Etiopathogenesis of endometriosis-associated infertility (a review)

Adamyan L.V.; Martirosyan Y.O.; Asaturova A.V.

doi:https://doi.org/10.17116/repro201824228-33

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Abstract:

Endometriosis is a complex disease that occurs in 7—15% of women of reproductive age. It leads to a violation of the reproductive function in almost half of the women. Despite of numerous studies, mechanisms, underlying endometriosis-associated infertility, it is not clear enough. The involvement of the systematic inflammatory reactions of the body, the imbalance of cellular and secretory components of the immune system, hormonal disorders, violations of the expressions of the expressions of the endometrial receptivity markers, oxidative stress in the processes of the oocyte quality reduction, embryo, impairment of fertilization and implantation of the fetal egg are discussed in this review.

Keywords:

endometriosis

infertility

STAT3

ARID1A

Authors:

Adamyan L.V.

Department of Reproductive Medicine and Surgery, Faculty of Postgraduate Professional Education, A.I. Evdokimov Moscow State University of Medicine and Dentistry, Ministry of Health of Russia, Moscow, Russia

SPIN RSCI: 9836-2713
Scopus AuthorID: 7006372422
ResearcherID: Q-1722-2018
ORCID: 0000-0002-3253-4512

Martirosyan Y.O.

I.M. Sechenov First Moscow State Medical University, Moscow, Russia, 119991

Asaturova A.V.

V.I. Kulakov Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia, Moscow, Russia

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References:

