.1038/s41598-017-01609-3.
46. Silva E., Greene A.F., Strauss K., Herrick J.R., Schoolcraft W.B., Krisher R.L. Antioxidant supplementation during in vitro culture improves mitochondrial function and development of embryos from aged female mice. Reprod. Fertil. Dev. 2015; 27(6): 975-83. https://doi.org/10.1071/RD14474.
47. He C., Wang J., Zhang Z., Yang M., Li Y., Tian X. Mitochondria synthesize melatonin to ameliorate its function and improve mice oocyte’s quality under in vitro conditions. Int. J. Mol. Sci. 2016; 17: 939. https://doi.org/10.3390/ijms17060939.
48. 48. Lopes S., Jurisicova A., Sun J.G., Casper R.F. Reactive oxygen species: potential cause for DNA fragmentation in human spermatozoa. Hum Repr 1998: 13 (4): 896–900.
49. Haghighian H.K., Haidari F., Mohammadi-Asl J., Dadfar M. Randomized, triple-blind, placebo-controlled clinical trial examining the effects of alpha-lipoic acid supplement on the spermatogram and seminal oxidative stress in infertile men. Fertil. Steril. 2015; 104(2): 318-24. https://doi.org/ 10.1016/j.fertnstert.2015.05.014.
50. Zhang Y., Qian D., Li Z., Huang Y., Wu Q., Ru G. Oxidative stress-induced DNA damage of mouse zygotes triggers G2/M checkpoint and phosphorylates Cdc25 and Cdc2. Cell Stress Chaperones. 2016; 21(4): 687-96. https://doi.org/10.1007/s12192-016-0693-5.

Received 07.04.2019

Accepted 19.04.2019