Lipidomic and transcriptomic characteristics of boar seminal plasma extracellular vesicles associated with sperm motility

IF 3.9 2区 生物学 Q2 BIOCHEMISTRY & MOLECULAR BIOLOGY
Ning Ding, Yu Zhang, Jiayao Wang, Jianfeng Liu, Jing Zhang, Chun Zhang, Lei Zhou, Jinkang Cao, Li Jiang
{"title":"Lipidomic and transcriptomic characteristics of boar seminal plasma extracellular vesicles associated with sperm motility","authors":"Ning Ding,&nbsp;Yu Zhang,&nbsp;Jiayao Wang,&nbsp;Jianfeng Liu,&nbsp;Jing Zhang,&nbsp;Chun Zhang,&nbsp;Lei Zhou,&nbsp;Jinkang Cao,&nbsp;Li Jiang","doi":"10.1016/j.bbalip.2024.159561","DOIUrl":null,"url":null,"abstract":"<div><p>Seminal plasma extracellular vesicles (SPEVs) play an important role in regulating sperm motility by delivering various cargoes, such as miRNAs, mRNAs, proteins and metabolites. However, information on the lipid compositions of SPEVs and their roles in semen quality is limited. Here, we performed high-throughput transcriptomic and lipidomic analysis on SPEVs isolated from 20 boars with high or low sperm motility. Then, we evaluated the lipid composition and gene expression characteristics of SPEVs and identified the specific lipids and genes related to sperm motility. As a result, a total of 26 lipid classes were identified in SPEVs, and five subclasses, CerG2, CerG3, LPE, LPS and TG, were significantly different in boars with high and low sperm motility. In addition, 195 important lipids and 334 important genes were identified by weighted gene coexpression analysis (WGCNA) and differential expression analysis. We observed that several important genes and lipids in SPEVs potentially influence sperm motility via glycerophospholipid metabolism, glycerolipid metabolism, the sphingolipid signaling pathway and the ferroptosis pathway. Furthermore, we found a significant correlation between the content of 22 lipids and the expression levels of 67 genes (|cor| &gt; 0.8, <em>P</em> &lt; 0.05). Moreover, we observed that three important gene-lipid linkages (CerG1 (d22:0/24:0) - <em>RCAN3</em>, Cer (d18:1/24:0) - <em>SCFD2</em> and CerG1 (d18:0/24:1) - <em>SCFD2</em>) were strongly correlated with sperm motility. Based on the results, some genes and lipids in SPEVs may play important roles in sperm motility by interacting with sperm through important pathways.</p></div>","PeriodicalId":8815,"journal":{"name":"Biochimica et biophysica acta. Molecular and cell biology of lipids","volume":"1870 1","pages":"Article 159561"},"PeriodicalIF":3.9000,"publicationDate":"2024-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S1388198124001112/pdfft?md5=866d0705aaf225c6174f73f4242897f6&pid=1-s2.0-S1388198124001112-main.pdf","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Biochimica et biophysica acta. Molecular and cell biology of lipids","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S1388198124001112","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Seminal plasma extracellular vesicles (SPEVs) play an important role in regulating sperm motility by delivering various cargoes, such as miRNAs, mRNAs, proteins and metabolites. However, information on the lipid compositions of SPEVs and their roles in semen quality is limited. Here, we performed high-throughput transcriptomic and lipidomic analysis on SPEVs isolated from 20 boars with high or low sperm motility. Then, we evaluated the lipid composition and gene expression characteristics of SPEVs and identified the specific lipids and genes related to sperm motility. As a result, a total of 26 lipid classes were identified in SPEVs, and five subclasses, CerG2, CerG3, LPE, LPS and TG, were significantly different in boars with high and low sperm motility. In addition, 195 important lipids and 334 important genes were identified by weighted gene coexpression analysis (WGCNA) and differential expression analysis. We observed that several important genes and lipids in SPEVs potentially influence sperm motility via glycerophospholipid metabolism, glycerolipid metabolism, the sphingolipid signaling pathway and the ferroptosis pathway. Furthermore, we found a significant correlation between the content of 22 lipids and the expression levels of 67 genes (|cor| > 0.8, P < 0.05). Moreover, we observed that three important gene-lipid linkages (CerG1 (d22:0/24:0) - RCAN3, Cer (d18:1/24:0) - SCFD2 and CerG1 (d18:0/24:1) - SCFD2) were strongly correlated with sperm motility. Based on the results, some genes and lipids in SPEVs may play important roles in sperm motility by interacting with sperm through important pathways.

与精子活力相关的公猪精浆细胞外囊泡的脂质组和转录组特征
精浆细胞外囊泡(SPEVs)通过运送各种货物,如 miRNAs、mRNAs、蛋白质和代谢物,在调节精子活力方面发挥着重要作用。然而,有关 SPEVs 的脂质成分及其在精液质量中的作用的信息却很有限。在这里,我们对从20头精子活力高或低的公猪体内分离出的SPEV进行了高通量转录组和脂质组分析。然后,我们评估了 SPEVs 的脂质组成和基因表达特征,并确定了与精子活力相关的特定脂质和基因。结果发现,SPEVs中共有26类脂质,其中CerG2、CerG3、LPE、LPS和TG这5个亚类在精子活力高的公猪和精子活力低的公猪中存在显著差异。此外,通过加权基因共表达分析(WGCNA)和差异表达分析,确定了 195 种重要脂质和 334 个重要基因。我们观察到,SPEVs中的几个重要基因和脂质可能会通过甘油磷脂代谢、甘油脂质代谢、鞘脂信号通路和铁突变通路影响精子活力。此外,我们还发现 22 种脂类的含量与 67 个基因的表达水平之间存在明显的相关性(|cor| > 0.8, P <0.05)。此外,我们还观察到三个重要的基因-脂质联系(CerG1 (d22:0/24:0) - RCAN3、Cer (d18:1/24:0) - SCFD2 和 CerG1 (d18:0/24:1) - SCFD2)与精子活力密切相关。根据这些结果,SPEVs 中的一些基因和脂质可能通过重要途径与精子相互作用,从而在精子活力中发挥重要作用。
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
CiteScore
11.00
自引率
2.10%
发文量
109
审稿时长
53 days
期刊介绍: BBA Molecular and Cell Biology of Lipids publishes papers on original research dealing with novel aspects of molecular genetics related to the lipidome, the biosynthesis of lipids, the role of lipids in cells and whole organisms, the regulation of lipid metabolism and function, and lipidomics in all organisms. Manuscripts should significantly advance the understanding of the molecular mechanisms underlying biological processes in which lipids are involved. Papers detailing novel methodology must report significant biochemical, molecular, or functional insight in the area of lipids.
×
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