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Оценка экспрессии гликанов в эпителиальных структурах эндометрия как предиктивный фактор рецептивности эндометрия
Оценка экспрессии гликанов в эпителиальных структурах эндометрия как предиктивный фактор рецептивности эндометрия
Зиганшина М.М., Долгушина Н.В., Куликова Г.В. и др. Оценка экспрессии гликанов в эпителиальных структурах эндометрия как предиктивный фактор рецептивности эндометрия. Гинекология. 2020; 22 (6): 38–43. DOI: 10.26442/20795696.2020.6.200490
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Аннотация
Цель. Оценить гликотип эндометрия в «окно имплантации» у пациенток с бесплодием в программах вспомогательных репродуктивных технологий (ВРТ) и разработать критерии оценки рецептивности эндометрия на основе анализа комплексного изменения функциональных групп гликанов в основных эпителиальных структурах эндометрия для использования в клинической практике.
Материалы и методы. В исследование включены 32 пациентки с бесплодием, проходящие лечение в программах ВРТ. Пайпель-биопсия эндометрия проводились в период «окна имплантации» в цикле, предшествующем циклу овариальной стимуляции и переноса эмбрионов. С помощью лектиновой гистохимии и иммуногистохимии исследовано содержание гликанов в гликокаликсе поверхностного эпителия (ПЭ) и железистого эпителия (ЖЭ) эндометрия.
Результаты. Выявлены различия в экспрессии маннозобогатых гликанов в ПЭ и N-ацетилгалактозаминтерминированных гликанов в ЖЭ эндометрия и оценена связь экспрессии гликанов, окрашиваемых лектинами: ConA, VVL, UEA-I, SNA, MAL-II, ECL и моноклональными антителами: анти-МЕСА-79 мАТ и анти-LeY мАТ в ПЭ и ЖЭ эндометрия у пациенток с бесплодием в зависимости от исхода программы ВРТ. Рассчитанные пороговые уровни экспрессии гликанов и отношение шансов наступления беременности позволили дать характеристики диагностической ценности для исследованных гликомаркеров и разработать критерии оценки рецептивности эндометрия.
Заключение. На основании комплексной оценки гликанов в основных эпителиальных структурах эндометрия в цикле, предшествующем циклу ВРТ, разработаны критерии оценки вероятности наступления беременности, что может повысить эффективность программ ВРТ у пациенток с бесплодием.
Ключевые слова: бесплодие, вспомогательные репродуктивные технологии, гликотип эндометрия, иммуногистохимия, лектиновая гистохимия, критерии оценки рецептивности эндометрия.
Materials and methods. The study included 32 infertile patients who took part in ART programs. Pipelle endometrial biopsy was performed during the "implantation window" in the cycle preceding the cycle of ovarian stimulation and embryo transfer. Using lectin histochemistry and immunohistochemistry, glycans levels in the glycocalyx of endometrial surface epithelium (SE) and glandular epithelium (GE) was studied.
Results. Differences in the expression of mannose-rich glycans in SE and N-acetylgalactosamine--terminated glycans in the GE of the endometrium were revealed, as well as the link between the expression of lectin staining glycans: ConA, VVL, UEA-I, SNA, MAL-II, ECL and monoclonal antibodies: anti-MECA -79 mAb and anti-LeY mAb in SE and GE of the endometrium was assessed in patients with infertility, depending on the outcome of the ART program. The estimated threshold levels in glycan expression and the odds ratio for pregnancy occurrence allow to characterize the diagnostic value for the studied glycomarkers and to develop criteria for assessing endometrial receptivity.
Conclusion. Based on a comprehensive evaluation of glycans in the main endometrial epithelial structures in the cycle preceding the ART cycle, criteria for assessment of the likelihood of pregnancy have been developed, which can increase the effectiveness of ART programs in patients with infertility.
Key words: infertility, assisted reproductive technologies, endometrial glycotype, immunohistochemistry, lectin histochemistry, criteria for assessment of endometrial receptivity.
