Morphological and molecular features of decidual endometrial cells in miscarriage

Abstract

Decidualization is a dynamic, multistep process that results in the differentiation of elongated endometrial stromal cells into round, epithelioid-like decidual cells in response to increasing progesterone levels. Throughout pregnancy, decidual stromal cells play an important role by creating a tolerant microenvironment, the decidua, to suppress the maternal immune response and prevent rejection of the allogeneic fetus. Decidualization is considered significant not only in the establishment and maintenance of pregnancy, prevention of early losses, and modulation of the immune response but also in the control of the onset of labor, regulation of trophoblast invasion, and embryo selection. Decidual cells have immunomodulatory properties in relation to cells of innate and adaptive immunity. Pregnancy maintenance requires selective elimination of proinflammatory senescent decidual cells by activated uterine natural killer cells. Data on various populations of decidualizing endometrial stromal cells revealed subtypes with different functional characteristics, namely, predecidual, decidual, transitional, and senescent subpopulations. An increase in the number of the latter with a proinflammatory phenotype leads to miscarriages. This paper analyzes the literature data on decidualization and its role in the genesis of miscarriage and highlights the contribution of decidual stromal cells to the microenvironment and their direct or indirect influence on the recruitment, distribution, and function of immune cells, extracellular matrix remodeling, and placenta formation.

Keywords

decidual cells / endometrium / early missed abortion / senescent cells / chorion

References

[1] Habiba M, Heyn R, Bianchi P, et al. The development of the human uterus: morphogenesis to menarche. Hum Reprod Update. 2021;27(1):1–26. doi: 10.1093/humupd/dmaa036

[2] Habiba M., Heyn R., Bianchi P., et al. The development of the human uterus: morphogenesis to menarche // Hum Reprod Update. 2021. Vol. 27, N 1. P. 1–26. doi: 10.1093/humupd/dmaa036

[3] Koos RD. Minireview: putting physiology back into estrogens’ mechanism of action. Endocrinology. 2011;152(12):4481–4488. doi: 10.1210/en.2011-1449

[4] Koos R.D. Minireview: putting physiology back into estrogens’ mechanism of action // Endocrinology. 2011. Vol. 152, N 12. P. 4481–4488. doi: 10.1210/en.2011-1449

[5] Lucas ES, Vrljicak P, Muter J, et al. Recurrent pregnancy loss is associated with a pro-senescent decidual response during the peri-implantation window. Commun Biol. 2020;3(1):37. doi: 10.1038/s42003-020-0763-1

[6] Lucas E.S., Vrljicak P., Muter J., et al. Recurrent pregnancy loss is associated with a pro-senescent decidual response during the peri-implantation window // Commun Biol. 2020. Vol. 3, N 1. P. 37. doi: 10.1038/s42003-020-0763-1

[7] Rawlings TM, Makwana K, Taylor DM, et al. Modelling the impact of decidual senescence on embryo implantation in human endometrial assembloids. Elife. 2021;10:e69603. doi: 10.7554/eLife.69603

[8] Rawlings T.M., Makwana K., Taylor D.M., et al. Modelling the impact of decidual senescence on embryo implantation in human endometrial assembloids // Elife. 2021. Vol. 10. P. e69603. doi: 10.7554/eLife.69603

[9] Wang W, Vilella F, Alama P, et al. Single-cell transcriptomic atlas of the human endometrium during the menstrual cycle. Nat Med. 2020;26(10):1644–1653. doi: 10.1038/s41591-020-1040-z

[10] Wang W., Vilella F., Alama P., et al. Single-cell transcriptomic atlas of the human endometrium during the menstrual cycle // Nat Med. 2020. Vol. 26, N 10. P. 1644–1653. doi: 10.1038/s41591-020-1040-z

[11] Wetendorf M, DeMayo FJ. The progesterone receptor regulates implantation, decidualization, and glandular development via a complex paracrine signaling network. Mol Cell Endocrinol. 2012;357(1-2): 108–118. doi: 10.1016/j.mce.2011.10.028

