Hostname: page-component-f554764f5-nwwvg Total loading time: 0 Render date: 2025-04-23T00:24:25.386Z Has data issue: false hasContentIssue false

The role of microRNAs in the regulation of critical genes and signalling pathways that determine endometrial receptivity

Published online by Cambridge University Press:  18 September 2024

Yumei Wang
Affiliation:
College of Animal Science and Technology, Ningxia University, Yin Chuan, NingXia, 750021, China
Zhongxiang Ji
Affiliation:
College of Animal Science and Technology, Ningxia University, Yin Chuan, NingXia, 750021, China
Ni Yao
Affiliation:
College of Animal Science and Technology, Ningxia University, Yin Chuan, NingXia, 750021, China
Ximin Hu
Affiliation:
College of Animal Science and Technology, Ningxia University, Yin Chuan, NingXia, 750021, China
Ran Zhou
Affiliation:
College of Animal Science and Technology, Ningxia University, Yin Chuan, NingXia, 750021, China
Xingping Wang*
Affiliation:
College of Animal Science and Technology, Ningxia University, Yin Chuan, NingXia, 750021, China
Zhuoma Luoreng*
Affiliation:
College of Animal Science and Technology, Ningxia University, Yin Chuan, NingXia, 750021, China
*
Corresponding authors: Xingping Wang; Email: [email protected]; Zhuoma Luoreng; Email: [email protected]
Corresponding authors: Xingping Wang; Email: [email protected]; Zhuoma Luoreng; Email: [email protected]

Summary

Endometrial receptivity is the ability of the endometrium to accept embryos. Thus, endometrial receptivity dysfunction is an important factor leading to embryo implantation failure. A good endometrial receptivity provides a suitable environment for embryo implantation, improving the embryo implantation rate. The “implantation window” stage, or the receptive stage of the endometrium, is regulated by various hormones, genes, proteins and cytokines, among which microRNAs (miRNAs) and their target genes have a regulatory effect on endometrial receptivity. This review outlines the relationship between endometrial receptivity and pregnancy, the mRNAs and related signalling pathways that regulate endometrial receptivity, and the regulatory role of miRNA in endometrial receptivity, providing a deeper understanding of the regulatory mechanisms of miRNA on endometrial receptivity in humans and animals and reference for the endometrial receptivity-related research.

Type
Review Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Akbar, R., Ullah, K., Rahman, T. U., Cheng, Y., Pang, H. Y., Jin, L. Y., Wang, Q. J., Huang, H. F. and Sheng, J. Z. (2020) miR-183-5p regulates uterine receptivity and enhances embryo implantation. Journal of Molecular Endocrinology, 64, 4352.CrossRefGoogle ScholarPubMed
An, X., Liu, X., Zhang, L., Liu, J., Zhao, X., Chen, K., Ma, H., Li, G., Cao, B. and Song, Y. (2017) MiR-449a regulates caprine endometrial stromal cell apoptosis and endometrial receptivity. Scientific Reports, 7, 12248.CrossRefGoogle ScholarPubMed
Balaguer, N., Moreno, I., Herrero, M., Gonzalez-Monfort, M., Vilella, F. and Simon, C. (2019) MicroRNA-30d deficiency during preconception affects endometrial receptivity by decreasing implantation rates and impairing fetal growth. American Journal of Obstetrics and Gynecology, 221, 4146.CrossRefGoogle ScholarPubMed
Barton, S., Zhou, W., Santos, L. L., Menkhorst, E., Yang, G., Tinn, T. W., Ang, C., Lucky, T. and Dimitriadis, E. (2023) miR-23b-3p regulates human endometrial epithelial cell adhesion implying a role in implantation. Reproduction, 165, 407416.CrossRefGoogle ScholarPubMed
Blanco-Breindel, M. F., Singh, M. and Kahn, J. (2023) Endometrial Receptivity. StatPearls Publishing.Google ScholarPubMed
Bui, A. H., Timmons, D. B. and Young, S. L. (2022) Evaluation of endometrial receptivity and implantation failure. Current Opinion in Obstetrics and Gynecology, 34, 107113.CrossRefGoogle ScholarPubMed
Cai, J. L., Liu, L. L., Hu, Y., Jiang, X. M., Qiu, H. L., Sha, A. G., Wang, C. G., Zuo, Z. H. and Ren, J. Z. (2016) Polychlorinated biphenyls impair endometrial receptivity in vitro via regulating miR-30d expression and epithelial mesenchymal transition. Toxicology, 365, 2534.CrossRefGoogle ScholarPubMed
