Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2021-0131
Animal Reproduction (AR)
ORIGINAL ARTICLE

Profiling and Functional Analysis of long non-coding RNAs in yak healthy and atretic follicles

Yilong Yao; Zhaoyi Meng; Wangchang Li; Yefen Xu; Yunlu Wang; Sizhu Suolang; Guangyin Xi; Lei Cao; Min Guo

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Abstract

Yak is the livestock on which people live in plateau areas, but its fecundity is low. Follicular development plays a decisive role in yak reproductive performance. As an important regulatory factor, the expression of long non-coding RNA (lncRNAs) in yak follicular development and its regulatory mechanism remains unclear. To explore the differentially expressed lncRNAs between healthy and atretic follicular in yaks. We used RNA-seq to construct lncRNA, miRNA, and mRNA expression profiles in yak atretic and healthy follicles, and the RNA sequence results were identified by qPCR. In addition, the correlation of lncRNA and targeted mRNA was also analyzed by Starbase software. Moreover, lncRNA/miRNA/mRNA networks were constructed by Cytoscape software, and the network was verified by dual-luciferase analysis. A total of 682 novel lncRNAs, 259 bta-miRNAs, and 1704 mRNAs were identified as differentially expressed between healthy and atretic follicles. Among them, 135 mRNAs were positively correlated with lncRNA expression and 97 were negatively correlated, which may be involved in the yak follicular development. In addition, pathway enrichment analysis of differentially expressed lncRNA host genes by Kyoto Genome Encyclopedia (KEGG) showed that host genes were mainly involved in hormone secretion, granulosa cell apoptosis, and follicular development. In conclusion, we identified a series of novel lncRNAs, constructed the lncRNA ceRNA regulatory network, and provided comprehensive resources for exploring the role of lncRNAs in yak ovarian follicular development.

Keywords

yak, RNA-seq, healthy follicles, atretic follicles, lncRNA

References

Brown JB, Boley N, Eisman R, May GE, Stoiber MH, Duff MO, Booth BW, Wen J, Park S, Suzuki AM, Wan KH, Yu C, Zhang D, Carlson JW, Cherbas L, Eads BD, Miller D, Mockaitis K, Roberts J, Davis CA, Frise E, Hammonds AS, Olson S, Shenker S, Sturgill D, Samsonova AA, Weiszmann R, Robinson G, Hernandez J, Andrews J, Bickel PJ, Carninci P, Cherbas P, Gingeras TR, Hoskins RA, Kaufman TC, Lai EC, Oliver B, Perrimon N, Graveley BR, Celniker SE. Diversity and dynamics of the Drosophila transcriptome. Nature. 2014;512(7515):393-9. http://dx.doi.org/10.1038/nature12962. PMid:24670639.

Caballero J, Gilbert I, Fournier E, Gagné D, Scantland S, Macaulay A, Robert C. Exploring the function of long non-coding RNA in the development of bovine early embryos. Reprod Fertil Dev. 2014;27(1):40-52. http://dx.doi.org/10.1071/RD14338. PMid:25472043.

Chen H, Palmer JS, Thiagarajan RD, Dinger ME, Lesieur E, Chiu H, Schulz A, Spiller C, Grimmond SM, Little MH, Koopman P, Wilhelm D. Identification of novel markers of mouse fetal ovary development. PLoS One. 2012;7(7):e41683. http://dx.doi.org/10.1371/journal.pone.0041683. PMid:22844512.

Chen X, Xie M, Liu D, Shi K. Downregulation of microRNA‑146a inhibits ovarian granulosa cell apoptosis by simultaneously targeting interleukin‑1 receptor‑associated kinase and tumor necrosis factor receptor‑associated factor 6. Mol Med Rep. 2015;12(4):5155-62. http://dx.doi.org/10.3892/mmr.2015.4036. PMid:26151128.

Chen Y, Zhang X, An Y, Liu B, Lu M. LncRNA HCP5 promotes cell proliferation and inhibits apoptosis via miR-27a-3p/IGF-1 axis in human granulosa-like tumor cell line KGN. Mol Cell Endocrinol. 2020;503:110697. http://dx.doi.org/10.1016/j.mce.2019.110697. PMid:31891769.

Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21(18):3674-6. http://dx.doi.org/10.1093/bioinformatics/bti610. PMid:16081474.

Dai X, Chen C, Xue J, Xiao T, Mostofa G, Wang D, Chen X, Xu H, Sun Q, Li J, Wei Y, Chen F, Quamruzzaman Q, Zhang A, Liu Q. Exosomal MALAT1 derived from hepatic cells is involved in the activation of hepatic stellate cells via miRNA-26b in fibrosis induced by arsenite. Toxicol Lett. 2019;316:73-84. http://dx.doi.org/10.1016/j.toxlet.2019.09.008. PMid:31513886.

Du X, Zhang L, Li X, Pan Z, Liu H, Li Q. TGF-β signaling controls FSHR signaling-reduced ovarian granulosa cell apoptosis through the SMAD4/miR-143 axis. Cell Death Dis. 2016;7(11):e2476. http://dx.doi.org/10.1038/cddis.2016.379. PMid:27882941.

