Dynamic replacement of histone H3 variants reprograms epigenetic marks in early mouse embryos

Tomohiko Akiyama, Osamu Suzuki, Junichiro Matsuda, Fugaku Aoki

Research output: Contribution to journalArticle

83 Citations (Scopus)

Abstract

Upon fertilization, reprogramming of gene expression is required for embryo development. This step is marked by DNA demethylation and changes in histone variant composition. However, little is known about the molecular mechanisms causing these changes and their impact on histone modifications. We examined the global deposition of the DNA replication-dependent histone H3.1 and H3.2 variants and the DNA replication-independent H3.3 variant after fertilization in mice. We showed that H3.3, a euchromatic marker of gene activity, transiently disappears from the maternal genome, suggesting erasure of the oocyte-specific modifications carried by H3.3. After fertilization, H3.2 is incorporated into the transcriptionally silent heterochromatin, whereas H3.1 and H3.3 occupy unusual heterochromatic and euchromatin locations, respectively. After the two-cell stage, H3.1 and H3.3 variants resume their usual respective locations on heterochromatin and euchromatin. Preventing the incorporation of H3.1 and H3.2 by knockdown of the histone chaperone CAF-1 induces a reciprocal increase in H3.3 deposition and impairs heterochromatin formation. We propose that the deposition of different H3 variants influences the functional organization of chromatin. Taken together, these findings suggest that dynamic changes in the deposition of H3 variants are critical for chromatin reorganization during epigenetic reprogramming.

Original languageEnglish
Article numbere1002279
JournalPLoS Genetics
Volume7
Issue number10
DOIs
Publication statusPublished - 2011 Oct 1
Externally publishedYes

Fingerprint

Heterochromatin
Fertilization
Epigenomics
histones
epigenetics
Histones
Euchromatin
embryo
embryo (animal)
heterochromatin
Embryonic Structures
replacement
DNA Replication
Chromatin
mice
DNA replication
Histone Code
Histone Chaperones
DNA
chromatin

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

Dynamic replacement of histone H3 variants reprograms epigenetic marks in early mouse embryos. / Akiyama, Tomohiko; Suzuki, Osamu; Matsuda, Junichiro; Aoki, Fugaku.

In: PLoS Genetics, Vol. 7, No. 10, e1002279, 01.10.2011.

Research output: Contribution to journalArticle

Akiyama, Tomohiko ; Suzuki, Osamu ; Matsuda, Junichiro ; Aoki, Fugaku. / Dynamic replacement of histone H3 variants reprograms epigenetic marks in early mouse embryos. In: PLoS Genetics. 2011 ; Vol. 7, No. 10.
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