Cai, X., Xu, M., Zhang, H., Zhang, M., Wang, J., Mei, J., Zhang, Y., Zhou, J., Zhen, X., Kang, N., Yue, Q., Sun, H., Jiang, R. and Yan, G. (2022) Endometrial stromal PRMT5 plays a crucial role in decidualization by regulating NF-kappaB signaling in endometriosis. Cell Death Discovery, 8, 408.CrossRefGoogle Scholar
Camargo-Diaz, F., Garcia, V., Ocampo-Barcenas, A., Gonzalez-Marquez, H. and Lopez-Bayghen, E. (2017) Colony stimulating factor-1 and leukemia inhibitor factor expression from current-cycle cannula isolated endometrial cells are associated with increased endometrial receptivity and pregnancy. BMC Women’s Health, 17, 63.CrossRefGoogle ScholarPubMed
Cao, D., Liang, J., Feng, F., Shi, S., Tan, Q. and Wang, Z. (2020) MiR-183 impeded embryo implantation by regulating Hbegf and Lamc1 in mouse uterus. Theriogenology, 158, 218226.CrossRefGoogle ScholarPubMed
Capece, D., Verzella, D., Flati, I., Arboretto, P., Cornice, J. and Franzoso, G. (2022) NF-kappaB: blending metabolism, immunity, and inflammation. Trends in Immunology, 43, 757775.CrossRefGoogle ScholarPubMed
Chen, C., Zhao, Y., Yu, Y., Li, R. and Qiao, J. (2016) MiR-125b regulates endometrial receptivity by targeting MMP26 in women undergoing IVF-ET with elevated progesterone on HCG priming day. Scientific Reports, 6, 25302.CrossRefGoogle ScholarPubMed
Chen, Q., Ni, Y., Han, M., Zhou, W. J., Zhu, X. B. and Zhang, A. J. (2020) Integrin-linked kinase improves uterine receptivity formation by activating Wnt/beta-catenin signaling and up-regulating MMP-3/9 expression. American Journal of Translational Research, 12, 30113022.Google ScholarPubMed
Cheng, J., Li, C., Ying, Y., Lv, J., Qu, X., McGowan, E., Lin, Y. and Zhu, X. (2022) Metformin alleviates endometriosis and potentiates endometrial receptivity via decreasing VEGF and MMP9 and increasing leukemia inhibitor factor and HOXA10. Frontiers in Pharmacology, 13, 750208.CrossRefGoogle ScholarPubMed
Choi, H. J., Chung, T. W., Park, M. J., Jung, Y. S., Lee, S. O., Kim, K. J. and Ha, K. T. (2017) Water-extracted tubers of Cyperus rotundus L. enhance endometrial receptivity through leukemia inhibitory factor-mediated expression of integrin alphaVbeta3 and alphaVbeta5. Journal of Ethnopharmacology, 208, 1623.CrossRefGoogle ScholarPubMed
Chu, B., Zhong, L., Dou, S., Wang, J., Li, J., Wang, M., Shi, Q., Mei, Y. and Wu, M. (2015) miRNA-181 regulates embryo implantation in mice through targeting leukemia inhibitory factor. Journal of Molecular Cell Biology, 7, 1222.CrossRefGoogle ScholarPubMed
Chung, T. W., Park, M. J., Lee, H., Kim, K. J., Kim, C. H., Choi, H. J. and Ha, K. T. (2019) Enhancement of endometrial receptivity by cnidium officinale through expressing LIF and integrins. Evidence-Based Complementary and Alternative Medicine, 2019, 7560631.CrossRefGoogle ScholarPubMed
Crha, I., Ventruba, P., Zakova, J., Jeseta, M., Pilka, R., Lousova, E. and Papikova, Z. (2019) Uterine microbiome and endometrial receptivity. Ceska Gynekologie, 84, 4954.Google ScholarPubMed
Cui, J., Liu, X., Yang, L., Che, S., Guo, H., Han, J., Zhu, Z., Cao, B., An, X., Zhang, L. and Song, Y. (2020) MiR-184 combined with STC2 promotes endometrial epithelial cell apoptosis in dairy goats via RAS/RAF/MEK/ERK pathway. Genes, 11, 1052.CrossRefGoogle ScholarPubMed
Dong, X., Sui, C., Huang, K., Wang, L., Hu, D., Xiong, T., Wang, R. and Zhang, H. (2016) MicroRNA-223-3p suppresses leukemia inhibitory factor expression and pinopodes formation during embryo implantation in mice. American Journal of Translational Research, 8, 11551163.Google ScholarPubMed
Dubey, P., Batra, V., Sarwalia, P., Nayak, S., Baithalu, R., Kumar, R. and Datta, T. K. (2023) miR-1246 is implicated as a possible candidate for endometrium remodelling facilitating implantation in buffalo (Bubalus bubalis). Veterinary Medicine and Science, 9, 443456.CrossRefGoogle ScholarPubMed
Dvorak, H. F. (2000) VPF/VEGF and the angiogenic response. Seminars in Perinatology, 24, 7578.CrossRefGoogle ScholarPubMed
Eun-Yeong, K., Tae-Wook, C., Hee-Jung, C., Ki-Tae, H., Yeon-Seop, J., Syng-Ook, L., Jun-Yong, C., Hyung, S. K., Sooseong, Y. and Myeong, S. L. (2019) Extracts from Paeonia lactiflora Pallas, Rehmannia Glutinosa var. Purpurea Makino, Perilla Frutescens var. Acuta Kudo may increase the endometrial receptivity through expression of leukemia inhibitory factor and adhesion molecules. Journal of Traditional Chinese Medicine, 39, 1525.Google ScholarPubMed
