Embryo-endometrium dialogue: key factors in implantation

1. Кадыров З.А., Фаниев М.В., Прокопьев Я.В., Фаустова К.В., Севрюков Ф.А., Водолажский Д.И., Крупин В.Н. Репродуктивное здоровье населения России как ключевой фактор демографической динамики. Вестник современной клинической медицины. 2022; 15(5): 100-6. https://dx.doi.org/10.20969/VSKM.2022.15(5).100-106 [Kadyrov Z.A., Faniev M.V., Prokopiev Y.V., Faustova K.V., Sevryukov F.A., Vodolazhsky D.I., Krupin V.N. Reproductive health of the Russian population as a key factor of demographic dynamics. The Bulletin of Contemporary Clinical Medicine. 2022; 15(5): 100-6 (in Russian). https://dx.doi.org/10.20969/VSKM.2022.15(5).100-106].
2. Kushnir V.A., Smith G.D., Adashi E.Y. The future of IVF : the new normal in human reproduction. Reprod. Sci. 2022; 29(3): 849-56. https://dx.doi.org/10.1007/s43032-021-00829-3
3. Tschare L., Ennemoser A., Carli L., Vaccari E., Feichtinger M. Impact of maternally derived meiotic aneuploidies on early embryonic development in vitro. J. Assist. Reprod. Genet. 2023; 40(11): 2715-23. https://dx.doi.org/10.1007/s10815-023-02922-9
4. Karimi S., Baharaghdam S., Danaii S., Yousefi M. Embryo-maternal cross-talk: key players in successful implantation and live birth rates. Reprod. Biol. Endocrinol. 2025; 23(1): 136. https://dx.doi.org/10.1186/s12958-025-01477-x
5. Cozzolino M., Diaz-Gimeno P., Pellicer A., Garrido N. Evaluation of the endometrial receptivity assay and the preimplantation genetic test for aneuploidy in overcoming recurrent implantation failure. J. Assist. Reprod. Genet. 2020; 37(12): 2989-97. https://dx.doi.org/10.1007/s10815-020-01948-7
6. Cimadomo D., de Los Santos M.J., Griesinger G., Lainas G., Le Clef N., McLernon D.J. et al.; ESHRE Working Group on Recurrent Implantation Failure. ESHRE good practice recommendations on recurrent implantation failure. Hum. Reprod. Open. 2023; 2023(3): hoad023. https://dx.doi.org/10.1093/hropen/hoad023
7. Matsumoto H., Fukui E., Yoshizawa M. Molecular and cellular events involved in the completion of blastocyst implantation. Reprod. Med. Biol. 2016; 15(2): 53-8. https://dx.doi.org/10.1007/s12522-015-0222-8
8. Paulson R.J. Introduction: Endometrial receptivity: evaluation, induction and inhibition. Fertil. Steril. 2019; 111(4): 609-10. https://dx.doi.org/10.1016/j.fertnstert.2019.02.029
9. Maziotis E., Kalampokas T., Giannelou P., Grigoriadis S., Rapani A., Anifantakis M. et al. Commercially available molecular approaches to evaluate endometrial receptivity: a systematic review and critical analysis of the literature. Diagnostics. 2022; 12(11): 2611. https://dx.doi.org/10.3390/diagnostics12112611
10. Harvey A.J., Willson B.E., Surrey E.S., Gardner D.W. Ovarian stimulation protocols: impact on oocyte and endometrial quality and function. Fertil. Steril. 2025; 123(1): 10-21. https://dx.doi.org/10.1016/j.fertnstert.2024.08.340
11. Ochoa-Bernal M.A., Fazleabas A.T. Physiologic events of embryo implantation and decidualization in human and non-human primates. Int. J. Mol. Sci. 2020; 21(6): 1973. https://dx.doi.org/10.3390/ijms21061973
12. Liu K.E., Hartman M., Hartman A., Luo Z.C., Mahutte N. The impact of a thin endometrial lining on fresh and frozen–thaw IVF outcomes: an analysis of over 40 000 embryo transfers. Hum. Reprod. 2018; 33(10): 1883-8. https://dx.doi.org/10.1093/humrep/dey281
13. Noyes R.W., Hertig A.T., Rock J. Reprint of: Dating the endometrial biopsy. Fertil. Steril. 2019; 112(4 Suppl1):e93-e115. https://dx.doi.org/10.1016/j.fertnstert.2019.08.079
14. Quinn K.E., Matson B.C., Wetendorf M., Caron K.M. Pinopodes: recent advancements, current perspectives, and future directions. Mol. Cell. Endocrinol. 2020; 501: 110644. https://dx.doi.org/10.1016/j.mce.2019.110644
