LncRNAs 60248.51 and 9826.1 are identified as potential regulators of endometrial receptivity in Tibetan Northwest Cashmere goats

Authors

DOI:

https://doi.org/10.5327/fst.132222

Keywords:

Tibetan Northwest cashmere goats, endometrial receptivity, lncRNA 60248.51 and lncRNA 9826.1, primary goat endometrial epithelial cells, the Wnt and Hippo signaling pathways

Abstract

Endometrial receptivity is a key determinant of embryo implantation, which is the initial step of a successful pregnancy. In this study, high-throughput RNA sequencing was conducted in pre-receptive endometrium (PE) and receptive endometrium (RE) derived from Tibetan Northwest Cashmere goats. There were only a handful of miRNAs and circRNAs differentially expressed between PE and RE tissues, while there were 250 upregulated coding genes and 193 upregulated lncRNAs and 135 downregulated coding genes and 123 downregulated lncRNAs in RE tissues, suggesting the predominant role of coding genes and lncRNAs in the regulation of endometrial receptivity. Moreover, gene ontology and Kyoto Encyclopedia of Genes and Genomes analyses revealed that differentially expressed lncRNAs are significantly enriched in Wnt, Hedgehog, and Hippo signaling pathways. Furthermore, the two most upregulated lncRNAs, MSTRG.60248.51 (1264 bp) and MSTRG.9826.1 (1362 bp), were screened as candidate lncRNAs, and both upregulation of 60248.51 and 9826.1 could activate Wnt and Hippo signaling and promote cell viability, migration, and secretion of endothelin-1, epidermal growth factor, and colony stimulating factor in primary goat endometrial epithelial cells. In summary, lncRNAs 60248.51 and 9826.1, identified as potential regulators of endometrial receptivity in Tibetan Northwest Cashmere goats, improve cell viability, migration, and secretion functions in endometrial epithelial cells, which may be associated with the Wnt and Hippo signaling pathways.

Keywords: Tibetan Northwest cashmere goats; endometrial receptivity; lncRNA 60248.51 and lncRNA 9826.1; primary goat endometrial epithelial cells; the Wnt and Hippo signaling pathways.

Downloads

Download data is not yet available.

References

Aljubran, F., & Nothnick, W. B. (2021). Long non-coding RNAs in endometrial physiology and pathophysiology. Molecular and Cellular Endocrinology, 525, 111190. https://doi.org/10.1016/j.mce.2021.111190

Altmäe, S., Martinez-Conejero, J. A., Esteban, F. J., Ruiz-Alonso, M., Stavreus-Evers, A., Horcajadas, J. A., & Salumets, A. (2013). MicroRNAs miR-30b, miR-30d, and miR-494 regulate human endometrial receptivity. Reproductive Sciences, 20(3), 308-317. https://doi.org/10.1177/1933719112453507

Ashary, N., Tiwari, A., & Modi, D. (2018). Embryo Implantation: War in Times of Love. Endocrinology, 159(2), 1188-1198. https://doi.org/10.1210/en.2017-03082

Bouckenheimer, J., Assou, S., Riquier, S., Hou, C., Philippe, N., Sansac, C., Lavabre-Bertrand, T., Commes, T., Lemaitre, J.-M., Boureux, A., & De Vos, J. (2016). Long non-coding RNAs in human early embryonic development and their potential in ART. Human Reproduction Update, 23(1), 19-40. https://doi.org/10.1093/humupd/dmw035

Critchley, H. O. D., Maybin, J. A., Armstrong, G. M., & Williams, A. R. W. (2020). Physiology of the Endometrium and Regulation of Menstruation. Physiological Reviews, 100(3), 1149-1179. https://doi.org/10.1152/physrev.00031.2019

Cui, J., Liu, X., Yang, L., Che, S., Guo, H., Han, J., Zhu, Z., Cao, B., An, X., Zhang, L., & Song, Y. (2020). MiR-184 Combined with STC2 Promotes Endometrial Epithelial Cell Apoptosis in Dairy Goats via RAS/RAF/MEK/ERK Pathway. Genes (Basel), 11(9), 1052. https://doi.org/10.3390/genes11091052