Feng, R., Qin, X., Li, Q., Olugbenga, A. S., Huang, F., Li, Y., Zhao, Q. and Zheng, P. (2022) Progesterone regulates inflammation and receptivity of cells via the NF-kappaB and LIF/STAT3 pathways. Theriogenology, 186, 5059.CrossRefGoogle ScholarPubMed
Gebril, M., Hirota, Y., Aikawa, S., Fukui, Y., Kaku, T., Matsuo, M., Hirata, T., Akaeda, S., Hiraoka, T., Shimizu-Hirota, R., Takeda, N., Taha, T., Balah, O. A., Elnoury, M., Fujii, T. and Osuga, Y. (2020) Uterine Epithelial Progesterone Receptor Governs Uterine Receptivity Through Epithelial Cell Differentiation. Endocrinology, 161, bqaa195.CrossRefGoogle ScholarPubMed
Goharitaban, S., Abedelahi, A., Hamdi, K., Khazaei, M., Esmaeilivand, M. and Niknafs, B. (2022) Role of endometrial microRNAs in repeated implantation failure (mini-review). Frontiers in Cell and Developmental Biology, 10, 936173.CrossRefGoogle ScholarPubMed
Governini, L., Luongo, F. P., Haxhiu, A., Piomboni, P. and Luddi, A. (2021) Main actors behind the endometrial receptivity and successful implantation. Tissue and Cell, 73, 101656.CrossRefGoogle ScholarPubMed
Griffiths, M., Van Sinderen, M., Rainczuk, K. and Dimitriadis, E. (2019) miR-29c overexpression and COL4A1 downregulation in infertile human endometrium reduces endometrial epithelial cell adhesive capacity in vitro implying roles in receptivity. Scientific Reports, 9, 8644.CrossRefGoogle ScholarPubMed
Guan, X., Liu, D., Zhou, H., Dai, C., Wang, T., Fang, Y., Jia, Y. and Li, K. (2022) Melatonin improves pregnancy outcomes in adenomyosis mice by restoring endometrial receptivity via NF-kappaB/apoptosis signaling. Annals of Translational Medicine, 10, 1317.CrossRefGoogle ScholarPubMed
Guo, X., Yi, H., Li, T. C., Wang, Y., Wang, H. and Chen, X. (2021) Role of vascular endothelial growth factor (VEGF) in human embryo implantation: clinical implications. Biomolecules, 11, 253.CrossRefGoogle ScholarPubMed
Hajipour, H., Sambrani, R., Ghorbani, M., Mirzamohammadi, Z. and Nouri, M. (2021) Sildenafil citrate-loaded targeted nanostructured lipid carrier enhances receptivity potential of endometrial cells via LIF and VEGF upregulation. Naunyn-Schmiedeberg’s Archives of Pharmacology, 394, 23232331.CrossRefGoogle ScholarPubMed
He, B., Teng, X. M., Hao, F., Zhao, M., Chen, Z. Q., Li, K. M. and Yan, Q. (2022) Decreased intracellular IL-33 impairs endometrial receptivity in women with adenomyosis. Frontiers in Endocrinology, 13, 928024.CrossRefGoogle ScholarPubMed
Hesam, S. M., Seghinsara, A. M., Shokrzadeh, N. and Niknafs, B. (2019) The effect of fludrocortisone on the uterine receptivity partially mediated by ERK1/2-mTOR pathway. Journal of Cellular Physiology, 234, 2009820110.CrossRefGoogle Scholar
Hu, W., Liang, Y. X., Luo, J. M., Gu, X. W., Chen, Z. C., Fu, T., Zhu, Y. Y., Lin, S., Diao, H. L., Jia, B. and Yang, Z. M. (2019) Nucleolar stress regulation of endometrial receptivity in mouse models and human cell lines. Cell Death & Disease, 10, 831.CrossRefGoogle ScholarPubMed
Hua, R., Zhang, X., Li, W., Lian, W., Liu, Q., Gao, D., Wang, Y. and Lei, M. (2020) Ssc-miR-21-5p regulates endometrial epithelial cells proliferation, apoptosis and migration via the PDCD4/AKT pathway. Journal of Cell Science, 133, jcs248898.CrossRefGoogle ScholarPubMed
Huang, K., Chen, G., Fan, W. and Hu, L. (2020) miR-23a-3p increases endometrial receptivity via CUL3 during embryo implantation. Journal of Molecular Endocrinology, 65, 3544.CrossRefGoogle ScholarPubMed
Jana, S. K., Banerjee, P., Mukherjee, R., Chakravarty, B. and Chaudhury, K. (2013) HOXA-11 mediated dysregulation of matrix remodeling during implantation window in women with endometriosis. Journal of Assisted Reproduction and Genetics, 30, 15051512.CrossRefGoogle ScholarPubMed
Kang, Y. J., Lees, M., Matthews, L. C., Kimber, S. J., Forbes, K. and Aplin, J. D. (2015) MiR-145 suppresses embryo-epithelial juxtacrine communication at implantation by modulating maternal IGF1R. Journal of Cell Science, 128, 804814.Google ScholarPubMed