[12] Wetendorf M., DeMayo F.J. The progesterone receptor regulates implantation, decidualization, and glandular development via a complex paracrine signaling network // Mol Cell Endocrinol. 2012. Vol. 357, N 1-2. P. 108–118. doi: 10.1016/j.mce.2011.10.028

[13] Maruyama T, Yoshimura Y. Molecular and cellular mechanisms for differentiation and regeneration of the uterine endometrium. Endocr J. 2008;55(5):795–810. doi: 10.1507/endocrj.k08e-067

[14] Maruyama T., Yoshimura Y. Molecular and cellular mechanisms for differentiation and regeneration of the uterine endometrium // Endocr J. 2008. Vol. 55, N 5. P. 795–810. doi: 10.1507/endocrj.k08e-067

[15] Bhurke AS, Bagchi IC, Bagchi MK. Progesterone-regulated endometrial factors controlling implantation. Am J Reprod Immunol. 2016;75(3):237–245. doi: 10.1111/aji.12473

[16] Bhurke A.S., Bagchi I.C., Bagchi M.K. Progesterone-regulated endometrial factors controlling implantation // Am J Reprod Immunol. 2016. Vol. 75, N 3. P. 237–245. doi: 10.1111/aji.12473

[17] Gellersen B, Brosens JJ. Cyclic decidualization of the human endometrium in reproductive health and failure. Endocr Rev. 2014;35(6):851–905. doi: 10.1210/er.2014-1045

[18] Gellersen B., Brosens J.J. Cyclic decidualization of the human endometrium in reproductive health and failure // Endocr Rev. 2014. Vol. 35, N 6. P. 851–905. doi: 10.1210/er.2014-1045

[19] Erkenbrack EM, Maziarz JD, Griffith OW, et al. The mammalian decidual cell evolved from a cellular stress response. PLoS Biol. 2018;16(8):e2005594. doi: 10.1371/journal.pbio.2005594

[20] Erkenbrack E.M., Maziarz J.D., Griffith O.W., et al. The mammalian decidual cell evolved from a cellular stress response // PLoS Biol. 2018. Vol. 16, N 8. P. e2005594. doi: 10.1371/journal.pbio.2005594

[21] Valdes CT, Schutt A, Simon C. Implantation failure of endometrial origin: it is not pathology, but our failure to synchronize the developing embryo with a receptive endometrium. Fertil Steril. 2017;108(1):15–18. doi: 10.1016/j.fertnstert.2017.05.033

[22] Valdes C.T., Schutt A., Simon C. Implantation failure of endometrial origin: it is not pathology, but our failure to synchronize the developing embryo with a receptive endometrium // Fertil Steril. 2017. Vol. 108, N 1. P. 15–18. doi: 10.1016/j.fertnstert.2017.05.033

[23] Franasiak JM, Ruiz-Alonso M, Scott RT, Simón C. Both slowly developing embryos and a variable pace of luteal endometrial progression may conspire to prevent normal birth in spite of a capable embryo. Fertil Steril. 2016;105(4):861–866. doi: 10.1016/j.fertnstert.2016.02.030

[24] Franasiak J.M., Ruiz-Alonso M., Scott R.T., Simón C. Both slowly developing embryos and a variable pace of luteal endometrial progression may conspire to prevent normal birth in spite of a capable embryo // Fertil Steril. 2016. Vol. 105, N 4. P. 861–866. doi: 10.1016/j.fertnstert.2016.02.030

[25] Kajihara T, Tanaka K, Oguro T, et al. Androgens modulate the morphological characteristics of human endometrial stromal cells decidualized in vitro. Reprod Sci. 2014;21(3):372–380. doi: 10.1177/1933719113497280

[26] Kajihara T., Tanaka K., Oguro T., et al. Androgens modulate the morphological characteristics of human endometrial stromal cells decidualized in vitro // Reprod Sci. 2014. Vol. 21, N 3. P. 372–380. doi: 10.1177/1933719113497280

[27] Wu HM, Chen LH, Hsu LT, Lai CH. Immune tolerance of embryo implantation and pregnancy: the role of human decidual stromal cell- and embryonic-derived extracellular vesicles. Int J Mol Sci. 2022;23(21):13382. doi: 10.3390/ijms232113382

