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J. Biol. Chem., Vol. 281, Issue 36, 25926-25939, September 8, 2006

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Interplay between Chromatin and Trans-acting Factors Regulating the Hoxd4 Promoter during Neural Differentiation^*

From the McGill Cancer Centre, McGill University, Montréal, Québec H3G 1Y6 Canada

Correct patterning of the antero-posterior axis of the embryonic trunk is dependent on spatiotemporally restricted Hox gene expression. In this study, we identified components of the Hoxd4 P1 promoter directing expression in neurally differentiating retinoic acid-treated P19 cells. We mapped three nucleosomes that are subsequently remodeled into an open chromatin state upon retinoic acid-induced Hoxd4 transcription. These nucleosomes spanned the Hoxd4 transcriptional start site in addition to a GC-rich positive regulatory element located 3' to the initiation site. We further identified two major cis-acting regulatory elements. An autoregulatory element was shown to recruit HOXD4 and its cofactor PBX1 and to positively regulate Hoxd4 expression in differentiating P19 cells. Conversely, the Polycomb group (PcG) protein Ying-Yang 1 (YY1) binds to an internucleosomal linker and represses Hoxd4 transcription before and during transcriptional activation. Sequential chromatin immunoprecipitation studies revealed that the PcG protein MEL18 was co-recruited with YY1 only in undifferentiated P19 cells, suggesting a role for MEL18 in silencing Hoxd4 transcription in undifferentiated P19 cells. This study links for the first time local chromatin remodeling events that take place during transcriptional activation with the dynamics of transcription factor association and DNA accessibility at a Hox regulatory region.

Received for publication, March 17, 2006 , and in revised form, May 8, 2006.

^* This work was supported by Grant 49498 from the Canadian Institutes of Health Research (to M. F.). 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 M. R. was supported by a CIHR Cancer Consortium Training Grant Fellowship Award from the McGill Cancer Centre, and by a Conrad F. Harrington Fellowship Award from the Faculty of Medicine, McGill University.

² A Chercheur-National of the Fonds de la Recherche en Santé du Québec. To whom correspondence should be addressed: Mark Featherstone, McGill Cancer Centre, McGill University, 3655 Promenade Sir William Osler, Montreal, QC, Canada H3G 1Y6. Tel.: 514-398-8937; Fax: 514-398-6769; E-mail: mark.featherstone{at}mcgill.ca.

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