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Экспрессия маркеров апоптоза NF-κB, Bcl-2 и Caspase-8 в эндометрии при наружном генитальном эндометриозе и хроническом эндометрите
Экспрессия маркеров апоптоза NF-κB, Bcl-2 и Caspase-8 в эндометрии при наружном генитальном эндометриозе и хроническом эндометрите
Табеева Г.И., Трегубова А.В., Асатурова А.В., Думановская М.Р., Магнаева А.С., Сметник А.А., Павлович C.В. Экспрессия маркеров апоптоза NF-κB, Bcl-2 и Caspase-8 в эндометрии при наружном генитальном эндометриозе и хроническом эндометрите. Гинекология. 2023;25(2):158–163.
DOI: 10.26442/20795696.2023.2.202003
© ООО «КОНСИЛИУМ МЕДИКУМ», 2023 г.
DOI: 10.26442/20795696.2023.2.202003
© ООО «КОНСИЛИУМ МЕДИКУМ», 2023 г.
________________________________________________
Материалы доступны только для специалистов сферы здравоохранения. Авторизуйтесь или зарегистрируйтесь.
Аннотация
Цель. Изучить особенности регуляции апоптоза в эндометрии женщин с хроническим эндометритом (ХЭ) и наружным генитальным эндометриозом (НГЭ) на основе изучения экспрессии таких его регуляторов, как транскрипционный фактор (NF-Κβ), Bcl-2 и Caspase-8.
Материалы и методы. В исследовании проведена оценка экспрессии таких факторов апоптоза, как Caspase-8, транскрипционный фактор, Bcl-2, у пациенток с ХЭ (n=23), наружным генитальным эндометриозом – НГЭ (n=20), неизмененным эндометрием (контрольная группа; n=7). Статистически значимые различия выявлены в отношении всех исследуемых маркеров (p<0,05).
Результаты. Усиление экспрессии факторов апоптоза, вероятно, демонстрирует высокую провоспалительную активность эндометрия как при ХЭ, так и при НГЭ. В случае НГЭ данный эффект более выражен на транскрипционном уровне в виде повышения экспрессии транскрипционного фактора как в железистых, так и в стромальных клетках эндометрия. Вероятно, это обусловлено системным характером хронического воспалительного процесса. Для ХЭ, несмотря на антиапоптотическую активность Bcl-2, повышение экспрессии Сaspase-8 в эндометрии, возможно, также указывает именно на преобладание активации врожденного иммунитета.
Заключение. Дисбаланс про- и антиапоптотических факторов может являться одновременно индуктором цитотоксических и цитопротективных звеньев в генезе НГЭ и ХЭ, что требует дальнейшего изучения.
Ключевые слова: наружный генитальный эндометриоз, хронический эндометрит, иммуногистохимия, апоптоз, Caspase-8, транскрипционный фактор, Bcl-2
Materials and methods. The study evaluated the expression of apoptosis factors such as Caspase-8, NF-κB transcription factor, and Bcl-2, in patients with chronic endometritis (CE, n=23), external genital endometriosis (EGE, n=20), and intact endometrium (control group; n=7). Statistically significant differences were found for all test markers (p<0.05).
Results. The increased expression of apoptosis factors is probably related to high endometrial pro-inflammatory activity in both CE and EGE. For EGE, this effect is more pronounced at the transcription level in the form of an increase in the expression of the transcription factor NF-κB in both glandular and stromal endometrial cells. It is probably due to the systemic nature of the chronic inflammatory process. For CE, despite the antiapoptotic activity of Bcl-2, an increase in Caspase-8 expression in the endometrium may also indicate a predominance of innate immunity activation.
Conclusion. The imbalance of pro- and antiapoptotic factors can be an inducer of both cytotoxic and cytoprotective mechanisms of EGE and CE. However, it requires further research.
Keywords: external genital endometriosis, chronic endometritis, immunohistochemistry, apoptosis, Caspase-8, transcription factor, Bcl-2
Материалы и методы. В исследовании проведена оценка экспрессии таких факторов апоптоза, как Caspase-8, транскрипционный фактор, Bcl-2, у пациенток с ХЭ (n=23), наружным генитальным эндометриозом – НГЭ (n=20), неизмененным эндометрием (контрольная группа; n=7). Статистически значимые различия выявлены в отношении всех исследуемых маркеров (p<0,05).
Результаты. Усиление экспрессии факторов апоптоза, вероятно, демонстрирует высокую провоспалительную активность эндометрия как при ХЭ, так и при НГЭ. В случае НГЭ данный эффект более выражен на транскрипционном уровне в виде повышения экспрессии транскрипционного фактора как в железистых, так и в стромальных клетках эндометрия. Вероятно, это обусловлено системным характером хронического воспалительного процесса. Для ХЭ, несмотря на антиапоптотическую активность Bcl-2, повышение экспрессии Сaspase-8 в эндометрии, возможно, также указывает именно на преобладание активации врожденного иммунитета.