[28] Wu H.M., Chen L.H., Hsu L.T., Lai C.H. Immune tolerance of embryo implantation and pregnancy: the role of human decidual stromal cell- and embryonic-derived extracellular vesicles // Int J Mol Sci. 2022. Vol. 23, N 21. P. 13382. doi: 10.3390/ijms232113382

[29] Vinketova K, Mourdjeva M, Oreshkova T. Human decidual stromal cells as a component of the implantation niche and a modulator of maternal immunity. J Pregnancy. 2016;2016:8689436. doi: 10.1155/2016/8689436

[30] Vinketova K., Mourdjeva M., Oreshkova T. Human decidual stromal cells as a component of the implantation niche and a modulator of maternal immunity // J Pregnancy. 2016. Vol. 2016. P. 8689436. doi: 10.1155/2016/8689436

[31] Muter J, Kong CS, Brosens JJ. The role of decidual subpopulations in implantation, menstruation and miscarriage. Front Reprod Health. 2021;3:804921. doi: 10.3389/frph.2021.804921

[32] Muter J., Kong C.S., Brosens J.J. The role of decidual subpopulations in implantation, menstruation and miscarriage // Front Reprod Health. 2021. Vol. 3. P. 804921. doi: 10.3389/frph.2021.804921

[33] Christian M, Zhang X, Schneider-Merck T, et al. Cyclic AMP-induced forkhead transcription factor, FKHR, cooperates with CCAAT/enhancer-binding protein beta in differentiating human endometrial stromal cells. J Biol Chem. 2002;277(23):20825–20832. doi: 10.1074/jbc.M201018200

[34] Christian M., Zhang X., Schneider-Merck T., et al. Cyclic AMP-induced forkhead transcription factor, FKHR, cooperates with CCAAT/enhancer-binding protein beta in differentiating human endometrial stromal cells // J Biol Chem. 2002. Vol. 277, N 23. P. 20825–20832. doi: 10.1074/jbc.M201018200

[35] Brighton PJ, Maruyama Y, Fishwick K, et al. Clearance of senescent decidual cells by uterine natural killer cells in cycling human endometrium. Elife. 2017;6:e31274. doi: 10.7554/eLife.31274

[36] Brighton P.J., Maruyama Y., Fishwick K., et al. Clearance of senescent decidual cells by uterine natural killer cells in cycling human endometrium // Elife. 2017. Vol. 6. P. e31274. doi: 10.7554/eLife.31274

[37] Al-Sabbagh M, Fusi L, Higham J, et al. NADPH oxidase-derived reactive oxygen species mediate decidualization of human endometrial stromal cells in response to cyclic AMP signaling. Endocrinology. 2011;152(2):730–740. doi: 10.1210/en.2010-0899

[38] Al-Sabbagh M., Fusi L., Higham J., et al. NADPH oxidase-derived reactive oxygen species mediate decidualization of human endometrial stromal cells in response to cyclic AMP signaling // Endocrinology. 2011. Vol. 152, N 2. P. 730–740. doi: 10.1210/en.2010-0899

[39] Salker MS, Nautiyal J, Steel JH, et al. Disordered IL-33/ST2 activation in decidualizing stromal cells prolongs uterine receptivity in women with recurrent pregnancy loss. PLoS One. 2012;7(12):e52252. doi: 10.1371/journal.pone.0052252

[40] Salker M.S., Nautiyal J., Steel J.H., et al. Disordered IL-33/ST2 activation in decidualizing stromal cells prolongs uterine receptivity in women with recurrent pregnancy loss // PLoS One. 2012. Vol. 7, N 12. P. e52252. doi: 10.1371/journal.pone.0052252

[41] Vrljicak P, Lucas ES, Lansdowne L, et al. Analysis of chromatin accessibility in decidualizing human endometrial stromal cells. FASEB J. 2018;32(5):2467–2477. doi: 10.1096/fj.201701098R

[42] Vrljicak P., Lucas E.S., Lansdowne L., et al. Analysis of chromatin accessibility in decidualizing human endometrial stromal cells // FASEB J. 2018. Vol. 32, N 5. P. 2467–2477. doi: 10.1096/fj.201701098R

