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First published online 21 April 2004
doi: 10.1242/dev.01116
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Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Chiba 277-8562, Japan
Author for correspondence (e-mail:
aokif{at}k.u-tokyo.ac.jp)
Accepted 3 February 2004
Epigenetic modifications of the genome, such as covalent modification of
histone residues, ensure appropriate gene activation during pre-implantation
development, and are probably involved in the asymmetric reprogramming of the
parental genomes after fertilization. We investigated the methylation patterns
of histone H3 at lysine 9 (H3/K9), and the regulatory mechanism involved in
the asymmetric remodeling of parental genomes during early preimplantation
development in mice. Immunocytochemistry with an antibody that specifically
recognizes methylated H3/K9 showed a very weak or absent methylation signal in
the male pronucleus, whereas a distinct methylation signal was detected in the
female pronucleus. This asymmetric H3/K9 methylation pattern in the different
parental genomes persisted until the two-cell stage. However, de novo
methylation of H3/K9 occurred and the asymmetry was lost during the four-cell
stage. The unmethylated male pronucleus underwent de novo methylation when it
was transferred into enucleated GV- or MII-stage oocytes, which suggests that
histone H3 methylase is active before fertilization, but not afterwards, and
that the asymmetric methylation pattern is generated by this change in
methylase activity in the cytoplasm after fertilization. Thus, histone H3 is
methylated only in the maternal chromosomes, which are present in the oocytes
before fertilization, and is not methylated in the paternal chromosomes, which
are absent. The maintenance of asymmetric H3/K9 methylation patterns in early
embryos is an active process that depends on protein synthesis and zygotic
transcription, as de novo methylation in the male pronucleus occurred when
either protein synthesis or gene expression was inhibited by cycloheximide or
-amanitin, respectively. In addition, corresponding de novo methylation
of H3/K9 and DNA occurred when the male pronucleus was transferred to an
enucleated GV oocyte. Our results suggest that H3/K9 methylation is an
epigenetic marker of parental genome origin during early preimplantation
development.
Key words: Embryo, Oocyte, Histone H3, Lysine 9, Methylation, Nuclear transfer
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