The role of polymorphic variants of the kisspeptin gene in the pathogenesis of ovarian insufficiency in patients with type 1 diabetes mellitus, genital endometriosis and combination of these diseases

Abstract

BACKGROUND: Type 1 diabetes mellitus and genital endometriosis have a negative impact on female reproductive system. There is an opinion that kisspeptin plays an important role in the pathogenesis of ovarian insufficiency in patients with diabetes and endometriosis.

AIM: The aim of this study was to evaluate the role of the kisspeptin gene (KISS1) polymorphism in the pathogenesis of ovarian insufficiency in patients with type 1 diabetes mellitus, genital endometriosis and in women with combination of these diseases.

MATERIALS AND METHODS: The allele and genotype frequencies of the polymorphic variants rs5780218 (c.–145delT) and rs3924587 (c.–89G>A) of the KISS1 gene were evaluated in 258 women using polymerase chain reaction-restriction fragment length polymorphism technique. This study included 73 patients with type 1 diabetes mellitus, 83 patients with genital endometriosis, 35 patients with combination of type 1 diabetes mellitus and genital endometriosis, and 67 control subjects. The control group is represented by women of the population.

RESULTS: The analysis of the KISS1 gene showed that incidence rates of type 1 diabetes mellitus, genital endometriosis and combination of these diseases do not differ in the presence of the ins/del, del/del, and ins/ins (rs5780218) genotypes. Thus, the del allele and the ins/del and del/del genotypes are not associated with an increased risk of these diseases. It was found that in patients with type 1 diabetes mellitus, the frequency of normogonadotropic ovarian insufficiency was higher (odds ratio 15.955; 95% confidence interval 4,47–57,0; p < 0.05) in the presence of the G/A genotype according to the polymorphic variant rs3924587 compared to the G/G genotype.

CONCLUSIONS: The data obtained allow for explaining the high incidence of ovarian insufficiency in women with type 1 diabetes mellitus. In patients with type 1 diabetes mellitus with the G/A genotype who are planning pregnancy, even in case of regular menstrual cycle, it is advisable to perform hormone blood tests in dynamics for timely diagnosis of ovarian insufficiency and prescription of hormonal therapy.

Keywords

kisspeptin 1 gene (KISS1) / kisspeptin 1 receptor gene (KISS1R) / kisspeptin / type 1 diabetes mellitus / genital endometriosis / normogonadotropic ovarian insufficiency

References

[1] Dedov II, Shestakova MV, Vikulova OK, et al. Epidemiological characteristics of diabetes mellitus in the Russian Federation: clinical and statistical analysis according to the Federal diabetes register data of 01.01.2021. Diabetes mellitus. 2021;24(3):204–221. (In Russ.) DOI: 10.14341/DM12759

[2] Дедов И.И., Шестакова М.В., Викулова О.К., и др. Эпидемиологические характеристики сахарного диабета в Российской Федерации: клинико-статистический анализ по данным регистра сахарного диабета на 01.01.2021 // Сахарный диабет. 2021. Т. 24. № 3. С. 204–221. DOI: 10.14341/DM12759

[3] Deltsidou A, Lemonidou C, Zarikas V, et al. Oligomenorrhoea in adolescents with type 1 diabetes mellitus: relationship to glycaemic control. Eur J Obstet Gynecol Reprod Biol. 2010;153(1):62–66. DOI: 10.1016/j.ejogrb.2010.07.027

[4] Deltsidou A., Lemonidou C., Zarikas V., et al. Oligomenorrhoea in adolescents with type 1 diabetes mellitus: relationship to glycaemic control // Eur. J. Obstet. Gynecol. Reprod. Biol. 2010. Vol. 153. No. 1. P. 62–66. DOI: 10.1016/j.ejogrb.2010.07.027

[5] Sibirskaia EV, Adamyan LV, Koltunov IE, et al. Menstrual function in girls with diabetes mellitus 1 type. Russian Journal of Human Reproduction. 2015;21(3):84-88. (In Russ.) DOI: 10.17116/repro201521384-88

