Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny

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  • dc.contributor.author Valcárcel, David
  • dc.contributor.author Riesco, Marta F.
  • dc.contributor.author Cuesta-Martín, Leyre
  • dc.contributor.author Esteve-Codina, Anna
  • dc.contributor.author Martínez-Vázquez, Juan Manuel
  • dc.contributor.author Robles, Vanesa
  • dc.date.accessioned 2023-06-15T06:00:16Z
  • dc.date.available 2023-06-15T06:00:16Z
  • dc.date.issued 2023
  • dc.description.abstract Background: Chronic stress can produce a severe negative impact on health not only in the exposed individuals but also in their offspring. Indeed, chronic stress may be contributing to the current worldwide scenario of increasing infertility and decreasing gamete quality in human populations. Here, we evaluate the effect of chronic stress on behavior and male reproductive parameters in zebrafish. Our goal is to provide information on the impact that chronic stress has at molecular, histological, and physiological level in a vertebrate model species. Results: We evaluated the effects of a 21-day chronic stress protocol covering around three full waves of spermatogenesis in Danio rerio adult males. The induction of chronic stress produced anxiety-like behavior in stressed males as assessed by a novel tank test. At a molecular level, the induction of chronic stress consistently resulted in the overexpression of two genes related to endoplasmic reticulum (ER) stress in the brain. Gene set enrichment analysis (GSEA) of testes suggested a dysregulation of the nonsense-mediated decay (NMD) pathway, which was also confirmed on qPCR analysis. Histological analysis of the testicle did not show significant differences in terms of the relative proportions of each germ-cell type; however, the quality of sperm from stressed males was compromised in terms of motility. RNA-seq analysis in stress-derived larval progenies revealed molecular alterations, including those predicted to affect translation initiation, DNA repair, cell cycle control, and response to stress. Conclusions: Induction of chronic stress during a few cycles of spermatogenesis in the vertebrate zebrafish model affects behavior, gonadal gene expression, final gamete quality, and progeny. The NMD surveillance pathway (a key cellular mechanism that regulates the stability of both normal and mutant transcripts) is severely affected in the testes by chronic stress and therefore the control and regulation of RNAs during spermatogenesis may be affected altering the molecular status in the progeny.
  • dc.description.sponsorship This study was supported by MCIN/AEI/10.13039/501100011033, grant PID2019-108509RB-I00. DGV was funded by MCIN/AEI/10.13039/501100011033, grants FJC2018-037566-I and IJC2020-044091-I. AEC is funded by ISCIII /MINECO (PT17/0009/0019) and co-funded by FEDER.
  • dc.format.mimetype application/pdf
  • dc.identifier.citation Valcarce DG, Riesco MF, Cuesta-Martín L, Esteve-Codina A, Martínez-Vázquez JM, Robles V. Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny. BMC Biol. 2023 Apr 3;21(1):70. DOI: 10.1186/s12915-023-01570-w
  • dc.identifier.doi http://dx.doi.org/10.1186/s12915-023-01570-w
  • dc.identifier.issn 1741-7007
  • dc.identifier.uri http://hdl.handle.net/10230/57168
  • dc.language.iso eng
  • dc.publisher BioMed Central
  • dc.relation.ispartof BMC Biol. 2023 Apr 3;21(1):70
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/PID2019-108509RB-I00
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/FJC2018-037566-I
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/IJC2020-044091-I
  • dc.rights © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
  • dc.rights.accessRights info:eu-repo/semantics/openAccess
  • dc.rights.uri http://creativecommons.org/licenses/by/4.0/
  • dc.subject.keyword Chronic stress
  • dc.subject.keyword NMD
  • dc.subject.keyword Progeny
  • dc.subject.keyword Sperm
  • dc.subject.keyword Testis
  • dc.subject.keyword Zebrafish
  • dc.title Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny
  • dc.type info:eu-repo/semantics/article
  • dc.type.version info:eu-repo/semantics/publishedVersion

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