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Changes in histone acetylation during mouse oocyte meiosis.

Kim JM, Liu H, Tazaki M, Nagata M, Aoki F - J. Cell Biol. (2003)

Bottom Line: When the somatic cell nuclei were transferred into enucleated oocytes, the acetylation of lysines decreased markedly.Meiosis-specific deacetylation may be a consequence of the accessibility of HDAC1 to the chromosome, because HDAC1 colocalized with the chromosome during meiosis but not during mitosis.As histone acetylation is thought to play a role in propagating the gene expression pattern to the descendent generation during mitosis, and the gene expression pattern of differentiated oocytes is reprogrammed during meiosis to allow the initiation of a new program by totipotent zygotes of the next generation, our results suggest that the oocyte cytoplasm initializes a program of gene expression by deacetylating histones.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Chiba 277-8562, Japan. aokif@k.u-tokyo.ac.jp

ABSTRACT
We examined global changes in the acetylation of histones in mouse oocytes during meiosis. Immunocytochemistry with specific antibodies against various acetylated lysine residues on histones H3 and H4 showed that acetylation of all the lysines decreased to undetectable or negligible levels in the oocytes during meiosis, whereas most of these lysines were acetylated during mitosis in preimplantation embryos and somatic cells. When the somatic cell nuclei were transferred into enucleated oocytes, the acetylation of lysines decreased markedly. This type of deacetylation was inhibited by trichostatin A, a specific inhibitor of histone deacetylase (HDAC), thereby indicating that HDAC is able to deacetylate histones during meiosis but not during mitosis. Meiosis-specific deacetylation may be a consequence of the accessibility of HDAC1 to the chromosome, because HDAC1 colocalized with the chromosome during meiosis but not during mitosis. As histone acetylation is thought to play a role in propagating the gene expression pattern to the descendent generation during mitosis, and the gene expression pattern of differentiated oocytes is reprogrammed during meiosis to allow the initiation of a new program by totipotent zygotes of the next generation, our results suggest that the oocyte cytoplasm initializes a program of gene expression by deacetylating histones.

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In situ analysis of the histone acetyltransferase and deacetylase in oocytes during the first meiosis. Oocytes in the first meiosis were immunostained with the anti–acetyl histone H4/lysine 12 (H4/K12) antibody. The GV-stage oocytes (A) were cultured in vitro for 4 h to induce the first meiosis (B) and subsequently cultured for 3 h with TSA (D) or without TSA (C). Oocytes that were undergoing the first meiosis after in vitro culture for 4 h in TSA (E) were either washed free of TSA and cultured for a further 3 h (G), or cultured continuously in TSA for 3 h (F). Each sample was counterstained with DAPI. The results of analysis for histone H3/lysine 14 are shown in Fig. S6, available at http://www.jcb.org/cgi/content/full/jcb.200303047/DC1.
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fig4: In situ analysis of the histone acetyltransferase and deacetylase in oocytes during the first meiosis. Oocytes in the first meiosis were immunostained with the anti–acetyl histone H4/lysine 12 (H4/K12) antibody. The GV-stage oocytes (A) were cultured in vitro for 4 h to induce the first meiosis (B) and subsequently cultured for 3 h with TSA (D) or without TSA (C). Oocytes that were undergoing the first meiosis after in vitro culture for 4 h in TSA (E) were either washed free of TSA and cultured for a further 3 h (G), or cultured continuously in TSA for 3 h (F). Each sample was counterstained with DAPI. The results of analysis for histone H3/lysine 14 are shown in Fig. S6, available at http://www.jcb.org/cgi/content/full/jcb.200303047/DC1.

Mentions: In situ analysis of the histone acetyltransferase and deacetylase in MII-stage oocytes. Oocytes at the GV and MII stages were immunostained with the anti–acetyl histone H4/lysine 12 (H4/K12) antibody. The GV-stage oocytes (A) were cultured in vitro for 14 h to mature into the MII stage (B) and were subsequently cultured for 3 h with TSA (D) or without TSA (C). The oocytes were matured in vitro for 14 h in TSA (E), and either washed to remove the TSA followed by culturing for 3 h (G), or cultured continuously in TSA for 3 h (F). Each sample was counterstained with DAPI to visualize the DNA. The results of analysis for histone H3/lysine 14 are shown in Fig. S5, available at http://www.jcb.org/cgi/content/full/jcb.200303047/DC1.