Заключение. Дисбаланс про- и антиапоптотических факторов может являться одновременно индуктором цитотоксических и цитопротективных звеньев в генезе НГЭ и ХЭ, что требует дальнейшего изучения.
Ключевые слова: наружный генитальный эндометриоз, хронический эндометрит, иммуногистохимия, апоптоз, Caspase-8, транскрипционный фактор, Bcl-2
________________________________________________
Materials and methods. The study evaluated the expression of apoptosis factors such as Caspase-8, NF-κB transcription factor, and Bcl-2, in patients with chronic endometritis (CE, n=23), external genital endometriosis (EGE, n=20), and intact endometrium (control group; n=7). Statistically significant differences were found for all test markers (p<0.05).
Results. The increased expression of apoptosis factors is probably related to high endometrial pro-inflammatory activity in both CE and EGE. For EGE, this effect is more pronounced at the transcription level in the form of an increase in the expression of the transcription factor NF-κB in both glandular and stromal endometrial cells. It is probably due to the systemic nature of the chronic inflammatory process. For CE, despite the antiapoptotic activity of Bcl-2, an increase in Caspase-8 expression in the endometrium may also indicate a predominance of innate immunity activation.
Conclusion. The imbalance of pro- and antiapoptotic factors can be an inducer of both cytotoxic and cytoprotective mechanisms of EGE and CE. However, it requires further research.
Keywords: external genital endometriosis, chronic endometritis, immunohistochemistry, apoptosis, Caspase-8, transcription factor, Bcl-2
Полный текст
Список литературы
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23. González-Ramos R, Defrère S, Devoto L. Nuclear factor-kappaB: a main regulator of inflammation and cell survival in endometriosis pathophysiology. Fertil Steril. 2012;98(3):520-8. DOI:10.1016/j.fertnstert.2012.06.021
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DOI:10.1016/s0303-7207(00)00261-6
2. Cicinelli E, Trojano G, Mastromauro M, et al. Higher prevalence of chronic endometritis in women with endometriosis: a possible etiopathogenetic link. Fertil Steril. 2017;108(2):289-95.e1. DOI:10.1016/j.fertnstert.2017.05
3. Meresman GF, Vighi S, Buquet RA, et al. Apoptosis and expression of Bcl-2 and Bax in eutopic endometrium from women with endometriosis. Fertil Steril. 2000;74(4):760-6. DOI:10.1016/s0015-0282(00)01522-3
4. Watanabe H, Kanzaki H, Narukawa S, et al. Bcl-2 and Fas expression in eutopic and ectopic human endometrium during the menstrual cycle in relation to endometrial cell apoptosis. Am J Obstet Gynecol. 1997;176(2):360-8. DOI:10.1016/s0002-9378(97)70499-x
5. Kondrat'ieva PG, Sokolov DI, Iarmolinskaia MI, et al. Apoptoz pri naruzhnom genital'nom endometrioze (obzor literatury). Vestnik Sankt-peterburgskogo universiteta. 2009;11(4):213-21 (in Russian).
6. Grishkina AA, Chistyakova GN, Remizova II, et al. Morphological changes and features of the expression of the apoptosis factors in endometrium from women with endometriosis-associated infertility. Sovremennyie problemy nauki i obrazovaniia. 2019;5 (in Russian)].
7. Di Pietro C, Cicinelli E, Guglielmino MR, et al. Altered transcriptional regulation of cytokines, growth factors, and apoptotic proteins in the endometrium of infertile women with chronic endometritis. Am J Reprod Immunol. 2013;69(5):509-17. DOI:10.1111/aji.12076
8. Han JH, Park J, Kang TB, Lee KH. Regulation of Caspase-8 Activity at the Crossroads of Pro-Inflammation and Anti-Inflammation. Int J Mol Sci. 2021;22(7):3318. DOI:10.3390/ijms22073318
9. Wan FC, Zhang C, Jin Q, et al. Protective effects of astaxanthin on lipopolysaccharide-induced inflammation in bovine endometrial epithelial cells. Biol Reprod. 2020;102(2):339-47. DOI:10.1093/biolre/ioz187
10. Kelly P, Meade KG, O'Farrelly C. Non-canonical Inflammasome-Mediated IL-1β Production by Primary Endometrial Epithelial and Stromal Fibroblast Cells Is NLRP3 and Caspase-4 Dependent. Front Immunol. 2019;10:102. DOI:10.3389/fimmu.2019.00102
11. Margulies SL, Dhingra I, Flores V, et al. The Diagnostic Criteria for Chronic Endometritis: A Survey of Pathologists. Int J Gynecol Pathol. 2021;40(6):556-62. DOI:10.1097/PGP.0000000000000737
12. Rotello RJ, Lieberman RC, Lepoff RB, Gerschenson LE. Characterization of uterine epithelium apoptotic cell death kinetics and regulation by progesterone and RU 486. Am J Pathol. 1992;140(2):449-56.
