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Epigenetic homogeneity in histone methylation underlies sperm programming for embryonic transcription

Sperm contributes genetic and epigenetic information to the embryo to efficiently support development. However, the mechanism underlying such developmental competence remains elusive. Here, we investigated whether all sperm cells have a common epigenetic configuration that primes transcriptional pro...

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Autores principales: Oikawa, Mami, Simeone, Angela, Hormanseder, Eva, Teperek, Marta, Gaggioli, Vincent, O’Doherty, Alan, Falk, Emma, Sporniak, Matthieu, D’Santos, Clive, Franklin, Valar Nila Roamio, Kishore, Kamal, Bradshaw, Charles R., Keane, Declan, Freour, Thomas, David, Laurent, Grzybowski, Adrian T., Ruthenburg, Alexander J., Gurdon, John, Jullien, Jerome
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7359334/
https://www.ncbi.nlm.nih.gov/pubmed/32661239
http://dx.doi.org/10.1038/s41467-020-17238-w
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author Oikawa, Mami
Simeone, Angela
Hormanseder, Eva
Teperek, Marta
Gaggioli, Vincent
O’Doherty, Alan
Falk, Emma
Sporniak, Matthieu
D’Santos, Clive
Franklin, Valar Nila Roamio
Kishore, Kamal
Bradshaw, Charles R.
Keane, Declan
Freour, Thomas
David, Laurent
Grzybowski, Adrian T.
Ruthenburg, Alexander J.
Gurdon, John
Jullien, Jerome
author_facet Oikawa, Mami
Simeone, Angela
Hormanseder, Eva
Teperek, Marta
Gaggioli, Vincent
O’Doherty, Alan
Falk, Emma
Sporniak, Matthieu
D’Santos, Clive
Franklin, Valar Nila Roamio
Kishore, Kamal
Bradshaw, Charles R.
Keane, Declan
Freour, Thomas
David, Laurent
Grzybowski, Adrian T.
Ruthenburg, Alexander J.
Gurdon, John
Jullien, Jerome
author_sort Oikawa, Mami
collection PubMed
description Sperm contributes genetic and epigenetic information to the embryo to efficiently support development. However, the mechanism underlying such developmental competence remains elusive. Here, we investigated whether all sperm cells have a common epigenetic configuration that primes transcriptional program for embryonic development. Using calibrated ChIP-seq, we show that remodelling of histones during spermiogenesis results in the retention of methylated histone H3 at the same genomic location in most sperm cell. This homogeneously methylated fraction of histone H3 in the sperm genome is maintained during early embryonic replication. Such methylated histone fraction resisting post-fertilisation reprogramming marks developmental genes whose expression is perturbed upon experimental reduction of histone methylation. A similar homogeneously methylated histone H3 fraction is detected in human sperm. Altogether, we uncover a conserved mechanism of paternal epigenetic information transmission to the embryo through the homogeneous retention of methylated histone in a sperm cells population.
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spelling pubmed-73593342020-07-20 Epigenetic homogeneity in histone methylation underlies sperm programming for embryonic transcription Oikawa, Mami Simeone, Angela Hormanseder, Eva Teperek, Marta Gaggioli, Vincent O’Doherty, Alan Falk, Emma Sporniak, Matthieu D’Santos, Clive Franklin, Valar Nila Roamio Kishore, Kamal Bradshaw, Charles R. Keane, Declan Freour, Thomas David, Laurent Grzybowski, Adrian T. Ruthenburg, Alexander J. Gurdon, John Jullien, Jerome Nat Commun Article Sperm contributes genetic and epigenetic information to the embryo to efficiently support development. However, the mechanism underlying such developmental competence remains elusive. Here, we investigated whether all sperm cells have a common epigenetic configuration that primes transcriptional program for embryonic development. Using calibrated ChIP-seq, we show that remodelling of histones during spermiogenesis results in the retention of methylated histone H3 at the same genomic location in most sperm cell. This homogeneously methylated fraction of histone H3 in the sperm genome is maintained during early embryonic replication. Such methylated histone fraction resisting post-fertilisation reprogramming marks developmental genes whose expression is perturbed upon experimental reduction of histone methylation. A similar homogeneously methylated histone H3 fraction is detected in human sperm. Altogether, we uncover a conserved mechanism of paternal epigenetic information transmission to the embryo through the homogeneous retention of methylated histone in a sperm cells population. Nature Publishing Group UK 2020-07-13 /pmc/articles/PMC7359334/ /pubmed/32661239 http://dx.doi.org/10.1038/s41467-020-17238-w Text en © The Author(s) 2020 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Oikawa, Mami
Simeone, Angela
Hormanseder, Eva
Teperek, Marta
Gaggioli, Vincent
O’Doherty, Alan
Falk, Emma
Sporniak, Matthieu
D’Santos, Clive
Franklin, Valar Nila Roamio
Kishore, Kamal
Bradshaw, Charles R.
Keane, Declan
Freour, Thomas
David, Laurent
Grzybowski, Adrian T.
Ruthenburg, Alexander J.
Gurdon, John
Jullien, Jerome
Epigenetic homogeneity in histone methylation underlies sperm programming for embryonic transcription
title Epigenetic homogeneity in histone methylation underlies sperm programming for embryonic transcription
title_full Epigenetic homogeneity in histone methylation underlies sperm programming for embryonic transcription
title_fullStr Epigenetic homogeneity in histone methylation underlies sperm programming for embryonic transcription
title_full_unstemmed Epigenetic homogeneity in histone methylation underlies sperm programming for embryonic transcription
title_short Epigenetic homogeneity in histone methylation underlies sperm programming for embryonic transcription
title_sort epigenetic homogeneity in histone methylation underlies sperm programming for embryonic transcription
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7359334/
https://www.ncbi.nlm.nih.gov/pubmed/32661239
http://dx.doi.org/10.1038/s41467-020-17238-w
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