Transcriptome-wide Dynamics of m6A mRNA Methylation During Porcine Spermatogenesis.

IF 11.5 2区 生物学 Q1 GENETICS & HEREDITY
Genomics, Proteomics & Bioinformatics Pub Date : 2023-08-01 Epub Date: 2021-09-17 DOI:10.1016/j.gpb.2021.08.006
Zidong Liu, Xiaoxu Chen, Pengfei Zhang, Fuyuan Li, Lingkai Zhang, Xueliang Li, Tao Huang, Yi Zheng, Taiyong Yu, Tao Zhang, Wenxian Zeng, Hongzhao Lu, Yinghua Lv
{"title":"Transcriptome-wide Dynamics of m<sup>6</sup>A mRNA Methylation During Porcine Spermatogenesis.","authors":"Zidong Liu, Xiaoxu Chen, Pengfei Zhang, Fuyuan Li, Lingkai Zhang, Xueliang Li, Tao Huang, Yi Zheng, Taiyong Yu, Tao Zhang, Wenxian Zeng, Hongzhao Lu, Yinghua Lv","doi":"10.1016/j.gpb.2021.08.006","DOIUrl":null,"url":null,"abstract":"<p><p>Spermatogenesis is a continual process that occurs in the testes, in which diploid spermatogonial stem cells (SSCs) differentiate and generate haploid spermatozoa. This highly efficient and intricate process is orchestrated at multiple levels. N<sup>6</sup>-methyladenosine (m<sup>6</sup>A), an epigenetic modification prevalent in mRNAs, is implicated in the transcriptional regulation during spermatogenesis. However, the dynamics of m<sup>6</sup>A modification in non-rodent mammalian species remains unclear. Here, we systematically investigated the profile and role of m<sup>6</sup>A during spermatogenesis in pigs. By analyzing the transcriptomic distribution of m<sup>6</sup>A in spermatogonia, spermatocytes, and round spermatids, we identified a globally conserved m<sup>6</sup>A pattern between porcine and murine genes with spermatogenic function. We found that m<sup>6</sup>A was enriched in a group of genes that specifically encode the metabolic enzymes and regulators. In addition, transcriptomes in porcine male germ cells could be subjected to the m<sup>6</sup>A modification. Our data show that m<sup>6</sup>A plays the regulatory roles during spermatogenesis in pigs, which is similar to that in mice. Illustrations of this point are three genes (SETDB1, FOXO1, and FOXO3) that are crucial to the determination of the fate of SSCs. To the best of our knowledge, this study for the first time uncovers the expression profile and role of m<sup>6</sup>A during spermatogenesis in large animals and provides insights into the intricate transcriptional regulation underlying the lifelong male fertility in non-rodent mammalian species.</p>","PeriodicalId":12528,"journal":{"name":"Genomics, Proteomics & Bioinformatics","volume":null,"pages":null},"PeriodicalIF":11.5000,"publicationDate":"2023-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10787014/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Genomics, Proteomics & Bioinformatics","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1016/j.gpb.2021.08.006","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2021/9/17 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"GENETICS & HEREDITY","Score":null,"Total":0}
引用次数: 0

Abstract

Spermatogenesis is a continual process that occurs in the testes, in which diploid spermatogonial stem cells (SSCs) differentiate and generate haploid spermatozoa. This highly efficient and intricate process is orchestrated at multiple levels. N6-methyladenosine (m6A), an epigenetic modification prevalent in mRNAs, is implicated in the transcriptional regulation during spermatogenesis. However, the dynamics of m6A modification in non-rodent mammalian species remains unclear. Here, we systematically investigated the profile and role of m6A during spermatogenesis in pigs. By analyzing the transcriptomic distribution of m6A in spermatogonia, spermatocytes, and round spermatids, we identified a globally conserved m6A pattern between porcine and murine genes with spermatogenic function. We found that m6A was enriched in a group of genes that specifically encode the metabolic enzymes and regulators. In addition, transcriptomes in porcine male germ cells could be subjected to the m6A modification. Our data show that m6A plays the regulatory roles during spermatogenesis in pigs, which is similar to that in mice. Illustrations of this point are three genes (SETDB1, FOXO1, and FOXO3) that are crucial to the determination of the fate of SSCs. To the best of our knowledge, this study for the first time uncovers the expression profile and role of m6A during spermatogenesis in large animals and provides insights into the intricate transcriptional regulation underlying the lifelong male fertility in non-rodent mammalian species.

猪精子发生过程中 m6A mRNA 甲基化在整个转录组的动态变化
精子发生是睾丸中发生的一个持续过程,在这个过程中,二倍体精原干细胞(SSC)分化并生成单倍体精子。这一高效而复杂的过程在多个层面上进行协调。N6-甲基腺苷(m6A)是mRNA中普遍存在的一种表观遗传修饰,与精子发生过程中的转录调控有关。然而,m6A修饰在非啮齿类哺乳动物物种中的动态变化仍不清楚。在这里,我们系统地研究了猪精子发生过程中m6A的概况和作用。通过分析 m6A 在精原细胞、精母细胞和圆形精子中的转录组分布,我们发现了猪和鼠具有生精功能的基因之间全球保守的 m6A 模式。我们发现,m6A 富集在一组专门编码代谢酶和调节因子的基因中。此外,猪雄性生殖细胞的转录组也可能受到 m6A 的修饰。我们的数据表明,m6A 在猪的精子发生过程中起着调控作用,这与小鼠的情况类似。三个基因(SETDB1、FOXO1 和 FOXO3)对决定造精细胞的命运至关重要,它们就是这方面的例证。据我们所知,这项研究首次揭示了m6A在大型动物精子发生过程中的表达谱和作用,为我们深入了解非啮齿类哺乳动物物种中雄性终生生育能力背后错综复杂的转录调控提供了线索。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Genomics, Proteomics & Bioinformatics
Genomics, Proteomics & Bioinformatics Biochemistry, Genetics and Molecular Biology-Biochemistry
CiteScore
14.30
自引率
4.20%
发文量
844
审稿时长
61 days
期刊介绍: Genomics, Proteomics and Bioinformatics (GPB) is the official journal of the Beijing Institute of Genomics, Chinese Academy of Sciences / China National Center for Bioinformation and Genetics Society of China. It aims to disseminate new developments in the field of omics and bioinformatics, publish high-quality discoveries quickly, and promote open access and online publication. GPB welcomes submissions in all areas of life science, biology, and biomedicine, with a focus on large data acquisition, analysis, and curation. Manuscripts covering omics and related bioinformatics topics are particularly encouraged. GPB is indexed/abstracted by PubMed/MEDLINE, PubMed Central, Scopus, BIOSIS Previews, Chemical Abstracts, CSCD, among others.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信