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J. Biol. Chem., Vol. 281, Issue 39, 29064-29075, September 29, 2006

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Polycomb Complexes and the Propagation of the Methylation Mark at the Drosophila Ubx Gene^*

Tatyana G. Kahn¹, Yuri B. Schwartz¹, Gaetano I. Dellino², and Vincenzo Pirrotta³

From the Department of Molecular Biology and Biochemistry, Rutgers University, Piscataway, New Jersey 08854 and the Department of Zoology, University of Geneva, CH-1211 Geneva, Switzerland

Polycomb group proteins are transcriptional repressors that control many developmental genes. The Polycomb group protein Enhancer of Zeste has been shown in vitro to methylate specifically lysine 27 and lysine 9 of histone H3 but the role of this modification in Polycomb silencing is unknown. We show that H3 trimethylated at lysine 27 is found on the entire Ubx gene silenced by Polycomb. However, Enhancer of Zeste and other Polycomb group proteins stay primarily localized at their response elements, which appear to be the least methylated parts of the silenced gene. Our results suggest that, contrary to the prevailing view, the Polycomb group proteins and methyltransferase complexes are recruited to the Polycomb response elements independently of histone methylation and then loop over to scan the entire region, methylating all accessible nucleosomes. We propose that the Polycomb chromodomain is required for the looping mechanism that spreads methylation over a broad domain, which in turn is required for the stability of the Polycomb group protein complex. Both the spread of methylation from the Polycomb response elements, and the silencing effect can be blocked by the gypsy insulator.

Received for publication, June 6, 2006 , and in revised form, July 28, 2006.

The hybridization data were deposited to ArrayExpress data base with accession number: E-MEXP-535.

^* This work was supported in part by grants from the Human Frontiers Science Program, from the Swiss National Science Foundation and from the Frontiers in Genetics Pôle de Recherche National of the Swiss National Science Foundation (to V. P.). 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 Table S1 and Figs. S1 and S2.

¹ These authors contributed equally to the work.

² Present address: Dept. of Experimental Oncology, European Institute of Oncology, Via Ripamonti, 435 20141, Milano, Italy.

³ To whom correspondence should be addressed: Rutgers University, Dept. of Molecular Biology and Biochemistry, Nelson Laboratories, 604 Allison Rd., Piscataway, NJ 08854. Tel.: 732-445-2446; Fax: 732-445-2447; E-mail: pirrotta{at}biology.rutgers.edu.

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