[43] Grimaldi G, Christian M, Quenby S, Brosens JJ. Expression of epigenetic effectors in decidualizing human endometrial stromal cells. Mol Hum Reprod. 2012;18(9):451–438. doi: 10.1093/molehr/gas020

[44] Grimaldi G., Christian M., Quenby S., Brosens J.J. Expression of epigenetic effectors in decidualizing human endometrial stromal cells // Mol Hum Reprod. 2012. Vol. 18, N 9. P. 451–458. doi: 10.1093/molehr/gas020

[45] Leitao B, Jones MC, Fusi L, et al. Silencing of the JNK pathway maintains progesterone receptor activity in decidualizing human endometrial stromal cells exposed to oxidative stress signals. FASEB J. 2010; 24(5):1541–1551. doi: 10.1096/fj.09-149153

[46] Leitao B., Jones M.C., Fusi L., et al. Silencing of the JNK pathway maintains progesterone receptor activity in decidualizing human endometrial stromal cells exposed to oxidative stress signals // FASEB J. 2010. Vol. 24, N 5. P. 1541–1551. doi: 10.1096/fj.09-149153

[47] Aplin JD, Myers JE, Timms K, Westwood M. Tracking placental development in health and disease. Nat Rev Endocrinol. 2020;16(9):479–494. doi: 10.1038/s41574-020-0372-6

[48] Aplin J.D., Myers J.E., Timms K., Westwood M. Tracking placental development in health and disease // Nat Rev Endocrinol. 2020. Vol. 16, N 9. P. 479–494. doi: 10.1038/s41574-020-0372-6

[49] Marinić M, Mika K, Chigurupati S, Lynch VJ. Evolutionary transcriptomics implicates HAND2 in the origins of implantation and regulation of gestation length. Elife. 2021;10:e61257. doi: 10.7554/eLife.61257

[50] Marinić M., Mika K., Chigurupati S., Lynch V.J. Evolutionary transcriptomics implicates HAND2 in the origins of implantation and regulation of gestation length // Elife. 2021. Vol. 10. P. e61257. doi: 10.7554/eLife.61257

[51] Nancy P, Tagliani E, Tay CS, et al. Chemokine gene silencing in decidual stromal cells limits T cell access to the maternal-fetal interface. Science. 2012;336(6086):1317–1321. doi: 10.1126/science.1220030

[52] Nancy P., Tagliani E., Tay C.S., et al. Chemokine gene silencing in decidual stromal cells limits T cell access to the maternal-fetal interface // Science. 2012. Vol. 336, N 6086. P. 1317–1321. doi: 10.1126/science.1220030

[53] Gorgoulis V, Adams PD, Alimonti A, et al. Cellular senescence: defining a path forward. Cell. 2019;179(4):813–827. doi: 10.1016/j.cell.2019.10.005

[54] Gorgoulis V., Adams P.D., Alimonti A., et al. Cellular senescence: defining a path forward // Cell. 2019. Vol. 179, N 4. P. 813–827. doi: 10.1016/j.cell.2019.10.005

[55] Birch J, Gil J. Senescence and the SASP: many therapeutic avenues. Genes Dev. 2020;34(23-24):1565–1576. doi: 10.1101/gad.343129.120

[56] Birch J., Gil J. Senescence and the SASP: many therapeutic avenues // Genes Dev. 2020. Vol. 34. N 23-24. P. 1565–1576. doi: 10.1101/gad.343129.120

[57] Muñoz-Espín D, Serrano M. Cellular senescence: from physiology to pathology. Nat Rev Mol Cell Biol. 2014;15(7):482–496. doi: 10.1038/nrm3823

[58] Muñoz-Espín D., Serrano M. Cellular senescence: from physiology to pathology // Nat Rev Mol Cell Biol. 2014. Vol. 15, N 7. P. 482–496. doi: 10.1038/nrm3823

[59] Van Deursen JM. The role of senescent cells in ageing. Nature. 2014;509(7501):439–446. doi: 10.1038/nature13193

[60] Van Deursen J.M. The role of senescent cells in ageing // Nature. 2014. Vol. 509, N 7501. P. 439–446. doi: 10.1038/nature13193