13. Ponce C, Torres M, Galleguillos C, et al. Nuclear factor kappa-B pathway and interleukin-6 are affected in eutopic endometrium of women with endometriosis. Reproduction. 2009;137(4):727-37. DOI:10.1530/REP-08-0407
14. King AE, Critchley HO, Kelly RW. The NF-kappaB pathway in human endometrium and first trimester decidua. Mol Hum Reprod. 2001;7(2):175-83. DOI:10.1093/molehr/7.2.175
15. Lam M, Dubyak G, Chen L, et al. Evidence that BCL-2 represses apoptosis by regulating endoplasmic reticulum-associated Ca2+ fluxes. Proc Natl Acad Sci U S A. 1994;91(14):6569-73. DOI:10.1073/pnas.91.14.6569
16. Kang Q, Zou H, Yang X, et al. Characterization and prognostic significance of mortalin, Bcl-2 and Bax in intrahepatic cholangiocarcinoma. Oncol Lett. 2018;15(2):2161-8. DOI:10.3892/ol.2017.7570
17. Henriques S, Silva E, Cruz S, et al. Oestrous cycle-dependent expression of Fas and Bcl2 family gene products in normal canine endometrium. Reprod Fertil. Dev. 2015;28(9):1307-17. DOI:10.1071/RD14245
18. Otsuki Y. Apoptosis in human endometrium: apoptotic detection methods and signaling. Med Electron Microsc. 2001;34(3):166-73. DOI:10.1007/s007950100011
19. Otsuki Y, Misaki O, Sugimoto O, et al. Cyclic bcl-2 gene expression in human uterine endometrium during menstrual cycle. Lancet. 1994;344(8914):28-9.
DOI:10.1016/s0140-6736(94)91051-0
20. Wang S, El-Deiry WS. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene. 2003;22(53):8628-33. DOI:10.1038/sj.onc.1207232
21. Atasoy P, Bozdoğan O, Erekul S, et al. Fas-mediated pathway and apoptosis in normal, hyperplastic, and neoplastic endometrium. Gynecol. Oncol. 2003;91(2):309-17. DOI:10.1016/s0090-8258(03)00411-6
22. Qiao X, Wu L, Liu D, et al. Existence of chronic endometritis and its influence on pregnancy outcomes in infertile women with minimal/mild endometriosis. Int J Gynaecol Obstet. 2023;160(2):628-34. DOI:10.1002/ijgo.14326
23. González-Ramos R, Defrère S, Devoto L. Nuclear factor-kappaB: a main regulator of inflammation and cell survival in endometriosis pathophysiology. Fertil Steril. 2012;98(3):520-8. DOI:10.1016/j.fertnstert.2012.06.021
24. Turner ML, Cronin JG, Healey GD, Sheldon IM. Epithelial and stromal cells of bovine endometrium have roles in innate immunity and initiate inflammatory responses to bacterial lipopeptides in vitro via Toll-like receptors TLR2, TLR1, and TLR6. Endocrinology. 2014;155(4):1453-65. DOI:10.1210/en.2013-1822
25. Wang F, He YL, Peng DX, Liu MB. Expressions of nuclear factor-kappaB and intercellular adhesion molecule-1 in endometriosis. Di Yi Jun Yi Da Xue Xue Bao. 2005;25(6):703-5.
26. Kosareva РV, Tryastsina ЕN, Samodelkin EI. The study of immunohistochemical expression of certain pro- and antiapoptothic factors in endometry of patients with adenomiosis. HIV Infection and Immunosuppressive Disorders. 2018;10(3):56-63 (in Russian). DOI:10.22328/2077-9828-2018-10-3-56-63
27. Zaynetdinova LF, Koryaushkina AV, Telesheva LF, Sychugov GV. Peculiarities of cellular update processes in eutopic endometry in women with external genital endometriosis and chronic endometritis. Ural'skii meditsinskii zhurnal. 2020;3(186):71-7 (in Russian).
