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Originally published In Press as doi:10.1074/jbc.M011344200 on January 22, 2001

J. Biol. Chem., Vol. 276, Issue 16, 12645-12653, April 20, 2001
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Molecular Regulation of the Endothelin-1 Gene by Hypoxia
CONTRIBUTIONS OF HYPOXIA-INDUCIBLE FACTOR-1, ACTIVATOR PROTEIN-1, GATA-2, AND p300/CBP*

Kazuhito Yamashita, Daryl J. Discher, Jing Hu, Nanette H. Bishopric, and Keith A. WebsterDagger

From the Department of Molecular and Cellular Pharmacology, University of Miami Medical Center, Miami, Florida 33149

Endothelin-1 (ET-1) is a peptide hormone with potent vasoconstrictor properties which is synthesized and secreted predominantly by vascular endothelial cells. Its production is regulated by numerous stimuli including ischemia and hypoxia, and the enhanced levels that occur during myocardial ischemia may contribute to the progression of heart failure. We reported previously a preliminary characterization of a hypoxia-inducible factor-1 (HIF-1) binding site in the human ET-1 promoter which contributed to the activation of ET-1 expression in endothelial cells. We report here that the HIF-1 binding site alone is not sufficient for the response to hypoxia but requires an additional 50 base pairs of flanking sequence that includes binding sites for the factors activator protein-1 (AP-1), GATA-2, and CAAT-binding factor (NF-1). Mutation of any one of these sites or the HIF-1 site eliminated induction by hypoxia. Mutations of the AP-1 and GATA-2 sites, but not the HIF-1 site, were complemented by overexpressing AP-1, GATA-2, HIF-1alpha , or the activator protein p300/CBP, restoring the response to hypoxia. Binding studies in vitro confirmed physical associations among GATA-2, AP-1, and HIF-1 factors. Overexpression or depletion of p300/CBP modulated the level of ET-1 promoter expression as well as the endogenous ET-1 transcript but did not change the fold induction by hypoxia in either case. Regulation of the ET-1 promoter by hypoxia in non-endothelial cells required overexpression of GATA-2 and HIF-1alpha . The results support essential roles for AP-1, GATA-2, and NF-1 in stabilizing the binding of HIF-1 and promoting recruitment of p300/CBP to the ET-1 hypoxia response complex.

* This work was supported by Grant HL44578 from the National Institutes of Health (to K. A. W.) and by a postdoctoral fellowship from the American Heart Association, Florida Affiliate (to K. Y.). A preliminary report of this work has been published in abstract form (Yamashita, K., Discher, D. J., Hu, J., Bishopric, N. H., and Webster, K. A. (1999) Circulation 98, 74).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Dagger To whom correspondence should be addressed: Dept. of Molecular and Cellular Pharmacology, Rosenstiel Medical Science Bldg., Rm. 6038, University of Miami Medical Center, 1600 NW 10th Ave., Miami, FL 33136. Tel.: 305-243-6779; Fax: 305-243-3082; E-mail: kwebster@chroma.med.miami.edu.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.


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