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Yarmolinskaya M.I.

D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology;
I.I. Mechnikov North-Western State Medical University

Shalina M.A.

D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology

Netreba E.A.

FSBSI «The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott»

Beganova A.K.

FSBSI «The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott»

Endometrial receptivity in adenomyosis and the role of signaling pathways in the pathogenesis of the disease (literature review)

Authors:

Yarmolinskaya M.I., Shalina M.A., Netreba E.A., Beganova A.K.

More about the authors

Journal: Russian Journal of Human Reproduction. 2022;28(2): 25‑32

Read: 1371 times


To cite this article:

Yarmolinskaya MI, Shalina MA, Netreba EA, Beganova AK. Endometrial receptivity in adenomyosis and the role of signaling pathways in the pathogenesis of the disease (literature review). Russian Journal of Human Reproduction. 2022;28(2):25‑32. (In Russ.)
https://doi.org/10.17116/repro20222802125

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References:

  1. Yarmolinskaya MI, Shalina MA, Hachaturyan AR, Netreba EA, Florova MS, Mekhtihanova SV. Adenomyosis: from scientific discoveries to the practical aspects of prescribing drug therapy. Akusherstvo i ginekologiia. 2020;3:182-190. (In Russ.). https://doi.org/10.18565/aig.2020.3.182-190
  2. Younes G, Tulandi T. Effects of adenomyosis on in vitro fertilization treatment outcomes: a meta-analysis. Fertility and Sterility. 2017;108(3):483-490.e3.  https://doi.org/10.1016/j.fertnstert.2017.06.025
  3. Tomassetti C, Meuleman C, Timmerman D, D’Hooghe T. Adenomyosis and Subfertility: Evidence of Association and Causation. Seminars in Reproductive Medicine. 2013;31(02):101-108.  https://doi.org/10.1055/s-0032-1333475
  4. Vannuccini S, Petraglia F. Recent advances in understanding and managing adenomyosis. F1000Research. 2019;8:283.  https://doi.org/10.12688/f1000research.17242.1
  5. Hashimoto A, Iriyama T, Sayama S, Nakayama T, Komatsu A, Miyauchi A, Nishii O, Nagamatsu T, Osuga Y, Fujii T. Adenomyosis and adverse perinatal outcomes: increased risk of second trimester miscarriage, preeclampsia, and placental malposition. The Journal of Maternal-Fetal and Neonatal Medicine. 2017;31(3):364-369.  https://doi.org/10.1080/14767058.2017.1285895
  6. Kossaï M, Penault-Llorca F. Role of Hormones in Common Benign Uterine Lesions: Endometrial Polyps, Leiomyomas, and Adenomyosis. Advances in Experimental Medicine and Biology. 2020; 1242:37-58.  https://doi.org/10.1007/978-3-030-38474-6_3
  7. Bergeron C, Amant F, Ferenczy A. Pathology and physiopathology of adenomyosis. Best Practice and Research Clinical Obstetrics and Gynaecology. 2006;20(4):511-521.  https://doi.org/10.1016/j.bpobgyn.2006.01.016
  8. Gargett C. Uterine stem cells: What is the evidence? Human Reproduction Update. 2006;13(1):87-101.  https://doi.org/10.1093/humupd/dml045
  9. Vannuccini S, Tosti C, Carmona F, Huang SJ, Chapron C, Guo SW, Petraglia F. Pathogenesis of adenomyosis: an update on molecular mechanisms. Reproductive BioMedicine Online. 2017;35(5): 592-601.  https://doi.org/10.1016/j.rbmo.2017.06.016
  10. Riggs JC, Lim EK, Liang D, Bullwinkel R. Cesarean section as a risk factor for the development of adenomyosis uteri. The Journal of Reproductive Medicine. 2014;59(1-2):20-24. 
  11. Taran F, Weaver A, Coddington C, Stewart E. Understanding adenomyosis: a case control study. Fertility and Sterility. 2010;94(4): 1223-1228. https://doi.org/10.1016/j.fertnstert.2009.06.04
  12. Chan R, Schwab K, Gargett C. Clonogenicity of Human Endometrial Epithelial and Stromal Cells1. Biology of Reproduction. 2004; 70(6):1738-1750. https://doi.org/10.1095/biolreprod.103.024109