[6] Сибирская Е.В., Адамян Л.В., Колтунов И.Е., и др. Менструальная функция девочек, больных сахарным диабетом 1 типа // Проблемы репродукции. 2015. № 3. С. 84–88. DOI: 10.17116/repro201521384-88

[7] Tolpygina MG, Tarasova MA, Borovik NV, et al. Effect of diabetes compensation on ovarian function recovery in women of reproductive age with type 1 diabetes mellitus. Journal of Obstetrics and Women’s Diseases. 2018;67(5):42–49. DOI: 10.17816/JOWD67542-49

[8] Толпыгина М.Г., Тарасова М.А., Боровик Н.В., и др. Влияние компенсации углеводного обмена на восстановление овуляторной функции у женщин репродуктивного возраста с сахарным диабетом 1-го типа // Журнал акушерства и женских болезней. 2018. Т. 67. № 5. С. 42–49. DOI: 10/17816/JOWD67542-49

[9] Castellano JM, Bentsen AH, Mikkelsen JD, et al. Kisspeptins: bridging energy homeostasis and reproduction. Brain Res. 2010;1364:129–138. DOI: 10.1016/j.brainres.2010.08.057

[10] Castellano J.M., Bensen A.H., Mikkelsen J.D., et al. Kisspeptins: bridging energy homeostasis and reproduction // Brain Res. 2010. Vol. 1364. P. 129–138. DOI: 10.1016/j.drainres.2010.08.057

[11] Kauffman AS, Park JH, McPhie-Lalmansingh AA, et al. The kisspeptin receptor GPR54 is required for sexual differentiation of the brain and behavior. J Neurosci. 2007;27(33):8826–8835. DOI: 10.1523/JNEUROSCI.2099-07.2007

[12] Kauffman A.S., Park J.H., McPhie-Lalmansingh A.A., et al. The kisspeptin receptor GPR54 is required for sexual differentiation of the brain and behavior // J. Neurosci. 2007. Vol. 27. No. 33. P. 8826–8835. DOI: 10.1523/JNEUROSCI.2099-07.2007

[13] Liu N, Lapcevich RK, Underhill CB, et al. Metastatin: a hyaluronan-binding complex from cartilage that inhibits tumor growth. Cancer Res. 2001;61(3):1022–1028.

[14] Liu N., Lapcevich R.K., Underhill C.B., et al. Metastatin: a hyaluronan-binding complex from cartilage that inhibits tumor growth // Cancer Res. 2001. Vol. 61. No. 3. P. 1022–1028.

[15] Lapatto R, Pallais JC, Zhang D, et al. Kiss1-/- mice exhibit more variable hypogonadism than Gpr54-/- mice. Endocrinology. 2007;148(10):4927–4936. DOI: 10.1210/en.2007-0078

[16] Lapatto R., Pallais J.C., Zhang D., et al. Kiss1-/- mice exhibit more variable hypogonadism than Gpr54-/- mice // Endocrinology. 2007. Vol. 148. No. 10. P. 4927–4936. DOI: 10.1210/en.2007-0078

[17] Teles MG, Bianco SD, Brito VN, et al. A GPR54-activating mutation in a patient with central precocious puberty. N Engl J Med. 2008;358(7):709–715. DOI: 10.1056/NEJMoa073443

[18] Teles M.G., Bianco S.D., Brito V.N., et al. A GPR54-activating mutation in a patient with central precocious puberty // N. Engl. J. Med. 2008. Vol. 358. No. 7. P. 709–715. DOI: 10.1056/NEJMoa073443

[19] West A, Vojta PJ, Welch DR, et al. Chromosome localization and genomic structure of the KiSS-1 metastasis suppressor gene (KISS1). Genomics. 1998;54(1):145–148. DOI: 10.1006/geno.1998.5566

[20] West A., Vojta P.J., Welch D.R., et al. Chromosome localization and genomic structure of the KiSS-1 metastasis suppressor gene (KISS1) // Genomics. 1998. Vol. 54. No. 1. P. 145–148. DOI: 10.1006/geno.1998.5566

[21] Ohtaki T, Shintani Y, Honda S, et al. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature. 2001;411(6837):613–617. DOI: 10.1038/35079135