15. Li J., Liu H., Lim J., Xing H., Chen Y., Yang S. et al. Molecular and biological markers for assessing endometrial receptivity in infertile women: a narrative review. J. Int. Med. Res. 2025; 53(4): 03000605251328893. https://dx.doi.org/10.1177/03000605251328893
16. Fox C., Morin S., Jeong J.W., Scott R.T. Jr, Lessey B.A. Local and systemic factors and implantation: what is the evidence? Fertil. Steril. 2016; 105(4): 873-84. https://dx.doi.org/10.1016/j.fertnstert.2016.02.018
17. Massimiani M., Lacconi V., La Civita F., Ticconi C., Rago R., Campagnolo L. Molecular signaling regulating endometrium-blastocyst crosstalk. Int. J. Mol. Sci. 2019; 21(1): 23. https://dx.doi.org/10.3390/ijms21010023
18. Chung T.W., Park M.J., Kim H.S., Choi H.J., Ha K.T. Integrin αVβ3 and αVβ5 are required for leukemia inhibitory factor-mediated the adhesion of trophoblast cells to the endometrial cells. Biochem. Biophys. Res. Commun. 2016; 469(4): 936-40. https://dx.doi.org/10.1016/j.bbrc.2015.12.103
19. Zhang Y., Tang L., Liu H., Cheng Y. The multiple functions of HB-EGF in female reproduction and related cancer: molecular mechanisms and targeting strategies. Reprod. Sci. 2024; 31(9): 2588-603. https://dx.doi.org/10.1007/s43032-024-01454-6
20. Rottenstreich A., Coller B.S. The potential role of the αVβ3 integrin receptor in placental biology and normal and complicated pregnancies. Br. J. Haematol. 2025; 206(4): 1054-61. https://dx.doi.org/10.1111/bjh.20019
21. D’Occhio M.J., Campanile G., Zicarelli L., Visintin J.A., Baruselli P.S. Adhesion molecules in gamete transport, fertilization, early embryonic development, and implantation-role in establishing a pregnancy in cattle: A review. Mol. Reprod. Dev. 2020; 87(2): 206-22. https://dx.doi.org/10.1002/mrd.23312
22. Francis L.W., Yao S.N., Powell L.C., Griffiths S., Berquand A., Piasecki T. et al. Highly glycosylated MUC1 mediates high affinity L-selectin binding at the human endometrial surface. J. Nanobiotechnology. 2021; 19(1): 50. https://dx.doi.org/10.1186/s12951-021-00793-9
23. Zhou M., Tian T., Wu C. Mechanism underlying the regulation of mucin secretion in the uterus during pregnancy. Int. J. Mol. Sci. 2023; 24(21): 15896. https://dx.doi.org/10.3390/ijms242115896
24. Jain M., Samokhodskaya L., Mladova E., Panina O. Mucosal biomarkers for endometrial receptivity: A promising yet underexplored aspect of reproductive medicine. Syst. Biol. Reprod. Med. 2022; 68(1): 13-24. https://dx.doi.org/10.1080/19396368.2021.1985186
25. Wu F., Mao D., Liu Y., Chen X., Xu H., Li T.C. et al. Localization of Mucin 1 in endometrial luminal epithelium and its expression in women with reproductive failure during implantation window. J. Mol. Histol. 2019; 50(6): 563-72. https://dx.doi.org/10.1007/s10735-019-09848-6
26. Wu F., Chen X., Liu Y., Liang B., Xu H., Li T.C. et al. Decreased MUC1 in endometrium is an independent receptivity marker in recurrent implantation failure during implantation window. Reprod. Biol. Endocrinol. 2018; 16(1): 60. https://dx.doi.org/10.1186/s12958-018-0379-1
27. Shekibi M., Heng S., Nie G. MicroRNAs in the regulation of endometrial receptivity for embryo implantation. Int. J. Mol. Sci. 2022; 23(11): 6210. https://dx.doi.org/10.3390/ijms23116210
28. Altmäe S., Koel M., Võsa U., Adler P., Suhorutšenko M., Laisk-Podar T. et al. Meta-signature of human endometrial receptivity: a meta-analysis and validation study of transcriptomic biomarkers. Sci. Rep. 2017; 7(1): 10077. https://dx.doi.org/10.1038/s41598-017-10098-3