Материалы и методы. В исследование включены 32 пациентки с бесплодием, проходящие лечение в программах ВРТ. Пайпель-биопсия эндометрия проводились в период «окна имплантации» в цикле, предшествующем циклу овариальной стимуляции и переноса эмбрионов. С помощью лектиновой гистохимии и иммуногистохимии исследовано содержание гликанов в гликокаликсе поверхностного эпителия (ПЭ) и железистого эпителия (ЖЭ) эндометрия.
Результаты. Выявлены различия в экспрессии маннозобогатых гликанов в ПЭ и N-ацетилгалактозаминтерминированных гликанов в ЖЭ эндометрия и оценена связь экспрессии гликанов, окрашиваемых лектинами: ConA, VVL, UEA-I, SNA, MAL-II, ECL и моноклональными антителами: анти-МЕСА-79 мАТ и анти-LeY мАТ в ПЭ и ЖЭ эндометрия у пациенток с бесплодием в зависимости от исхода программы ВРТ. Рассчитанные пороговые уровни экспрессии гликанов и отношение шансов наступления беременности позволили дать характеристики диагностической ценности для исследованных гликомаркеров и разработать критерии оценки рецептивности эндометрия.
Заключение. На основании комплексной оценки гликанов в основных эпителиальных структурах эндометрия в цикле, предшествующем циклу ВРТ, разработаны критерии оценки вероятности наступления беременности, что может повысить эффективность программ ВРТ у пациенток с бесплодием.
Ключевые слова: бесплодие, вспомогательные репродуктивные технологии, гликотип эндометрия, иммуногистохимия, лектиновая гистохимия, критерии оценки рецептивности эндометрия.
________________________________________________
Materials and methods. The study included 32 infertile patients who took part in ART programs. Pipelle endometrial biopsy was performed during the "implantation window" in the cycle preceding the cycle of ovarian stimulation and embryo transfer. Using lectin histochemistry and immunohistochemistry, glycans levels in the glycocalyx of endometrial surface epithelium (SE) and glandular epithelium (GE) was studied.
Results. Differences in the expression of mannose-rich glycans in SE and N-acetylgalactosamine--terminated glycans in the GE of the endometrium were revealed, as well as the link between the expression of lectin staining glycans: ConA, VVL, UEA-I, SNA, MAL-II, ECL and monoclonal antibodies: anti-MECA -79 mAb and anti-LeY mAb in SE and GE of the endometrium was assessed in patients with infertility, depending on the outcome of the ART program. The estimated threshold levels in glycan expression and the odds ratio for pregnancy occurrence allow to characterize the diagnostic value for the studied glycomarkers and to develop criteria for assessing endometrial receptivity.
Conclusion. Based on a comprehensive evaluation of glycans in the main endometrial epithelial structures in the cycle preceding the ART cycle, criteria for assessment of the likelihood of pregnancy have been developed, which can increase the effectiveness of ART programs in patients with infertility.
Key words: infertility, assisted reproductive technologies, endometrial glycotype, immunohistochemistry, lectin histochemistry, criteria for assessment of endometrial receptivity.
Полный текст
Список литературы
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[Ziganshina M.M., Abdurakhmanova N.F., Pavlovich S.V. et al. Endometrial glycome in the menstrual cycle and endometrial receptivity. Obstet Gynecol. 2017: 17–24. DOI: 10.18565/aig.2017.12.17-24 (in Russian).]
5. Carson DD. The glycobiology of implantation. Front Biosci 2002; 7 (1): 1535–44. DOI: 10.2741/a858
6. Clark GF. Functional glycosylation in the human and mammalian uterus. Fertil Res Pract 2015; 1 (1): 1–12. DOI: 10.1186/s40738-015-0007-0
7. Aplin JD. Glycans as biochemical markers of human endometrial secretory differentiation. J Reprod Fertil 1991; 92 (2): 525–41. DOI: 10.1530/jrf.0.0920525
8. Aplin JD. Embryo implantation: The molecular mechanism remains elusive. Reprod Biomed Online 2006; 13 (6): 833–9. DOI: 10.1016/S1472-6483(10)61032-2
9. Gu J, Sui LL, Cui D et al. Effects of LeY glycan expression on embryo implantation. Eur Rev Med Pharmacol Sci 2016; 20: 3327–35.