[22] Ohtaki T., Shintani Y., Honda S., et al. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor // Nature. 2001. Vol. 411. No. 6837. P. 613–617. DOI: 10.1038/35079135

[23] Topaloglu AK, Tello JA, Kotan LD, et al. Inactivating KISS1 mutation and hypogonadotropic hypogonadism. N Engl J Med. 2012;366(7):629–635. DOI: 10.1056/NEJMoa1111184

[24] Topaloglu A.K., Tello J.A., Kotan L.D., et al. Inactivating KISS1 mutation and hypogonadotropic hypogonadism // N. Engl. J. Med. 2012. Vol. 366. No. 7. P. 629–635. DOI: 10.1056/NEJMoa1111184

[25] Seminara SB, Messager S, Chatzidaki EE, et al. The GPR54 gene as a regulator of puberty. N Engl J Med. 2003;349(17):1614–1627. DOI: 10.1056/NEJMoa035322

[26] Seminara S.B., Messager S., Chatzidaki E.E., et al. The GPR54 gene as a regulator of puberty // N. Engl. J. Med. 2003. Vol. 349. No. 17. P. 1614–1627. DOI: 10.1056/NEJMoa035322

[27] Funes S, Hedrick JA, Vassileva G, et al. The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun. 2003;312(4):1357–1363. DOI: 10.1016/j.bbrc.2003.11.066

[28] Funes S., Hedrick J.A., Vassileva G., et al. The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system // Biochem. Biophys. Res. Commun. 2003. Vol. 312. No. 4. P. 1357–1363. DOI: 10.1016/j.bbrc.2003.11.066

[29] : Endotext [Internet]. Marques P, Skorupskaite K, Rozario KS, et al. Physiology of GnRH and Gonadotropin Secretion. 2000 [cited 2023 Jun 13]. Available from: https://www.ncbi.nlm.nih.gov/books/NBK279070/

[30] Endotext [Internet]. Marques P., Skorupskaite K., Rozario K.S., et al. Physiology of GnRH and gonadotropin secretion [дата обращения: 13.06.2023]. Доступ по ссылке: https://www.ncbi.nlm.nih.gov/books/NBK279070/

[31] Goodman RL, Herbison AE, Lehman MN, et al. Neuroendocrine control of gonadotropin-releasing hormone: pulsatile and surge modes of secretion. J Neuroendocrinol. 2022;34(5). DOI: 10.1111/jne.13094

[32] Goodman R.L., Herbison A.E., Lehman M.N., et al. Neuroendocrine control of gonadotropin-releasing hormone: pulsatile and surge modes of secretion // J. Neuroendocrinol. 2022. Vol. 34. No. 5. DOI: 10.1111/jne.13094

[33] Ruohonen ST, Gaytan F, Usseglio Gaudi A, et al. Selective loss of kisspeptin signaling in oocytes causes progressive premature ovulatory failure. Hum Reprod. 2022;37(4):806–821. DOI: 10.1093/humrep/deab287

[34] Ruohonen S.T., Gaytan F., Usseglio Gaudi A., et al. Selective loss of kisspeptin signaling in oocytes causes progressive premature ovulatory failure // Hum. Reprod. 2022. Vol. 37, No. 4. P. 806–821. DOI: 10.1093/humrep/deab287

[35] Ruohonen ST, Poutanen M, Tena-Sempere M. Role of kisspeptins in the control of the hypothalamic-pituitary-ovarian axis: old dogmas and new challenges. Fertil Steril. 2020;114(3):465–474. DOI: 10.1016/j.fertnstert.2020.06.038

[36] Ruohonen S.T., Poutanen M., Tena-Sempere M. Role of kisspeptins in the control of the hypothalamic-pituitary-ovarian axis: old dogmas and new challenges // Fertil. Steril. 2020. Vol. 114. No. 3. P. 465–474. DOI: 10.1016/j.fertnstert.2020.06.038

[37] Masumi S, Lee EB, Dilower I, et al. The role of Kisspeptin signaling in Oocyte maturation. Front Endocrinol (Lausanne). 2022;13. DOI: 10.3389/fendo.2022.917464

