Imprinted X chromosome inactivation in marsupials: The paternal X arrives at the egg with a silent DNA methylation profile.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
03 Sep 2024
Historique:
medline: 27 8 2024
pubmed: 27 8 2024
entrez: 27 8 2024
Statut: ppublish

Résumé

X chromosome inactivation (XCI) is an epigenetic process that results in the transcriptional silencing of one X chromosome in the somatic cells of females. This phenomenon is common to both eutherian and marsupial mammals, but there are fundamental differences. In eutherians, the X chosen for silencing is random. DNA methylation on the eutherian inactive X is high at transcription start sites (TSSs) and their flanking regions, resulting in universally high DNA methylation. This contrasts XCI in marsupials where the paternally derived X is always silenced, and in which DNA methylation is low at TSSs and flanking regions. Here, we examined the DNA methylation status of the tammar wallaby X chromosome during spermatogenesis to determine the DNA methylation profile of the paternal X prior to and at fertilization. Whole genome enzymatic methylation sequencing was carried out on enriched flow-sorted populations of premeiotic, meiotic, and postmeiotic cells. We observed that the X displayed a pattern of DNA methylation from spermatogonia to mature sperm that reflected the inactive X in female somatic tissue. Therefore, the paternal X chromosome arrives at the egg with a DNA methylation profile that reflects the transcriptionally silent X in adult female somatic tissue. We present this epigenetic signature as a candidate for the long sought-after imprint for paternal XCI in marsupials.

Identifiants

pubmed: 39190362
doi: 10.1073/pnas.2412185121
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2412185121

Subventions

Organisme : Australian Research Council
ID : DP210103512
Organisme : Australian Research Council
ID : DP220101429
Organisme : National Health and Medical Research Council
ID : 2021172
Organisme : Spanish Ministry of Science and Innovation
ID : PID2020-112557 GB-I00
Organisme : Agencia de Gestio d'Ajuts Universitaris i de Recerca
ID : 2021SGR00122

Déclaration de conflit d'intérêts

Competing interests statement:The authors declare no competing interest.

Auteurs

Ashley M Milton (AM)

School of Biotechnology and Biomolecular Sciences, Faculty of Science, The University of New South Wales, Sydney, NSW 2052, Australia.

Laia Marín-Gual (L)

Departament de Biologia Cellular, Fisiologia i Immunologia, Universitat Autònoma de Barcelona, Cerdanyola del Vallès 08193, Spain.
Genome Integrity and Instability Group, Institut de Biotecnologia i Biomedicina, Universitat Autònoma de Barcelona, Cerdanyola del Vallès 08193, Spain.

Nicholas C Lister (NC)

School of Biotechnology and Biomolecular Sciences, Faculty of Science, The University of New South Wales, Sydney, NSW 2052, Australia.

Kim L McIntyre (KL)

School of Biotechnology and Biomolecular Sciences, Faculty of Science, The University of New South Wales, Sydney, NSW 2052, Australia.

Patrick G S Grady (PGS)

Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269.
Institute for Systems Genomics, University of Connecticut, Storrs, CT 06269.

Melanie K Laird (MK)

Department of Anatomy, University of Otago, Dunedin 9016, New Zealand.

Donna M Bond (DM)

Department of Anatomy, University of Otago, Dunedin 9016, New Zealand.

Timothy A Hore (TA)

Department of Anatomy, University of Otago, Dunedin 9016, New Zealand.

Rachel J O'Neill (RJ)

Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269.
Institute for Systems Genomics, University of Connecticut, Storrs, CT 06269.

Andrew J Pask (AJ)

School of BioSciences, The University of Melbourne, Parkville, VIC 3010, Australia.

Marilyn B Renfree (MB)

School of BioSciences, The University of Melbourne, Parkville, VIC 3010, Australia.

Aurora Ruiz-Herrera (A)

Departament de Biologia Cellular, Fisiologia i Immunologia, Universitat Autònoma de Barcelona, Cerdanyola del Vallès 08193, Spain.
Genome Integrity and Instability Group, Institut de Biotecnologia i Biomedicina, Universitat Autònoma de Barcelona, Cerdanyola del Vallès 08193, Spain.

Paul D Waters (PD)

School of Biotechnology and Biomolecular Sciences, Faculty of Science, The University of New South Wales, Sydney, NSW 2052, Australia.

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Classifications MeSH