10. Noci I, Gheri G, Gheri Bryk S et al. Aging of the human endometrium: Peri-implantation phase endometrium does not show any age-dependent variation in lectin binding. Eur J Obstet Gynecol Reprod Biol 1996; 64 (1): 11–21. DOI: 10.1016/0301-2115(95)02245-7
11. Nejatbakhsh R, Kabir-Salmani M, Dimitriadis E et al. Subcellular localization of L-selectin ligand in the endometrium implies a novel function for pinopodes in endometrial receptivity. Reprod Biol Endocrinol 2012; 10 (1): 1. DOI: 10.1186/1477-7827-10-46
12. Margarit L, Gonzalez D, Lewis PD et al. L-Selectin ligands in human endometrium: Comparison of fertile and infertile subjects. Hum Reprod 2009; 24 (11): 2767–77. DOI: 10.1093/humrep/dep247
13. Foulk RA, Zdravkovic T, Genbacev O, Prakobphol A. Expression of L-selectin ligand MECA-79 as a predictive marker of human uterine receptivity. J Assist Reprod Genet 2007; 24 (7): 316–21. DOI: 10.1007/s10815-007-9151-8
14. Wang B, Sheng JZ, He RH et al. High expression of L-selectin ligand in secretory endometrium is associated with better endometrial receptivity and facilitates embryo implantation in human being. Am J Reprod Immunol 2008; 60 (2): 127–34. DOI: 10.1111/j.1600-0897.2008.00604.x
15. Приказ Минздрава России №107н от 30 августа 2012 г. «О порядке использования вспомогательных репродуктивных технологий, противопоказаниях и ограничениях к их применению». 2012.
[Prikaz Minzdrava Rossii no. 107n ot 30 avgusta 2012 g “O porjadke ispol’zovanija vspomogatel’nyh reproduktivnyh tehnologij, protivopokazanijah i ogranichenijah k ih primeneniju”. 2012 (In Russian).]
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[Kulikova G.V., Abdurahmanova N.F., Fayzullina N.M. et al. Receptivity of thin endometrium in patients undergoing assisted reproduction. Obstet Gynecol. 2019: 100–7 (in Russian).]
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на Н.В. Результаты программ ВРТ у пациенток с «тонким» эндометрием. Гинекология. 2019; 21 (1): 23–27. DOI: 10.26442/20795696.2019.1.190232
[Abdurakhmanova N.F., Gvozdeva A.D., Ziganshina M.M., Dolgushi-
na N.V. The results of assisted reproductive technology programs in patients with “thin” endometrium. Gynecology. 2019; 21 (1): 23–7. DOI: 10.26442/20795696.2019.1.190232 (in Russian).]
19. Miwa I, Tamura H, Takasaki A et al. Pathophysiologic features of “thin” endometrium. Fertil Steril 2009; 91 (4): 998–1004. DOI: 10.1016/j.fertnstert.2008.01.029
20. Takasaki A, Tamura H, Taketani T et al. A pilot study to prevent a thin endometrium in patients undergoing clomiphene citrate treatment. J Ovarian Res 2013; 6 (1): 6–10. DOI: 10.1186/1757-2215-6-94
21. Weiss NS, van Vliet MN, Limpens J et al. Endometrial thickness in women undergoing IUI with ovarian stimulation. How thick is too thin? A systematic review and meta-analysis. Hum Reprod 2017; 32 (5): 1009–18. DOI: 10.1093/humrep/dex035
22. Rabinovich GA, Croci DO. Regulatory circuits mediated by lectin-glycan interactions in autoimmunity and cancer. Immunity 2012; 36 (3): 322–35. DOI: 10.1016/j.immuni.2012.03.004
23. Kane N, Kelly R, Saunders PTK, Critchley HOD. Proliferation of uterine natural killer cells is induced by human chorionic gonadotropin and mediated via the mannose receptor. Endocrinology 2009; 150 (6): 2882–8. DOI: 10.1210/en.2008-1309
24. Miller DL, Jones CJP, Aplin JD, Nardo LG. Altered glycosylation in peri-implantation phase endometrium in women with stages III and IV endometriosis. Hum Reprod 2010; 25 (2): 406–11. DOI: 10.1093/humrep/dep401