[38] Masumi S., Lee E.B., Dilower I., et al. The role of Kisspeptin signaling in Oocyte maturation // Front. Endocrinol. (Lausanne). 2022. Vol. 13. DOI: 10.3389/fendo.2022.917464

[39] Jayasena CN, Abbara A, Comninos AN, et al. Kisspeptin-54 triggers egg maturation in women undergoing in vitro fertilization. J Clin Invest. 2014;124(8):3667–3677. DOI: 10.1172/JCI75730

[40] Jayasena C.N., Abbara A., Comninos A.N., et al. Kisspeptin-54 triggers egg maturation in women undergoing in vitro fertilization // J. Clin. Invest. 2014. Vol. 124. No. 8. P. 3667–3677. DOI: 10.1172/JCI75730

[41] Abbara A, Jayasena CN, Christopoulos G, et al. Efficacy of kisspeptin-54 to trigger oocyte maturation in women at high risk of Ovarian Hyperstimulation Syndrome (OHSS) during In Vitro Fertilization (IVF) therapy. J Clin Endocrinol Metab. 2015;100(9):3322–3331. DOI: 10.1210/jc.2015-2332

[42] Abbara A., Jayasena C.N., Christopoulos G., et al. Efficacy of kisspeptin-54 to trigger oocyte maturation in women at high risk of Ovarian Hyperstimulation Syndrome (OHSS) during In Vitro Fertilization (IVF) therapy // J. Clin. Endocrinol. Metab. 2015. Vol. 100. No. 9. P. 3322–3331. DOI: 10.1210/jc.2015-2332

[43] Hu KL, Chen Z, Li X, et al. Advances in clinical applications of kisspeptin-GnRH pathway in female reproduction. Reprod Biol Endocrinol. 2022;20(1). DOI: 10.1186/s12958-022-00953-y

[44] Hu K.L., Chen Z., Li X., et al. Advances in clinical applications of kisspeptin-GnRH pathway in female reproduction // Reprod. Biol. Endocrinol. 2022. Vol. 20. No. 1. DOI: 10.1186/s12958-022-00953-y

[45] Abbara A, Clarke S, Islam R, et al. A second dose of kisspeptin-54 improves oocyte maturation in women at high risk of ovarian hyperstimulation syndrome: a phase 2 randomized controlled trial. Hum Reprod. 2017;32(9):1915–1924. DOI: 10.1093/humrep/dex253

[46] Abbara A., Clarke S., Islam R., et al. A second dose of kisspeptin-54 improves oocyte maturation in women at high risk of ovarian hyperstimulation syndrome: a Phase 2 randomized controlled trial // Hum. Reprod. 2017. Vol. 32. No. 9. P. 1915–1924. DOI: 10.1093/humrep/dex253

[47] Dudek M, Kołodziejski PA, Pruszyńska-Oszmałek E, et al. Effects of high-fat diet-induced obesity and diabetes on Kiss1 and GPR54 expression in the Hypothalamic-Pituitary-Gonadal (HPG) axis and peripheral organs (fat, pancreas and liver) in male rats. Neuropeptides. 2016;56:41–49. DOI: 10.1016/j.npep.2016.01.005

[48] Dudek M., Kołodziejski P.A., Pruszyńska-Oszmałek E., et al. Effects of high-fat diet-induced obesity and diabetes on Kiss1 and GPR54 expression in the hypothalamic-pituitary-gonadal (HPG) axis and peripheral organs (fat, pancreas and liver) in male rats // Neuropeptides. 2016. Vol. 56. P. 41–49. DOI: 10.1016/j.npep.2016.01.005

[49] Bowe JE, Foot VL, Amiel SA, et al. GPR54 peptide agonists stimulate insulin secretion from murine, porcine and human islets. Islets. 2012;4(1):20–23. DOI: 10.4161/isl.18261

[50] Bowe J.E., Foot V.L., Amiel S.A, et al. GPR54 peptide agonists stimulate insulin secretion from murine, porcine and human islets // Islets. 2012. Vol. 4. No. 1. P. 20–23. DOI: 10.4161/isl.18261

