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J. Biol. Chem., Vol. 280, Issue 45, 37908-37916, November 11, 2005

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Functional Characterization of Evolutionarily Conserved DNA Regions in Forkhead Box F1 Gene Locus^*

Il-Man Kim, Yan Zhou, Sneha Ramakrishna, Douglas E. Hughes, Julian Solway, Robert H. Costa, and Vladimir V. Kalinichenko¶1

From the Department of Medicine and ^¶Committee on Developmental Biology, the University of Chicago, Chicago, Illinois 60637 and the Department of Biochemistry and Molecular Genetics, College of Medicine, University of Illinois, Chicago, Illinois 60607

The Forkhead Box f1 (Foxf1) transcription factor (previously known as HFH-8 or Freac-1) is expressed in the septum transversum and splanchnic (visceral) mesoderm and is required for proper development of gut-derived organs. Sequence comparisons of mouse and human Foxf1 genes have revealed highly conserved DNA sequences located within the -5.3-kb Foxf1 promoter region and the 400-nucleotide regulatory element located 1 kb 3' to the Foxf1 gene (3'RE). To examine their transcriptional activity during mouse embryonic development, we generated transgenic mice in which the expression of the -galactosidase transgene was controlled by the -2.7-kb Foxf1 promoter region, the -5.3-kb Foxf1 promoter region, or the -5.3-kb Foxf1 promoter region fused to the 3'RE. The -5.3-kb Foxf1 promoter sequences induced appropriate transgene expression in the midgut and developing intestine, whereas the -2.7-kb Foxf1 promoter region was transcriptionally inactive. Addition of 3'RE to the -5.3-kb Foxf1 promoter restored proper transgene expression in the foregut, liver, and lung mesenchyme and prevented ectopic transgene expression in the developing nervous system. Cotransfection studies demonstrated that FoxA2 protein bound to the 3'RE region (+4506/+4529 bp) and was sufficient to inhibit expression of the -5.3-kb Foxf1 promoter. Furthermore, C/EBP and HNF-6 proteins bound to the 3'RE region (+4647/+4694 bp) and provided synergistic transcriptional activation of the -5.3-kb Foxf1 promoter in cotransfection assays. These studies demonstrated that the conserved Foxf1 3'RE region is essential for proper tissue-specific regulation of the Foxf1 promoter region during mouse embryogenesis.

Received for publication, June 15, 2005 , and in revised form, August 8, 2005.

^* This work was supported by American Heart Association Scientist Development Grant 0335036N (to V. V. K.), Research Grant 6-FY2005-325 from March of Dimes Birth Defects Foundation (to V. V. K.), and United States Public Health Service Grants HL 62446 and DK 54687-06 from the NHLBI and NIDDK, National Institutes of Health (to R. H. C.). 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 To whom correspondence should be addressed: The University of Chicago, Dept. of Medicine, 5841 S. Maryland Ave., MC 6076, Chicago, IL 60637. Tel.: 773-702-4024; Fax: 773-702-6500; E-mail: vkalin{at}medicine.bsd.uchicago.edu.

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