Duan, C., Zhang, L., Gao, K., Guo, Y., Liu, Y., & Zhang, Y. (2022). Cashmere production, skin characteristics, and mutated genes in crimped cashmere fibre goats. Animal, 16(7), 100565. https://doi.org/10.1016/j.animal.2022.100565

He, M., Li, L., Wei, X., Geng, D., Jiang, H., Xiangxiang, G., Zhang, Y., & Du, H. (2022). Xiaoyao powder improves endometrial receptivity via VEGFR-2-mediated angiogenesis through the activation of the JNK and P38 signaling pathways. Journal of Ethnopharmacology, 282, 114580. https://doi.org/10.1016/j.jep.2021.114580

Heng, S., Samarajeewa, N., Wang, Y., Paule, S. G., Breen, J., & Nie, G. (2021). Podocalyxin promotes an impermeable epithelium and inhibits pro-implantation factors to negatively regulate endometrial receptivity. Scientific Reports, 11(1), 24016. https://doi.org/10.1038/s41598-021-03425-2

Huang, K., Chen, G., Fan, W., & Hu, L. (2020). miR-23a-3p increases endometrial receptivity via CUL3 during embryo implantation. Journal of Molecular Endocrinology, 65(2), 35-44. https://doi.org/10.1530/jme-20-0053

Jin, M., Lu, J., Fei, X., Lu, Z., Quan, K., Liu, Y., Chu, M., Di, R., Wang, H., & Wei, C. (2020). Genetic Signatures of Selection for Cashmere Traits in Chinese Goats. Animals (Basel), 10(10), 1905. https://doi.org/10.3390/ani10101905

Lessey, B. A., & Young, S. L. (2019). What exactly is endometrial receptivity? Fertility and Sterility, 111(4), 611-617. https://doi.org/10.1016/j.fertnstert.2019.02.009

Li, C., Wu, Y., Chen, B., Cai, Y., Guo, J., Leonard, A. S., Kalds, P., Zhou, S., Zhang, J., Zhou, P., Gan, S., Jia, T., Pu, T., Suo, L., Li, Y., Zhang, K., Li, L., Purevdorj, M., Wang, X., Li, M., Wang, Y., Liu, Y., Huang, S., Sonstegard, T., Wang, M.-S., Kemp, S., Pausch, H., Chen, Y., Han, J.-L., Jiang, Y., & Wang, X. (2022). Markhor-derived Introgression of a Genomic Region Encompassing PAPSS2 Confers High-altitude Adaptability in Tibetan Goats. Molecular Biology and Evolution, 39(12), msac253. https://doi.org/10.1093/molbev/msac253

Li, L., Jiang, H., Wei, X., Geng, D., He, M., & Du, H. (2019). Bu Shen Zhu Yun Decoction Improves Endometrial Receptivity via VEGFR-2-Mediated Angiogenesis. Evidence-Based Complementary and Alternative Medicine, 2019, 3949824. https://doi.org/10.1155/2019/3949824

Lin, J., Ma, H., Li, H., Han, J., Guo, T., Qin, Z., Jia, L., & Zhang, Y. (2022). The Treatment of Complementary and Alternative Medicine on Female Infertility Caused by Endometrial Factors. Evidence-Based Complementary and Alternative Medicine, 2022, 4624311. https://doi.org/10.1155/2022/4624311

Liu, H., Wang, C., Li, Z., Shang, C., Zhang, X., Zhang, R., Wang, A., Jin, Y., & Lin, P. (2021). Transcriptomic Analysis of STAT1/3 in the Goat Endometrium During Embryo Implantation. Frontiers in Veterinary Science, 8, 757759. https://doi.org/10.3389/fvets.2021.757759

Liu, X., Zhang, L., Yang, L., Cui, J., Che, S., Liu, Y., Han, J., An, X., Cao, B., & 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(12), 10051-10067. https://doi.org/10.1002/jcp.29821

Nishino, D., Kotake, A., Yun, C. S., Rahman, A. M. I., El-Sharawy, M., Yamanaka, K. I., Khandoker, M. A. M. Y., & Yamauchi, N. (2021). Gene expression of bovine endometrial epithelial cells cultured in matrigel. Cell and Tissue Research, 385(1), 265-275. https://doi.org/10.1007/s00441-021-03418-7

