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CsA promotes trophoblast invasion accompanied by changes in leukaemic inhibitory factor and fibroblast growth factor in peri-implantation blastocysts

Published online by Cambridge University Press:  21 December 2023

Dan Li Open the ORCID record for Dan Li [Opens in a new window] ,
Qiuling Jie ,
Qi Li ,
Ping Long ,
Zhen Wang ,
Jiaxing Wang ,
Shengnan Tian ,
Menglan Wu ,
Yanlin Ma  and
Yuanhua Huang
Dan Li
Affiliation:
Hainan Provincial Key Laboratory for Human Reproductive Medicine and Genetic Research, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China Hainan Medical University, China Department of Reproductive Medicine, Haikou Women & Children Hospital, China
Qiuling Jie
Affiliation:
Hainan Provincial Key Laboratory for Human Reproductive Medicine and Genetic Research, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China Hainan Medical University, China Hainan Provincial Clinical Research Center for Thalassemia, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China Department of Reproductive Medicine, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China Haikou Key Laboratory for Preservation of Human Genetic Resource, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China
Qi Li
Affiliation:
Hainan Provincial Key Laboratory for Human Reproductive Medicine and Genetic Research, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China Hainan Provincial Clinical Research Center for Thalassemia, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China Department of Reproductive Medicine, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China Haikou Key Laboratory for Preservation of Human Genetic Resource, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China
Ping Long
Affiliation:
Guizhou Qiannan People’s Hospital, China
Zhen Wang
Affiliation:
Hainan Provincial Key Laboratory for Human Reproductive Medicine and Genetic Research, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China Department of Reproductive Medicine, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China Haikou Key Laboratory for Preservation of Human Genetic Resource, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China
Jiaxing Wang
Affiliation:
Hainan Medical University, China
Shengnan Tian
Affiliation:
Hainan Medical University, China
Menglan Wu
Affiliation:
Department of Reproductive Medicine, The First Affiliated Hospital of Zhengzhou University, China
Yanlin Ma
Affiliation:
Hainan Provincial Key Laboratory for Human Reproductive Medicine and Genetic Research, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China Hainan Medical University, China Hainan Provincial Clinical Research Center for Thalassemia, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China Department of Reproductive Medicine, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China Haikou Key Laboratory for Preservation of Human Genetic Resource, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China
Yuanhua Huang*
Affiliation:
Hainan Provincial Key Laboratory for Human Reproductive Medicine and Genetic Research, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China Hainan Medical University, China Hainan Provincial Clinical Research Center for Thalassemia, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China Department of Reproductive Medicine, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China Haikou Key Laboratory for Preservation of Human Genetic Resource, The First Affiliated Hospital of Hainan Medical University, Hainan Medical University, China
*
Corresponding author: Yuanhua Huang; Email: 13036095796@163.com
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Summary

During the early stages of human pregnancy, successful implantation of embryonic trophoblast cells into the endometrium depends on good communication between trophoblast cells and the endometrium. Abnormal trophoblast cell function can cause embryo implantation failure. In this study, we added cyclosporine A (CsA) to the culture medium to observe the effect of CsA on embryonic trophoblast cells and the related mechanism. We observed that CsA promoted the migration and invasion of embryonic trophoblast cells. CsA promoted the expression of leukaemic inhibitory factor (LIF) and fibroblast growth factor (FGF). In addition, CsA promoted the secretion and volume increase in vesicles in the CsA-treated group compared with the control group. Therefore, CsA may promote the adhesion and invasion of trophoblast cells through LIF and FGF and promote the vesicle dynamic process, which is conducive to embryo implantation.

Keywords

Cyclosporine AFibroblast growth factorInvasionLeukaemic inhibitory factorTrophoblast

Information

Type
Research Article
Information
Zygote , Volume 32 , Issue 1 , February 2024 , pp. 71 - 76
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Copyright
© The Author(s), 2023. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally.