[61] Owusu-Akyaw A, Krishnamoorthy K, Goldsmith LT, Morelli SS. The role of mesenchymal-epithelial transition in endometrial function. Hum Reprod Update. 2019;25(1):114–133. doi: 10.1093/humupd/dmy035

[62] Owusu-Akyaw A., Krishnamoorthy K., Goldsmith L.T., Morelli S.S. The role of mesenchymal-epithelial transition in endometrial function // Hum Reprod Update. 2019. Vol. 25, N 1. P. 114–133. doi: 10.1093/humupd/dmy035

[63] Salamonsen LA, Hutchison JC, Gargett CE. Cyclical endometrial repair and regeneration. Development. 2021;148(17):dev199577. doi: 10.1242/dev.199577

[64] Salamonsen L.A., Hutchison J.C., Gargett C.E. Cyclical endometrial repair and regeneration // Development. 2021. Vol. 148, N 17. P. dev199577. doi: 10.1242/dev.199577

[65] Lagnado A, Leslie J, Ruchaud-Sparagano MH, et al. Neutrophils induce paracrine telomere dysfunction and senescence in ROS-dependent manner. EMBO J. 2021;40(9):e106048. doi: 10.15252/embj.2020106048

[66] Lagnado A., Leslie J., Ruchaud-Sparagano M.H., et al. Neutrophils induce paracrine telomere dysfunction and senescence in ROS-dependent manner // EMBO J. 2021. Vol. 40, N 9. P. e106048. doi: 10.15252/embj.2020106048

[67] Vento-Tormo R, Efremova M, Botting RA, et al. Single-cell reconstruction of the early maternal–fetal interface in humans. Nature. 2018;563(7731):347–353. doi: 10.1038/s41586-018-0698-6

[68] Vento-Tormo R., Efremova M., Botting R.A., et al. Single-cell reconstruction of the early maternal–fetal interface in humans // Nature. 2018. Vol. 563, N 7731. P. 347–353. doi: 10.1038/s41586-018-0698-6

[69] Murata H, Tanaka S, Okada H. The regulators of human endometrial stromal cell decidualization. Biomolecules. 2022;12(9):1275. doi: 10.3390/biom12091275

[70] Murata H., Tanaka S., Okada H. The regulators of human endometrial stromal cell decidualization // Biomolecules. 2022. Vol. 12, N 9. P. 1275. doi: 10.3390/biom12091275

[71] Murata H, Tanaka S, Okada H. Immune tolerance of the human decidua. J Clin Med. 2021;10(2):351. doi: 10.3390/jcm10020351

[72] Murata H., Tanaka S., Okada H. Immune tolerance of the human decidua // J Clin Med. 2021. Vol. 10, N 2. P. 351. doi: 10.3390/jcm10020351

[73] Ticconi C, Pietropolli A, Di Simone N, et al. Endometrial immune dysfunction in recurrent pregnancy loss. Int J Mol Sci. 2019;20(21):5332. doi: 10.3390/ijms20215332

[74] Ticconi C., Pietropolli A., Di Simone N., et al. Endometrial immune dysfunction in recurrent pregnancy loss // Int J Mol Sci. 2019. Vol. 20, N 21. P. 5332. doi: 10.3390/ijms20215332

[75] Lu H, Yang HL, Zhou WJ. Rapamycin prevents spontaneous abortion by triggering decidual stromal cell autophagy-mediated NK cell residence. Autophagy. 2021;17(9):2511–2527. doi: 10.1080/15548627.2020.1833515

[76] Lu H., Yang H.L., Zhou W.J. Rapamycin prevents spontaneous abortion by triggering decidual stromal cell autophagy-mediated NK cell residence // Autophagy. 2021. Vol. 17, N 9. P. 2511–2527. doi: 10.1080/15548627.2020.1833515

[77] Croxatto D, Vacca P, Canegallo F. Stromal cells from human decidua exert a strong inhibitory effect on NK cell function and dendritic cell differentiation. PLoS One. 2014;9(2):e89006. doi: 10.1371/journal.pone.0089006