Adamyan LV, Andreeva EN, Apolikhina IA, Bezhenar VF, Gevorkyan MA, Gus AI, Demidov VN, Kalinina EA, Levakov SA, Marchenko LA, Popov AA, Sonova MM, Khashukoyeva AZ, Chernukha GE, Yarotskaya EL. Endometriosis: diagnosis, treatment and rehabilitation. Federal clinical guidelines for managing patients. Moscow: Russian Society of Obstetricians and Gynecologists; 2013. (In Russ.)
Singh N, Lata K, Naha M, Malhotra N, Tiwari A, Vanamail P. Effect of endometriosis on implantation rates, when compared to tubal factor in fresh non donor in vitro fertilization cycles. Journal of Human Reproductive Sciences. 2014;7:143-147. https://doi.org/10.4103/0974-1208.138874
Koninckx PR, Ussia A, Keckstein J, Adamian L, Zupi E, Wattiez A, Gomel V. Evidence based medicine: Pandora’s box of medical and surgical treatment of endometriosis. Journal of Minimally Invasive Gynecology. 2017;24:S1553-4650(17)31286-31287. https://doi.org/10.1016/j.mig.2017.11.012
Practice Committee of the American Society for Reproductive Medicine. Endometriosis and infertility: a committee opinion. Fertility and Sterility. 2012;98(3):591-598. https://doi.org/10.1016/j.fertnstert.2012.05.031
Leone Roberti Maggiore U, Scala C, Tafi E, Racca A, Biscaldi E, Vellone VG, Venturini PL, Ferrero S. Spontaneous fertility after expectant or surgical management of rectovaginal endometriosis in women with or without ovarian endometrioma: a retrospective analysis. Fertility and Sterility. 2017;107(4):969-976.e5. https://doi.org/10.1016/j.fertnstert.2017.02.106
Boujenah J, Cedrin-Durnerin I, Herbemont C, Sifer C, Poncelet C. Non-ART pregnancy predictive factors in infertile patients with peritoneal superficial endometriosis. European Journal of Obstetric, Gynecology, and Reproductive Biology. 2017;211:182-187. https://doi.org/10.1016/j.ejogrb.2017.03.008
Senapati S, Sammel MD, Morse C, Barnhart KT. Impact of endometriosis on in vitro fertilization outcomes: an evaluation of the Society for Assisted Reproductive Technologies Database. Fertility and Sterility. 2016;106:164-171. https://doi.org/10.1016/j.fertnstert.2016.03.037
González-Comadran M, Schwarze JE, Zegers-Hochschild F, Souza MD, Carreras R, Checa MÁ. The impact of endometriosis on the outcome of assisted reproductive technology. Reproductive Biology and Endocrinology. 2017;15(1):8. https://doi.org/10.1186/s12958-016-0217-2
Fox C, Morin S, Jeong J-W, Scott RT Jr, Lessey BA. Local and systemic factors and implantation: what is the evidence? Fertility and Sterility. 2016;105(4):873-884. https://doi.org/10.1016/j.fertnstert.2016.02.018
Heublein S, Vrekoussis T, Kuhn C, Friese K, Makrigiannakis A, Mayr D, Lenhard M, Jeschke U. Inducers of G-protein coupled estrogen receptor (GPER) in endometriosis: potential implications for macrophages and follicle maturation. Journal of Reproductive Immunology. 2013;97:95-103. https://doi.org/10.1016/j.jri.2012.10.013
Yoo JY, Jeong JW, Fazleabas AT, Tayade C, Young SL, Lessey BA. Protein inhibitor of activated stat3 (pias3) is down-regulated in eutopic endometrium of women with endometriosis. Biology of Reproduction. 2016;95(1):11. https://doi.org/10.1095/biolreprod.115.137158
Xiong W, Zhang L, Xiong Y, Liu H, Liu Y. Hypoxia promotes invasion of endometrial stromal cells via hypoxia-inducible factor 1α upregulation-mediated β-catenin activation in endometriosis. Reproductive Sciences. 2016;23(4):531-541. https://doi.org/10.1177/1933719115607999
Zhang L, Xiong W, Li N, Liu H, He H, Du Y, Zhang Z, Liu Y. Estrogen stabilizes hypoxia-inducible factor 1α through G protein-coupled estrogen receptor 1 in eutopic endometrium of endometriosis. Fertility and Sterility. 2017;107(2):439-447. https://doi.org/10.1016/j.fertnstert.2016.11.008
Evans-Hoeker E, Lessey BA, Jeong JW, Savaris RF, Palomino WA, Yuan L, Schammel DP, Young SL. Endometrial BCL6 overexpression in eutopic endometrium of women with endometriosis. Reproductive Sciences.2016;23(9):1234-1241. https://doi.org/10.1177/1933719116649711
Ahn SH, Khalaj K, Young SL, Lessey BA, Koti M, Tayade C. Immune inflammation gene signatures in endometriosis patients. Fertility and Sterility. 2016;106(6):1420-1431.e7. https://doi.org/10.1016/j.fertnstert.2016.07.005
Uimari O, Rahmioglu N, Nyholt DR, Vincent K, Missmer SA, Becker C, Morris AP, Montgomery GW, Zondervan KT. Genome-wide genetic analyses highlight mitogen-activated protein kinase (MAPK) signaling in the pathogenesis of endometriosis. Human Reproduction. 2017;32(4):780-793. https://doi.org/10.1093/humrep/dex024
Ahn SH, Edwards AK, Singh SS, Young SL, Lessey BA, Tayade C. IL-17A Contributes to the pathogenesis of endometriosis by triggering proinflammatory cytokines and angiogenic growth factors. Journal of Immunology. 2015;195(6):2591-2600. https://doi.org/10.4049/jimmunol.1501138
Jeung C, Cheon K, Kim M-R. Decreased cytotoxicity of peripheral and peritoneal natural killer cell in endometriosis. BioMed Research International. 2016;2016:2916070. https://doi.org/10.1155/2016/2916070
Adamyan L, Starodubtseva N, Borisova A, Stepanian A, Chagovets V, Salimova D, Wang Z, Kononikhin A, Popov I, Bugrova A, Chingin K, Kozachenko A, Chen H, Frankevich V. Direct mass spectrometry differentiation of ectopic and eutopic endometrium in patients with endometriosis. Journal of Minimally Invasive Gynecology. 2017;S1553-4650(17):31120-31122. https://doi.org/10.1016/j.jmig.2017.08.658