28. Kaponis A, Iwabe T, Taniguchi F, et al. The role of NF-kappaB in endometriosis. Front Biosci (Schol Ed). 2012;4(4):1213-34. DOI:10.2741/s327
29. Ponce C, Torres M, Galleguillos C, et al. Nuclear factor kappaB pathway and interleukin-6 are affected in eutopic endometrium of women with endometriosis. Reproduction. 2009;137(4):727-37. DOI:10.1530/REP-08-0407
30. Mohamed AAA, Yang D, Liu S, et al. Endoplasmic reticulum stress is involved in lipopolysaccharide-induced inflammatory response and apoptosis in goat endometrial stromal cells. Mol Reprod Dev. 2019;86(7):908-21. DOI:10.1002/mrd.23152
31. Vatansever HS, Lacin S, Ozbilgin MK. Changed Bcl:Bax ratio in endometrium of patients with unexplained infertility. Acta Histochem. 2005;107(5):345-55. DOI:10.1016/j.acthis.2005.06.012
32. Cicinelli E, Resta L, Nicoletti R, et al. Detection of chronic endometritis at fluid hysteroscopy. J Minim Invasive Gynecol. 2005;12(6):514-8. DOI:10.1016/j.jmig.2005.07.394
33. Cicinelli E, De Ziegler D, Nicoletti R, et al. Chronic endometritis: correlation among hysteroscopic, histologic, and bacteriologic findings in a prospective trial with 2190 consecutive office hysteroscopies. Fertil Steril. 2008;89(3):677-84. DOI:10.1016/j.fertnstert.2007.03.074
34. Sarhan J, Liu BC, Muendlein HI, et al. Caspase-8 induces cleavage of gasdermin D to elicit pyroptosis during Yersinia infection. Proc Natl Acad Sci U S A. 2018;115(46):E10888-97. DOI:10.1073/pnas.1809548115
35. Schwarzer R, Jiao H, Wachsmuth L, et al. FADD and Caspase-8 Regulate Gut Homeostasis and Inflammation by Controlling MLKL- and GSDMD-Mediated Death of Intestinal Epithelial Cells. Immunity. 2020;52(6):978-93.e6. DOI:10.1016/j.immuni.2020.04.002
36. Tummers B, Mari L, Guy CS, et al. Caspase-8-Dependent Inflammatory Responses Are Controlled by Its Adaptor, FADD, and Necroptosis. Immunity. 2020;52(6):994-1006.e8. DOI:10.1016/j.immuni.2020.04.010
DOI:10.1016/s0303-7207(00)00261-6
2. Cicinelli E, Trojano G, Mastromauro M, et al. Higher prevalence of chronic endometritis in women with endometriosis: a possible etiopathogenetic link. Fertil Steril. 2017;108(2):289-95.e1. DOI:10.1016/j.fertnstert.2017.05
3. Meresman GF, Vighi S, Buquet RA, et al. Apoptosis and expression of Bcl-2 and Bax in eutopic endometrium from women with endometriosis. Fertil Steril. 2000;74(4):760-6. DOI:10.1016/s0015-0282(00)01522-3
4. Watanabe H, Kanzaki H, Narukawa S, et al. Bcl-2 and Fas expression in eutopic and ectopic human endometrium during the menstrual cycle in relation to endometrial cell apoptosis. Am J Obstet Gynecol. 1997;176(2):360-8. DOI:10.1016/s0002-9378(97)70499-x
5. Кондратьева П.Г., Соколов Д.И., Ярмолинская М.И., и др. Апоптоз при наружном генитальном эндометриозе (обзор литературы). Вестник Санкт-Петербургского университета. 2009;11(4):213-21 [Kondrat'ieva PG, Sokolov DI, Iarmolinskaia MI, et al. Apoptoz pri naruzhnom genital'nom endometrioze (obzor literatury). Vestnik Sankt-peterburgskogo universiteta. 2009;11(4):213-21 (in Russian)].
6. Гришкина А.А., Чистякова Г.Н., Ремизова И.И., и др. Морфологические изменения и особенности экспрессии факторов апоптоза в эндометрии женщин с бесплодием, обусловленным эндометриозом. Современные проблемы науки и образования. 2019;5 [Grishkina AA, Chistyakova GN, Remizova II, et al. Morphological changes and features of the expression of the apoptosis factors in endometrium from women with endometriosis-associated infertility. Sovremennyie problemy nauki i obrazovaniia. 2019;5 (in Russian)].