[51] Cockwell H, Wilkinson DA, Bouzayen R, et al. KISS1 expression in human female adipose tissue. Arch Gynecol Obstet. 2013;287(1):143–147. DOI: 10.1007/s00404-012-2514-0

[52] Cockwell H., Wilkinson D.A., Bouzayen R., et al. KISS1 expression in human female adipose tissue // Arch. Gynecol. Obstet. 2013. Vol. 287. No. 1. P. 143–147. DOI: 10.1007/s00404-012-2514-0

[53] Yamasaki M, Kuwahara A, Iwasa T, et al. Development-related changes in the expression of the ovarian Kiss1 and Kiss1r genes and their sensitivity to human chorionic gonadotropin in prepubertal female rats. J Reprod Dev. 2017;63(4):409–414. DOI: 10.1262/jrd.2016-179

[54] Yamasaki M., Kuwahara A., Iwasa T., et al. Development-related changes in the expression of the ovarian Kiss1 and Kiss1r genes and their sensitivity to human chorionic gonadotropin in prepubertal female rats // J. Reprod. Dev. 2017. Vol. 63. No. 4. P. 409–414. DOI: 10.1262/jrd.2016-179

[55] Chakravarthi VP, Khristi V, Ghosh S, et al. ESR2 is essential for gonadotropin-induced Kiss1 expression in granulosa cells. Endocrinology. 2018;159(11):3860–3873. DOI: 10.1210/en.2018-00608

[56] Chakravarthi V.P., Khristi V., Ghosh S., et al. ESR2 is essential for gonadotropin-induced kiss1 expression in granulosa cells // Endocrinology. 2018. Vol. 159. No. 11. P. 3860–3873. DOI: 10.1210/en.2018-00608

[57] Radovick S, Babwah AV. Regulation of Pregnancy: evidence for major roles by the uterine and placental kisspeptin/KISS1R signaling systems. Semin Reprod Med. 2019;37(4):182–190. DOI: 10.1055/s-0039-3400966

[58] Radovick S., Babwah A.V. Regulation of pregnancy: evidence for major roles by the uterine and placental kisspeptin/KISS1R signaling systems // Semin. Reprod. Med. 2019. Vol. 37. No. 4. P. 182–190. DOI: 10.1055/s-0039-3400966

[59] Schaefer J, Vilos AG, Vilos GA, et al. Uterine kisspeptin receptor critically regulates epithelial estrogen receptor α transcriptional activity at the time of embryo implantation in a mouse model. Mol Hum Reprod. 2021;27(10). DOI: 10.1093/molehr/gaab060

[60] Schaefer J., Vilos A.G., Vilos G.A., et al. Uterine kisspeptin receptor critically regulates epithelial estrogen receptor α transcriptional activity at the time of embryo implantation in a mouse model // Mol. Hum. Reprod. 2021. Vol. 27. No. 10. DOI: 10.1093/molehr/gaab060

[61] Navarro VM, Castellano JM, Fernández-Fernández R, et al. Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology. 2005;146(1):156–163. DOI: 10.1210/en.2004-0836

[62] Navarro V.M., Castellano J.M., Fernández-Fernández R., et al. Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54 // Endocrinology. 2005. Vol. 146. No. 1. P. 156–163. DOI: 10.1210/en.2004-0836

[63] Backholer K, Bowden M, Gamber K, et al. Melanocortins mimic the effects of leptin to restore reproductive function in lean hypogonadotropic ewes. Neuroendocrinology. 2010;91(1):27–40. DOI: 10.1159/000260060

[64] Backholer K., Bowden M., Gamber K., et al. Melanocortins mimic the effects of leptin to restore reproductive function in lean hypogonadotropic ewes // Neuroendocrinology. 2010. Vol. 91. No. 1. P. 27–40. DOI: 10.1159/000260060

[65] Yarmolinskaya MI, Ailamazyan EK. Genital’nyi endometrioz. Razlichnye grani problemy. Saint Petersburg: Eсo-Veсtor; 2017. (In Russ.)

[66] Ярмолинская М.И., Айламазян Э.К. Генитальный эндометриоз. Различные грани проблемы. Санкт Петербург: Эко-Вектор, 2017.