Kuznetsova MV, Pshenichnyuk EYu, Burmenskaya OV, Asaturova AV, Trofimov DYu, Adamyan LV. Study of gene expressions in the eutopic endometrium of women with endometrioid ovarian cysts. Problemy reproduktsii. 2017;8:93-102. (In Russ.) https://doi.org/10.18565/aig.2017.8.93-102
Schmitz CR, Oehninger S, Genro VK, Chandra N, Lattanzio F, Yu L, Cunha-Filho JS. Alterations in expression of endometrial milk fat globule-EGF factor 8 (MFG-E8) and leukemia inhibitory factor (LIF) in patients with infertility and endometriosis. JBRA Assisted Reproduction. 2017;21(4):313-320. https://doi.org/10.5935/1518-0557.20170056
Xiao Y, Li T, Xia E, Yang X, Sun X, Zhou Y. Expression of integrin β3 and osteopontin in the eutopic endometrium of adenomyosis during the implantation window. European Journal of Obstetrics, Gynecology and Reproductive Biology. 2013;170(2):419-422. https://doi.org/10.1016/j.ejogrb
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(10):e76808. https://doi.org/10.1371/journal.pone.0076808
Su R-W, Strug MR, Joshi NR, Jeong J-W, Miele L, Lessey BA, Young SL, Fazleabas AT. Decreased notch pathway signaling in the endometrium of women with endometriosis impairs decidualization. The Journal of Clinical Endocrinology and Metabolism. 2015;100(10):E433-E442. https://doi.org/10.1210/jc.2014-3720
Naqvi HI, Ilagan Y, Krikun G, Taylor HS. Altered genome-wide methylation in endometriosis. Reproductive Sciences. 2014;21:1237-1243. https://doi.org/10.1177/1933719114532841
Yang H, Yin J, Ficarrotta K, Hsu SH, Zhang W, Cheng C. Aberrant expression and hormonal regulation of Galectin-3 in endometriosis women with infertility. Journal of Endocrinological Investigation. 2016;39(7):785-791. https://doi.org/10.1007/s40618-016-0435-7
Kim TH, Yoo JY, Wang Z, Lydon JP, Khatri S, Hawkins SM, Leach RE, Fazleabas AT, Young SL, Lessey BA, Ku BJ, Jeong JW. ARID1A is essential for endometrial function during early pregnancy. PLoS genetics. 2015;11(9):e1005537. https://doi.org/10.1371/journal.pgen.1005537
Ray S, Pollard JW. KLF15 negatively regulates estrogen-induced epithelial cell proliferation by inhibition of DNA replication licensing. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(21):E1334-E1343. https://doi.org/10.1073/pnas.1118515109
Winarto H, Tan MI, Sadikin M, Wanandi SI. ARID1A Expression is down-regulated by oxidative stress in endometriosis and endometriosis-associated ovarian cancer. Translational oncogenomics. 2017;9:1177272716689818. https://doi.org/10.1177/1177272716689818
Sofiyeva N, Ekizoglu S, Gezer A, Yilmaz H, Kolomuc Gayretli T, Buyru N, Oral E. Does telomerase activity have an effect on infertility in patients with endometriosis? European Journal of Obstetric, Gynecology, and Reproductive Biology. 2017;213:116-122. https://doi.org/10.1016/j.ejogrb.2017.04.027
Rahmanto YS, Jung JG, Wu RC, Kobayashi Y, Heaphy CM, Meeker AK, Wang TL, Shih IM. Inactivating ARID1A tumor suppressor enhances TERT transcription and maintains telomere length in cancer cells. The Journal of Biological Chemistry. 2016;291:9690-9699. https://doi.org/10.1074/jbc.m115.707612
Da Broi MG, Malvezzi H, Paz CC, Ferriani RA, Navarro PA. Follicular fluid from infertile women with mild endometriosis may compromise the meiotic spindles of bovine metaphase II oocytes. Human Reproduction. 2014;29:315-323. https://doi.org/10.1093/humrep/det37
Jianini BTGM, Giorgi VSI, Da Broi MG, de Paz CCP, Rosa E, Silva JC, Ferriani RA, Navarro PA.Peritoneal fluid from infertile women with minimal/mild endometriosis compromises the meiotic spindle of metaphase ii bovine oocytes: a pilot study. Reproductive Sciences. 2017;24(9):1304-1311. https://doi.org/10.1177/1933719116687658
Hamdan M, Jones KT, Cheong Y, Lane SI. The sensitivity of the DNA damage checkpoint prevents oocyte maturation in endometriosis. Scientific reports. 2016;6:36994. https://doi.org/10.1038/srep36994
Juneau C, Kraus E, Werner M, Franasiak J, Morin S, Patounakis G, Molinaro T, de Ziegler D, Scott RT. American Society for Reproductive Medicine. Patients with endometriosis have aneuploidy rates equivalent to their age-matched peers in the in vitro fertilization population. Fertility and Sterility. 2017;108(2):284-288. https://doi.org/10.1016/j.fertnstert.2017.05.038
Ceviren AK, Ozcelik NT, Urfan A, Donmez L, Isikoglu M. Characteristic cytoplasmic morphology of oocytes in endometriosis patients and its effect on the outcome of assisted reproduction treatments cycles. IVF Lite. 2014;1:88-93. https://doi.org/10.4103/2348-2907.140123
Russell DL, Gilchrist RB, Brown HM, Thompson JG. Bidirectional communication between cumulus cells and the oocyte: old hands and new players? Theriogenology. 2016;86(1):62-68. https://doi.org/10.1016/j.theriogenology.2016.04.019
Singh AK, Dutta M, Chattopadhyay R, Chakravarty B, Chaudhury K. Intrafollicular interleukin-8, interleukin-12, and adrenomedullin are the promising prognostic markers of oocyte and embryo quality in women with endometriosis. Journal of Assisted Reproduction and Genetics. 2016;33(10):1363-1372. https://doi.org/10.1007/s10815-016-0782-5
Santanam N, Zoneraich N, Parthasarathy S. Myeloperoxidase as a potential target in women with endometriosis undergoing IVF. Reproductive Sciences. 2017;24(4):619-626. https://doi.org/10.1177/1933719116667225