7. Di Pietro C, Cicinelli E, Guglielmino MR, et al. Altered transcriptional regulation of cytokines, growth factors, and apoptotic proteins in the endometrium of infertile women with chronic endometritis. Am J Reprod Immunol. 2013;69(5):509-17. DOI:10.1111/aji.12076
8. Han JH, Park J, Kang TB, Lee KH. Regulation of Caspase-8 Activity at the Crossroads of Pro-Inflammation and Anti-Inflammation. Int J Mol Sci. 2021;22(7):3318. DOI:10.3390/ijms22073318
9. Wan FC, Zhang C, Jin Q, et al. Protective effects of astaxanthin on lipopolysaccharide-induced inflammation in bovine endometrial epithelial cells. Biol Reprod. 2020;102(2):339-47. DOI:10.1093/biolre/ioz187
10. Kelly P, Meade KG, O'Farrelly C. Non-canonical Inflammasome-Mediated IL-1β Production by Primary Endometrial Epithelial and Stromal Fibroblast Cells Is NLRP3 and Caspase-4 Dependent. Front Immunol. 2019;10:102. DOI:10.3389/fimmu.2019.00102
11. Margulies SL, Dhingra I, Flores V, et al. The Diagnostic Criteria for Chronic Endometritis: A Survey of Pathologists. Int J Gynecol Pathol. 2021;40(6):556-62. DOI:10.1097/PGP.0000000000000737
12. Rotello RJ, Lieberman RC, Lepoff RB, Gerschenson LE. Characterization of uterine epithelium apoptotic cell death kinetics and regulation by progesterone and RU 486. Am J Pathol. 1992;140(2):449-56.
13. Ponce C, Torres M, Galleguillos C, et al. Nuclear factor kappa-B pathway and interleukin-6 are affected in eutopic endometrium of women with endometriosis. Reproduction. 2009;137(4):727-37. DOI:10.1530/REP-08-0407
14. King AE, Critchley HO, Kelly RW. The NF-kappaB pathway in human endometrium and first trimester decidua. Mol Hum Reprod. 2001;7(2):175-83. DOI:10.1093/molehr/7.2.175
15. Lam M, Dubyak G, Chen L, et al. Evidence that BCL-2 represses apoptosis by regulating endoplasmic reticulum-associated Ca2+ fluxes. Proc Natl Acad Sci U S A. 1994;91(14):6569-73. DOI:10.1073/pnas.91.14.6569
16. Kang Q, Zou H, Yang X, et al. Characterization and prognostic significance of mortalin, Bcl-2 and Bax in intrahepatic cholangiocarcinoma. Oncol Lett. 2018;15(2):2161-8. DOI:10.3892/ol.2017.7570
17. Henriques S, Silva E, Cruz S, et al. Oestrous cycle-dependent expression of Fas and Bcl2 family gene products in normal canine endometrium. Reprod Fertil. Dev. 2015;28(9):1307-17. DOI:10.1071/RD14245
18. Otsuki Y. Apoptosis in human endometrium: apoptotic detection methods and signaling. Med Electron Microsc. 2001;34(3):166-73. DOI:10.1007/s007950100011
19. Otsuki Y, Misaki O, Sugimoto O, et al. Cyclic bcl-2 gene expression in human uterine endometrium during menstrual cycle. Lancet. 1994;344(8914):28-9.
DOI:10.1016/s0140-6736(94)91051-0
20. Wang S, El-Deiry WS. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene. 2003;22(53):8628-33. DOI:10.1038/sj.onc.1207232
21. Atasoy P, Bozdoğan O, Erekul S, et al. Fas-mediated pathway and apoptosis in normal, hyperplastic, and neoplastic endometrium. Gynecol. Oncol. 2003;91(2):309-17. DOI:10.1016/s0090-8258(03)00411-6
22. Qiao X, Wu L, Liu D, et al. Existence of chronic endometritis and its influence on pregnancy outcomes in infertile women with minimal/mild endometriosis. Int J Gynaecol Obstet. 2023;160(2):628-34. DOI:10.1002/ijgo.14326
23. González-Ramos R, Defrère S, Devoto L. Nuclear factor-kappaB: a main regulator of inflammation and cell survival in endometriosis pathophysiology. Fertil Steril. 2012;98(3):520-8. DOI:10.1016/j.fertnstert.2012.06.021
24. Turner ML, Cronin JG, Healey GD, Sheldon IM. Epithelial and stromal cells of bovine endometrium have roles in innate immunity and initiate inflammatory responses to bacterial lipopeptides in vitro via Toll-like receptors TLR2, TLR1, and TLR6. Endocrinology. 2014;155(4):1453-65. DOI:10.1210/en.2013-1822
25. Wang F, He YL, Peng DX, Liu MB. Expressions of nuclear factor-kappaB and intercellular adhesion molecule-1 in endometriosis. Di Yi Jun Yi Da Xue Xue Bao. 2005;25(6):703-5.
