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J. Biol. Chem., Vol. 279, Issue 46, 48329-48341, November 12, 2004

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TIF1, a Novel HP1-interacting Member of the Transcriptional Intermediary Factor 1 (TIF1) Family Expressed by Elongating Spermatids^*

Konstantin Khetchoumian, Marius Teletin¶, Manuel Mark¶, Thierry Lerouge, Margarita Cerviño, Mustapha Oulad-Abdelghani, Pierre Chambon¶, and Régine Losson||

From the Institut de Génétique et de Biologie Moléculaire et Cellulaire, CNRS/INSERM/ULP/Collège de France and ^¶Institut Clinique de la Souris, BP 10142, 67 404 Illkirch-Cedex, France

TIF1 (transcriptional intermediary factor 1) proteins are encoded by an expanding family of developmental and physiological control genes that are conserved from flies to man. These proteins are characterized by an N-terminal RING-B box-coiled-coil (RBCC) motif and a C-terminal PHD finger/bromodomain unit, and have been implicated in epigenetic mechanisms of transcriptional repression involving histone modifiers and heterochromatin-binding proteins. We describe here the isolation and functional characterization of a fourth murine TIF1 gene, TIF1. The predicted TIF1 protein displays all the structural hallmarks of a bona fide TIF1 family member and resembles the other TIF1s in that it can exert a deacetylase-dependent silencing effect when tethered to a promoter region. Moreover, like TIF1 and TIF1, TIF1 can homodimerize and contains a PXVXL motif necessary and sufficient for HP1 (heterochromatin protein 1) binding. Although TIF1 and TIF1 also bind nuclear receptors and Krüppel-associated boxes specifically and respectively, TIF1 appears to lack nuclear receptor- and Krüppel-associated box binding activity. Furthermore, TIF1 is unique among the TIF1 family proteins in that its expression is largely restricted to the testis and confined to haploid elongating spermatids, where it associates preferentially with HP1 isotype (HP1) and forms discrete foci dispersed within the centromeric chromocenter and the surrounding nucleoplasm. Collectively, these data are consistent with specific, nonredundant functions for the TIF1 family members in vivo and suggest a role for TIF1 in heterochromatin-mediated gene silencing during postmeiotic phases of spermatogenesis.

Received for publication, April 29, 2004 , and in revised form, August 16, 2004.

^* This work was supported in part by the CNRS, the INSERM, les Hôpitaux Universitaires de Strasbourg, the Association pour la Recherche sur le Cancer, the Collège de France, and the Fondation pour la Recherche Médicale. 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.

Supported by the Ligue Nationale Contre le Cancer.

^|| To whom correspondence should be addressed. Tel.: 33-3-88-65-34-71; Fax: 33-3-88-65-32-01; E-mail: losson{at}igbmc.u-strasbg.fr.

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