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Mol Cell. 2019 Jul 11;75(1):154-171.e5. doi: 10.1016/j.molcel.2019.04.014. Epub 2019 May 2.

Maintenance of CTCF- and Transcription Factor-Mediated Interactions from the Gametes to the Early Mouse Embryo.

Author information

1
Department of Biology, Emory University, 1510 Clifton Rd. NE, Atlanta, GA 30322, USA.
2
Yerkes National Primate Research Center, 954 Gatewood Rd. NE, Atlanta, GA 39329, USA; Department of Human Genetics, Emory University School of Medicine, 615 Michael St., Atlanta, GA 30322, USA.
3
Yerkes National Primate Research Center, 954 Gatewood Rd. NE, Atlanta, GA 39329, USA; Department of Human Genetics, Emory University School of Medicine, 615 Michael St., Atlanta, GA 30322, USA; Genetics and Molecular Biology Program, Graduate Division of Biological and Biomedical Sciences, 1462 Clifton Rd., Atlanta, GA 30322, USA.
4
Department of Biology, Emory University, 1510 Clifton Rd. NE, Atlanta, GA 30322, USA; Genetics and Molecular Biology Program, Graduate Division of Biological and Biomedical Sciences, 1462 Clifton Rd., Atlanta, GA 30322, USA.
5
Department of Biology, Emory University, 1510 Clifton Rd. NE, Atlanta, GA 30322, USA; Genetics and Molecular Biology Program, Graduate Division of Biological and Biomedical Sciences, 1462 Clifton Rd., Atlanta, GA 30322, USA. Electronic address: vgcorces@gmail.com.

Abstract

The epigenetic information present in mammalian gametes and whether it is transmitted to the progeny are relatively unknown. We find that many promoters in mouse sperm are occupied by RNA polymerase II (Pol II) and Mediator. The same promoters are accessible in GV and MII oocytes and preimplantation embryos. Sperm distal ATAC-seq sites containing motifs for various transcription factors are conserved in monkeys and humans. ChIP-seq analyses confirm that Foxa1, ERα, and AR occupy distal enhancers in sperm. Accessible sperm enhancers containing H3.3 and H2A.Z are also accessible in oocytes and preimplantation embryos. Furthermore, their interactions with promoters in the gametes persist during early development. Sperm- or oocyte-specific interactions mediated by CTCF and cohesin are only present in the paternal or maternal chromosomes, respectively, in the zygote and 2-cell stages. These interactions converge in both chromosomes by the 8-cell stage. Thus, mammalian gametes contain complex patterns of 3D interactions that can be transmitted to the zygote after fertilization.

KEYWORDS:

Foxa1; androgen; chromatin; development; enhancer; estrogen; fertilization; oocyte; sperm; transcription

PMID:
31056445
PMCID:
PMC6625867
[Available on 2020-07-11]
DOI:
10.1016/j.molcel.2019.04.014

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