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J. Biol. Chem., Vol. 283, Issue 19, 13471-13481, May 9, 2008

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Unconventional Association of the Polycomb Group Proteins with Cytokine Genes in Differentiated T Helper Cells^*

From the Department of Immunology, Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 31096, Israel

The cytokine transcription profiles of developing T helper 1 and T helper 2 cells are imprinted and induced appropriately following stimulation of differentiated cells. Epigenetic regulation combines several mechanisms to ensure the inheritance of transcriptional programs. We found that the expression of the polycomb group proteins, whose role in maintaining gene silencing is well documented, was induced during development in both T helper lineages. Nevertheless, the polycomb proteins, YY1, Mel-18, Ring1A, Ezh2, and Eed, bound to the Il4 and Ifng loci in a differential pattern. In contrast to the prevailing dogma, the binding activity of the polycomb proteins in differentiated T helper cells was associated with cytokine transcription. The polycomb proteins bound to the cytokine genes under resting conditions, and their binding was induced dynamically following stimulation. The recruitment of the polycomb proteins Mel-18 and Ezh2 to the cytokine promoters was inhibited in the presence of cyclosporine A, suggesting the involvement of NFAT. Considering their binding pattern at the cytokine genes and their known function in higher order folding of regulatory elements, we propose a model whereby the polycomb proteins, in some contexts, positively regulate gene expression by mediating long-distance chromosomal interactions.

Received for publication, December 4, 2007 , and in revised form, January 22, 2008.

^* This work was supported in part by grants from the Israel Science Foundation (Grant No. 986/04), the State of Lower Saxony, the Volkswagen Foundation Hannover Germany, and the Rappaport Family Institute for Research. 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.

¹ Both authors contributed equally to this work.

² To whom correspondence should be addressed: Efron 1 St., Haifa 31096, Israel. Tel.: 972-4-829-5241; Fax: 972-4-829-5245; E-mail: oavni{at}tx.technion.ac.il.

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