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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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Acetylation of lysine 14 on histone H3 at interphase (I) and metaphase (M). Oocytes, preimplantation embryos, and NIH 3T3 cells were immunostained with the anti–acetyl histone H3/lysine 14 (H3/K14) antibody. GV, oocytes at the GV stage; GVBD 3 h, oocytes after a 3-h incubation without IBMX in the first meiosis; Egg, oocytes at MII; 1-cell (I), one-cell embryos at interphase; 1-cell (M), one-cell embryos at the M phase; 2-cell (I), two-cell embryos at interphase; 2-cell (M), two-cell embryos at the M phase; Blastocyst, blastocyst-stage embryos; NIH 3T3 (I), NIH 3T3 cells at interphase; NIH 3T3 (M), NIH 3T3 cells at the M phase. Arrows indicate the condensed mitotic chromosomes in the blastocysts. Each sample was counterstained with DAPI to visualize the DNA. The acetylation of lysine 9 on histone H3 is shown in Fig. S4, available at http://www.jcb.org/cgi/content/full/jcb.200303047/DC1.
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fig1: Acetylation of lysine 14 on histone H3 at interphase (I) and metaphase (M). Oocytes, preimplantation embryos, and NIH 3T3 cells were immunostained with the anti–acetyl histone H3/lysine 14 (H3/K14) antibody. GV, oocytes at the GV stage; GVBD 3 h, oocytes after a 3-h incubation without IBMX in the first meiosis; Egg, oocytes at MII; 1-cell (I), one-cell embryos at interphase; 1-cell (M), one-cell embryos at the M phase; 2-cell (I), two-cell embryos at interphase; 2-cell (M), two-cell embryos at the M phase; Blastocyst, blastocyst-stage embryos; NIH 3T3 (I), NIH 3T3 cells at interphase; NIH 3T3 (M), NIH 3T3 cells at the M phase. Arrows indicate the condensed mitotic chromosomes in the blastocysts. Each sample was counterstained with DAPI to visualize the DNA. The acetylation of lysine 9 on histone H3 is shown in Fig. S4, available at http://www.jcb.org/cgi/content/full/jcb.200303047/DC1.

Mentions: The acetylation levels of various lysine residues on histones H3 and H4 were examined in NIH 3T3 cells, mouse oocytes, and preimplantation embryos. Immunocytochemistry with specific antibodies against acetylated lysines 9 and 14 on histone H3 (Ac-H3/K9 and Ac-H3/K14) and acetylated lysines 5, 8, 12, and 16 on histone H4 (Ac-H4/K5, Ac-H4/K8, Ac-H4/K12, and Ac-H4/K16) showed intense fluorescence signals in the nuclei of the NIH 3T3 cells at interphase (Figs. 1 and 2Figure 1.


Changes in histone acetylation during mouse oocyte meiosis.

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

Acetylation of lysine 14 on histone H3 at interphase (I) and metaphase (M). Oocytes, preimplantation embryos, and NIH 3T3 cells were immunostained with the anti–acetyl histone H3/lysine 14 (H3/K14) antibody. GV, oocytes at the GV stage; GVBD 3 h, oocytes after a 3-h incubation without IBMX in the first meiosis; Egg, oocytes at MII; 1-cell (I), one-cell embryos at interphase; 1-cell (M), one-cell embryos at the M phase; 2-cell (I), two-cell embryos at interphase; 2-cell (M), two-cell embryos at the M phase; Blastocyst, blastocyst-stage embryos; NIH 3T3 (I), NIH 3T3 cells at interphase; NIH 3T3 (M), NIH 3T3 cells at the M phase. Arrows indicate the condensed mitotic chromosomes in the blastocysts. Each sample was counterstained with DAPI to visualize the DNA. The acetylation of lysine 9 on histone H3 is shown in Fig. S4, available at http://www.jcb.org/cgi/content/full/jcb.200303047/DC1.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2172711&req=5

fig1: Acetylation of lysine 14 on histone H3 at interphase (I) and metaphase (M). Oocytes, preimplantation embryos, and NIH 3T3 cells were immunostained with the anti–acetyl histone H3/lysine 14 (H3/K14) antibody. GV, oocytes at the GV stage; GVBD 3 h, oocytes after a 3-h incubation without IBMX in the first meiosis; Egg, oocytes at MII; 1-cell (I), one-cell embryos at interphase; 1-cell (M), one-cell embryos at the M phase; 2-cell (I), two-cell embryos at interphase; 2-cell (M), two-cell embryos at the M phase; Blastocyst, blastocyst-stage embryos; NIH 3T3 (I), NIH 3T3 cells at interphase; NIH 3T3 (M), NIH 3T3 cells at the M phase. Arrows indicate the condensed mitotic chromosomes in the blastocysts. Each sample was counterstained with DAPI to visualize the DNA. The acetylation of lysine 9 on histone H3 is shown in Fig. S4, available at http://www.jcb.org/cgi/content/full/jcb.200303047/DC1.
Mentions: The acetylation levels of various lysine residues on histones H3 and H4 were examined in NIH 3T3 cells, mouse oocytes, and preimplantation embryos. Immunocytochemistry with specific antibodies against acetylated lysines 9 and 14 on histone H3 (Ac-H3/K9 and Ac-H3/K14) and acetylated lysines 5, 8, 12, and 16 on histone H4 (Ac-H4/K5, Ac-H4/K8, Ac-H4/K12, and Ac-H4/K16) showed intense fluorescence signals in the nuclei of the NIH 3T3 cells at interphase (Figs. 1 and 2Figure 1.

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