Epigenetic homogeneity in histone methylation underlies sperm programming for embryonic transcription

Mami Oikawa, Angela Simeone, Eva Hormanseder, Marta Teperek, Vincent Gaggioli, Alan O’Doherty, Emma Falk, Matthieu Sporniak, Clive D’Santos, Valar Nila Roamio Franklin, Kamal Kishore, Charles R. Bradshaw, Declan Keane, Thomas Freour, Laurent David, Adrian T. Grzybowski, Alexander J. Ruthenburg, John Gurdon and Jerome Jullien ()
Additional contact information
Mami Oikawa: Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge
Angela Simeone: Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge
Eva Hormanseder: Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge
Marta Teperek: Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge
Vincent Gaggioli: Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge
Alan O’Doherty: University College Dublin
Emma Falk: CRTI, INSERM, UNIV Nantes
Matthieu Sporniak: CRTI, INSERM, UNIV Nantes
Clive D’Santos: Cancer Research UK Cambridge Institute, University of Cambridge
Valar Nila Roamio Franklin: Cancer Research UK Cambridge Institute, University of Cambridge
Kamal Kishore: Cancer Research UK Cambridge Institute, University of Cambridge
Charles R. Bradshaw: Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge
Declan Keane: ReproMed Ireland
Thomas Freour: Service de Biologie de la Reproduction, CHU Nantes
Laurent David: CRTI, INSERM, UNIV Nantes
Adrian T. Grzybowski: The University of Chicago
Alexander J. Ruthenburg: The University of Chicago
John Gurdon: Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge
Jerome Jullien: Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge

Nature Communications, 2020, vol. 11, issue 1, 1-16

Abstract: Abstract 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.

Date: 2020
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DOI: 10.1038/s41467-020-17238-w

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