References

Alzahrani, F. A. (2019). Synergistic effect of basic fibroblast growth factor (bFGF) and epidermal growth factor on derivation of camel (Camelus dromedarius) trophoblast stem cells. Zygote, 27(4), 255–258. doi: 10.1017/S0967199419000169 CrossRefGoogle ScholarPubMed
Bonometti, S., Menarim, B. C., Reinholt, B. M., Ealy, A. D. and Johnson, S. E. (2019). Growth factor modulation of equine trophoblast mitosis and prostaglandin gene expression. Journal of Animal Science, 97(2), 865–873. doi: 10.1093/jas/sky473 CrossRefGoogle ScholarPubMed
Carvajal, L., Gutiérrez, J., Morselli, E. and Leiva, A. (2021). Autophagy process in trophoblast cells invasion and differentiation: Similitude and differences with cancer cells. Frontiers in Oncology, 11, 637594. doi: 10.3389/fonc.2021.637594 CrossRefGoogle ScholarPubMed
Desrochers, L. M., Bordeleau, F., Reinhart-King, C. A., Cerione, R. A. and Antonyak, M. A. (2016). Microvesicles provide a mechanism for intercellular communication by embryonic stem cells during embryo implantation. Nature Communications, 7, 11958. doi: 10.1038/ncomms11958 CrossRefGoogle ScholarPubMed
Devi, H. L., Kumar, S., Konyak, Y. Y., Bharati, J., Bhimte, A., Pandey, Y., Kumar, K., Paul, A., Kala, A., Samad, H. A., Verma, M. R., Singh, G., Bag, S., Sarkar, M. and Chouhan, V. S. (2020). Expression and functional role of fibroblast growth factors (FGF) in placenta during different stages of pregnancy in water buffalo (Bubalus bubalis). Theriogenology, 143, 98–112. doi: 10.1016/j.theriogenology.2019.11.034 CrossRefGoogle ScholarPubMed
Fukui, Y., Hirota, Y., Matsuo, M., Gebril, M., Akaeda, S., Hiraoka, T. and Osuga, Y. (2019). Uterine receptivity, embryo attachment, and embryo invasion: Multistep processes in embryo implantation. Reproductive Medicine and Biology, 18(3), 234–240. doi: 10.1002/rmb2.12280 CrossRefGoogle ScholarPubMed
Hamelin-Morrissette, J., Dallagi, A., Girouard, J., Ravelojaona, M., Oufqir, Y., Vaillancourt, C., Van Themsche, C., Carrier, C. and Reyes-Moreno, C. (2020). Leukemia inhibitory factor regulates the activation of inflammatory signals in macrophages and trophoblast cells. Molecular Immunology, 120, 32–42. doi: 10.1016/j.molimm.2020.01.021 CrossRefGoogle ScholarPubMed
He, B., Li, Q. Y., Wu, Y. Y., Ruan, J. L., Teng, X. M., Li, D. J. and Tang, C. L. (2020). Cyclosporin A protects JEG-3 cells against oxidative stress-induced apoptosis by inhibiting the p53 and JNK/p38 signaling pathways. Reproductive Biology and Endocrinology: RB&E, 18(1), 100. doi: 10.1186/s12958-020-00658-0 CrossRefGoogle ScholarPubMed
Huang, Y. H., Ma, Y. L., Ma, L., Mao, J. L., Zhang, Y., Du, M. R. and Li, D. J. (2014). Cyclosporine A improves adhesion and invasion of mouse preimplantation embryos via upregulating integrin β3 and matrix metalloproteinase-9. International Journal of Clinical and Experimental Pathology, 7(4), 1379–1388.Google ScholarPubMed
Huang, W., Lu, W., Li, Q., Zhang, Y., Xie, B., Luo, S., Wei, Y., Ma, Y. and Huang, Y. (2020). Effects of cyclosporine A on proliferation, invasion and migration of HTR-8/SVneo human extravillous trophoblasts. Biochemical and Biophysical Research Communications, 533(4), 645–650. doi: 10.1016/j.bbrc.2020.09.072 CrossRefGoogle ScholarPubMed
