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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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Localization of HDAC1 during meiosis and mitosis. The GV-stage oocytes (GV), oocytes that were incubated for 3 h in IBMX-free medium (GVBD 3 h), and NIH 3T3 cells at interphase (NIH [I]), natural mitotic phase (NIH [M] noco [−]), or nocodazole-arrested mitotic phase (NIH [M] noco [+]) were immunostained with the antibody against HDAC1 (top) and costained with DAPI (middle). The bottom row shows the merged images from the top and middle rows.
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fig6: Localization of HDAC1 during meiosis and mitosis. The GV-stage oocytes (GV), oocytes that were incubated for 3 h in IBMX-free medium (GVBD 3 h), and NIH 3T3 cells at interphase (NIH [I]), natural mitotic phase (NIH [M] noco [−]), or nocodazole-arrested mitotic phase (NIH [M] noco [+]) were immunostained with the antibody against HDAC1 (top) and costained with DAPI (middle). The bottom row shows the merged images from the top and middle rows.

Mentions: Therefore, we examined the localization of HDAC1 in oocytes during meiosis to investigate the potential involvement of HDAC1 in histone deacetylation. The NIH 3T3 cells were immunostained with the anti-HDAC1 antibody and costained with DAPI. HDAC1 was detected in the interphase nuclei, although no HDAC1 was detected in the mitotic chromosomes (Fig. 6)Figure 6.


Changes in histone acetylation during mouse oocyte meiosis.

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

Localization of HDAC1 during meiosis and mitosis. The GV-stage oocytes (GV), oocytes that were incubated for 3 h in IBMX-free medium (GVBD 3 h), and NIH 3T3 cells at interphase (NIH [I]), natural mitotic phase (NIH [M] noco [−]), or nocodazole-arrested mitotic phase (NIH [M] noco [+]) were immunostained with the antibody against HDAC1 (top) and costained with DAPI (middle). The bottom row shows the merged images from the top and middle rows.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2172711&req=5

fig6: Localization of HDAC1 during meiosis and mitosis. The GV-stage oocytes (GV), oocytes that were incubated for 3 h in IBMX-free medium (GVBD 3 h), and NIH 3T3 cells at interphase (NIH [I]), natural mitotic phase (NIH [M] noco [−]), or nocodazole-arrested mitotic phase (NIH [M] noco [+]) were immunostained with the antibody against HDAC1 (top) and costained with DAPI (middle). The bottom row shows the merged images from the top and middle rows.
Mentions: Therefore, we examined the localization of HDAC1 in oocytes during meiosis to investigate the potential involvement of HDAC1 in histone deacetylation. The NIH 3T3 cells were immunostained with the anti-HDAC1 antibody and costained with DAPI. HDAC1 was detected in the interphase nuclei, although no HDAC1 was detected in the mitotic chromosomes (Fig. 6)Figure 6.

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