Changes in histone acetylation during mouse oocyte meiosis.

Kim JM, Liu H, Tazaki M, Nagata M, Aoki F - J. Cell Biol. (2003)

In situ analysis of the histone acetyltransferase and deacetylase in oocytes during the first meiosis. Oocytes in the first meiosis were immunostained with the anti–acetyl histone H4/lysine 12 (H4/K12) antibody. The GV-stage oocytes (A) were cultured in vitro for 4 h to induce the first meiosis (B) and subsequently cultured for 3 h with TSA (D) or without TSA (C). Oocytes that were undergoing the first meiosis after in vitro culture for 4 h in TSA (E) were either washed free of TSA and cultured for a further 3 h (G), or cultured continuously in TSA for 3 h (F). Each sample was counterstained with DAPI. The results of analysis for histone H3/lysine 14 are shown in Fig. S6, available at http://www.jcb.org/cgi/content/full/jcb.200303047/DC1.
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Related In: Results  -  Collection

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fig4: In situ analysis of the histone acetyltransferase and deacetylase in oocytes during the first meiosis. Oocytes in the first meiosis were immunostained with the anti–acetyl histone H4/lysine 12 (H4/K12) antibody. The GV-stage oocytes (A) were cultured in vitro for 4 h to induce the first meiosis (B) and subsequently cultured for 3 h with TSA (D) or without TSA (C). Oocytes that were undergoing the first meiosis after in vitro culture for 4 h in TSA (E) were either washed free of TSA and cultured for a further 3 h (G), or cultured continuously in TSA for 3 h (F). Each sample was counterstained with DAPI. The results of analysis for histone H3/lysine 14 are shown in Fig. S6, available at http://www.jcb.org/cgi/content/full/jcb.200303047/DC1.
Mentions: In situ analysis of the histone acetyltransferase and deacetylase in MII-stage oocytes. Oocytes at the GV and MII stages were immunostained with the anti–acetyl histone H4/lysine 12 (H4/K12) antibody. The GV-stage oocytes (A) were cultured in vitro for 14 h to mature into the MII stage (B) and were subsequently cultured for 3 h with TSA (D) or without TSA (C). The oocytes were matured in vitro for 14 h in TSA (E), and either washed to remove the TSA followed by culturing for 3 h (G), or cultured continuously in TSA for 3 h (F). Each sample was counterstained with DAPI to visualize the DNA. The results of analysis for histone H3/lysine 14 are shown in Fig. S5, available at http://www.jcb.org/cgi/content/full/jcb.200303047/DC1.

Bottom Line: When the somatic cell nuclei were transferred into enucleated oocytes, the acetylation of lysines decreased markedly.Meiosis-specific deacetylation may be a consequence of the accessibility of HDAC1 to the chromosome, because HDAC1 colocalized with the chromosome during meiosis but not during mitosis.As histone acetylation is thought to play a role in propagating the gene expression pattern to the descendent generation during mitosis, and the gene expression pattern of differentiated oocytes is reprogrammed during meiosis to allow the initiation of a new program by totipotent zygotes of the next generation, our results suggest that the oocyte cytoplasm initializes a program of gene expression by deacetylating histones.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Chiba 277-8562, Japan. aokif@k.u-tokyo.ac.jp

ABSTRACT
We examined global changes in the acetylation of histones in mouse oocytes during meiosis. Immunocytochemistry with specific antibodies against various acetylated lysine residues on histones H3 and H4 showed that acetylation of all the lysines decreased to undetectable or negligible levels in the oocytes during meiosis, whereas most of these lysines were acetylated during mitosis in preimplantation embryos and somatic cells. When the somatic cell nuclei were transferred into enucleated oocytes, the acetylation of lysines decreased markedly. This type of deacetylation was inhibited by trichostatin A, a specific inhibitor of histone deacetylase (HDAC), thereby indicating that HDAC is able to deacetylate histones during meiosis but not during mitosis. Meiosis-specific deacetylation may be a consequence of the accessibility of HDAC1 to the chromosome, because HDAC1 colocalized with the chromosome during meiosis but not during mitosis. As histone acetylation is thought to play a role in propagating the gene expression pattern to the descendent generation during mitosis, and the gene expression pattern of differentiated oocytes is reprogrammed during meiosis to allow the initiation of a new program by totipotent zygotes of the next generation, our results suggest that the oocyte cytoplasm initializes a program of gene expression by deacetylating histones.

Show MeSH