Glick G, Hogeg M, Moallem U, Lavon Y, Wolfenson D. Follicular characteristics and luteal development after follicle-stimulating hormone induced multiple ovulations in heifers. J Anim Sci. 2013;91(1):188-94. http://dx.doi.org/10.2527/jas.2012-5536. PMid:23097398.

Hamazaki N, Uesaka M, Nakashima K, Agata K, Imamura T. Gene activation-associated long noncoding RNAs function in mouse preimplantation development. Development. 2015;142(5):910-20. http://dx.doi.org/10.1242/dev.116996. PMid:25633350.

Hu H, Jia Q, Xi J, Zhou B, Li Z. Integrated analysis of lncRNA, miRNA and mRNA reveals novel insights into the fertility regulation of large white sows. BMC Genomics. 2020;21(1):636. http://dx.doi.org/10.1186/s12864-020-07055-2. PMid:32928107.

Kaneko S, Son J, Shen SS, Reinberg D, Bonasio R. PRC2 binds active promoters and contacts nascent RNAs in embryonic stem cells. Nat Struct Mol Biol. 2013;20(11):1258-64. http://dx.doi.org/10.1038/nsmb.2700. PMid:24141703.

Kim SK, Nam JW, Rhee JK, Lee WJ, Zhang BT. miTarget: microRNA target gene prediction using a support vector machine. BMC Bioinformatics. 2006;7(1):411. http://dx.doi.org/10.1186/1471-2105-7-411. PMid:16978421.

Kong X, Duan Y, Sang Y, Li Y, Zhang H, Liang Y, Liu Y, Zhang N, Yang Q. LncRNA-CDC6 promotes breast cancer progression and function as ceRNA to target CDC6 by sponging MicroRNA-215. J Cell Physiol. 2019;234(6):9105-17. PMid:30362551.

La Y, Tang J, He X, Di R, Wang X, Liu Q, Zhang L, Zhang X, Zhang J, Hu W, Chu M. Identification and characterization of mRNAs and lncRNAs in the uterus of polytocous and monotocous Small Tail Han sheep (Ovis aries). PeerJ. 2019;7:e6938. http://dx.doi.org/10.7717/peerj.6938. PMid:31198626.

Li A, Zhang J, Zhou Z, Wang L, Sun X, Liu Y. Genome-scale identification of miRNA-mRNA and miRNA-lncRNA interactions in domestic animals. Anim Genet. 2015;46(6):716-9. http://dx.doi.org/10.1111/age.12329. PMid:26360131.

Li Q, Zhang S, Wang M, Dong S, Wang Y, Liu S, Lu T, Fu Y, Wang X, Chen G. Downregulated miR-21 mediates matrine-induced apoptosis via the PTEN/Akt signaling pathway in FTC-133 human follicular thyroid cancer cells. Oncol Lett. 2019;18(4):3553-60. http://dx.doi.org/10.3892/ol.2019.10693. PMid:31579406.

Ling Y, Zheng Q, Sui M, Zhu L, Xu L, Zhang Y, Liu Y, Fang F, Chu M, Ma Y, Zhang X. Comprehensive analysis of LncRNA reveals the temporal-specific module of goat skeletal muscle development. Int J Mol Sci. 2019;20(16):3950. http://dx.doi.org/10.3390/ijms20163950. PMid:31416143.

Liu J, Du X, Zhou J, Pan Z, Liu H, Li Q. MicroRNA-26b functions as a proapoptotic factor in porcine follicular Granulosa cells by targeting Sma-and Mad-related protein 4. Biol Reprod. 2014;91(6):146. http://dx.doi.org/10.1095/biolreprod.114.122788. PMid:25395673.

Luan X, Wang Y. LncRNA XLOC_006390 facilitates cervical cancer tumorigenesis and metastasis as a ceRNA against miR-331-3p and miR-338-3p. J Gynecol Oncol. 2018;29(6):e95. http://dx.doi.org/10.3802/jgo.2018.29.e95. PMID: 30207103.

Luo H, Xu C, Le W, Ge B, Wang T. lncRNA CASC11 promotes cancer cell proliferation in bladder cancer through miRNA-150. J Cell Biochem. 2019;120(8):13487-93. http://dx.doi.org/10.1002/jcb.28622.

Matsui M, Sonntag B, Hwang SS, Byerly T, Hourvitz A, Adashi EY, Shimasaki S, Erickson GF. Pregnancy-associated plasma protein-a production in rat granulosa cells: stimulation by follicle-stimulating hormone and inhibition by the oocyte-derived bone morphogenetic protein-15. Endocrinology. 2004;145(8):3686-95. http://dx.doi.org/10.1210/en.2003-1642. PMid:15087430.

Murdoch WJ, McCormick RJ. Enhanced degradation of collagen within apical vs. basal wall of ovulatory ovine follicle. Am J Physiol. 1992;263(2 Pt 1):E221-5. PMid:1325123.