26. Косарева П.В., Трясицина Е.Н., Самоделкин Е.И. Изучение иммуногистохимической экспрессии отдельных про- и антиапоптотических факторов в эндометрии пациенток с аденомиозом. ВИЧ-инфекция и иммуносупрессии. 2018;10(3):56-63 [Kosareva РV, Tryastsina ЕN, Samodelkin EI. The study of immunohistochemical expression of certain pro- and antiapoptothic factors in endometry of patients with adenomiosis. HIV Infection and Immunosuppressive Disorders. 2018;10(3):56-63 (in Russian)].
DOI:10.22328/2077-9828-2018-10-3-56-63
27. Зайнетдинова Л.Ф., Коряушкина А.В., Телешева Л.Ф., Сычугов Г.В. Особенности процессов клеточного обновления в эутопическом эндометрии у женщин с наружным генитальным эндометриозом и хроническим эндометритом. Уральский медицинский журнал. 2020;3(186):71-7 [Zaynetdinova LF, Koryaushkina AV, Telesheva LF, Sychugov GV. Peculiarities of cellular update processes in eutopic endometry in women with external genital endometriosis and chronic endometritis. Ural'skii meditsinskii zhurnal. 2020;3(186):71-7 (in Russian)].
28. Kaponis A, Iwabe T, Taniguchi F, et al. The role of NF-kappaB in endometriosis. Front Biosci (Schol Ed). 2012;4(4):1213-34. DOI:10.2741/s327
29. Ponce C, Torres M, Galleguillos C, et al. Nuclear factor kappaB pathway and interleukin-6 are affected in eutopic endometrium of women with endometriosis. Reproduction. 2009;137(4):727-37. DOI:10.1530/REP-08-0407
30. Mohamed AAA, Yang D, Liu S, et al. Endoplasmic reticulum stress is involved in lipopolysaccharide-induced inflammatory response and apoptosis in goat endometrial stromal cells. Mol Reprod Dev. 2019;86(7):908-21. DOI:10.1002/mrd.23152
31. Vatansever HS, Lacin S, Ozbilgin MK. Changed Bcl:Bax ratio in endometrium of patients with unexplained infertility. Acta Histochem. 2005;107(5):345-55. DOI:10.1016/j.acthis.2005.06.012
32. Cicinelli E, Resta L, Nicoletti R, et al. Detection of chronic endometritis at fluid hysteroscopy. J Minim Invasive Gynecol. 2005;12(6):514-8. DOI:10.1016/j.jmig.2005.07.394
33. Cicinelli E, De Ziegler D, Nicoletti R, et al. Chronic endometritis: correlation among hysteroscopic, histologic, and bacteriologic findings in a prospective trial with 2190 consecutive office hysteroscopies. Fertil Steril. 2008;89(3):677-84. DOI:10.1016/j.fertnstert.2007.03.074
34. Sarhan J, Liu BC, Muendlein HI, et al. Caspase-8 induces cleavage of gasdermin D to elicit pyroptosis during Yersinia infection. Proc Natl Acad Sci U S A. 2018;115(46):E10888-97. DOI:10.1073/pnas.1809548115
35. Schwarzer R, Jiao H, Wachsmuth L, et al. FADD and Caspase-8 Regulate Gut Homeostasis and Inflammation by Controlling MLKL- and GSDMD-Mediated Death of Intestinal Epithelial Cells. Immunity. 2020;52(6):978-93.e6. DOI:10.1016/j.immuni.2020.04.002
36. Tummers B, Mari L, Guy CS, et al. Caspase-8-Dependent Inflammatory Responses Are Controlled by Its Adaptor, FADD, and Necroptosis. Immunity. 2020;52(6):994-1006.e8. DOI:10.1016/j.immuni.2020.04.010
________________________________________________
DOI:10.1016/s0303-7207(00)00261-6
2. Cicinelli E, Trojano G, Mastromauro M, et al. Higher prevalence of chronic endometritis in women with endometriosis: a possible etiopathogenetic link. Fertil Steril. 2017;108(2):289-95.e1. DOI:10.1016/j.fertnstert.2017.05
3. Meresman GF, Vighi S, Buquet RA, et al. Apoptosis and expression of Bcl-2 and Bax in eutopic endometrium from women with endometriosis. Fertil Steril. 2000;74(4):760-6. DOI:10.1016/s0015-0282(00)01522-3
4. Watanabe H, Kanzaki H, Narukawa S, et al. Bcl-2 and Fas expression in eutopic and ectopic human endometrium during the menstrual cycle in relation to endometrial cell apoptosis. Am J Obstet Gynecol. 1997;176(2):360-8. DOI:10.1016/s0002-9378(97)70499-x
5. Kondrat'ieva PG, Sokolov DI, Iarmolinskaia MI, et al. Apoptoz pri naruzhnom genital'nom endometrioze (obzor literatury). Vestnik Sankt-peterburgskogo universiteta. 2009;11(4):213-21 (in Russian).