Oghbaei, F., Zarezadeh, R., Jafari-Gharabaghlou, D., Ranjbar, M., Nouri, M., Fattahi, A., & Imakawa, K. (2022). Epithelial-mesenchymal transition process during embryo implantation. Cell and Tissue Research, 388(1), 1-17. https://doi.org/10.1007/s00441-021-03574-w

Okada, C. T. C., Kaps, M., Reichart, U., Walter, I., Gautier, C., Aurich, J., & Aurich, C. (2022). Low plasma progesterone concentration during the early luteal phase delays endometrial development and the beginning of placentation in mares. Animal Reproductive Science, 247, 107149. https://doi.org/10.1016/j.anireprosci.2022.107149

Shen, H. H., Zhang, T., Yang, H. L., Lai, Z. Z., Zhou, W. J., Mei, J., Shi, J.-W., Zhu, R., Xu, F.-Y., Li, D.-J., Ye, J.-F., Li, M.-Q. (2021). Ovarian hormones-autophagy-immunity axis in menstruation and endometriosis. Theranostics, 11(7), 3512-3526. https://doi.org/10.7150/thno.55241

Song, Y., Han, J., Cao, F., Ma, H., Cao, B., & An, X. (2019). Endometrial genome-wide DNA methylation patterns of Guanzhong dairy goats at days 5 and 15 of the gestation period. Animal Reproductive Science, 208, 106124. https://doi.org/10.1016/j.anireprosci.2019.106124

Tepekoy, F., Akkoyunlu, G., & Demir, R. (2015). The role of Wnt signaling members in the uterus and embryo during pre-implantation and implantation. Journal of Assisted Reproductive and Genetics, 32(3), 337-346. https://doi.org/10.1007/s10815-014-0409-7

Yi, T., Liu, M., Li, X., Liu, X., Ding, Y., He, J., Xu, H., Gao, R., Mu, X., Geng, Y., Wang, Y., & Chen, X. (2019). Benzo(a)pyrene inhibits endometrial cell apoptosis in early pregnant mice via the WNT5A pathway. Journal of Cellular Physiology, 234(7), 11119-11129. https://doi.org/10.1002/jcp.27762

Yue, C., Chen, A. C. H., Tian, S., Fong, S. W., Lee, K. C., Zhang, J., Ng, E. H., Y., Lee, K. F., & Lee, Y. L. (2020). Human embryonic stem cell-derived blastocyst-like spheroids resemble human trophectoderm during early implantation process. Fertility and Sterility, 114(3), 653-664.E6. https://doi.org/10.1016/j.fertnstert.2020.01.009

Zhang, L., An, X. P., Liu, X. R., Fu, M. Z., Han, P., Peng, J. Y., Hou, J.-X., Zhou, Z.-Q., Cao, B.-Y., & Song, Y. X. (2015). Characterization of the Transcriptional Complexity of the Receptive and Pre-receptive Endometria of Dairy Goats. Scientific Reports, 5, 14244. https://doi.org/10.1038/srep14244

Zhang, L., Liu, X., Cui, J., Che, S., Liu, Y., An, X., Cao, B., & 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(4), 4754-4767. https://doi.org/10.1002/jcp.27272

Zhang, L., Liu, X., Liu, J., Ma, X., Zhou, Z., Song, Y., & 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(6), 4688-4706. https://doi.org/10.1002/jcp.26252

Zhou, S., Huang, C., Wang, W., & Liu, J. (2021). MiR-370-3p inhibits the development of human endometriosis by downregulating EDN1 expression in endometrial stromal cells. Cellular Biology International, 45(6), 1183-1190. https://doi.org/10.1002/cbin.11552

Downloads

Published

2023-10-11

How to Cite

SUO, L., WEI, Y., WANG, B., DE, J., AWANG, C., RENQING, C., CUI, J., LIU, X., BA, G., & ZHANG, L. (2023). LncRNAs 60248.51 and 9826.1 are identified as potential regulators of endometrial receptivity in Tibetan Northwest Cashmere goats. Food Science and Technology, 43. https://doi.org/10.5327/fst.132222

Issue

Section

Original Articles