Long noncoding RNA 2193 regulates meiosis through global epigenetic modification and cytoskeleton organization in pig oocytes

Abstract

Long noncoding RNAs (lncRNAs) regulate a variety of physiological and pathological processes. However, the biological function of lncRNAs in mammalian germ cells remains largely unexplored. Here we identified one novel lncRNA (lncRNA2193) from single‐cell RNA sequencing performed on porcine oocytes and investigated its function in oocyte meiosis. During in vitro maturation (IVM), from germinal vesicle (GV, 0 hr), GV breakdown (GVBD, 24 hr), to metaphase II stage (MII, 44 hr), the transcriptional abundance of lncRNA2193 remained stable and high. LncRNA2193 interference by small interfering RNA microinjection into porcine GV oocytes could significantly inhibit rates of GVBD and the first polar body extrusion, but enhance the rates of oocytes with a nuclear abnormality. Moreover, lncRNA2193 knockdown disturbed cytoskeletal organization (F‐actin and spindle), and decreased DNA 5‐methylcytosine (5mC) and histone trimethylation (H3K4me3, H3K9me3, H3K27me3, and H3K36me3) levels. The lncRNA2193 downregulation induced a decrease of 5mC level could be partially due to the reduction of DNA methyltransferase 3A and 3B, and the elevation of 5mC‐hydroxylase ten‐11 translocation 2 (TET2). After parthenogenetic activation of MII oocytes, parthenotes exhibited higher fragmentation but lower cleavage rates in the lncRNA2193 downregulated group. However, lncRNA2193 interference performed on mature MII oocytes and parthenotes at 1‐cell stage did not affect the cleavage and blasctocyst rates of pathenotes. Taken together, lncRNA2193 plays an important role in porcine oocyte maturation, providing more insights for relevant investigations on mammalian germ cells.

Comparative Transcriptome Profiling of mRNA and lncRNA of Ovaries in High and Low Egg Production Performance in Domestic Pigeons (Columba livia)

“…Specifically, we identified 148 DE lncRNAs and 811 DE mRNAs in ovaries between the groups of high and low egg production performance. In the last few years, numerous studies had found that lncRNAs played important roles in the oogenesis in ovaries of different species, including pigs, cattle, mice and ducks (Nakagawa et al, 2014;Ren et al, 2017;Yang et al, 2020). The present study is the first to report the transcriptome profiling of lncRNAs and mRNA in the ovaries of pigeons.…”

“…LncRNAs have also been found to be key regulators in a wide range of biological processes, including reproduction, but most of the mechanisms of lncRNA related regulation in biological processes remain unclear (Taylor et al, 2015). In the terms of animal genetics, the effects of lncRNAs on economically important phenotypic traits had been studied in the last decade (Zhang et al, 2019;Yang et al, 2020), particularly for the possible application in poultry breeding (Fulton, 2012). However, lncRNAs, as the crucial regulation factors in many biological processes, have not been systematically researched in the ovaries of domestic pigeons related to egg production.…”

Transcriptomics of Meiosis in the Male Mouse

“…Similarly, a role for meiosis progression has been suggested for Tsx, an X-linked lncRNA differentially expressed in PS, as knockout mice show increased PS apoptosis (Anguera et al, 2011). On the other hand, 2193 lncRNA has been identified by means of scRNAseq, and shown to play an important role in porcine oocyte maturation through epigenetic modification (Yang et al, 2020).…”

Ascorbic acid promotes the reproductive function of porcine immature Sertoli cells through transcriptome reprogramming

“…In humans with testicular cancer, SCs showed aberrant MAPK, AMPK and TGF-β/Smad signaling pathways [ 51 ]. LncRNAs was longer than 200 nt, which could not be translated into any protein, but could regulate the expression of target genes and function in multiple biological processes [ 56 ]. Recently, lncWNT3-IT has been shown to regulate WNT3 expression and affect proliferation of goat SCs, confirming the vital function of lncRNAs in SCs [ 57 ].…”