Kara, M., Ozcan, S. S., Aran, T., Kara, O. and Yilmaz, N. (2019) Evaluation of endometrial receptivity by measuring HOXA-10, HOXA-11, and leukemia inhibitory factor expression in patients with polycystic ovary syndrome. Gynecology and Minimally Invasive Therapy, 8, 118122.CrossRefGoogle ScholarPubMed
Kelleher, A. M., Behura, S. K., Burns, G. W., Young, S. L., DeMayo, F. J. and Spencer, T. E. (2019) Integrative analysis of the forkhead box A2 (FOXA2) cistrome for the human endometrium. The FASEB Journal, 33, 85438554.CrossRefGoogle ScholarPubMed
Khan, A. W., Farooq, M., Hwang, M. J., Haseeb, M. and Choi, S. (2023) Autoimmune neuroinflammatory diseases: Role of interleukins. International Journal of Molecular Sciences, 24, 7960.CrossRefGoogle ScholarPubMed
Kong, C., Sun, L., Zhang, M., Ding, L., Zhang, Q., Cheng, X., Diao, Z., Yan, Q., Zhang, H., Fang, T., Zhen, X., Hu, Y., Sun, H. and Yan, G. (2016) miR-133b reverses the hydrosalpinx-induced impairment of embryo attachment through down-regulation of SGK1. The Journal of Clinical Endocrinology & Metabolism, 101, 14781489.CrossRefGoogle ScholarPubMed
Kresowik, J. D., Devor, E. J., Van Voorhis, B. J. and Leslie, K. K. (2014) MicroRNA-31 is significantly elevated in both human endometrium and serum during the window of implantation: a potential biomarker for optimum receptivity. Biology of Reproduction, 91, 17.CrossRefGoogle ScholarPubMed
Lessey, B. A. and Young, S. L. (2019) What exactly is endometrial receptivity? Fertility and Sterility, 111, 611617.CrossRefGoogle ScholarPubMed
Li, J. (2019) Talin1/miR-1285-3p/PIPK1 Axis Regulating Endometrial Adhesionvia Influencing PI3K/AKT Signaling Pathway. Doctoral thesis. Guangxi Medical University (In Chinese).Google Scholar
Li, L., Jiang, H., Wei, X., Geng, D., He, M. and Du, H. (2019) Bu Shen Zhu Yun decoction improves endometrial receptivity via VEGFR-2-mediated angiogenesis. Evidence-Based Complementary and Alternative Medicine, 2019, 114.Google Scholar
Li, Q., Liu, W., Chiu, P. and Yeung, W. (2020) MiR-let-7a/g enhances uterine receptivity via suppressing Wnt/beta-catenin under the modulation of ovarian hormones. Reproductive Sciences, 27, 11641174.CrossRefGoogle ScholarPubMed
Li, X., Yao, X., Li, K., Guo, J., Deng, K., Liu, Z., Yang, F., Fan, Y., Yang, Y., Zhu, H. and Wang, F. (2023) CREB1 is involved in miR-134-5p-mediated endometrial stromal cell proliferation, apoptosis, and autophagy. Cells, 12, 2554.CrossRefGoogle ScholarPubMed
Liang, J., Cao, D., Zhang, X., Liu, L., Tan, Q., Shi, S., Chen, K., Liang, J. and Wang, Z. (2020) miR-192-5p suppresses uterine receptivity formation through impeding epithelial transformation during embryo implantation. Theriogenology, 157, 360371.CrossRefGoogle ScholarPubMed
Liang, J., Li, K., Chen, K., Liang, J., Qin, T., He, J., Shi, S., Tan, Q. and Wang, Z. (2021) Regulation of ARHGAP19 in the endometrial epithelium: a possible role in the establishment of uterine receptivity. Reproductive Biology and Endocrinology, 19, 2.CrossRefGoogle Scholar
Liang, J., Wang, S. and Wang, Z. (2017) Role of microRNAs in embryo implantation. Reproductive Biology and Endocrinology, 15, 90.CrossRefGoogle ScholarPubMed
Liang, L., Yang, Y., Yang, L., Zhang, X., Xu, S., Liu, Y., Wu, X. and Chao, L. (2023) HIF-1alpha is positively associated with endometrial receptivity by regulating PKM2. Journal of Obstetrics and Gynaecology Research, 49, 27342745.CrossRefGoogle ScholarPubMed
Liang, Y. X., Liu, L., Jin, Z. Y., Liang, X. H., Fu, Y. S., Gu, X. W. and Yang, Z. M. (2018) The high concentration of progesterone is harmful for endometrial receptivity and decidualization. Scientific Reports, 8, 712.CrossRefGoogle ScholarPubMed
Liang, Y., Shuai, Q., Wang, Y., Jin, S., Feng, Z., Chen, B., Liang, T., Liu, Z., Zhao, H., Chen, Z., Wang, C. and Xie, J. (2021) 1-Nitropyrene exposure impairs embryo implantation through disrupting endometrial receptivity genes expression and producing excessive ROS. Ecotoxicology and Environmental Safety, 227, 112939.CrossRefGoogle ScholarPubMed
Liu, D. X., Hao, S. L. and Yang, W. X. (2023) Crosstalk between beta-CATENIN-mediated cell adhesion and the WNT signaling pathway. DNA and Cell Biology, 42, 113.CrossRefGoogle ScholarPubMed
