Circular RNA WRNIP1 Activates the PI3K-AKT and ERK1/2 Signaling Pathways by Binding to MiR-129-5p/IGF2 Axis and Facilitates Ovarian Follicle Development in Chickens

Overview

Journal Poult Sci

Publisher Elsevier

Specialty Veterinary Medicine

Date 2025 Jan 5

PMID 39756109

Authors

Xiyu Zhao

Yuanhang Wei

Xinyan Li

Xinghong Yu

Zhenyu Lei

Yao Zhang

Shunshun Han

Huadong Yin

Can Cui

Affiliations

Soon will be listed here.

Abstract

The healthy and orderly development of ovarian follicles is the basic premise to maintain normal and continuous egg production of chickens. Emerging researches continue to reveal the crucial functions of circular RNAs (circRNAs) involved in follicle development. In the present study, a novel circular RNA WRNIP1 (circWRNIP1) with higher abundance in healthy follicles than in atretic follicles was identified, suggesting its important regulatory role in follicle selection and maturation. In this study, we demonstrate that circWRNIP1 promotes chicken ovarian follicle development by enhancing granulosa cell proliferation and inhibiting apoptosis. Furthermore, we validated the targeting relationships between circWRNIP1 and miR-129-5p, as well as between miR-129-5p and IGF2. Mechanistically, through co-transfection experiments, we show that circWRNIP1 activates the PI3K-AKT and ERK1/2 signaling pathways via the miR-129-5p/IGF2 axis. The present study provides new insights into the downstream molecular mechanism of circRNAs regulating follicle development, and is expected to provide reliable targets for the subsequent establishment of new molecular breeding strategies.

References

Yoshimura A, Seki M, Enomoto T . The role of WRNIP1 in genome maintenance. Cell Cycle. 2017; 16(6):515-521. PMC: 5384577. DOI: 10.1080/15384101.2017.1282585. View

Wu Y, Xiao H, Pi J, Zhang H, Pan A, Pu Y . The circular RNA aplacirc_13267 upregulates duck granulosa cell apoptosis by the apla-miR-1-13/THBS1 signaling pathway. J Cell Physiol. 2020; 235(7-8):5750-5763. DOI: 10.1002/jcp.29509. View

Bian J, Ding H, Hu A, Wang J . Circ_0001361/miR-490-5p/IGF2 Axis Regulates the Viability and Apoptosis of Neuroblastoma Cells. Neurochem Res. 2024; 49(11):3060-3068. DOI: 10.1007/s11064-024-04225-6. View

He H, Li D, Tian Y, Wei Q, Amevor F, Sun C . miRNA sequencing analysis of healthy and atretic follicles of chickens revealed that miR-30a-5p inhibits granulosa cell death via targeting Beclin1. J Anim Sci Biotechnol. 2022; 13(1):55. PMC: 9003977. DOI: 10.1186/s40104-022-00697-0. View

Guo T, Huang L, Yao W, Du X, Li Q, Ma M . The potential biological functions of circular RNAs during the initiation of atresia in pig follicles. Domest Anim Endocrinol. 2020; 72:106401. DOI: 10.1016/j.domaniend.2019.106401. View

Chen R, Wang S, Belk J, Amaya L, Li Z, Cardenas A . Engineering circular RNA for enhanced protein production. Nat Biotechnol. 2022; 41(2):262-272. PMC: 9931579. DOI: 10.1038/s41587-022-01393-0. View

Richard S, Zhou Y, Jasoni C, Pankhurst M . Ovarian follicle size or growth rate can both be determinants of ovulatory follicle selection in mice†. Biol Reprod. 2023; 110(1):130-139. PMC: 10790341. DOI: 10.1093/biolre/ioad134. View

Johnson A . Ovarian follicle selection and granulosa cell differentiation. Poult Sci. 2014; 94(4):781-5. DOI: 10.3382/ps/peu008. View

Shen X, Zhao X, He H, Zhao J, Wei Y, Chen Y . Evolutionary conserved circular MEF2A RNAs regulate myogenic differentiation and skeletal muscle development. PLoS Genet. 2023; 19(9):e1010923. PMC: 10508632. DOI: 10.1371/journal.pgen.1010923. View

10.

Wei Y, Shen X, Zhao X, He H, Zhang Y, Zhu Q . Circular RNA circRPS19 promotes chicken granulosa cell proliferation and steroid hormone synthesis by interrupting the miR-218-5p/INHBB axis. Theriogenology. 2024; 219:103-115. DOI: 10.1016/j.theriogenology.2024.02.026. View

11.

Huo L, Wang Y, Bai X, Zheng H, Wang M . circKIF4A promotes tumorogenesis of glioma by targeting miR-139-3p to activate Wnt5a signaling. Mol Med. 2020; 26(1):29. PMC: 7144061. DOI: 10.1186/s10020-020-00159-1. View

12.

Misir S, Wu N, Yang B . Specific expression and functions of circular RNAs. Cell Death Differ. 2022; 29(3):481-491. PMC: 8901656. DOI: 10.1038/s41418-022-00948-7. View

13.

Cai H, Li Y, Li H, Niringiyumukiza J, Zhang M, Chen L . Identification and characterization of human ovary-derived circular RNAs and their potential roles in ovarian aging. Aging (Albany NY). 2018; 10(9):2511-2534. PMC: 6188495. DOI: 10.18632/aging.101565. View

14.

Fu Y, Jiang H, Liu J, Sun X, Zhang Z, Li S . Genome-wide analysis of circular RNAs in bovine cumulus cells treated with BMP15 and GDF9. Sci Rep. 2018; 8(1):7944. PMC: 5962577. DOI: 10.1038/s41598-018-26157-2. View

15.

Li D, Xu W, Wang X, Dang Y, Xu L, Lu G . lncRNA participates in premature ovarian insufficiency through regulating and . Mol Ther Nucleic Acids. 2021; 26:1092-1106. PMC: 8571528. DOI: 10.1016/j.omtn.2021.10.015. View

16.

Zhou S, Ma Y, Yao J, Zhao A, Xie C, Mi Y . TGF-β1-induced collagen promotes chicken ovarian follicle development via an intercellular cooperative pattern. Cell Biol Int. 2021; 45(6):1336-1348. DOI: 10.1002/cbin.11580. View

17.

Shen M, Li T, Zhang G, Wu P, Chen F, Lou Q . Dynamic expression and functional analysis of circRNA in granulosa cells during follicular development in chicken. BMC Genomics. 2019; 20(1):96. PMC: 6354403. DOI: 10.1186/s12864-019-5462-2. View

18.

Zhao W, Steinfeld J, Liang F, Chen X, Maranon D, Ma C . BRCA1-BARD1 promotes RAD51-mediated homologous DNA pairing. Nature. 2017; 550(7676):360-365. PMC: 5800781. DOI: 10.1038/nature24060. View

19.

Tian Q, Mu Q, Liu S, Huang K, Tang Y, Zhang P . m6A-modified circASXL1 promotes proliferation and migration of ovarian cancer through the miR-320d/RACGAP1 axis. Carcinogenesis. 2023; 44(12):859-870. DOI: 10.1093/carcin/bgad066. View

20.

Cao Z, Gao D, Xu T, Zhang L, Tong X, Zhang D . Circular RNA profiling in the oocyte and cumulus cells reveals that circARMC4 is essential for porcine oocyte maturation. Aging (Albany NY). 2019; 11(18):8015-8034. PMC: 6781969. DOI: 10.18632/aging.102315. View