Isaac, E. and Pfeffer, P. L. (2021). Growing cattle embryos beyond Day 8 – An investigation of media components. Theriogenology, 161, 273–284. doi: 10.1016/j.theriogenology.2020.12.010 CrossRefGoogle ScholarPubMed
Johnson, M. H. (2019). A short history of in vitro fertilization (IVF). International Journal of Developmental Biology, 63(3–4), 83–92. doi: 10.1387/ijdb.180364mj CrossRefGoogle Scholar
Kshitiz, Afzal, J., Maziarz, J. D., Hamidzadeh, A., Liang, C., Erkenbrack, E. M., Kim, H. N., Haeger, J. D., Pfarrer, C., Hoang, T., Ott, T., Spencer, T., Pavličev, M., Antczak, D. F., Levchenko, A. and Wagner, G. P. (2019). Evolution of placental invasion and cancer metastasis are causally linked. Nature Ecology & Evolution, 3, 1743–1753. doi: 10.1038/s41559-019-1046-4 CrossRefGoogle Scholar
Ling, Y., Huang, Y., Chen, C., Mao, J. and Zhang, H. (2017). Low dose cyclosporin A treatment increases live birth rate of unexplained recurrent abortion – Initial cohort study. Clinical and Experimental Obstetrics and Gynecology, 44(2), 230–235. doi: 10.12891/ceog3375.2017 CrossRefGoogle ScholarPubMed
Massimiani, M., Lacconi, V., La Civita, F., Ticconi, C., Rago, R. and Campagnolo, L. (2019). Molecular signaling regulating endometrium-blastocyst crosstalk. International Journal of Molecular Sciences, 21(1). doi: 10.3390/ijms21010023 CrossRefGoogle ScholarPubMed
Menkhorst, E., Winship, A., Van Sinderen, M. and Dimitriadis, E. (2016). Human extravillous trophoblast invasion: Intrinsic and extrinsic regulation. Reproduction, Fertility, and Development, 28(4), 406–415. doi: 10.1071/RD14208 CrossRefGoogle ScholarPubMed
Mishra, A., Ashary, N., Sharma, R. and Modi, D. (2021). Extracellular vesicles in embryo implantation and disorders of the endometrium. American Journal of Reproductive Immunology, 85(2), e13360. doi: 10.1111/aji.13360 CrossRefGoogle ScholarPubMed
Molè, M. A., Coorens, T. H. H., Shahbazi, M. N., Weberling, A., Weatherbee, B. A. T., Gantner, C. W., Sancho-Serra, C., Richardson, L., Drinkwater, A., Syed, N., Engley, S., Snell, P., Christie, L., Elder, K., Campbell, A., Fishel, S., Behjati, S., Vento-Tormo, R. and Zernicka-Goetz, M. (2021). A single cell characterisation of human embryogenesis identifies pluripotency transitions and putative anterior hypoblast centre. Nature Communications, 12(1), 3679. doi: 10.1038/s41467-021-23758-w CrossRefGoogle ScholarPubMed
Mor, A., Mondal, S., Reddy, I. J., Nandi, S. and Gupta, P. (2018). Molecular cloning and expression of FGF2 gene in pre-implantation developmental stages of in vitro-produced sheep embryos. Reproduction in Domestic Animals = Zuchthygiene, 53(4), 895–903. doi: 10.1111/rda.13182 CrossRefGoogle ScholarPubMed
Moser, G. and Huppertz, B. (2017). Implantation and extravillous trophoblast invasion: From rare archival specimens to modern biobanking. Placenta, 56, 19–26. doi: 10.1016/j.placenta.2017.02.007 CrossRefGoogle ScholarPubMed
Pantos, K., Grigoriadis, S., Maziotis, E., Pistola, K., Xystra, P., Pantou, A., Kokkali, G., Pappas, A., Lambropoulou, M., Sfakianoudis, K. and Simopoulou, M. (2022). The role of interleukins in recurrent implantation failure: A comprehensive review of the literature. International Journal of Molecular Sciences, 23(4). doi: 10.3390/ijms23042198 CrossRefGoogle ScholarPubMed