Liu, N., Zhou, C., Chen, Y. and Zhao, J. (2013) The involvement of osteopontin and beta3 integrin in implantation and endometrial receptivity in an early mouse pregnancy model. European Journal of Obstetrics & Gynecology and Reproductive Biology, 170, 171176.CrossRefGoogle Scholar
Liu, X., Zhang, L., Liu, Y., Cui, J., Che, S., An, X., Song, Y. and Cao, B. (2018) Circ-8073 regulates CEP55 by sponging miR-449a to promote caprine endometrial epithelial cells proliferation via the PI3K/AKT/mTOR pathway. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1865, 11301147.CrossRefGoogle ScholarPubMed
Liu, X., Zhang, L., Yang, L., Cui, J., Che, S., Liu, Y., Han, J., An, X., Cao, B. and Song, Y. (2020) miR-34a/c induce caprine endometrial epithelial cell apoptosis by regulating circ-8073/CEP55 via the RAS/RAF/MEK/ERK and PI3K/AKT/mTOR pathways. Journal of Cellular Physiology, 235, 1005110067.CrossRefGoogle ScholarPubMed
Luo, X., Yang, R., Bai, Y., Li, L., Lin, N., Sun, L., Liu, J. and Wu, Z. (2021) Binding of microRNA-135a (miR-135a) to homeobox protein A10 (HOXA10) mRNA in a high-progesterone environment modulates the embryonic implantation factors beta3-integrin (ITGbeta3) and empty spiracles homeobox-2 (EMX2). Annals of Translational Medicine, 9, 662.CrossRefGoogle Scholar
Lyu, S., Zhai, Y., Zhu, X., Shi, Q., Chen, F., Zhang, G., Zhang, Z. and Wang, E. (2023) Bta-miR-200b promotes endometrial epithelial cell apoptosis by targeting MYB in cattle. Theriogenology, 195, 7784.CrossRefGoogle ScholarPubMed
Ma, Q., Yu, J., Zhang, X., Wu, X. and Deng, G. (2023) Wnt/beta-catenin signaling pathway-a versatile player in apoptosis and autophagy. Biochimie, 211, 5767.CrossRefGoogle ScholarPubMed
Makrigiannakis, A., Makrygiannakis, F. and Vrekoussis, T. (2021) Approaches to improve endometrial receptivity in case of repeated implantation failures. Frontiers in Cell and Developmental Biology, 9, 613277.CrossRefGoogle ScholarPubMed
Michlewski, G. and Caceres, J. F. (2019) Post-transcriptional control of miRNA biogenesis. RNA, 25, 116.CrossRefGoogle ScholarPubMed
Naydenov, M., Nikolova, M., Apostolov, A., Glogovitis, I., Salumets, A., Baev, V. and Yahubyan, G. (2022) The dynamics of miR-449a/c expression during uterine cycles are associated with endometrial development. Biology, 12, 55.CrossRefGoogle ScholarPubMed
Neykova, K., Tosto, V., Giardina, I., Tsibizova, V. and Vakrilov, G. (2022) Endometrial receptivity and pregnancy outcome. The Journal of Maternal-Fetal & Neonatal Medicine, 35, 25912605.CrossRefGoogle ScholarPubMed
Niknafs, B., Shokrzadeh, N., Reza, A. M. and Bakhtiar, H. S. M. (2022) The effect of dexamethasone on uterine receptivity, mediated by the ERK1/2-mTOR pathway, and the implantation window: An experimental study. International Journal of Reproductive Biomedicine, 20, 4758.Google ScholarPubMed
Park, H. R., Choi, H. J., Kim, B. S., Chung, T. W., Kim, K. J., Joo, J. K., Ryu, D., Bae, S. J. and Ha, K. T. (2021) Paeoniflorin enhances endometrial receptivity through leukemia inhibitory factor. Biomolecules, 11, 439.CrossRefGoogle ScholarPubMed
Paule, S. G., Heng, S., Samarajeewa, N., Li, Y., Mansilla, M., Webb, A. I., Nebl, T., Young, S. L., Lessey, B. A., Hull, M. L., Scelwyn, M., Lim, R., Vollenhoven, B., Rombauts, L. J. and Nie, G. (2021). Podocalyxin is a key negative regulator of human endometrial epithelial receptivity for embryo implantation. Human Reproduction, 36, 13531366.CrossRefGoogle ScholarPubMed
Paulson, E. E. and Comizzoli, P. (2021) Endometrial receptivity and embryo implantation in carnivores-commonalities and differences with other mammalian species. Biology of Reproduction, 104, 771783.CrossRefGoogle ScholarPubMed
Pirtea, P., Cicinelli, E., De Nola, R., de Ziegler, D. and Ayoubi, J. M. (2021) Endometrial causes of recurrent pregnancy losses: Endometriosis, adenomyosis, and chronic endometritis. Fertility and Sterility, 115, 546560.CrossRefGoogle ScholarPubMed
Qi, Y., Wang, X., Hou, S., Wu, Z., Xu, X. and Pang, C. (2022) Intracavitary physiotherapy combined with acupuncture mediated AMPK/mTOR signalling to improve endometrial receptivity in patients with thin endometrium. European Journal of Obstetrics & Gynecology and Reproductive Biology, 277, 3241.CrossRefGoogle ScholarPubMed