  13. Zhou S, Yi T, Liu R, Bian C, Qi X, He X, Wang K, Li J, Zhao X, Huang C, Wei Y. Proteomics Identification of Annexin A2 as a Key Mediator in the Metastasis and Proangiogenesis of Endometrial Cells in Human Adenomyosis. Molecular and Cellular Proteomics. 2012;11(7):M112.017988. https://doi.org/10.1074/mcp.m112.017988
  14. Zeng YY, Guan YG, Li KY. Role of estrogen, estrogen receptors, and aromatase in the pathogenesis of uterine adenomyosis. Nan Fang Yi Ke Da Xue Xue Bao. 2017;37(3):383-387.  https://doi.org/10.3969/j.issn.1673-4254.2017.03.18
  15. Nie J, Lu Y, Liu X, Guo S. Immunoreactivity of progesterone receptor isoform B, nuclear factor κB, and IκBα in adenomyosis. Fertility and Sterility. 2009;92(3):886-889.  https://doi.org/10.1016/j.fertnstert.2009.01.084
  16. Shklyar AA, Adamyan LV, Kogan EA, Paramonova NB, Kozachenko IPh, Gavrilova TYu, Kononov SN. Receptor status of endometrioid heterotopias as the indication for hormonal therapy of nodular and diffuse forms of adenomyosis. Problemy reprodukcii. 2015; 21(2):88-93. (In Russ.). https://doi.org/10.17116/repro201521288-93]
  17. Mehasseb M, Panchal R, Taylor A, Brown L, Bell S, Habiba M. Estrogen and progesterone receptor isoform distribution through the menstrual cycle in uteri with and without adenomyosis. Fertility and Sterility. 2011;95(7):2228-2235. https://doi.org/10.1016/j.fertnstert.2011.02.051
  18. Miravet-Valenciano J, Rincon-Bertolin A, Vilella F, Simon C. Understanding and improving endometrial receptivity. Current Opinion in Obstetrics and Gynecology. 2015;27(3):187-192.  https://doi.org/10.1097/GCO.0000000000000173
  19. Herndon CN, Aghajanova L, Balayan S, Erikson D, Barragan F, Goldfien G, Vo KC, Hawkins S, Giudice LC. Global Transcriptome Abnormalities of the Eutopic Endometrium from Women with Adenomyosis. Reproductive Sciences. 2016;23(10):1289-1303. https://doi.org/10.1177/1933719116650758
  20. Munro M. Uterine polyps, adenomyosis, leiomyomas, and endometrial receptivity. Fertility and Sterility. 2019;111(4):629-640.  https://doi.org/10.1016/j.fertnstert.2019.02.008
  21. Mavrelos D, Holland TK, O’Donovan O, Khalil M, Ploumpidis G, Jurkovic D, Khalaf Y. The impact of adenomyosis on the outcome of IVF-embryo transfer. Reproductive BioMedicine Online. 2017; 35(5):549-554.  https://doi.org/10.1016/j.rbmo.2017.06.026
  22. Bourdon M, Santulli P, Oliveira J, Marcellin L, Maignien C, Melka L, Bordonne C, Millisher AE, Plu-Bureau G, Cormier J, Chapron C. Focal adenomyosis is associated with primary infertility. Fertility and Sterility. 2020;114(6):1271-1277. https://doi.org/10.1016/j.fertnstert.2020.06.018
  23. Harada T, Khine Y, Kaponis A, Nikellis T, Decavalas G, Taniguchi F. The Impact of Adenomyosis on Women’s Fertility. Obstetrical and Gynecological Survey. 2016;71(9):557-568.  https://doi.org/10.1097/ogx.0000000000000346
  24. Lessey B, Castelbaum A, Buck C, Lei Y, Yowell C, Sun J. Further characterization of endometrial integrins during the menstrual cycle and in pregnancy. Fertility and Sterility. 1994;62(3):497-506.  https://doi.org/10.1016/s0015-0282(16)56937-4
  25. Surrey E, Minjarez D, Schoolcraft W. The incidence of aberrant endometrial αvβ3 vitronectin expression in a high risk infertility population: could prolonged GnRH agonist therapy play a role? Journal of Assisted Reproduction and Genetics. 2007;24(11):553-556.  https://doi.org/10.1007/s10815-007-9164-3
  26. Wei Q, St. Clair J, Fu T, Stratton P, Nieman L. Reduced expression of biomarkers associated with the implantation window in women with endometriosis. Fertility and Sterility. 2009;91(5):1686-1691. https://doi.org/10.1016/j.fertnstert.2008.02.121