25. Miravet-Valenciano JA, Rincon-Bertolin A, Vilella F, Simon C. Understanding and improving endometrial receptivity. Curr Opin Obstet Gynecol 2015; 27 (3): 187–92. DOI: 10.1097/GCO.0000000000000173
26. Gu J, Isaji T, Xu Q et al. Potential roles of N-glycosylation in cell adhesion. Glycoconj J 2012; 29 (8–9): 599–607. DOI: 10.1007/s10719-012-9386-1
27. Lessey BA. Adhesion molecules and implantation. J Reprod Immunol 2002; 55 (1–2): 101–12. DOI: 10.1016/S0165-0378(01)00139-5
28. Li Y, Ma K, Sun P et al. LeY oligosaccharide upregulates DAG/PKC signaling pathway in the human endometrial cells. Mol Cell Biochem 2009; 331 (1–2): 1–7. DOI: 10.1007/s11010-009-0137-y
2. Oron G, Hiersch L, Rona S et al. Endometrial thickness of less than
7.5 mm is associated with obstetric complications in fresh IVF cycles: a retrospective cohort study. Reprod Biomed Online 2018; 37 (3): 341–8. DOI: 10.1016/j.rbmo.2018.05.013
3. Bashiri A, Halper KI, Orvieto R. Recurrent Implantation Failure-update overview on etiology, diagnosis, treatment and future directions. Reprod Biol Endocrinol 2018; 16 (1): 1–18. DOI: 10.1186/s12958-018-0414-2
4. Ziganshina M.M., Abdurakhmanova N.F., Pavlovich S.V. et al. Endometrial glycome in the menstrual cycle and endometrial receptivity. Obstet Gynecol. 2017: 17–24. DOI: 10.18565/aig.2017.12.17-24 (in Russian).
5. Carson DD. The glycobiology of implantation. Front Biosci 2002; 7 (1): 1535–44. DOI: 10.2741/a858
6. Clark GF. Functional glycosylation in the human and mammalian uterus. Fertil Res Pract 2015; 1 (1): 1–12. DOI: 10.1186/s40738-015-0007-0
7. Aplin JD. Glycans as biochemical markers of human endometrial secretory differentiation. J Reprod Fertil 1991; 92 (2): 525–41. DOI: 10.1530/jrf.0.0920525
8. Aplin JD. Embryo implantation: The molecular mechanism remains elusive. Reprod Biomed Online 2006; 13 (6): 833–9. DOI: 10.1016/S1472-6483(10)61032-2
9. Gu J, Sui LL, Cui D et al. Effects of LeY glycan expression on embryo implantation. Eur Rev Med Pharmacol Sci 2016; 20: 3327–35.
10. Noci I, Gheri G, Gheri Bryk S et al. Aging of the human endometrium: Peri-implantation phase endometrium does not show any age-dependent variation in lectin binding. Eur J Obstet Gynecol Reprod Biol 1996; 64 (1): 11–21. DOI: 10.1016/0301-2115(95)02245-7
11. Nejatbakhsh R, Kabir-Salmani M, Dimitriadis E et al. Subcellular localization of L-selectin ligand in the endometrium implies a novel function for pinopodes in endometrial receptivity. Reprod Biol Endocrinol 2012; 10 (1): 1. DOI: 10.1186/1477-7827-10-46
12. Margarit L, Gonzalez D, Lewis PD et al. L-Selectin ligands in human endometrium: Comparison of fertile and infertile subjects. Hum Reprod 2009; 24 (11): 2767–77. DOI: 10.1093/humrep/dep247
13. Foulk RA, Zdravkovic T, Genbacev O, Prakobphol A. Expression of L-selectin ligand MECA-79 as a predictive marker of human uterine receptivity. J Assist Reprod Genet 2007; 24 (7): 316–21. DOI: 10.1007/s10815-007-9151-8
14. Wang B, Sheng JZ, He RH et al. High expression of L-selectin ligand in secretory endometrium is associated with better endometrial receptivity and facilitates embryo implantation in human being. Am J Reprod Immunol 2008; 60 (2): 127–34. DOI: 10.1111/j.1600-0897.2008.00604.x
15. Prikaz Minzdrava Rossii no. 107n ot 30 avgusta 2012 g “O porjadke ispol’zovanija vspomogatel’nyh reproduktivnyh tehnologij, protivopokazanijah i ogranichenijah k ih primeneniju”. 2012 (In Russian).