Rehman, R., Jawed, S., Zaidi, S. F., Baig, M. and Ahmeds, K. (2015) Role of interleukin-l 3 in conception after intracytoplasmic sperm injection. Journal of the Pakistan Medical Association, 65, 4953.Google ScholarPubMed
Sanchez-Lopez, J. A., Caballero, I., Montazeri, M., Maslehat, N., Elliott, S., Fernandez-Gonzalez, R., Calle, A., Gutierrez-Adan, A. and Fazeli, A. (2014) Local activation of uterine Toll-like receptor 2 and 2/6 decreases embryo implantation and affects uterine receptivity in mice. Biology of Reproduction, 90, 87.CrossRefGoogle ScholarPubMed
Shan, L., Zhou, Y., Peng, S., Wang, X., Shan, Z. and Teng, W. (2019) Implantation failure in rats with subclinical hypothyroidism is associated with LIF/STAT3 signaling. Endocrine Connections, 8, 718727.CrossRefGoogle ScholarPubMed
Shariati, M., Niknafs, B., Seghinsara, A. M., Shokrzadeh, N. and Alivand, M. R. (2019) Administration of dexamethasone disrupts endometrial receptivity by alteration of expression of miRNA-223, 200a, LIF, Muc1, SGK1, and ENaC via the ERK1/2-mTOR pathway. Journal of Cellular Physiology, 234, 1962919639.CrossRefGoogle ScholarPubMed
Shekibi, M., Heng, S. and Nie, G. (2022) MicroRNAs in the regulation of endometrial receptivity for embryo implantation. International Journal of Molecular Sciences, 23, 6210.CrossRefGoogle ScholarPubMed
Shekibi, M., Heng, S., Wang, Y., Samarajeewa, N., Rombauts, L. and Nie, G. (2022) Progesterone suppresses podocalyxin partly by up-regulating miR-145 and miR-199 in human endometrial epithelial cells to enhance receptivity in in vitro models. Molecular Human Reproduction, 28, gaac034.CrossRefGoogle ScholarPubMed
Shen, M., Liu, Y., Ma, X. and Zhu, Q. (2023) Erbu Zhuyu decoction improves endometrial angiogenesis via uterine natural killer cells and the PI3K/Akt/eNOS pathway a mouse model of embryo implantation dysfunction. American Journal of Reproductive Immunology, 89, e13634.CrossRefGoogle ScholarPubMed
Shi, S., Tan, Q., Liang, J., Cao, D., Wang, S., Liang, J., Chen, K. and Wang, Z. (2021) Placental trophoblast cell-derived exosomal microRNA-1290 promotes the interaction between endometrium and embryo by targeting LHX6. Molecular Therapy-Nucleic Acids, 26, 760772.CrossRefGoogle ScholarPubMed
Shokrzadeh, N., Alivand, M. R., Abedelahi, A., Hessam, S. M. and Niknafs, B. (2018) Upregulation of HB-EGF, Msx.1, and miRNA Let-7a by administration of calcitonin through mTOR and ERK1/2 pathways during a window of implantation in mice. Molecular Reproduction and Development, 85, 790801.CrossRefGoogle ScholarPubMed
Shokrzadeh, N., Alivand, M. R., Abedelahi, A., Hessam, S. M. and Niknafs, B. (2019) Calcitonin administration improves endometrial receptivity via regulation of LIF, Muc-1 and microRNA Let-7a in mice. Journal of Cellular Physiology, 234, 1298913000.CrossRefGoogle ScholarPubMed
Smith, J., Zyoud, A. and Allegrucci, C. (2019) A case of identity: HOX genes in normal and cancer stem cells. Cancers, 11, 512.CrossRefGoogle ScholarPubMed
Soni, U. K., Chadchan, S. B., Gupta, R. K., Kumar, V. and Kumar, J. R. (2021) miRNA-149 targets PARP-2 in endometrial epithelial and stromal cells to regulate the trophoblast attachment process. Molecular Human Reproduction, 27, gaab039.CrossRefGoogle ScholarPubMed
Stavast, C. J. and Erkeland, S. J. (2019) The non-canonical aspects of microRNAs: many roads to gene regulation. Cells, 8, 1465.CrossRefGoogle ScholarPubMed
Steens, J. and Klein, D. (2022) HOX genes in stem cells: Maintaining cellular identity and regulation of differentiation. Frontiers in Cell and Developmental Biology, 10, 1002909.CrossRefGoogle ScholarPubMed
Sutaji, Z., Abu, M. A., Sayutti, N., Elias, M. H., Ahmad, M. F., Nur, A. A., Chew, K. T., Abdul, K. A., Aziz, N., Mokhtar, M. H., Zin, R. and Hussein, Z. (2023) Endometrial heparin-binding epidermal growth factor gene expression and hormone level changes in implantation window of obese women with polycystic ovarian syndrome. Biomedicines, 11, 276.CrossRefGoogle ScholarPubMed
Verma, R. K., Soni, U. K., Chadchan, S. B., Maurya, V. K., Soni, M., Sarkar, S., Pratap, J. V. and Jha, R. K. (2022) miR-149-PARP-2 signaling regulates E-cadherin and N-cadherin expression in the murine model of endometrium receptivity. Reproductive Sciences, 29, 975992.CrossRefGoogle ScholarPubMed