[67] Simmen RCM, Brown DM, Quick CM, et al. Co-morbidity of type 1 diabetes and endometriosis: bringing a new paradigm into focus. J Endocrinol. 2019;243: R47–R57. DOI: 10.1530/JOE-19-0248

[68] Simmen R.C.M., Brown D.M,. Quick C.M., et al. Co-morbidity of type 1 diabetes and endometriosis: bringing a new paradigm into focus // J. Endocrinol. 2019. Vol. 243. P. R47–R57. DOI: 10.1530/JOE-19-0248

[69] Osum KC, Burrack AL, Martinov T, et al. Interferon-gamma drives programmed death-ligand 1 expression on islet β cells to limit T cell function during autoimmune diabetes. Sci Rep. 2018;8(1). DOI: 10.1038/s41598-018-26471-9

[70] Osum K.C., Burrack A.L., Martinov T., et al. Interferon-gamma drives programmed death-ligand 1 expression on islet β cells to limit T cell function during autoimmune diabetes // Sci. Rep. 2018. Vol. 8. No. 1. DOI: 10.1038/s41598-018-26471-9

[71] Gueuvoghlanian-Silva BY, Bellelis P, Barbeiro DF, et al. Treg and NK cells related cytokines are associated with deep rectosigmoid endometriosis and clinical symptoms related to the disease. J Reprod Immunol. 2018;126:32–38. DOI: 10.1016/j.jri.2018.02.003

[72] Gueuvoghlanian-Silva B.Y., Bellelis P., Barbeiro D.F., et al. Treg and NK cells related cytokines are associated with deep rectosigmoid endometriosis and clinical symptoms related to the disease // J. Reprod. Immunol. 2018. Vol. 126. P. 32–38. DOI: 10.1016/j.jri.2018.02.003

[73] Kocbek V, Grandi G, Blank F, et al. TNFα-induced IKKβ complex activation influences epithelial, but not stromal cell survival in endometriosis. Mol Hum Reprod. 2016;22(11):768–777. DOI: 10.1093/molehr/gaw054

[74] Kocbek V., Grandi G., Blank F., et al. TNFα-induced IKKβ complex activation influences epithelial, but not stromal cell survival in endometriosis // Mol. Hum. Reprod. 2016. Vol. 22. No. 11. P. 768–777. DOI: 10.1093/molehr/gaw054

[75] Qiao YC, Chen YL, Pan YH, et al. The change of serum tumor necrosis factor alpha in patients with type 1 diabetes mellitus: a systematic review and meta-analysis. PLoS One. 2017;12(4). DOI: 10.1371/journal.pone.0176157

[76] Qiao Y.C., Chen Y.L., Pan Y.H., et al. The change of serum tumor necrosis factor alpha in patients with type 1 diabetes mellitus: a systematic review and meta-analysis // PLoS One. 2017. Vol. 12. No. 4. DOI: 10.1371/journal.pone.0176157

[77] Nothnick WB, Falcone T, Olson MR, et al. macrophage migration inhibitory factor receptor, CD74, is overexpressed in human and baboon (papio anubis) endometriotic lesions and modulates endometriotic epithelial cell survival and interleukin 8 expression. Reprod Sci. 2018;25(11):1557–1566. DOI: 10.1177/1933719118766262

[78] Nothnick W.B., Falcone T., Olson M.R., et al. Macrophage migration inhibitory factor receptor, cd74, is overexpressed in human and baboon (papio anubis) endometriotic lesions and modulates endometriotic epithelial cell survival and interleukin 8 expression // Reprod. Sci. 2018. Vol. 25. No. 11. P. 1557–1566. DOI: 10.1177/1933719118766262

[79] Sánchez-Zamora YI, Juarez-Avelar I, Vazquez-Mendoza A, et al. Altered macrophage and dendritic cell response in Mif-/- mice reveals a role of Mif for inflammatory-Th1 response in type 1 diabetes. J Diabetes Res. 2016;2016. DOI: 10.1155/2016/7053963

[80] Sánchez-Zamora Y.I., Juarez-Avelar I., Vazquez-Mendoza A., et al. Altered macrophage and dendritic cell response in Mif-/- mice reveals a role of Mif for inflammatory-Th1 response in type 1 diabetes // J. Diabetes Res. 2016. Vol. 2016. DOI: 10.1155/2016/7053963