16. Ziganshina MM, Kulikova GV, Fayzullina NM et al. Expression of fucosylated glycans in endothelial glycocalyces of placental villi at early and late fetal growth restriction. Placenta 2020; 90: 98–102. DOI: 10.1016/j.placenta.2019.12.005
17. Kulikova G.V., Abdurahmanova N.F., Fayzullina N.M. et al. Receptivity of thin endometrium in patients undergoing assisted reproduction. Obstet Gynecol. 2019: 100–7 (in Russian).
18. Abdurakhmanova N.F., Gvozdeva A.D., Ziganshina M.M., Dolgushi-
na N.V. The results of assisted reproductive technology programs in patients with “thin” endometrium. Gynecology. 2019; 21 (1): 23–7. DOI: 10.26442/20795696.2019.1.190232 (in Russian).
19. Miwa I, Tamura H, Takasaki A et al. Pathophysiologic features of “thin” endometrium. Fertil Steril 2009; 91 (4): 998–1004. DOI: 10.1016/j.fertnstert.2008.01.029
20. Takasaki A, Tamura H, Taketani T et al. A pilot study to prevent a thin endometrium in patients undergoing clomiphene citrate treatment. J Ovarian Res 2013; 6 (1): 6–10. DOI: 10.1186/1757-2215-6-94
21. Weiss NS, van Vliet MN, Limpens J et al. Endometrial thickness in women undergoing IUI with ovarian stimulation. How thick is too thin? A systematic review and meta-analysis. Hum Reprod 2017; 32 (5): 1009–18. DOI: 10.1093/humrep/dex035
22. Rabinovich GA, Croci DO. Regulatory circuits mediated by lectin-glycan interactions in autoimmunity and cancer. Immunity 2012; 36 (3): 322–35. DOI: 10.1016/j.immuni.2012.03.004
23. Kane N, Kelly R, Saunders PTK, Critchley HOD. Proliferation of uterine natural killer cells is induced by human chorionic gonadotropin and mediated via the mannose receptor. Endocrinology 2009; 150 (6): 2882–8. DOI: 10.1210/en.2008-1309
24. Miller DL, Jones CJP, Aplin JD, Nardo LG. Altered glycosylation in peri-implantation phase endometrium in women with stages III and IV endometriosis. Hum Reprod 2010; 25 (2): 406–11. DOI: 10.1093/humrep/dep401
25. Miravet-Valenciano JA, Rincon-Bertolin A, Vilella F, Simon C. Understanding and improving endometrial receptivity. Curr Opin Obstet Gynecol 2015; 27 (3): 187–92. DOI: 10.1097/GCO.0000000000000173
26. Gu J, Isaji T, Xu Q et al. Potential roles of N-glycosylation in cell adhesion. Glycoconj J 2012; 29 (8–9): 599–607. DOI: 10.1007/s10719-012-9386-1
27. Lessey BA. Adhesion molecules and implantation. J Reprod Immunol 2002; 55 (1–2): 101–12. DOI: 10.1016/S0165-0378(01)00139-5
28. Li Y, Ma K, Sun P et al. LeY oligosaccharide upregulates DAG/PKC signaling pathway in the human endometrial cells. Mol Cell Biochem 2009; 331 (1–2): 1–7. DOI: 10.1007/s11010-009-0137-y
2. Oron G, Hiersch L, Rona S et al. Endometrial thickness of less than
7.5 mm is associated with obstetric complications in fresh IVF cycles: a retrospective cohort study. Reprod Biomed Online 2018; 37 (3): 341–8. DOI: 10.1016/j.rbmo.2018.05.013
3. Bashiri A, Halper KI, Orvieto R. Recurrent Implantation Failure-update overview on etiology, diagnosis, treatment and future directions. Reprod Biol Endocrinol 2018; 16 (1): 1–18. DOI: 10.1186/s12958-018-0414-2
4. Зиганшина М.М., Абдурахманова Н.Ф., Павлович С.В. и др. Гликом эндометрия в менструальном цикле и рецептивность эндометрия. Акушерство и гинекология. 2017: 17–24. DOI: 10.18565/aig.2017.12.17-24
[Ziganshina M.M., Abdurakhmanova N.F., Pavlovich S.V. et al. Endometrial glycome in the menstrual cycle and endometrial receptivity. Obstet Gynecol. 2017: 17–24. DOI: 10.18565/aig.2017.12.17-24 (in Russian).]
