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Vol. 20, Issue 1, 296-305, January 1, 2009

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Disruption of the Interaction between Transcriptional Intermediary Factor 1β and Heterochromatin Protein 1 Leads to a Switch from DNA Hyper- to Hypomethylation and H3K9 to H3K27 Trimethylation on the MEST Promoter Correlating with Gene Reactivation

Raphaël Riclet^*, Mariam Chendeb^*, Jean-Luc Vonesch^*, Dirk Koczan, Hans-Juergen Thiesen, Régine Losson^*, and Florence Cammas^*

*Institut de Génétique et de Biologie Moléculaire et Cellulaire, Centre National de la Recherche Scientifique/Institut National de la Santé et de la Recherche Médicale/Université Louis Pasteur/Collège de France, 67404 Illkirch-Cedex, France; and Institute for Immunology, Medical Faculty, 18057 Rostock, Germany

Submitted May 22, 2008; Revised September 26, 2008; Accepted October 3, 2008
Monitoring Editor: Wendy Bickmore

Here, we identified the imprinted mesoderm-specific transcript (MEST) gene as an endogenous TIF1β primary target gene and demonstrated that transcriptional intermediary factor (TIF) 1β, through its interaction with heterochromatin protein (HP) 1, is essential in establishing and maintaining a local heterochromatin-like structure on MEST promoter region characterized by H3K9 trimethylation and hypoacetylation, H4K20 trimethylation, DNA hypermethylation, and enrichment in HP1 that correlates with preferential association to foci of pericentromeric heterochromatin and transcriptional repression. On disruption of the interaction between TIF1β and HP1, TIF1β is released from the promoter region, and there is a switch from DNA hypermethylation and histone H3K9 trimethylation to DNA hypomethylation and histone H3K27 trimethylation correlating with rapid reactivation of MEST expression. Interestingly, we provide evidence that the imprinted MEST allele DNA methylation is insensitive to TIF1β loss of function, whereas the nonimprinted allele is regulated through a distinct TIF1β–DNA methylation mechanism.

Address correspondence to: Régine Losson (losson{at}igbmc.u-strasbg.fr).

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