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Alterations in sperm DNA methylation, non-coding RNA expression, and histone retention mediate vinclozolin-induced epigenetic transgenerational inheritance of disease

Epigenetic transgenerational inheritance of disease and phenotypic variation can be induced by several toxicants, such as vinclozolin. This phenomenon can involve DNA methylation, non-coding RNA (ncRNA) and histone retention, and/or modification in the germline (e.g. sperm). These different epigenet...

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Autores principales: Ben Maamar, Millissia, Sadler-Riggleman, Ingrid, Beck, Daniel, McBirney, Margaux, Nilsson, Eric, Klukovich, Rachel, Xie, Yeming, Tang, Chong, Yan, Wei, Skinner, Michael K
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5920293/
https://www.ncbi.nlm.nih.gov/pubmed/29732173
http://dx.doi.org/10.1093/eep/dvy010
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author Ben Maamar, Millissia
Sadler-Riggleman, Ingrid
Beck, Daniel
McBirney, Margaux
Nilsson, Eric
Klukovich, Rachel
Xie, Yeming
Tang, Chong
Yan, Wei
Skinner, Michael K
author_facet Ben Maamar, Millissia
Sadler-Riggleman, Ingrid
Beck, Daniel
McBirney, Margaux
Nilsson, Eric
Klukovich, Rachel
Xie, Yeming
Tang, Chong
Yan, Wei
Skinner, Michael K
author_sort Ben Maamar, Millissia
collection PubMed
description Epigenetic transgenerational inheritance of disease and phenotypic variation can be induced by several toxicants, such as vinclozolin. This phenomenon can involve DNA methylation, non-coding RNA (ncRNA) and histone retention, and/or modification in the germline (e.g. sperm). These different epigenetic marks are called epimutations and can transmit in part the transgenerational phenotypes. This study was designed to investigate the vinclozolin-induced concurrent alterations of a number of different epigenetic factors, including DNA methylation, ncRNA, and histone retention in rat sperm. Gestating females (F0 generation) were exposed transiently to vinclozolin during fetal gonadal development. The directly exposed F1 generation fetus, the directly exposed germline within the fetus that will generate the F2 generation, and the transgenerational F3 generation sperm were studied. DNA methylation and ncRNA were altered in each generation rat sperm with the direct exposure F1 and F2 generations being distinct from the F3 generation epimutations. Interestingly, an increased number of differential histone retention sites were found in the F3 generation vinclozolin sperm, but not in the F1 or F2 generations. All three different epimutation types were affected in the vinclozolin lineage transgenerational sperm (F3 generation). The direct exposure generations (F1 and F2) epigenetic alterations were distinct from the transgenerational sperm epimutations. The genomic features and gene pathways associated with the epimutations were investigated to help elucidate the integration of these different epigenetic processes. Our results show that the three different types of epimutations are involved and integrated in the mediation of the epigenetic transgenerational inheritance phenomenon.
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spelling pubmed-59202932018-05-04 Alterations in sperm DNA methylation, non-coding RNA expression, and histone retention mediate vinclozolin-induced epigenetic transgenerational inheritance of disease Ben Maamar, Millissia Sadler-Riggleman, Ingrid Beck, Daniel McBirney, Margaux Nilsson, Eric Klukovich, Rachel Xie, Yeming Tang, Chong Yan, Wei Skinner, Michael K Environ Epigenet Research Article Epigenetic transgenerational inheritance of disease and phenotypic variation can be induced by several toxicants, such as vinclozolin. This phenomenon can involve DNA methylation, non-coding RNA (ncRNA) and histone retention, and/or modification in the germline (e.g. sperm). These different epigenetic marks are called epimutations and can transmit in part the transgenerational phenotypes. This study was designed to investigate the vinclozolin-induced concurrent alterations of a number of different epigenetic factors, including DNA methylation, ncRNA, and histone retention in rat sperm. Gestating females (F0 generation) were exposed transiently to vinclozolin during fetal gonadal development. The directly exposed F1 generation fetus, the directly exposed germline within the fetus that will generate the F2 generation, and the transgenerational F3 generation sperm were studied. DNA methylation and ncRNA were altered in each generation rat sperm with the direct exposure F1 and F2 generations being distinct from the F3 generation epimutations. Interestingly, an increased number of differential histone retention sites were found in the F3 generation vinclozolin sperm, but not in the F1 or F2 generations. All three different epimutation types were affected in the vinclozolin lineage transgenerational sperm (F3 generation). The direct exposure generations (F1 and F2) epigenetic alterations were distinct from the transgenerational sperm epimutations. The genomic features and gene pathways associated with the epimutations were investigated to help elucidate the integration of these different epigenetic processes. Our results show that the three different types of epimutations are involved and integrated in the mediation of the epigenetic transgenerational inheritance phenomenon. Oxford University Press 2018-04-26 /pmc/articles/PMC5920293/ /pubmed/29732173 http://dx.doi.org/10.1093/eep/dvy010 Text en © The Author(s) 2018. Published by Oxford University Press. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Ben Maamar, Millissia
Sadler-Riggleman, Ingrid
Beck, Daniel
McBirney, Margaux
Nilsson, Eric
Klukovich, Rachel
Xie, Yeming
Tang, Chong
Yan, Wei
Skinner, Michael K
Alterations in sperm DNA methylation, non-coding RNA expression, and histone retention mediate vinclozolin-induced epigenetic transgenerational inheritance of disease
title Alterations in sperm DNA methylation, non-coding RNA expression, and histone retention mediate vinclozolin-induced epigenetic transgenerational inheritance of disease
title_full Alterations in sperm DNA methylation, non-coding RNA expression, and histone retention mediate vinclozolin-induced epigenetic transgenerational inheritance of disease
title_fullStr Alterations in sperm DNA methylation, non-coding RNA expression, and histone retention mediate vinclozolin-induced epigenetic transgenerational inheritance of disease
title_full_unstemmed Alterations in sperm DNA methylation, non-coding RNA expression, and histone retention mediate vinclozolin-induced epigenetic transgenerational inheritance of disease
title_short Alterations in sperm DNA methylation, non-coding RNA expression, and histone retention mediate vinclozolin-induced epigenetic transgenerational inheritance of disease
title_sort alterations in sperm dna methylation, non-coding rna expression, and histone retention mediate vinclozolin-induced epigenetic transgenerational inheritance of disease
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5920293/
https://www.ncbi.nlm.nih.gov/pubmed/29732173
http://dx.doi.org/10.1093/eep/dvy010
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