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J. Biol. Chem., Vol. 283, Issue 4, 2275-2285, January 25, 2008

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A Role for Basic Transcription Element-binding Protein 1 (BTEB1) in the Autoinduction of Thyroid Hormone Receptor β^*

Pia Bagamasbad¹, Kembra L. Howdeshell¹², Laurent M. Sachs, Barbara A. Demeneix, and Robert J. Denver³

From the Department of Molecular, Cellular, and Developmental Biology, the University of Michigan, Ann Arbor, Michigan 48109 and UMR5166 CNRS, USM-501 Muséum National d'Histoire Naturelle, Département Régulation Développement et Diversité Moléculaire, Case 32, 7 Rue Cuvier, 75231 Paris Cedex 05, France

Thyroid hormone (T₃) induces gene regulation programs necessary for tadpole metamorphosis. Among the earliest responses to T₃ are the up-regulation of T₃ receptor β (TRβ; autoinduction) and BTEB1 (basic transcription element-binding protein 1). BTEB1 is a member of the Krüppel family of transcription factors that bind to GC-rich regions in gene promoters. The proximal promoter of the Xenopus laevis TrβA gene has seven GC-rich sequences, which led us to hypothesize that BTEB1 binds to and regulates TrβA. In tadpoles and the frog fibroblast-derived cell line XTC-2, T₃ up-regulated Bteb1 mRNA with faster kinetics than TrβA, and Bteb1 mRNA correlated with increased BTEB1 protein expression. BTEB1 bound to GC-rich sequences in the proximal TrβA promoter in vitro. By using chromatin immunoprecipitation assay, we show that BTEB1 associates with the TrβA promoter in vivo in a T₃ and developmental stage-dependent manner. Induced expression of BTEB1 in XTC-2 cells caused accelerated and enhanced autoinduction of the TrβA gene. This enhancement was lost in N-terminal truncated mutants of BTEB1. However, point mutations in the zinc fingers of BTEB1 that destroyed DNA binding did not alter the activity of the protein on TrβA autoinduction, suggesting that BTEB1 can function in this regard through protein-protein interactions. Our findings support the hypothesis that BTEB1 associates with the TrβA promoter in vivo and enhances autoinduction, but this action does not depend on its DNA binding activity. Cooperation among the protein products of immediate early genes may be a common mechanism for driving developmental signaling pathways.

Received for publication, November 13, 2007 , and in revised form, November 27, 2007.

^* This work was supported in part by National Science Foundation Grants IBN9974672 and IBN0235401 (to R. J. D.), NINDS Grant 1 R01 NS046690 from the National Institutes of Health (to R. J. D.), and funding from the CNRS and the Muséum National d'Histoire Naturelle (to L. M. S. and B. A. D.). 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 1.

¹ Both authors contributed equally to this work.

² Supported by an NIEHS, National Institutes of Health, postdoctoral trainee-ship through the Environmental Toxicology Research Training Grant, University of Michigan, Ann Arbor, MI. Present address: Reproductive Toxicology Division, MD-72, NHEERL, ORD, Environmental Protection Agency, Research Triangle Park, NC 27711.

³ To whom correspondence should be addressed: Dept. of Molecular, Cellular, and Developmental Biology, 830 North University Ave., University of Michigan, Ann Arbor, MI 48109-1048. Fax: 734-647-0884; E-mail: rdenver{at}umich.edu.

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