Epigenetic discrimination by mouse metaphase II oocytes mediates asymmetric chromatin remodeling independently of meiotic exit

N Yoshida, M Brahmajosyula, S Shoji, M Amanai, Anthony C F Perry

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Abstract

In mammalian fertilization, paternal chromatin is exhaustively remodeled, yet the maternal contribution to this process is unknown. To address this, we prevented the induction of mciotic exit by spermatozoa and examined sperm chromatin remodeling in metaphase II (mII) oocytes. Methylation of paternal H3-K4 and H3-K9 remained low, unlike maternal H3, although paternal H3-K4 methylation increased in zygotes. Thus, mII cytoplasm can sustain epigenetic asymmetry in a cell-cycle dependent manner. Paternal genomic DNA underwent oocyte-mediated cytosine demethylation and acquired maternally-derived K12-acetylated H4 (AcH4-K12) independently of microtubule assembly and maternal chromatin. AcH4-K12 persisted without typical maturation-associated deacetylation, irrespective of paternal pan-genomic cytosine methylation. Contrastingly, somatic cell nuclei underwent rapid H4 deacetylation; sperm and somatic chromatin exhibited asymmetric AcH4-K12 dynamics simultaneously within the same mII oocyte. Inhibition of somatic histone deacetylation revealed endogenous histone acetyl transferase activity. Oocytes thus specify the histone acetylation status of given nuclei by differentially targeting histone deacetylase and acetyl transferase activities. Asymmetric H4 acetylation during and immediately after fertilization was dispensable for development when both parental chromatin sets were hyperacetylated. These studies delineate non-zygotic chromatin remodeling and suggest a powerful model with which to study de novo genomic reprogramming.
Original languageEnglish
Pages (from-to)464-477
Number of pages14
JournalDevelopmental Biology
Volume301
Issue number2
DOIs
Publication statusPublished - 2007

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Chromatin Assembly and Disassembly
Metaphase
Epigenomics
Oocytes
Histones
Methylation
Chromatin
Spermatozoa
Cytosine
Mothers
Acetylation
Transferases
Fertilization
Histone Deacetylases
Zygote
Cell Nucleus
Microtubules
Cell Cycle
Cytoplasm
DNA

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Epigenetic discrimination by mouse metaphase II oocytes mediates asymmetric chromatin remodeling independently of meiotic exit. / Yoshida, N; Brahmajosyula, M; Shoji, S; Amanai, M; Perry, Anthony C F.

In: Developmental Biology, Vol. 301, No. 2, 2007, p. 464-477.

Research output: Contribution to journalArticle

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