Park, J. Y., Mani, S., Clair, G., Olson, H. M., Paurus, V. L., Ansong, C. K., Blundell, C., Young, R., Kanter, J., Gordon, S., Yi, A. Y., Mainigi, M. and Huh, D. D. (2022). A microphysiological model of human trophoblast invasion during implantation. Nature Communications, 13(1), 1252. doi: 10.1038/s41467-022-28663-4 CrossRefGoogle ScholarPubMed
Rooney, K. L. and Domar, A. D. (2018). The relationship between stress and infertility. Dialogues in Clinical Neuroscience, 20(1), 41–47. doi: 10.31887/DCNS.2018.20.1/klrooney CrossRefGoogle ScholarPubMed
Serrano Albal, M., Silvestri, G., Kiazim, L. G., Vining, L. M., Zak, L. J., Walling, G. A., Haigh, A. M., Harvey, S. C., Harvey, K. E. and Griffin, D. K. (2022). Supplementation of porcine in vitro maturation medium with FGF2, LIF, and IGF1 enhances cytoplasmic maturation in prepubertal gilts oocytes and improves embryo quality. Zygote, 30(6), 801–808. doi: 10.1017/S0967199422000284 CrossRefGoogle ScholarPubMed
Smith, A. G., Heath, J. K., Donaldson, D. D., Wong, G. G., Moreau, J., Stahl, M. and Rogers, D. (1988). Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature, 336(6200), 688–690. doi: 10.1038/336688a0 CrossRefGoogle ScholarPubMed
Tani, K., Mitsui, T., Mishima, S., Ohira, A., Maki, J., Eto, E., Hayata, K., Nakamura, K. and Masuyama, H. (2021). EG-VEGF induces invasion of a human trophoblast cell line via PROKR2. Acta Medica Okayama, 75(6), 677–684. doi: 10.18926/AMO/62806 Google ScholarPubMed
Wang, J., Mayernik, L. and Armant, D. R. (2002). Integrin signaling regulates blastocyst adhesion to fibronectin at implantation: Intracellular calcium transients and vesicle trafficking in primary trophoblast cells. Developmental Biology, 245(2), 270–279. doi: 10.1006/dbio.2002.0644 CrossRefGoogle ScholarPubMed
Wang, N., Ge, H. and Zhou, S. (2021). Cyclosporine A to treat unexplained recurrent spontaneous abortions: A prospective, randomized, double-blind, placebo-controlled, single-center trial. International Journal of Women’s Health, 13, 1243–1250. doi: 10.2147/IJWH.S330921 CrossRefGoogle ScholarPubMed
Wang, J., Long, P., Tian, S., Zu, W., Liu, J., Wu, B., Mao, J., Li, D., Ma, Y. and Huang, Y. (2023). Cyclosporin A promotes invasion and migration of extravillous trophoblast cells derived from human-induced pluripotent stem cells and human embryonic stem cells. Stem Cells and Development, 32(3–4), 60–74. doi: 10.1089/scd.2022.0144 CrossRefGoogle ScholarPubMed
Xiong, L., Ye, X., Chen, Z., Fu, H., Li, S., Xu, P., Yu, J., Wen, L., Gao, R., Fu, Y., Qi, H., Kilby, M. D., Saffery, R., Baker, P. N. and Tong, C. (2021). Advanced maternal age-associated SIRT1 deficiency compromises trophoblast epithelial-mesenchymal transition through an increase in vimentin acetylation. Aging Cell, 20(10), e13491. doi: 10.1111/acel.13491 CrossRefGoogle ScholarPubMed
Yamada, A., Ohtsuki, K., Shiga, N., Green, J. A., Matsuno, Y. and Imakawa, K. (2022). Epithelial-mesenchymal transition and bi- and multi-nucleated trophoblast cell formation in ovine conceptuses during the peri-implantation period. Journal of Reproduction and Development, 68(2), 110–117. doi: 10.1262/jrd.2021-088 CrossRefGoogle ScholarPubMed
Yu, M., Wang, J., Liu, S., Wang, X. and Yan, Q. (2017). Novel function of pregnancy-associated plasma protein A: Promotes endometrium receptivity by up-regulating N-fucosylation. Scientific Reports, 7(1), 5315. doi: 10.1038/s41598-017-04735-0 CrossRefGoogle ScholarPubMed