[78] Croxatto D., Vacca P., Canegallo F. Stromal cells from human decidua exert a strong inhibitory effect on NK cell function and dendritic cell differentiation // PLoS One. 2014. Vol. 9, N 2. P. e89006. doi: 10.1371/journal.pone.0089006

[79] Hisamatsu Y, Murata H, Tsubokura H, et al. Matrix metalloproteinases in human decidualized endometrial stromal cells. Curr Issues Mol Biol. 2021;43(3):2111–2123. doi: 10.3390/cimb43030146

[80] Hisamatsu Y., Murata H., Tsubokura H., et al. Metalloproteinases in human decidualized endometrial stromal cells // Curr Issues Mol Biol. 2021. Vol. 43, N 3. P. 2111–2123. doi: 10.3390/cimb43030146

[81] Okada H, Tsuzuki T, Murata H. Decidualization of the human endometrium. Reprod Med Biol. 2018;17(3):220–227. doi: 10.1002/rmb2.12088

[82] Okada H., Tsuzuki T., Murata H. Decidualization of the human endometrium // Reprod Med Biol. 2018. Vol. 17, N 3. P. 220–227. doi: 10.1002/rmb2.12088

[83] Halari CD, Nandi P, Jeyarajah MJ, et al. Decorin production by the human decidua: role in decidual cell maturation. Mol Hum Reprod. 2020;26(10):784–796. doi: 10.1093/molehr/gaaa058

[84] Halari C.D., Nandi P., Jeyarajah M.J., et al. Decorin production by the human decidua: role in decidual cell maturation // Mol Hum Reprod. 2020. Vol. 26, N 10. P. 784–796. doi: 10.1093/molehr/gaaa058

[85] Sharma S, Godbole G, Modi D. Decidual control of trophoblast invasion. Am J Reprod Immunol. 2016;75(3):341–350. doi: 10.1111/aji.12466

[86] Sharma S., Godbole G., Modi D. Decidual control of trophoblast invasion // Am J Reprod Immunol. 2016. Vol. 75, N 3. P. 341–350. doi: 10.1111/aji.12466

[87] Liu H, Huang X, Mor G, Liao A. Epigenetic modifications working in the decidualization and endometrial receptivity. Cell Mol Life Sci. 2020;77:2091–2101. doi: 10.1007/s00018-019-03395-9

[88] Liu H., Huang X., Mor G., Liao A. Epigenetic modifications working in the decidualization and endometrial receptivity // Cell Mol Life Sci. 2020. Vol. 77. P. 2091–2101. doi: 10.1007/s00018-019-03395-9

[89] Ma Q, Beal JR, Bhurke A, et al. Extracellular vesicles secreted by human uterine stromal cells regulate decidualization, angiogenesis, and trophoblast differentiation. Proc Natl Acad Sci U S A. 2022;119(38):e2200252119. doi: 10.1073/pnas.2200252119

[90] Ma Q., Beal J.R., Bhurke A., et al. Extracellular vesicles secreted by human uterine stromal cells regulate decidualization, angiogenesis, and trophoblast differentiation // Proc Natl Acad Sci U S A. 2022. Vol. 119, N 38. P. e2200252119. doi: 10.1073/pnas.2200252119

[91] Wu HM, Lo TC, Tsai CL, et al. Extracellular vesicle-associated microRNA-138-5p regulates embryo implantation and early pregnancy by adjusting GPR124. Pharmaceutics. 2022;14(6):1172. doi: 10.3390/pharmaceutics14061172

[92] Wu H.M., Lo T.C., Tsai C.L., et al. Extracellular vesicle-associated microRNA-138-5p regulates embryo implantation and early pregnancy by adjusting GPR124 // Pharmaceutics. 2022. Vol. 14, N 6. P. 1172. doi: 10.3390/pharmaceutics14061172

[93] Vyas N, Dhawan J. Exosomes: mobile platforms for targeted and synergistic signaling across cell boundaries. Cell Mol Life Sci. 2017;74(9):1567–1576. doi: 10.1007/s00018-016-2413-9

[94] Vyas N., Dhawan J. Exosomes: mobile platforms for targeted and synergistic signaling across cell boundaries // Cell Mol Life Sci. 2017. Vol. 74, N 9. P. 1567–1576. doi: 10.1007/s00018-016-2413-9