Peng Y, Chang L, Wang Y, Wang R, Hu L, Zhao Z, Geng L, Liu Z, Gong Y, Li J, Li X, Zhang C. Genome-wide differential expression of long noncoding RNAs and mRNAs in ovarian follicles of two different chicken breeds. Genomics. 2019;111(6):1395-403. http://dx.doi.org/10.1016/j.ygeno.2018.09.012. PMid:30268779.

Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell. 2009;136(4):629-41. http://dx.doi.org/10.1016/j.cell.2009.02.006. PMid:19239885.

Song YX, Sun JX, Zhao JH, Yang YC, Shi JX, Wu ZH, Chen XW, Gao P, Miao ZF, Wang ZN. Non-coding RNAs participate in the regulatory network of CLDN4 via ceRNA mediated miRNA evasion. Nat Commun. 2017;8(1):289. http://dx.doi.org/10.1038/s41467-017-00304-1. PMid:28819095.

Sun B, Ma Y, Wang F, Hu L, Sun Y. miR-644-5p carried by bone mesenchymal stem cell-derived exosomes targets regulation of p53 to inhibit ovarian granulosa cell apoptosis. Stem Cell Res Ther. 2019;10(1):360. http://dx.doi.org/10.1186/s13287-019-1442-3. PMid:31783913.

Sun XF, Li YP, Pan B. Molecular regulation of miR-378 on the development of mouse follicle and the maturation of oocyte in vivo. Cell Cycle. 2018;17(18):2230-42. http://dx.doi.org/10.1080/15384101.2018.1520557. PMID: 30244637.

String. [database on the Internet]. 2021 [cited 2021 Dec 25]. Available from: https://cn.string-db.org/

Vasconcelos EJR, Mesel VC, daSilva LF, Pires DS, Lavezzo GM, Pereira ASA, Amaral MS, Verjovski-Almeida S. Atlas of Schistosoma mansoni long non-coding RNAs and their expression correlation to protein-coding genes. Database: The J Biol Databases Curation. 2018:1-5. http://dx.doi.org/10.1093/database/bay068.

Venø MT, Hansen TB, Venø ST, Clausen BH, Grebing M, Finsen B, Holm IE, Kjems J. Spatio-temporal regulation of circular RNA expression during porcine embryonic brain development. Genome Biol. 2015;16(1):245. http://dx.doi.org/10.1186/s13059-015-0801-3. PMid:26541409.

Yan L, Yang M, Guo H, Yang L, Wu J, Li R, Liu P, Lian Y, Zheng X, Yan J, Huang J, Li M, Wu X, Wen L, Lao K, Li R, Qiao J, Tang F. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol. 2013;20(9):1131-9. http://dx.doi.org/10.1038/nsmb.2660. PMid:23934149.

Yang R, Chen J, Wang L, Deng A. LncRNA BANCR participates in polycystic ovary syndrome by promoting cell apoptosis. Mol Med Rep. 2019;19(3):1581-6. PMid:30592281.

Yao Y, Niu J, Sizhu S, Li B, Chen Y, Li R, Yangzong Q, Li Q, Xu Y. MicroRNA-125b regulates apoptosis by targeting bone morphogenetic protein receptor 1B in yak granulosa cells. DNA Cell Biol. 2018;37(11):878-87. http://dx.doi.org/10.1089/dna.2018.4354. PMid:30260685.

Yoshimura Y, Barua A. Female reproductive system and immunology. Adv Exp Med Biol. 2017;1001:33-57. http://dx.doi.org/10.1007/978-981-10-3975-1_3. PMid:28980228.

Zhang M, Zhang Q, Hu Y, Xu L, Jiang Y, Zhang C, Ding L, Jiang R, Sun J, Sun H, Yah G. miR-181a increases FoxO1 acetylation and promotes granulosa cell apoptosis via SIRT1 downregulation. 2017;8:e3088. http://dx.doi.org/10.1038/cddis.2017.467.

Zhang J, Xu Y, Liu H, Pan Z. MicroRNAs in ovarian follicular atresia and granulosa cell apoptosis. Reprod Biol Endocrinol. 2019a;17(1):9. PMid:30630485.

Zhang Z, Chen CZ, Xu MQ, Zhang LQ, Liu JB, Gao Y, Jiang H, Yuan B, Zhang JB. MiR-31 and miR-143 affect steroid hormone synthesis and inhibit cell apoptosis in bovine granulosa cells through FSHR. Theriogenology. 2019b;123:45-53. http://dx.doi.org/10.1016/j.theriogenology.2018.09.020. PMid:30278258.

Zhao H, Ge J, Wei J, Liu J, Liu C, Ma C, Zhao X, Wei Q, Ma B. Effect of FSH on E(2)/GPR30-mediated mouse oocyte maturation in vitro. Cell Signal. 2020;66:109464. http://dx.doi.org/10.1016/j.cellsig.2019.109464. PMid:31704004.
 


Submitted date:
12/25/2021

Accepted date:
09/13/2022

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