Epigenetic homogeneity in histone methylation underlies sperm programming for embryonic transcription

Autor: Vincent Gaggioli, Declan Keane, Laurent David, Valar Nila Roamio Franklin, Matthieu Sporniak, Mami Oikawa, Kamal Kishore, Thomas Fréour, John B. Gurdon, Marta Teperek, Alan M. O'Doherty, Angela Simeone, Clive D'Santos, Charles R. Bradshaw, Jerome Jullien, Eva Hormanseder, Emma Falk, Adrian T. Grzybowski, Alexander J. Ruthenburg
Přispěvatelé: Teperek, Marta [0000-0001-8520-5598], O’Doherty, Alan [0000-0001-5071-6793], Falk, Emma [0000-0001-5836-3531], Sporniak, Matthieu [0000-0001-9116-522X], Bradshaw, Charles R. [0000-0002-3528-458X], Freour, Thomas [0000-0002-7243-7709], David, Laurent [0000-0003-3594-0353], Ruthenburg, Alexander J. [0000-0003-2709-4564], Apollo - University of Cambridge Repository, Kishore, Kamal [0000-0002-4650-8745], Bradshaw, Charles [0000-0002-3528-458X], Gurdon, John [0000-0002-5621-3799], Bodescot, Myriam, University of Cambridge [UK] (CAM), University College Dublin [Dublin] (UCD), Centre de Recherche en Transplantation et Immunologie (U1064 Inserm - CRTI), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Nantes - UFR de Médecine et des Techniques Médicales (UFR MEDECINE), Université de Nantes (UN)-Université de Nantes (UN), ReproMed Ireland [Dublin, Irlande], Service de Biologie de la Reproduction [Nantes], Centre hospitalier universitaire de Nantes (CHU Nantes), University of Illinois [Chicago] (UIC), University of Illinois System, J.J. is funded from a Wellcome Trust grant (101050/Z/13/Z). M.O is funded from a Wellcome Trust (101050/Z/13/Z), MRC (MR/K011022/1) grant and postdoctoral fellowship from the Japan Society for the Promotion of Science (JSPS). A.S. is funded from a Wellcome Trust (101050/Z/13/Z) and MRC (MR/K011022/1) grant. All members of the Gurdon group acknowledge the core support provided by the Gurdon Institute core grant from Cancer Research UK (C6946/A14492) and the Wellcome Trust (092096/Z/10/Z). A.O.D. is supported by a grant from the Science Foundation Ireland Industry Fellowship (SFI:15/IFB/350). C.D.S. and V.N.R.F. are supported by Cancer Research UK. The Fusion Lumos Orbitrap mass spectrometer was purchased with the support from a Wellcome Trust Multi-user Equipment Grant (Grant #108467/Z/15/Z). This study was supported by the National Institutes of Health (R01-GM115945) to A.J.R.
Rok vydání: 2020
Předmět:
0301 basic medicine
Male
Xenopus
General Physics and Astronomy
[SDV.BBM.BM] Life Sciences [q-bio]/Biochemistry
Molecular Biology/Molecular biology
Epigenesis
Genetic
Histones
13/1
0302 clinical medicine
Histone methylation
38/22
lcsh:Science
[SDV.BDD]Life Sciences [q-bio]/Development Biology
64
education.field_of_study
Multidisciplinary
biology
article
45/77
Embryo
Chromatin
Cell biology
Histone
Embryogenesis
embryonic structures
Reprogramming
animal structures
Science
Population
631/136/2086
Embryonic Development
45/23
General Biochemistry
Genetics and Molecular Biology
45/29
03 medical and health sciences
Histone H3
[SDV.BDD] Life Sciences [q-bio]/Development Biology
Animals
Epigenetics
education
Spermatogenesis
urogenital system
631/136/2434/1822
64/114
[SDV.BBM.BM]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Molecular biology
General Chemistry
DNA Methylation
45/15
Sperm
030104 developmental biology
biology.protein
lcsh:Q
030217 neurology & neurosurgery
Zdroj: Nature Communications, Vol 11, Iss 1, Pp 1-16 (2020)
Nature Communications
Nature Communications, 2020, 11 (1), pp.3491. ⟨10.1038/s41467-020-17238-w⟩
Nature Communications, Nature Publishing Group, 2020, 11 (1), pp.3491. ⟨10.1038/s41467-020-17238-w⟩
ISSN: 2041-1723
DOI: 10.1038/s41467-020-17238-w⟩
Popis: 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.
In addition to paternal genetic material, sperm contributes epigenetic information to the embryo to efficiently support development. Here, the authors demonstrate a homogeneous paternal contribution to epigenetic information via sperm-derived modified histone transmission to the developing vertebrate embryo.
Databáze: OpenAIRE
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