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J. Biol. Chem., Vol. 283, Issue 27, 18905-18915, July 4, 2008

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Polycomb Group Protein-associated Chromatin Is Reproduced in Post-mitotic G₁ Phase and Is Required for S Phase Progression^*

From the Department of Regeneration Medicine, Institute of Molecular Embryology and Genetics, Kumamoto University, 2-2-1 Honjo, Kumamoto 860-0811, Japan

Polycomb group (PcG) proteins form two distinct complexes, PRC1 and PRC2, to regulate developmental target genes by maintaining the epigenetic state in cells. PRC2 methylates histone H3 at lysine 27 (H3K27), and PRC1 then recognizes methyl-H3K27 to form repressive chromatin. However, it remains unknown how PcG proteins maintain stable and plastic chromatin during cell division. Here we report that PcG-associated chromatin is reproduced in the G₁ phase in post-mitotic cells and is required for subsequent S phase progression. In dividing cells, H3K27 trimethylation (H3K27Me³) marked mitotic chromosome arms where PRC2 (Suz12 and Ezh2) co-existed, whereas PRC1 (Bmi1 and Pc2) appeared in distinct foci in the pericentromeric regions. As each PRC complex was increasingly assembled from mitosis to G₁ phase, PRC1 formed H3K27Me³-based chromatin intensively during middle and late G₁ phase; this chromatin was highly resistant to in situ nuclease treatment. Thus, the transition from mitosis to G₁ phase is crucial for PcG-mediated chromatin inheritance. Knockdown of Suz12 markedly reduced the amount of H3K27Me³ on mitotic chromosomes, and as a consequence, PRC1 foci were not fully transmitted to post-mitotic daughter cells. S phase progression was markedly delayed in these Suz12-knockdown cells. The fact that PcG-associated chromatin is reproduced during post-mitotic G₁ phase suggests the possibility that PcG proteins enable their target chromatin to be remodeled in response to stimuli in the G₁ phase.

Received for publication, November 13, 2007 , and in revised form, April 8, 2008.

^* This work was supported in part by a grant-in-aid for scientific research on priority areas (to M. N. and N. S.) and by the Global COE Program (Cell Fate Regulation Research and Education Unit) from the Ministry of Education, Culture, Sports, Science and Technology, Japan. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Tables 1 and 2, Figs. 1–7, and additional references.

¹ COE Junior Research Associate of the 21st Century Center of Excellence.

² To whom correspondence may be addressed. Tel.: 81-96-373-6802; Fax: 81-96-373-6804; E-mail: norikos{at}kumamoto-u.ac.jp. ³ To whom correspondence may be addressed. Tel.: 81-96-373-6800; Fax: 81-96-373-6804; E-mail: mnakao{at}gpo.kumamoto-u.ac.jp.

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