Wang, H., Shi, G., Li, M., Fan, H., Ma, H. and Sheng, L. (2018) Correlation of IL-1 and HB-EGF with endometrial receptivity. Experimental and Therapeutic Medicine, 16, 51305136.Google ScholarPubMed
Wang, J., Huang, C., Jiang, R., Du, Y, Zhou, J., Jiang, Y., Yan, Q., Xing, J., Hou, X., Zhou, J., Sun, H. and Yan, G. (2018) Decreased endometrial IL-10 impairs endometrial receptivity by downregulating HOXA10 expression in women with adenomyosis. BioMed Research International, 2018, 2549789.CrossRefGoogle ScholarPubMed
Wang, J., Xie, D., Liu, M., Gong, Y., Shi, X., Wei, J. Y. and Quan, S. (2016) Uterine macrophages affect embryo implantation via regulating vascular endothelial growth factor A in mice. Journal of Southern Medical University, 36, 909914.Google ScholarPubMed
Wang, L., Liu, D., Wei, J., Yuan, L., Zhao, S., Huang, Y., Ma, J. and Yang, Z. (2021) MiR-543 inhibits the migration and epithelial-to-mesenchymal transition of TGF-β-treated endometrial stromal cells via the MAPK and Wnt/β-catenin signaling pathways. Pathology and Oncology Research, 27, 1609761.CrossRefGoogle ScholarPubMed
Wang, W., Ge, L., Zhang, L. L., Wang, L. R., Lu, Y. Y., Gou, L., Gou, R. Q., Xu, T. Y., Ma, X. L. and Zhang, X. H. (2023) Mechanism of human chorionic gonadotropin in endometrial receptivity via the miR-126-3p/PI3K/Akt/eNOS axis. The Kaohsiung Journal of Medical Sciences, 39, 468477.CrossRefGoogle ScholarPubMed
Wei, P., Wang, H., Li, Y. and Guo, R. (2021) Nucleolar small molecule RNA SNORA75 promotes endometrial receptivity by regulating the function of miR-146a-3p and ZNF23. Aging, 13, 1492414939.CrossRefGoogle ScholarPubMed
Xing, L., Chen, Y., He, Z., He, M., Sun, Y., Xu, J., Wang, J., Zhuang, H., Ren, Z., Chen, Y., Yang, J., Cheng, S. and Zhao, R. (2022) Acupuncture improves endometrial angiogenesis by activating PI3K/AKT pathway in a rat model with PCOS. Evidence-Based Complementary and Alternative Medicine, 2022, 115.Google Scholar
Xu, B., Geerts, D., Bu, Z., Ai, J., Jin, L., Li, Y., Zhang, H. and Zhu, G. (2014) Regulation of endometrial receptivity by the highly expressed HOXA9, HOXA11 and HOXD10 HOX-class homeobox genes. Human Reproduction, 29, 781790.CrossRefGoogle ScholarPubMed
Yang, C. (2021) The Study on miR-20b Targeting NCOA3 to Regulate Progesterone-Induced Immune Response in Bovine Endometrium. Master’s thesis. Huazhong Agricultural University (In Chinese).Google Scholar
Yang, D., Liu, A., Wu, Y., Li, B., Nan, S., Yin, R., Zhu, H., Chen, J., Ding, Y. and Ding, M. (2020) BCL2L15 depletion inhibits endometrial receptivity via the STAT1 signaling pathway. Genes, 11, 816.CrossRefGoogle ScholarPubMed
Yang, P., Wu, Z., Ma, C., Pan, N., Wang, Y. and Yan, L. (2019) Endometrial miR-543 is downregulated during the implantation window in women with endometriosis-related infertility. Reproductive Sciences, 26, 900908.CrossRefGoogle ScholarPubMed
Yang, Y., Sun, Y., Cheng, L., Li, A., Shen, Y., Jiang, L., Deng, X. and Chao, L. (2017) GRIM-19, a gene associated with retinoid-interferon-induced mortality, affects endometrial receptivity and embryo implantation. Reproduction, Fertility and Development, 29, 14471455.CrossRefGoogle ScholarPubMed
Yao, K., Kang, Q., Chen, K., Shi, B. and Jin, X. (2024) MiR-124-3p negatively impacts embryo implantation via suppressing uterine receptivity formation and embryo development. Reproductive Biology and Endocrinology, 22, 16.CrossRefGoogle ScholarPubMed
You, F., Du, X, Zhang, T., Wang, Y., Lv, Y. and Zeng, L. (2021) High-frequency electroacupuncture improves endometrial receptivity via regulating cell adhesion molecules and leukemia inhibitory factor/signal transducer and activator of transcription signaling pathway. Bioengineered, 12, 1047010479.CrossRefGoogle ScholarPubMed
You, F., Du, X, Zhang, T., Wang, Y., Lv, Y. and Zeng, L. (2022a) TJZYF improves endometrial receptivity through regulating VEGF and PI3K/AKT signaling pathway. BioMed Research International, 2022, 9212561.CrossRefGoogle ScholarPubMed
You, F., Du, X, Zhang, T., Wang, Y., Lv, Y. and Zeng, L. (2022b) Electroacupuncture improves endometrial receptivity through miRNA-223-3p-mediated regulation of leukemia inhibitory factor/signal transducer and activator of transcription 3 signaling pathway. Bioengineered, 13, 1029810312.CrossRefGoogle ScholarPubMed