6. Grishkina AA, Chistyakova GN, Remizova II, et al. Morphological changes and features of the expression of the apoptosis factors in endometrium from women with endometriosis-associated infertility. Sovremennyie problemy nauki i obrazovaniia. 2019;5 (in Russian)].
7. Di Pietro C, Cicinelli E, Guglielmino MR, et al. Altered transcriptional regulation of cytokines, growth factors, and apoptotic proteins in the endometrium of infertile women with chronic endometritis. Am J Reprod Immunol. 2013;69(5):509-17. DOI:10.1111/aji.12076
8. Han JH, Park J, Kang TB, Lee KH. Regulation of Caspase-8 Activity at the Crossroads of Pro-Inflammation and Anti-Inflammation. Int J Mol Sci. 2021;22(7):3318. DOI:10.3390/ijms22073318
9. Wan FC, Zhang C, Jin Q, et al. Protective effects of astaxanthin on lipopolysaccharide-induced inflammation in bovine endometrial epithelial cells. Biol Reprod. 2020;102(2):339-47. DOI:10.1093/biolre/ioz187
10. Kelly P, Meade KG, O'Farrelly C. Non-canonical Inflammasome-Mediated IL-1β Production by Primary Endometrial Epithelial and Stromal Fibroblast Cells Is NLRP3 and Caspase-4 Dependent. Front Immunol. 2019;10:102. DOI:10.3389/fimmu.2019.00102
11. Margulies SL, Dhingra I, Flores V, et al. The Diagnostic Criteria for Chronic Endometritis: A Survey of Pathologists. Int J Gynecol Pathol. 2021;40(6):556-62. DOI:10.1097/PGP.0000000000000737
12. Rotello RJ, Lieberman RC, Lepoff RB, Gerschenson LE. Characterization of uterine epithelium apoptotic cell death kinetics and regulation by progesterone and RU 486. Am J Pathol. 1992;140(2):449-56.
13. Ponce C, Torres M, Galleguillos C, et al. Nuclear factor kappa-B pathway and interleukin-6 are affected in eutopic endometrium of women with endometriosis. Reproduction. 2009;137(4):727-37. DOI:10.1530/REP-08-0407
14. King AE, Critchley HO, Kelly RW. The NF-kappaB pathway in human endometrium and first trimester decidua. Mol Hum Reprod. 2001;7(2):175-83. DOI:10.1093/molehr/7.2.175
15. Lam M, Dubyak G, Chen L, et al. Evidence that BCL-2 represses apoptosis by regulating endoplasmic reticulum-associated Ca2+ fluxes. Proc Natl Acad Sci U S A. 1994;91(14):6569-73. DOI:10.1073/pnas.91.14.6569
16. Kang Q, Zou H, Yang X, et al. Characterization and prognostic significance of mortalin, Bcl-2 and Bax in intrahepatic cholangiocarcinoma. Oncol Lett. 2018;15(2):2161-8. DOI:10.3892/ol.2017.7570
17. Henriques S, Silva E, Cruz S, et al. Oestrous cycle-dependent expression of Fas and Bcl2 family gene products in normal canine endometrium. Reprod Fertil. Dev. 2015;28(9):1307-17. DOI:10.1071/RD14245
18. Otsuki Y. Apoptosis in human endometrium: apoptotic detection methods and signaling. Med Electron Microsc. 2001;34(3):166-73. DOI:10.1007/s007950100011
19. Otsuki Y, Misaki O, Sugimoto O, et al. Cyclic bcl-2 gene expression in human uterine endometrium during menstrual cycle. Lancet. 1994;344(8914):28-9.
DOI:10.1016/s0140-6736(94)91051-0
20. Wang S, El-Deiry WS. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene. 2003;22(53):8628-33. DOI:10.1038/sj.onc.1207232
21. Atasoy P, Bozdoğan O, Erekul S, et al. Fas-mediated pathway and apoptosis in normal, hyperplastic, and neoplastic endometrium. Gynecol. Oncol. 2003;91(2):309-17. DOI:10.1016/s0090-8258(03)00411-6
22. Qiao X, Wu L, Liu D, et al. Existence of chronic endometritis and its influence on pregnancy outcomes in infertile women with minimal/mild endometriosis. Int J Gynaecol Obstet. 2023;160(2):628-34. DOI:10.1002/ijgo.14326
23. González-Ramos R, Defrère S, Devoto L. Nuclear factor-kappaB: a main regulator of inflammation and cell survival in endometriosis pathophysiology. Fertil Steril. 2012;98(3):520-8. DOI:10.1016/j.fertnstert.2012.06.021
24. Turner ML, Cronin JG, Healey GD, Sheldon IM. Epithelial and stromal cells of bovine endometrium have roles in innate immunity and initiate inflammatory responses to bacterial lipopeptides in vitro via Toll-like receptors TLR2, TLR1, and TLR6. Endocrinology. 2014;155(4):1453-65. DOI:10.1210/en.2013-1822
25. Wang F, He YL, Peng DX, Liu MB. Expressions of nuclear factor-kappaB and intercellular adhesion molecule-1 in endometriosis. Di Yi Jun Yi Da Xue Xue Bao. 2005;25(6):703-5.