5. Carson DD. The glycobiology of implantation. Front Biosci 2002; 7 (1): 1535–44. DOI: 10.2741/a858
6. Clark GF. Functional glycosylation in the human and mammalian uterus. Fertil Res Pract 2015; 1 (1): 1–12. DOI: 10.1186/s40738-015-0007-0
7. Aplin JD. Glycans as biochemical markers of human endometrial secretory differentiation. J Reprod Fertil 1991; 92 (2): 525–41. DOI: 10.1530/jrf.0.0920525
8. Aplin JD. Embryo implantation: The molecular mechanism remains elusive. Reprod Biomed Online 2006; 13 (6): 833–9. DOI: 10.1016/S1472-6483(10)61032-2
9. Gu J, Sui LL, Cui D et al. Effects of LeY glycan expression on embryo implantation. Eur Rev Med Pharmacol Sci 2016; 20: 3327–35.
10. Noci I, Gheri G, Gheri Bryk S et al. Aging of the human endometrium: Peri-implantation phase endometrium does not show any age-dependent variation in lectin binding. Eur J Obstet Gynecol Reprod Biol 1996; 64 (1): 11–21. DOI: 10.1016/0301-2115(95)02245-7
11. Nejatbakhsh R, Kabir-Salmani M, Dimitriadis E et al. Subcellular localization of L-selectin ligand in the endometrium implies a novel function for pinopodes in endometrial receptivity. Reprod Biol Endocrinol 2012; 10 (1): 1. DOI: 10.1186/1477-7827-10-46
12. Margarit L, Gonzalez D, Lewis PD et al. L-Selectin ligands in human endometrium: Comparison of fertile and infertile subjects. Hum Reprod 2009; 24 (11): 2767–77. DOI: 10.1093/humrep/dep247
13. Foulk RA, Zdravkovic T, Genbacev O, Prakobphol A. Expression of L-selectin ligand MECA-79 as a predictive marker of human uterine receptivity. J Assist Reprod Genet 2007; 24 (7): 316–21. DOI: 10.1007/s10815-007-9151-8
14. Wang B, Sheng JZ, He RH et al. High expression of L-selectin ligand in secretory endometrium is associated with better endometrial receptivity and facilitates embryo implantation in human being. Am J Reprod Immunol 2008; 60 (2): 127–34. DOI: 10.1111/j.1600-0897.2008.00604.x
15. Приказ Минздрава России №107н от 30 августа 2012 г. «О порядке использования вспомогательных репродуктивных технологий, противопоказаниях и ограничениях к их применению». 2012.
[Prikaz Minzdrava Rossii no. 107n ot 30 avgusta 2012 g “O porjadke ispol’zovanija vspomogatel’nyh reproduktivnyh tehnologij, protivopokazanijah i ogranichenijah k ih primeneniju”. 2012 (In Russian).]
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15. Prikaz Minzdrava Rossii no. 107n ot 30 avgusta 2012 g “O porjadke ispol’zovanija vspomogatel’nyh reproduktivnyh tehnologij, protivopokazanijah i ogranichenijah k ih primeneniju”. 2012 (In Russian).