29. von Grothusen C., Frisendahl C., Modhukur V., Lalitkumar P.G., Peters M., Faridani O.R. et al. Uterine fluid microRNAs are dysregulated in women with recurrent implantation failure. Hum. Reprod. 2022; 37(4): 734-46. https://dx.doi.org/10.1093/humrep/deac019
30. Glujovsky D., Lattes K., Miguens M., Pesce R., Ciapponi A. Personalized embryo transfer guided by endometrial receptivity analysis: a systematic review with meta-analysis. Hum. Reprod. 2023; 38(7): 1305-17. https://dx.doi.org/10.1093/humrep/dead098
31. Hashimoto T., Koizumi M., Doshida M., Toya M., Sagara E., Oka N. et al. Efficacy of the endometrial receptivity array for repeated implantation failure in Japan: A retrospective, two‐centers study. Reprod. Med. Biol. 2017; 16(3): 290-6. https://dx.doi.org/10.1002/rmb2.12041
32. Enciso M., Aizpurua J., Rodríguez-Estrada B., Jurado I., Ferrández-Rives M., Rodríguez E. et al. The precise determination of the window of implantation significantly improves ART outcomes. Sci. Rep. 2021; 11(1): 13420. https://dx.doi.org/10.1038/s41598-021-92955-w
33. Enciso M., Carrascosa J.P., Sarasa J., Martínez-Ortiz P.A., Munné S., Horcajadas J.A. et al. Development of a new comprehensive and reliable endometrial receptivity map (ER Map/ER Grade) based on RT-qPCR gene expression analysis. Hum. Reprod. 2018; 33(2): 220-8. https://dx.doi.org/10.1093/humrep/dex370
34. Burmenskaya O.V., Bozhenko V.K., Smolnikova V.Y., Kalinina E.A., Korneeva I.E., Donnikov A.E. et al. Transcription profile analysis of the endometrium revealed molecular markers of the personalized ‘window of implantation’ during in vitro fertilization. Gynecol. Endocrinol. 2017; 33(supl. 1): 22-7. https://dx.doi.org/10.1080/09513590.2017.1404236
35. Li J., Liu H., Lim J., Xing H., Chen Y., Yang S. et al. Molecular and biological markers for assessing endometrial receptivity in infertile women: A narrative review. 2025; 53(4): 03000605251328893. https://dx.doi.org/10.1177/03000605251328893
36. Li N., Zhang Y., Li R., Chen Y., Huang L., Tan Z. et al. Personalized embryo transfer guided by rsERT improves pregnancy outcomes in patients with repeated implantation failure. Front. Med. 2024; 11: 1369317. https://dx.doi.org/10.3389/fmed.2024.1369317
37. Meltsov A., Saare M., Teder H., Paluoja P., Arffman R.K., Piltonen T. et al. Targeted gene expression profiling for accurate endometrial receptivity testing. Sci. Rep. 2023; 13(1): 13959. https://dx.doi.org/10.1038/s41598-023-40991-z
38. Gurung S., Greening D.W., Catt S., Salamonsen L., Evans J. Exosomes and soluble secretome from hormone-treated endometrial epithelial cells direct embryo implantation. Mol. Hum. Reprod. 2020; 26(7): 510-20. https://dx.doi.org/10.1093/molehr/gaaa034
39. Rai A., Poh L., Fatmous M., Fang H.A., Gurung Sh., Vollenhoven B. et al. Proteomic profiling of human uterine extracellular vesicles reveal dynamic regulation of key players of embryo implantation and fertility during menstrual cycle. Proteomics. 2021; 21(13-14). https://dx.doi.org/10.1002/pmic.202000211
40. Poh Q.H., Rai A., Salamonsen L.A., Greening D.W. Omics insights into extracellular vesicles in embryo implantation and their therapeutic utility. Proteomics. 2023. 23(6): 1-28. https://dx.doi.org/10.1002/pmic.202200107
41. Welsh J.A., Goberdhan D.C.I., O'Driscoll L., Buzas E.I., Blenkiron C., Bussolati B. et al. Minimal information for studies of extracellular vesicles (MISEV2023): From basic to advanced approaches. J. Extracell. Vesicles. 2024; 13(2): e12404. https://dx.doi.org/10.1002/jev2.12451
42. Salamonsen L.A., Evans J., Nguyen H.P.T., Edgell T.A. The microenvironment of human implantation: Determinant of reproductive success. Am. J. Reprod. Immunol. 2016; 75(3): 218-25. https://dx.doi.org/10.1111/aji.12450

Received 25.02.2026

Accepted 26.06.2026