Yu, S. L., Jeong, D. U., Noh, E. J., Jeon, H. J., Lee, D. C., Kang, M., Kim, T. H., Lee, S. K., Han, A. R., Kang, J. and Park, S. R. (2023) Exosomal miR-205-5p improves endometrial receptivity by upregulating E-cadherin expression through ZEB1 inhibition. International Journal of Molecular Sciences, 24, 15149.CrossRefGoogle ScholarPubMed
Yu, S., Kang, Y., Jeong, D., Lee, D. C., Jeon, H. J., Kim, T., Lee, S. K., Han, A. R., Kang, J. and Park, S. (2022) The miR-182-5p/NDRG1 axis controls endometrial receptivity through the NF-κB/ZEB1/E-cadherin pathway. International Journal of Molecular Sciences, 23, 12303.CrossRefGoogle Scholar
Yu, Y., Cao, Y., Huang, W., Liu, Y., Lu, Y. and Zhao, J. (2021) β-Sitosterol ameliorates endometrium receptivity in PCOS-like mice: The mediation of gut microbiota. Frontiers in Nutrition, 8, 667130.CrossRefGoogle ScholarPubMed
Yuan, L., Feng, F., Mao, Z., Huang, J. Z., Liu, Y., Li, Y. L. and Jiang, R. X. (2021) Regulation mechanism of miR-494-3p on endometrial receptivity in mice via PI3K/AKT/mTOR pathway. General Physiology & Biophysics, 40, 351363.CrossRefGoogle ScholarPubMed
Zarei, R., Nikpour, P., Rashidi, B., Eskandari, N. and Aboutorabi, R. (2019) Evaluation of diabetes effects on the expression of leukemia inhibitory factor and vascular endothelial growth factor A genes and proteins at the time of endometrial receptivity after superovulation in rat model. Advanced Biomedical Research, 8, 66.Google ScholarPubMed
Zarrin, Y., Bakhteyari, A., Nikpour, P., Mostafavi, F. S., Eskandari, N., Matinfar, M. and Aboutorabi, R. (2020) A study on the presence of osteopontin and alpha3beta1 integrin in the endometrium of diabetic rats at the time of embryo implantation. Journal of Reproduction & Infertility, 21, 8793.Google Scholar
Zhang, L., Liu, X. R., Liu, J. Z., Song, Y. X., Zhou, Z. Q. and Cao, B. Y. (2017) miR-182 selectively targets HOXA10 in goat endometrial epithelium cells in vitro. Reproduction in Domestic Animals, 52, 10811092.CrossRefGoogle ScholarPubMed
Zhang, L., Liu, X., Cui, J., Che, S., Liu, Y., An, X., Cao, B. and Song, Y. (2019) LncRNA882 regulates leukemia inhibitory factor (LIF) by sponging miR-15b in the endometrial epithelium cells of dairy goat. Journal of Cellular Physiology, 234, 47544767.CrossRefGoogle ScholarPubMed
Zhang, L., Liu, X., Liu, J., Ma, X., Zhou, Z., Song, Y. and Cao, B. (2018) miR-26a promoted endometrial epithelium cells (EECs) proliferation and induced stromal cells (ESCs) apoptosis via the PTEN-PI3K/AKT pathway in dairy goats. Journal of Cellular Physiology, 233, 46884706.CrossRefGoogle ScholarPubMed
Zhang, L., Liu, X., Liu, J., Zhou, Z., Song, Y., Cao, B. and An, X. (2017) miR-182 aids in receptive endometrium development in dairy goats by down-regulating PTN expression. Plos One, 12, e179783.Google ScholarPubMed
Zhang, Y. M., Zhang, Y. Y., Bulbul, A., Shan, X., Wang, X. Q. and Yan, Q. (2015) Baicalin promotes embryo adhesion and implantation by upregulating fucosyltransferase IV (FUT4) via Wnt/beta-catenin signaling pathway. FEBS Letters, 589, 12251233.CrossRefGoogle ScholarPubMed
Zhang, Z., Li, T., Xu, L., Wang, Q., Li, H. and Wang, X. (2021) Extracellular superoxide produced by Enterococcus faecalis reduces endometrial receptivity via inflammatory injury. American Journal of Reproductive Immunology, 86, e13453.CrossRefGoogle ScholarPubMed
Zhao, D. M., Shan, Y. H., Li, F. H., Jiang, L. and Qu, Q. L. (2019) Correlation between endometrial receptivity with expressions of IL-1 and VEGF in rats with polycystic ovary syndrome. European Review for Medical & Pharmacological Sciences, 23, 55755580.Google ScholarPubMed
Zheng, P., Qin, X., Feng, R., Li, Q., Huang, F., Li, Y., Zhao, Q. and Huang, H. (2022) Alleviative effect of melatonin on the decrease of uterine receptivity caused by blood ammonia through ROS/NF-kappaB pathway in dairy cow. Ecotoxicology and Environmental Safety, 231, 113166.CrossRefGoogle ScholarPubMed
Zheng, Q., Zhang, D., Yang, Y. U., Cui, X., Sun, J., Liang, C., Qin, H., Yang, X., Liu, S. and Yan, Q. (2017) MicroRNA-200c impairs uterine receptivity formation by targeting FUT4 and alpha1,3-fucosylation. Cell Death & Differentiation, 24, 21612172.CrossRefGoogle ScholarPubMed