[95] Tabeeva GI, Dumanovskaja MR, Asaturova AV, et al. Features of regulation and function of inflammasomes in inflammatory diseases of the female reproductive system. Clinical and Experimental Morphology. 2020;9(3):12–20. (In Russ). doi: 10.31088/CEM2020.9.3.12-20

[96] Табеева Г.И., Думановская М.Р., Асатурова А.В., и др. Особенности регуляции и функции инфламмасом при воспалительных заболеваниях органов женской репродуктивной системы // Клиническая и экспериментальная морфология. 2020. Т. 9, № 3. С. 12–20. doi: 10.31088/CEM2020.9.3.12-20

[97] Teklenburg G, Salker M, Molokhia M, et al. Natural selection of human embryos: decidualizing endometrial stromal cells serve as sensors of embryo quality upon implantation. PLoS One. 2010;5(4):e10258. doi: 10.1371/journal.pone.0010258

[98] Teklenburg G., Salker M., Molokhia M., et al. Natural selection of human embryos: decidualizing endometrial stromal cells serve as sensors of embryo quality upon implantation // PLoS One. 2010. Vol. 5, N 4. P. e10258. doi: 10.1371/journal.pone.0010258

[99] Bogdanova IM, Boltovskaja MN. Natural selection of human embryos: immune mechanisms of quality controi. Immunologiya. 2019;40(1):68–73. (In Russ). doi: 10.24411/0206-4952-2019-11008

[100] Богданова И.М., Болтовская М.Н. Естественная селекция эмбрионов человека: иммунные механизмы контроля качества // Иммунология. 2019. Т. 40, № 1. С. 68–73. doi: 10.24411/0206-4952-2019-11008

[101] Kong CS, Ordoñez AA, Turner S. Embryo biosensing by uterine natural killer cells determines endometrial fate decisions at implantation. FASEB J. 2021;35(4):e21336. doi: 10.1096/fj.202002217R

[102] Kong C.S., Ordoñez A.A., Turner S. Embryo biosensing by uterine natural killer cells determines endometrial fate decisions at implantation // FASEB J. 2021. Vol. 35, N 4. P. e21336. doi: 10.1096/fj.202002217R

[103] Deryabin PI, Borodkina AV. Stromal cell senescence contributes to impaired endometrial decidualization and defective interaction with trophoblast cells. Hum Reprod. 2022;37(7):1505–1524. doi: 10.1093/humrep/deac112

[104] Deryabin P.I., Borodkina A.V. Stromal cell senescence contributes to impaired endometrial decidualization and defective interaction with trophoblast cells // Hum Reprod. 2022. Vol. 37, N 7. P. 1505–1524. doi: 10.1093/humrep/deac112

[105] Tapia-Pizarro A, Figueroa P, Brito J, et al. Endometrial gene expression reveals compromised progesterone signaling in women refractory to embryo implantation. Reprod Biol Endocrinol. 2014;12:92. doi: 10.1186/1477-7827-12-92

[106] Tapia-Pizarro A., Figueroa P., Brito J., et al. Endometrial gene expression reveals compromised progesterone signaling in women refractory to embryo implantation // Reprod Biol Endocrinol. 2014. Vol. 12. P. 92. doi: 10.1186/1477-7827-12-92

[107] Woods L, Perez-Garcia V, Kieckbusch J, et al. Decidualisation and placentation defects are a major cause of age-related reproductive decline. Nat Commun. 2017;8(1):352. doi: 10.1038/s41467-017-00308-x

[108] Woods L., Perez-Garcia V., Kieckbusch J., et al. Decidualisation and placentation defects are a major cause of age-related reproductive decline // Nat Commun. 2017. Vol. 8, N 1. P. 352. doi: 10.1038/s41467-017-00308-x

[109] Lucas ES, Dyer NP, Murakami K, et al. Loss of endometrial plasticity in recurrent pregnancy loss. Stem Cells. 2016;34(2):346–356. doi: 10.1002/stem.2222