[81] Gou Y, Li X, Li P, et al. Estrogen receptor β upregulates CCL2 via NF-κB signaling in endometriotic stromal cells and recruits macrophages to promote the pathogenesis of endometriosis. Hum Reprod. 2019;34(4):646–658. DOI: 10.1093/humrep/dez019

[82] Gou Y., Li X., Li P., et al. Estrogen receptor β upregulates CCL2 via NF-κB signaling in endometriotic stromal cells and recruits macrophages to promote the pathogenesis of endometriosis // Hum. Reprod. 2019. Vol. 34. No. 4. P. 646–658. DOI: 10.1093/humrep/dez019

[83] Burns KA, Thomas SY, Hamilton KJ, et al. Early endometriosis in females is directed by immune-mediated estrogen receptor α and IL-6 cross-talk. Endocrinology. 2018;159(1):103–118. DOI: 10.1210/en.2017-00562

[84] Burns K.A., Thomas S.Y., Hamilton K.J., et al. Early endometriosis in females is directed by immune-mediated estrogen receptor α and IL-6 cross-talk // Endocrinology. 2018. Vol. 159. No. 1. P. 103–118. DOI: 10.1210/en.2017-00562

[85] Waugh K, Snell-Bergeon J, Michels A, et al. Increased inflammation is associated with islet autoimmunity and type 1 diabetes in the Diabetes Autoimmunity Study in the Young (DAISY). PLoS One. 2017;12(4). DOI: 10.1371/journal.pone.0174840

[86] Waugh K., Snell-Bergeon J., Michels A., et al. Increased inflammation is associated with islet autoimmunity and type 1 diabetes in the Diabetes Autoimmunity Study in the Young (DAISY) // PLoS One. 2017. Vol. 12. No. 4. DOI: 10.1371/journal.pone.0174840

[87] Medikamentoznaya terapiya genital’nogo endometrioza: realii i erspektivy: rukoodstvo dlya vrachei Ed. by M.I. Yarmolinskaya. Moscow: GEOTAR-Media; 2021. (In Russ.) DOI: 10.33029/9704-6034-4-MET-2021-1-384

[88] Медикаментозная терапия генитального эндометриоза: реалии и перспективы: руководство для врачей / под ред. М.И. Ярмолинской. Москва: ГЭОТАР-Медиа, 2021. DOI: 10.33029/9704-6034-4-МЕТ-2021-1-384

[89] Yarmolinskaya M.I. Cytokine profile of peritoneal fluid and paerpheral blood in patients with pelvic endometriosis. Journal of Obstetrics and Women’s Diseases. 2008;57(3):30–34. (In Russ.)

[90] Ярмолинская М.И. Цитокиновый профиль перитонеальной жидкости и периферической крови больных с наружным генитальным эндометриозом // Журнал акушерства и женских болезней. 2008. Т. 57. № 3. С. 30–34.

[91] Yarmolinskaya MI, Ganbarli NF, Tkachenko NN, et al. Kisspeptin and polycystic ovary syndrome — is there any connection? Journal of Obstetrics and Women’s Diseases. 2017;66(6):73–80. (In Russ.) DOI: 10.17816/JOWD66673-80

[92] Ярмолинская М.И., Ганбарли Н.Ф., Ткаченко Н.Н., и др. Кисспептин и синдром поликистозных яичников — есть ли связь? // Журнал акушерства и женских болезней. 2017. Т. 66. № 6. C. 73–80. DOI: 10.17816/JOWD66673-80

[93] Timologou A, Zafrakas M, Grimbizis G, et al. Immunohistochemical expression pattern of metastasis suppressors KAI1 and KISS1 in endometriosis and normal endometrium. Eur J Obstet Gynecol Reprod Biol. 2016;199:110–115. DOI: 10.1016/j.ejogrb.2016.02.004