  27. 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 and Gynecology and Reproductive Biology. 2013;170(2):419-422.  https://doi.org/10.1016/j.ejogrb.2013.05.007
  28. Takahashi Y, Takahashi M, Carpino N, Jou ST, Chao JR, Tanaka S, Shigeyoshi Y, Parganas E, Ihle JN. Leukemia Inhibitory Factor Regulates Trophoblast Giant Cell Differentiation via Janus Kinase 1-Signal Transducer and Activator of Transcription 3-Suppressor of Cytokine Signaling 3 Pathway. Molecular Endocrinology. 2008;22(7): 1673-1681. https://doi.org/10.1210/me.2008-0058
  29. Xiao Y, Sun X, Yang X, Zhang J, Xue Q, Cai B, Zhou Y. Leukemia inhibitory factor is dysregulated in the endometrium and uterine flushing fluid of patients with adenomyosis during implantation window. Fertility and Sterility. 2010;94(1):85-89.  https://doi.org/10.1016/j.fertnstert.2009.03.012
  30. Yang JH, Chen MJ, Chen HF, Lee TH, Ho HN, Yang YS. Decreased expression of killer cell inhibitory receptors on natural killer cells in eutopic endometrium in women with adenomyosis. Human Reproduction. 2004;19(9):1974-1978. https://doi.org/10.1093/humrep/deh372
  31. Prathoomthong S, Tingthanatikul Y, Lertvikool S, Rodratn N, Waiyaput W, Dittharot K, Sroyraya M, Sophonsritsuk A. The Effects of Dienogest on Macrophage and Natural Killer Cells in Adenomyosis: A Randomized Controlled Study. International Journal of Fertility and Sterility. 2018;11(4):279-286.  https://doi.org/10.22074/ijfs.2018.5137
  32. Guo S, Zhang D, Lu X, Zhang Q, Gu R, Sun B, Sun Y. Hypoxia and its possible relationship with endometrial receptivity in adenomyosis: a preliminary study. Reproductive Biology and Endocrinology. 2021;19(1):7.  https://doi.org/10.1186/s12958-020-00692-y
  33. Taylor H. The role of HOX genes in human implantation. Human Reproduction Update. 2000;6(1):75-79.  https://doi.org/10.1093/humupd/6.1.75
  34. Fischer C, Kayisli U, Taylor H. HOXA10 expression is decreased in endometrium of women with adenomyosis. Fertility and Sterility. 2010;94(4):175.  https://doi.org/10.1016/j.fertnstert.2010.07.693
  35. Jiang C, Liu C, Guo J, Chen L, Luo N, Qu X, Yang W, Ren Q, Cheng Z. The Expression of Toll-like receptors in eutopic and ectopic endometrium and its implication in the inflammatory pathogenesis of adenomyosis. Scientific Reports. 2017;7(1):7365. https://doi.org/10.1038/s41598-017-07859-5
  36. Guo J, Chen L, Luo N, Li C, Chen R, Qu X, Liu M, Kang L, Cheng Z. LPS/TLR4-mediated stromal cells acquire an invasive phenotype and are implicated in the pathogenesis of adenomyosis. Scientific Reports. 2016;6(1):21416. https://doi.org/10.1038/srep21416
  37. Luo X, Zhou W, Tao Y, Wang X, Li D. TLR4 Activation Promotes the Secretion of IL-8 Which Enhances the Invasion and Proliferation of Endometrial Stromal Cells in an Autocrine Manner via the FAK Signal Pathway. American Journal of Reproductive Immunology. 2015;74(6):467-479.  https://doi.org/10.1111/aji.12425
  38. Qi S, Zhao X, Li M, Zhang X, Lu Z, Yang C, Zhang C, Zhang H, Zhang N. Aberrant expression of Notch1/numb/snail signaling, an epithelial mesenchymal transition related pathway, in adenomyosis. Reproductive Biology and Endocrinology. 2015;13:96.  https://doi.org/10.1186/s12958-015-0084-2
  39. Cai X, Shen M, Liu X, Nie J. The Possible Role of Eukaryotic Translation Initiation Factor 3 Subunit e (eIF3e) in the Epithelial-Mesenchymal Transition in Adenomyosis. Reproductive Sciences. 2018; 26(3):377-385.  https://doi.org/10.1177/1933719118773490
  40. Wang Z, Li Y, Kong D, Sarkar FH. The Role of Notch Signaling Pathway in Epithelial-Mesenchymal Transition (EMT) During Development and Tumor Aggressiveness. Current Drug Targets. 2010; 11(6):745-751.  https://doi.org/10.2174/138945010791170860
