Cargando…

Transcriptome profiling of histone writers/erasers enzymes across spermatogenesis, mature sperm and pre-cleavage embryo: Implications in paternal epigenome transitions and inheritance mechanisms

Accumulating evidence points out that sperm carry epigenetic instructions to embryo in the form of retained histones marks and RNA cargo that can transmit metabolic and behavioral traits to offspring. However, the mechanisms behind epigenetic inheritance of paternal environment are still poorly unde...

Descripción completa

Detalles Bibliográficos
Autores principales: Barbero, Gastón, de Sousa Serro, Maximiliano G., Perez Lujan, Camila, Vitullo, Alfredo D., González, Candela R., González, Betina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9911891/
https://www.ncbi.nlm.nih.gov/pubmed/36776561
http://dx.doi.org/10.3389/fcell.2023.1086573
_version_ 1784885093504909312
author Barbero, Gastón
de Sousa Serro, Maximiliano G.
Perez Lujan, Camila
Vitullo, Alfredo D.
González, Candela R.
González, Betina
author_facet Barbero, Gastón
de Sousa Serro, Maximiliano G.
Perez Lujan, Camila
Vitullo, Alfredo D.
González, Candela R.
González, Betina
author_sort Barbero, Gastón
collection PubMed
description Accumulating evidence points out that sperm carry epigenetic instructions to embryo in the form of retained histones marks and RNA cargo that can transmit metabolic and behavioral traits to offspring. However, the mechanisms behind epigenetic inheritance of paternal environment are still poorly understood. Here, we curated male germ cells RNA-seq data and analyzed the expression profile of all known histone lysine writers and erasers enzymes across spermatogenesis, unraveling the developmental windows at which they are upregulated, and the specific activity related to canonical and non-canonical histone marks deposition and removal. We also characterized the epigenetic enzymes signature in the mature sperm RNA cargo, showing most of them positive translation at pre-cleavage zygote, suggesting that paternally-derived enzymes mRNA cooperate with maternal factors to embryo chromatin assembly. Our study shows several histone modifying enzymes not described yet in spermatogenesis and even more, important mechanistic aspects behind transgenerational epigenetics. Epigenetic enzymes not only can respond to environmental stressors, but could function as vectors of epigenetic information and participate in chromatin organization during maternal-to-zygote transition.
format Online
Article
Text
id pubmed-9911891
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-99118912023-02-11 Transcriptome profiling of histone writers/erasers enzymes across spermatogenesis, mature sperm and pre-cleavage embryo: Implications in paternal epigenome transitions and inheritance mechanisms Barbero, Gastón de Sousa Serro, Maximiliano G. Perez Lujan, Camila Vitullo, Alfredo D. González, Candela R. González, Betina Front Cell Dev Biol Cell and Developmental Biology Accumulating evidence points out that sperm carry epigenetic instructions to embryo in the form of retained histones marks and RNA cargo that can transmit metabolic and behavioral traits to offspring. However, the mechanisms behind epigenetic inheritance of paternal environment are still poorly understood. Here, we curated male germ cells RNA-seq data and analyzed the expression profile of all known histone lysine writers and erasers enzymes across spermatogenesis, unraveling the developmental windows at which they are upregulated, and the specific activity related to canonical and non-canonical histone marks deposition and removal. We also characterized the epigenetic enzymes signature in the mature sperm RNA cargo, showing most of them positive translation at pre-cleavage zygote, suggesting that paternally-derived enzymes mRNA cooperate with maternal factors to embryo chromatin assembly. Our study shows several histone modifying enzymes not described yet in spermatogenesis and even more, important mechanistic aspects behind transgenerational epigenetics. Epigenetic enzymes not only can respond to environmental stressors, but could function as vectors of epigenetic information and participate in chromatin organization during maternal-to-zygote transition. Frontiers Media S.A. 2023-01-27 /pmc/articles/PMC9911891/ /pubmed/36776561 http://dx.doi.org/10.3389/fcell.2023.1086573 Text en Copyright © 2023 Barbero, de Sousa Serro, Perez Lujan, Vitullo, González and González. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Barbero, Gastón
de Sousa Serro, Maximiliano G.
Perez Lujan, Camila
Vitullo, Alfredo D.
González, Candela R.
González, Betina
Transcriptome profiling of histone writers/erasers enzymes across spermatogenesis, mature sperm and pre-cleavage embryo: Implications in paternal epigenome transitions and inheritance mechanisms
title Transcriptome profiling of histone writers/erasers enzymes across spermatogenesis, mature sperm and pre-cleavage embryo: Implications in paternal epigenome transitions and inheritance mechanisms
title_full Transcriptome profiling of histone writers/erasers enzymes across spermatogenesis, mature sperm and pre-cleavage embryo: Implications in paternal epigenome transitions and inheritance mechanisms
title_fullStr Transcriptome profiling of histone writers/erasers enzymes across spermatogenesis, mature sperm and pre-cleavage embryo: Implications in paternal epigenome transitions and inheritance mechanisms
title_full_unstemmed Transcriptome profiling of histone writers/erasers enzymes across spermatogenesis, mature sperm and pre-cleavage embryo: Implications in paternal epigenome transitions and inheritance mechanisms
title_short Transcriptome profiling of histone writers/erasers enzymes across spermatogenesis, mature sperm and pre-cleavage embryo: Implications in paternal epigenome transitions and inheritance mechanisms
title_sort transcriptome profiling of histone writers/erasers enzymes across spermatogenesis, mature sperm and pre-cleavage embryo: implications in paternal epigenome transitions and inheritance mechanisms
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9911891/
https://www.ncbi.nlm.nih.gov/pubmed/36776561
http://dx.doi.org/10.3389/fcell.2023.1086573
work_keys_str_mv AT barberogaston transcriptomeprofilingofhistonewriterserasersenzymesacrossspermatogenesismaturespermandprecleavageembryoimplicationsinpaternalepigenometransitionsandinheritancemechanisms
AT desousaserromaximilianog transcriptomeprofilingofhistonewriterserasersenzymesacrossspermatogenesismaturespermandprecleavageembryoimplicationsinpaternalepigenometransitionsandinheritancemechanisms
AT perezlujancamila transcriptomeprofilingofhistonewriterserasersenzymesacrossspermatogenesismaturespermandprecleavageembryoimplicationsinpaternalepigenometransitionsandinheritancemechanisms
AT vitulloalfredod transcriptomeprofilingofhistonewriterserasersenzymesacrossspermatogenesismaturespermandprecleavageembryoimplicationsinpaternalepigenometransitionsandinheritancemechanisms
AT gonzalezcandelar transcriptomeprofilingofhistonewriterserasersenzymesacrossspermatogenesismaturespermandprecleavageembryoimplicationsinpaternalepigenometransitionsandinheritancemechanisms
AT gonzalezbetina transcriptomeprofilingofhistonewriterserasersenzymesacrossspermatogenesismaturespermandprecleavageembryoimplicationsinpaternalepigenometransitionsandinheritancemechanisms