Cargando…

Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny

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,...

Descripción completa

Detalles Bibliográficos
Autores principales: Valcarce, David G., Riesco, Marta F., Cuesta-Martín, Leyre, Esteve-Codina, Anna, Martínez-Vázquez, Juan Manuel, Robles, Vanesa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10071778/
https://www.ncbi.nlm.nih.gov/pubmed/37013516
http://dx.doi.org/10.1186/s12915-023-01570-w
_version_ 1785019262736269312
author Valcarce, David G.
Riesco, Marta F.
Cuesta-Martín, Leyre
Esteve-Codina, Anna
Martínez-Vázquez, Juan Manuel
Robles, Vanesa
author_facet Valcarce, David G.
Riesco, Marta F.
Cuesta-Martín, Leyre
Esteve-Codina, Anna
Martínez-Vázquez, Juan Manuel
Robles, Vanesa
author_sort Valcarce, David G.
collection PubMed
description 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. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01570-w.
format Online
Article
Text
id pubmed-10071778
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-100717782023-04-05 Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny Valcarce, David G. Riesco, Marta F. Cuesta-Martín, Leyre Esteve-Codina, Anna Martínez-Vázquez, Juan Manuel Robles, Vanesa BMC Biol Research Article 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. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01570-w. BioMed Central 2023-04-03 /pmc/articles/PMC10071778/ /pubmed/37013516 http://dx.doi.org/10.1186/s12915-023-01570-w Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://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.
spellingShingle Research Article
Valcarce, David G.
Riesco, Marta F.
Cuesta-Martín, Leyre
Esteve-Codina, Anna
Martínez-Vázquez, Juan Manuel
Robles, Vanesa
Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny
title Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny
title_full Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny
title_fullStr Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny
title_full_unstemmed Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny
title_short Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny
title_sort stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10071778/
https://www.ncbi.nlm.nih.gov/pubmed/37013516
http://dx.doi.org/10.1186/s12915-023-01570-w
work_keys_str_mv AT valcarcedavidg stressdecreasesspermatozoaqualityandinducesmolecularalterationsinzebrafishprogeny
AT riescomartaf stressdecreasesspermatozoaqualityandinducesmolecularalterationsinzebrafishprogeny
AT cuestamartinleyre stressdecreasesspermatozoaqualityandinducesmolecularalterationsinzebrafishprogeny
AT estevecodinaanna stressdecreasesspermatozoaqualityandinducesmolecularalterationsinzebrafishprogeny
AT martinezvazquezjuanmanuel stressdecreasesspermatozoaqualityandinducesmolecularalterationsinzebrafishprogeny
AT roblesvanesa stressdecreasesspermatozoaqualityandinducesmolecularalterationsinzebrafishprogeny