[110] Lucas E.S., Dyer N.P., Murakami K., et al. Loss of endometrial plasticity in recurrent pregnancy loss // Stem Cells. 2016. Vol. 34, N 2. P. 346–356. doi: 10.1002/stem.2222

[111] Tabeeva GI, Dumanovskaja MR, Bogdanova IM, et al. Morphofunctional features of the uteroplacental unit and mouse embryo in the early stages of experimental miscarriage. Clinical and Experimental Morphology. 2020;9(3):50–60. (In Russ). doi: 10.31088/CEM2020.9.3.50-60

[112] Табеева Г.И., Думановская М.Р., Богданова И.М. Особенности морфофункционального состояния маточно-плацентарной единицы и эмбриона мыши на ранних сроках экспериментального невынашивания беременности // Клиническая и экспериментальная морфология. 2020. Т. 9, № 3. С. 50–60. doi: 10.31088/CEM2020.9.3.50-60

[113] Garrido-Gomez T, Dominguez F, Quiñonero A, et al. Defective decidualization during and after severe preeclampsia reveals a possible maternal contribution to the etiology. Proc Natl Acad Sci U S A. 2017;114(40):E8468–E8477. doi: 10.1073/pnas.1706546114

[114] Garrido-Gomez T., Dominguez F., Quiñonero A., et al. Defective decidualization during and after severe preeclampsia reveals a possible maternal contribution to the etiology // Proc Natl Acad Sci U S A. 2017. Vol. 114, N 40. P. E8468–E8477. doi: 10.1073/pnas.1706546114

[115] Bogdanova IM, Fokina TV, Stepanova II, et al. The role of the endometrial decidualization in the establishment and development of pregnancy. Clinical and Experimental Morphology. 2018;7(4):50–60. (In Russ). doi: 10.31088/2226-5988-2018-28-4-50-60

[116] Богданова И.М., Фокина Т.В., Степанова И.И. Роль децидуализации эндометрия в наступлении и развитии беременности // Клиническая и экспериментальная морфология. 2018. Т. 28, № 4. С. 50–60. doi: 10.31088/2226-5988-2018-28-4-50-60

[117] Grebenkina PV, Mikhailova VA, Oshkolova AA, et al. Decidual natural killer cells and trophoblast cells: cellular, humoral and molecular mechanisms of interaction. Medical Immunology (Russia). 2022;24(6):1085–1108. (In Russ). doi: 10.15789/1563-0625-DNK-2540

[118] Гребенкина П.В., Михайлова В.А., Ошколова А.А., и др. Децидуальные естественные киллеры и клетки трофобласта: клеточные, гуморальные и молекулярные механизмы взаимодействия // Медицинская иммунология. 2022. Т. 24, № 6. С. 1085–1108. doi: 10.15789/1563-0625-DNK-2540

[119] Milovanov AP, Ozhiganova IN. Embryochorionic insufficiency: anatomic and physiologic prerequisites, rationale, definitions and pathogenetic mechanisms. Arkhiv Patologii. 2014;76(3):4–8. (In Russ.)

[120] Милованов А.П., Ожиганова И.Н. Эмбриохориальная недостаточность: анатомофизиологические предпосылки, обоснование, дефиниции и патогенетические механизмы // Архив патологии. 2014. Т. 76, № 3. С. 4–8.

[121] Smits L, Bockstal MV, Frezin J. Deciduosis of the appendix: a rare cause of acute abdomen during pregnancy (a case report). Pan Afr Med J. 2020;37:316. doi: 10.11604/pamj.2020.37.316.26728

[122] Smits L., Bockstal M.V., Frezin J. Deciduosis of the appendix: a rare cause of acute abdomen during pregnancy (a case report) // Pan Afr Med J. 2020. Vol. 37. P. 316. doi: 10.11604/pamj.2020.37.316.26728

[123] Kong C-S, Ordoñez AA, Turner S, et al. Involvement of uterine natural killer cells in the natural selection of human embryos at implantation. BioRxiv. 2020. doi: 10.1101/2020.08.14.251033

[124] Kong C.-S., Orbonez A.A., Turner S., et al. Involvement of uterine natural killer cells in the natural selection of human embryos at implantation // BioRxiv. 2020. doi: 10.1101/2020.08.14.251033

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