  41. Cobellis L, Caprio F, Trabucco E, Mastrogiacomo A, Coppola G, Manente L, Colacurci N, De Falco M, De Luca A. The pattern of expression of Notch protein members in normal and pathological endometrium. Journal of Anatomy. 2008;213(4):464-472.  https://doi.org/10.1111/j.1469-7580.2008.00963.x
  42. Zhang Q, Duan J, Olson M, Fazleabas A, Guo S. Cellular Changes Consistent with Epithelial-Mesenchymal Transition and Fibroblast-to-Myofibroblast Transdifferentiation in the Progression of Experimental Endometriosis in Baboons. Reproductive Sciences. 2016;23(10):1409-1421. https://doi.org/10.1177/1933719116641763
  43. Liu X, Shen M, Qi Q, Zhang H, Guo S. Corroborating evidence for platelet-induced epithelial-mesenchymal transition and fibroblast-to-myofibroblast transdifferentiation in the development of adenomyosis. Human Reproduction. 2016;31(4):734-749.  https://doi.org/10.1093/humrep/dew018
  44. Huang TS, Chen YJ, Chou TY, Chen CY, Li HY, Huang BS, Tsai HW, Lan HY, Chang CH, Twu NF, Yen MS, Wang PH, Chao KC, Lee CC, Yang MH. Oestrogen-induced angiogenesis promotes adenomyosis by activating the Slug-VEGF axis in endometrial epithelial cells. Journal of Cellular and Molecular Medicine. 2014;18(7): 1358-1371. https://doi.org/10.1111/jcmm.12300
  45. Yang L, Tang L, Dai F, Meng G, Yin R, Xu X, Yao W. Raf-1/CK2 and RhoA/ROCK signaling promote TNF-α-mediated endothelial apoptosis via regulating vimentin cytoskeleton. Toxicology. 2017; 389:74-84.  https://doi.org/10.1016/j.tox.2017.07.010
  46. Ghasemi A, Hashemy S, Aghaei M, Panjehpour M. RhoA/ROCK pathway mediates leptin-induced uPA expression to promote cell invasion in ovarian cancer cells. Cellular Signalling. 2017;32:104-114.  https://doi.org/10.1016/j.cellsig.2017.01.020
  47. Wang S, Duan H, Zhang Y, Sun F. Abnormal Activation of RhoA/ROCK-I Signaling in Junctional Zone Smooth Muscle Cells of Patients with Adenomyosis. Reproductive Sciences. 2015;23(3):333-341.  https://doi.org/10.1177/1933719115602764
  48. Jiang Q, Xia J, Ding H, Fei X, Lin J, Wu R. RNAi-mediated blocking of ezrin reduces migration of ectopic endometrial cells in endometriosis. Molecular Human Reproduction. 2012;18(9):435-441.  https://doi.org/10.1093/molehr/gas019
  49. Jiang C, Gong W, Chen R, Ke H, Qu X, Yang W, Cheng Z. RhoA/ROCK/ARHGAP26 signaling in the eutopic and ectopic endometrium is involved in clinical characteristics of adenomyosis. Journal of International Medical Research. 2018;46(12):5019-5029. https://doi.org/10.1177/0300060518789038
  50. Makker A, Goel M. Tumor progression, metastasis, and modulators of epithelial-mesenchymal transition in endometrioid endometrial carcinoma: an update. Endocrine-Related Cancer. 2015;23(2): R85-R111. https://doi.org/10.1530/erc-15-0218
  51. Hu H, Li H, He Y. MicroRNA-17 downregulates expression of the PTEN gene to promote the occurrence and development of adenomyosis. Experimental and Therapeutic Medicine. 2017;14(4):3805-3811. https://doi.org/10.3892/etm.2017.5013
  52. Parasuraman P, Mulligan P, Walker JA, Li B, Boukhali M, Haas W, Bernards A. Interaction of p190A RhoGAP with eIF3A and Other Translation Preinitiation Factors Suggests a Role in Protein Biosynthesis. Journal of Biological Chemistry. 2017;292(7):2679-2689. https://doi.org/10.1074/jbc.m116.769216
  53. Cai X, Shen M, Liu X, Guo S. Reduced Expression of Eukaryotic Translation Initiation Factor 3 Subunit e and Its Possible Involvement in the Epithelial—Mesenchymal Transition in Endometriosis. Reproductive Sciences. 2017;25(1):102-109.  https://doi.org/10.1177/1933719117702248
  54. Shen X, Duan H, Wang S, Gan L, Xu Q, Li J. Decreased Expression of Cannabinoid Receptors in the Eutopic and Ectopic Endometrium of Patients with Adenomyosis. BioMed Research International. 2019;2019:5468954. https://doi.org/10.1155/2019/5468954

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