26. Kosareva РV, Tryastsina ЕN, Samodelkin EI. The study of immunohistochemical expression of certain pro- and antiapoptothic factors in endometry of patients with adenomiosis. HIV Infection and Immunosuppressive Disorders. 2018;10(3):56-63 (in Russian). DOI:10.22328/2077-9828-2018-10-3-56-63
27. Zaynetdinova LF, Koryaushkina AV, Telesheva LF, Sychugov GV. Peculiarities of cellular update processes in eutopic endometry in women with external genital endometriosis and chronic endometritis. Ural'skii meditsinskii zhurnal. 2020;3(186):71-7 (in Russian).
28. Kaponis A, Iwabe T, Taniguchi F, et al. The role of NF-kappaB in endometriosis. Front Biosci (Schol Ed). 2012;4(4):1213-34. DOI:10.2741/s327
29. Ponce C, Torres M, Galleguillos C, et al. Nuclear factor kappaB pathway and interleukin-6 are affected in eutopic endometrium of women with endometriosis. Reproduction. 2009;137(4):727-37. DOI:10.1530/REP-08-0407
30. Mohamed AAA, Yang D, Liu S, et al. Endoplasmic reticulum stress is involved in lipopolysaccharide-induced inflammatory response and apoptosis in goat endometrial stromal cells. Mol Reprod Dev. 2019;86(7):908-21. DOI:10.1002/mrd.23152
31. Vatansever HS, Lacin S, Ozbilgin MK. Changed Bcl:Bax ratio in endometrium of patients with unexplained infertility. Acta Histochem. 2005;107(5):345-55. DOI:10.1016/j.acthis.2005.06.012
32. Cicinelli E, Resta L, Nicoletti R, et al. Detection of chronic endometritis at fluid hysteroscopy. J Minim Invasive Gynecol. 2005;12(6):514-8. DOI:10.1016/j.jmig.2005.07.394
33. Cicinelli E, De Ziegler D, Nicoletti R, et al. Chronic endometritis: correlation among hysteroscopic, histologic, and bacteriologic findings in a prospective trial with 2190 consecutive office hysteroscopies. Fertil Steril. 2008;89(3):677-84. DOI:10.1016/j.fertnstert.2007.03.074
34. Sarhan J, Liu BC, Muendlein HI, et al. Caspase-8 induces cleavage of gasdermin D to elicit pyroptosis during Yersinia infection. Proc Natl Acad Sci U S A. 2018;115(46):E10888-97. DOI:10.1073/pnas.1809548115
35. Schwarzer R, Jiao H, Wachsmuth L, et al. FADD and Caspase-8 Regulate Gut Homeostasis and Inflammation by Controlling MLKL- and GSDMD-Mediated Death of Intestinal Epithelial Cells. Immunity. 2020;52(6):978-93.e6. DOI:10.1016/j.immuni.2020.04.002
36. Tummers B, Mari L, Guy CS, et al. Caspase-8-Dependent Inflammatory Responses Are Controlled by Its Adaptor, FADD, and Necroptosis. Immunity. 2020;52(6):994-1006.e8. DOI:10.1016/j.immuni.2020.04.010
Авторы
Г.И. Табеева*, А.В. Трегубова, А.В. Асатурова, М.Р. Думановская, А.С. Магнаева, А.А. Сметник, C.В. Павлович
ФГБУ «Национальный медицинский исследовательский центр акушерства, гинекологии и перинатологии им. акад. В.И. Кулакова» Минздрава России, Москва, Россия
*doctor.gtab@gmail.com
Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Moscow, Russia
*doctor.gtab@gmail.com
ФГБУ «Национальный медицинский исследовательский центр акушерства, гинекологии и перинатологии им. акад. В.И. Кулакова» Минздрава России, Москва, Россия
*doctor.gtab@gmail.com
________________________________________________
Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Moscow, Russia
*doctor.gtab@gmail.com
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