Changes in equine testicular and epididymal homeostasis in response to scrotal heating

IF 1.3 3区 农林科学 Q2 VETERINARY SCIENCES
M. Ferrer , M. Barletta , J. Williams , K. Moran , G. Bilbao , J. Bartolome
{"title":"Changes in equine testicular and epididymal homeostasis in response to scrotal heating","authors":"M. Ferrer ,&nbsp;M. Barletta ,&nbsp;J. Williams ,&nbsp;K. Moran ,&nbsp;G. Bilbao ,&nbsp;J. Bartolome","doi":"10.1016/j.jevs.2024.105284","DOIUrl":null,"url":null,"abstract":"<div><div>Heat stress is a common cause of testicular and epididymal dysfunction. While the effect of scrotal heating on ejaculated sperm and testicular histologic changes is known, the testicular and epididymal molecular events and changes in gene expression that cause them are largely unknown. Here, we hypothesized that early equine testicular and epididymal responses to heat stress are associated with oxidative stress and immune dysregulation. Normospermic adult light-breed stallions were divided into two treatments: control (CON, n=5) and scrotal insulation (SI, n=5). The scrotum of SI stallions was covered with an insulation bag for 24 h. The stallions were castrated immediately after the bags were removed. CON stallions did not undergo scrotal insulation. Tissue biopsies were collected from the testes, head, body, and tail of the epididymis for transcriptome analysis. The RNA sequencing libraries were generated using NEBNext<sup>Ⓡ</sup>Ultra™RNA Library Prep Kit (Illumina<sup>Ⓡ</sup>). Differential gene expression was compared between each SI and CON tissue using the DESeq2 R package and the ClusterProfiler sofware. Differentially expressed genes (DEGs) and pathways were identified (P&lt;0.05, log2 fold change ≥1) in the PANTHER Classification System. The number of DEGs in the testes, head, body, and tail of the epididymis of SI stallions was 507, 1198, 3420, and 1245, respectively. The main downregulated testicular pathways were associated with spermatogenesis. The SI upregulated testicular DEGs corresponded to 331 pathways (268 biological processes, 80.9%, 42 molecular functions, 12.7%, 21 cellular components, 6.3%). Upregulated DEGs were associated with oxidant-antioxidant balance (e.g. peroxidase activity GO:0004601), increased cell respiration, increased use of lipids and amino acids, purine metabolism, activation of the innate and adaptive immune response (e.g. activation of immune response GO:0002253; positive regulation of innate immune response GO:0045089; T cell activation GO:0050863; B cell proliferation GO:0030888; positive regulation of mast cell activation GO:0033005; e.g. FGR, LRRC32, CD226, TLR6, TRIM15, IL33, CD4), and deposition of amyloid. The epididymal head had dysregulation of pathways associated with spermatogenesis, energy metabolism, and antigen presentation and processing, with DEGs associated with macrophage and T cell signaling, regulatory T cell differentiation, and cytotoxic T cells. DEGs in the epididymal body were associated with microtubule formation, sperm flagellum components, and cell motility. DEGs in the epididymal tail were associated with energy metabolism and cell respiration. The findings support dysregulation of the local oxidant-antioxidant system, energy metabolic pathways, and immune system homeostasis in SI stallions and lay the foundation for understanding heat-induced reproductive dysfunction.</div></div>","PeriodicalId":15798,"journal":{"name":"Journal of Equine Veterinary Science","volume":"145 ","pages":"Article 105284"},"PeriodicalIF":1.3000,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Equine Veterinary Science","FirstCategoryId":"97","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0737080624002909","RegionNum":3,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"VETERINARY SCIENCES","Score":null,"Total":0}
引用次数: 0

Abstract

Heat stress is a common cause of testicular and epididymal dysfunction. While the effect of scrotal heating on ejaculated sperm and testicular histologic changes is known, the testicular and epididymal molecular events and changes in gene expression that cause them are largely unknown. Here, we hypothesized that early equine testicular and epididymal responses to heat stress are associated with oxidative stress and immune dysregulation. Normospermic adult light-breed stallions were divided into two treatments: control (CON, n=5) and scrotal insulation (SI, n=5). The scrotum of SI stallions was covered with an insulation bag for 24 h. The stallions were castrated immediately after the bags were removed. CON stallions did not undergo scrotal insulation. Tissue biopsies were collected from the testes, head, body, and tail of the epididymis for transcriptome analysis. The RNA sequencing libraries were generated using NEBNextUltra™RNA Library Prep Kit (Illumina). Differential gene expression was compared between each SI and CON tissue using the DESeq2 R package and the ClusterProfiler sofware. Differentially expressed genes (DEGs) and pathways were identified (P<0.05, log2 fold change ≥1) in the PANTHER Classification System. The number of DEGs in the testes, head, body, and tail of the epididymis of SI stallions was 507, 1198, 3420, and 1245, respectively. The main downregulated testicular pathways were associated with spermatogenesis. The SI upregulated testicular DEGs corresponded to 331 pathways (268 biological processes, 80.9%, 42 molecular functions, 12.7%, 21 cellular components, 6.3%). Upregulated DEGs were associated with oxidant-antioxidant balance (e.g. peroxidase activity GO:0004601), increased cell respiration, increased use of lipids and amino acids, purine metabolism, activation of the innate and adaptive immune response (e.g. activation of immune response GO:0002253; positive regulation of innate immune response GO:0045089; T cell activation GO:0050863; B cell proliferation GO:0030888; positive regulation of mast cell activation GO:0033005; e.g. FGR, LRRC32, CD226, TLR6, TRIM15, IL33, CD4), and deposition of amyloid. The epididymal head had dysregulation of pathways associated with spermatogenesis, energy metabolism, and antigen presentation and processing, with DEGs associated with macrophage and T cell signaling, regulatory T cell differentiation, and cytotoxic T cells. DEGs in the epididymal body were associated with microtubule formation, sperm flagellum components, and cell motility. DEGs in the epididymal tail were associated with energy metabolism and cell respiration. The findings support dysregulation of the local oxidant-antioxidant system, energy metabolic pathways, and immune system homeostasis in SI stallions and lay the foundation for understanding heat-induced reproductive dysfunction.
求助全文
约1分钟内获得全文 求助全文
来源期刊
Journal of Equine Veterinary Science
Journal of Equine Veterinary Science 农林科学-兽医学
CiteScore
2.70
自引率
7.70%
发文量
249
审稿时长
77 days
期刊介绍: Journal of Equine Veterinary Science (JEVS) is an international publication designed for the practicing equine veterinarian, equine researcher, and other equine health care specialist. Published monthly, each issue of JEVS includes original research, reviews, case reports, short communications, and clinical techniques from leaders in the equine veterinary field, covering such topics as laminitis, reproduction, infectious disease, parasitology, behavior, podology, internal medicine, surgery and nutrition.
×
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