A novel trans-acting lncRNA of ACTG1 that induces the remodeling of ovarian follicles

Nian Li; Yinqi Zhou; Jiali Cai; Yifei Wang; Xiaofeng Zhou; Mengting Hu; Yubin Li; Hao Zhang; Jiaqi Li; Bing Cai; Xiaolong Yuan

doi:10.1016/j.ijbiomac.2023.125170

A novel trans-acting lncRNA of ACTG1 that induces the remodeling of ovarian follicles

Int J Biol Macromol. 2023 Jul 1;242(Pt 4):125170. doi: 10.1016/j.ijbiomac.2023.125170. Epub 2023 Jun 3.

Authors

Nian Li¹, Yinqi Zhou¹, Jiali Cai¹, Yifei Wang¹, Xiaofeng Zhou¹, Mengting Hu¹, Yubin Li², Hao Zhang¹, Jiaqi Li¹, Bing Cai³, Xiaolong Yuan⁴

Affiliations

¹ Guangdong Laboratory of Lingnan Modern Agriculture, National Engineering Research Center for Breeding Swine Industry, State Key Laboratory of Livestock and Poultry Breeding, Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong 510642, China.
² Reproductive Medical Center, the First Affiliated Hospital of Sun Yat-sen University, Guangdong Provincial Key Laboratory of Reproductive Medicine, Guangzhou, Guangdong 510080, China.
³ Reproductive Medical Center, the First Affiliated Hospital of Sun Yat-sen University, Guangdong Provincial Key Laboratory of Reproductive Medicine, Guangzhou, Guangdong 510080, China. Electronic address: caib5@mail.sysu.edu.cn.
⁴ Guangdong Laboratory of Lingnan Modern Agriculture, National Engineering Research Center for Breeding Swine Industry, State Key Laboratory of Livestock and Poultry Breeding, Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong 510642, China. Electronic address: yxl@scau.edu.cn.

PMID: 37276900
DOI: 10.1016/j.ijbiomac.2023.125170

Abstract

Previous studies have implicated the attractive role of long noncoding RNAs (lncRNAs) in the remodeling of mammalian tissues. The migration of granulosa cells (GCs), which are the main supporting cells in ovarian follicles, stimulates the follicular remodeling. Here, with the cultured GCs as the follicular model, the actin gamma 1 (ACTG1) was observed to significantly promote the migration and proliferation while inhibit the apoptosis of GCs, suggesting that ACTG1 was required for ovarian remodeling. Moreover, we identified the trans-regulatory lncRNA of ACTG1 (TRLA), which was epigenetically targeted by histone H3 lysine 4 acetylation (H3K4ac). Mechanistically, the 2-375 nt of TRLA bound to ACTG1's mRNA to increase the expression of ACTG1. Furthermore, TRLA facilitated the migration and proliferation while inhibited the apoptosis of GCs, thereby accelerating follicular remodeling. Besides, TRLA acted as a ceRNA for miR-26a to increase the expression of high-mobility group AT-hook 1 (HMGA1). Collectively, TRLA induces the remodeling of ovarian follicles via complementary to ACTG1's mRNA and regulating miR-26a/HMGA1 axis in GCs. These observations revealed a novel and promising trans-acting lncRNA mechanism mediated by H3K4ac, and TRLA might be a new target to restore follicular remodeling and development.

Keywords: Follicular remodeling; Granulosa cells; Trans-acting lncRNAs.

MeSH terms

Animals
Apoptosis / genetics
Cell Proliferation / genetics
Female
HMGA1a Protein / metabolism
Mammals / genetics
MicroRNAs* / genetics
MicroRNAs* / metabolism
Ovarian Follicle
RNA, Long Noncoding* / genetics
RNA, Long Noncoding* / metabolism
RNA, Messenger / metabolism

Substances

RNA, Long Noncoding
HMGA1a Protein
RNA, Messenger
MicroRNAs