[94] Timologou A., Zafrakas M., Grimbizis G., et al. Immunohistochemical expression pattern of metastasis suppressors KAI1 and KISS1 in endometriosis and normal endometrium // Eur. J. Obstet. Gynecol. Reprod. Biol. 2016. Vol. 199. P. 110–115. DOI: 10.1016/j.ejogrb.2016.02.004

[95] Blasco V, Pinto FM, Fernández-Atucha A, et al. Female infertility is associated with an altered expression of the neurokinin B/neurokinin B receptor and kisspeptin/kisspeptin receptor systems in ovarian granulosa and cumulus cells. Fertil Steril. 2020;114(4):869–878. DOI: 10.1016/j.fertnstert.2020.05.006

[96] Blasco V., Pinto F.M., Fernández-Atucha A., et al. Female infertility is associated with an altered expression of the neurokinin B/neurokinin B receptor and kisspeptin/kisspeptin receptor systems in ovarian granulosa and cumulus cells // Fertil. Steril. 2020. Vol. 114. No. 4. P. 869–878. DOI: 10.1016/j.fertnstert.2020.05.006

[97] Codner E, Merino PM, Tena-Sempere M. Female reproduction and type 1 diabetes: from mechanisms to clinical findings. Hum Reprod Update. 2012;18(5):568–585. DOI: 10.1093/humupd/dms024

[98] Codner E., Merino P.M., Tena-Sempere M. Female reproduction and type 1 diabetes: from mechanisms to clinical findings // Hum. Reprod. Update. 2012. Vol. 18. No. 5. P. 568–585. DOI: 10.1093/humupd/dms024

[99] Sakharnyi diabet i reproduktivnaya sistema zhenshchiny: rukovodstvo dlya vrachei. Ed. by E.K. Ailamazyan, E.I. Abashova, O.N. Arzhanova, et al. Moscow: GEOTAR-Media; 2017. (In Russ.)

[100] Сахарный диабет и репродуктивная система женщины: руководство для врачей / под ред. Э.К. Айламазян, Е.И. Абашовой, О.Н. Аржановой, и др. Москва: ГЭОТАР-Медиа, 2017.

[101] Grigoryan OR, Krasnovskaya NS, Mikheev RK, et al. Ovarian reserve in reproductive age women with type 1 diabetes. Diabetes mellitus. 2018;21(4):264–270. (In Russ.) DOI: 10.14341/DM9480

[102] Григорян О.Р., Красновская Н.С., Михеев Р.К., и др. Состояние овариального резерва у женщин с сахарным диабетом 1 типа в репродуктивном периоде // Сахарный диабет. 2018. Т. 21. № 4. С. 264–270. DOI: 10.14341/DM9480

[103] Jonasson JM, Brismar K, Sparén P, et al. Fertility in women with type 1 diabetes: a population-based cohort study in Sweden. Diabetes Care. 2007;30(9):2271–2276. DOI: 10.2337/dc06-2574

[104] Jonasson J.M., Brismar K., Sparén P., et al. Fertility in women with type 1 diabetes: a population-based cohort study in Sweden // Diabetes Care. 2007. Vol. 30. No. 9. P. 2271–2276. DOI: 10.2337/dc06-2574

[105] Poteen VV, Borovik NV, Tiselko AV. Diabetes mellitus and female reproductive system. Journal of Obstetrics and Women’s Diseases. 2006;55(1):85–89. (In Russ.)

[106] Потин В.В., Боровик Н.В., Тиселько А.В. Сахарный диабет и репродуктивная система женщины // Журнал акушерства и женских болезней. 2006. Т. 55. № 1. С. 85–89.

[107] Ailamazyan EK, Yarmolinskaya MI, Ganbarli NF, et al. The role of metastin in pathogenesis of genital endometriosis. Journal of Obstetrics and Women’s Diseases. 2017;66(3):16–24. (In Russ.) DOI: 10.17816/JOWD66316-24

[108] Айламазян Э.К., Ярмолинская М.И., Ганбарли Н.Ф. и др. Роль метастина в патогенезе наружного генитального эндометриоза // Журнал акушерства и женских болезней. 2017. Т. 66. № 3. C. 16–24. DOI: 10.17816/JOWD66316-24

RIGHTS & PERMISSIONS

Eсо-Vector