16. Ziganshina MM, Kulikova GV, Fayzullina NM et al. Expression of fucosylated glycans in endothelial glycocalyces of placental villi at early and late fetal growth restriction. Placenta 2020; 90: 98–102. DOI: 10.1016/j.placenta.2019.12.005
17. Kulikova G.V., Abdurahmanova N.F., Fayzullina N.M. et al. Receptivity of thin endometrium in patients undergoing assisted reproduction. Obstet Gynecol. 2019: 100–7 (in Russian).
18. Abdurakhmanova N.F., Gvozdeva A.D., Ziganshina M.M., Dolgushi-
na N.V. The results of assisted reproductive technology programs in patients with “thin” endometrium. Gynecology. 2019; 21 (1): 23–7. DOI: 10.26442/20795696.2019.1.190232 (in Russian).
19. Miwa I, Tamura H, Takasaki A et al. Pathophysiologic features of “thin” endometrium. Fertil Steril 2009; 91 (4): 998–1004. DOI: 10.1016/j.fertnstert.2008.01.029
20. Takasaki A, Tamura H, Taketani T et al. A pilot study to prevent a thin endometrium in patients undergoing clomiphene citrate treatment. J Ovarian Res 2013; 6 (1): 6–10. DOI: 10.1186/1757-2215-6-94
21. Weiss NS, van Vliet MN, Limpens J et al. Endometrial thickness in women undergoing IUI with ovarian stimulation. How thick is too thin? A systematic review and meta-analysis. Hum Reprod 2017; 32 (5): 1009–18. DOI: 10.1093/humrep/dex035
22. Rabinovich GA, Croci DO. Regulatory circuits mediated by lectin-glycan interactions in autoimmunity and cancer. Immunity 2012; 36 (3): 322–35. DOI: 10.1016/j.immuni.2012.03.004
23. Kane N, Kelly R, Saunders PTK, Critchley HOD. Proliferation of uterine natural killer cells is induced by human chorionic gonadotropin and mediated via the mannose receptor. Endocrinology 2009; 150 (6): 2882–8. DOI: 10.1210/en.2008-1309
24. Miller DL, Jones CJP, Aplin JD, Nardo LG. Altered glycosylation in peri-implantation phase endometrium in women with stages III and IV endometriosis. Hum Reprod 2010; 25 (2): 406–11. DOI: 10.1093/humrep/dep401
25. Miravet-Valenciano JA, Rincon-Bertolin A, Vilella F, Simon C. Understanding and improving endometrial receptivity. Curr Opin Obstet Gynecol 2015; 27 (3): 187–92. DOI: 10.1097/GCO.0000000000000173
26. Gu J, Isaji T, Xu Q et al. Potential roles of N-glycosylation in cell adhesion. Glycoconj J 2012; 29 (8–9): 599–607. DOI: 10.1007/s10719-012-9386-1
27. Lessey BA. Adhesion molecules and implantation. J Reprod Immunol 2002; 55 (1–2): 101–12. DOI: 10.1016/S0165-0378(01)00139-5
28. Li Y, Ma K, Sun P et al. LeY oligosaccharide upregulates DAG/PKC signaling pathway in the human endometrial cells. Mol Cell Biochem 2009; 331 (1–2): 1–7. DOI: 10.1007/s11010-009-0137-y
Авторы
М.М. Зиганшина*, Н.В. Долгушина, Г.В. Куликова, Н.М. Файзуллина, А.А. Довгань, Н.Ф. Абдурахманова, А.И. Щеголев, А.В. Асатурова, Г.Т. Сухих
ФГБУ «Национальный медицинский исследовательский центр акушерства, гинекологии и перинатологии имени академика В.И. Кулакова» Минздрава России, Москва, Россия
*mmz@mail.ru
Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Moscow, Russia
*mmz@mail.ru
ФГБУ «Национальный медицинский исследовательский центр акушерства, гинекологии и перинатологии имени академика В.И. Кулакова» Минздрава России, Москва, Россия
*mmz@mail.ru
________________________________________________
Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Moscow, Russia
*mmz@mail.ru
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