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Originally published In Press as doi:10.1074/jbc.M409879200 on October 12, 2004

J. Biol. Chem., Vol. 279, Issue 52, 54937-54943, December 24, 2004
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Hairy-related Transcription Factors Inhibit GATA-dependent Cardiac Gene Expression through a Signal-responsive Mechanism*

Irfan S. Kathiriya,abcd Isabelle N. King,bce Masao Murakami,af Masayo Nakagawa,a John M. Astle,ad Kelly A. Gardner,ab Robert D. Gerard,gh Eric N. Olson,ai Deepak Srivastava, Supported by grants from NHLBI/National Institutes of Health, the American Heart Association, and the March of Dimes Birth Defects Foundation,abj and Osamu Nakagawa, Supported by grants from the American Heart Association Texas Affiliate, the Muscular Dystrophy Association, and Tanabe Medical Frontier Conferenceak

From the Departments of aMolecular Biology, bPediatrics, and gInternal Medicine, The University of Texas Southwestern Medical Center, Dallas, Texas 75390-9148

Combinatorial actions of transcription factors in multiprotein complexes dictate gene expression profiles in cardiac development and disease. The Hairy-related transcription factor (HRT) family of basic helix-loop-helix proteins is composed of transcriptional repressors highly expressed in the cardiovascular system. However, it has remained unclear whether HRT proteins modulate gene expression driven by cardiac transcriptional activators. Here, we have shown that HRT proteins inhibit cardiac gene transcription by interfering with GATA transcription factors that are implicated in cardiac development and hypertrophy. HRT proteins inhibited GATA-dependent transcriptional activation of cardiac gene promoters such as the atrial natriuretic factor (ANF) promoter. Adenovirus-mediated expression of Hrt2 suppressed mRNA expression of ANF and other cardiac-specific genes in cultured cardiomyocytes. Among various signaling molecules implicated in cardiomyocyte growth, constitutively active Akt1/protein kinase B{alpha} relieved Hrt2-mediated inhibition of GATA-dependent transcription. HRT proteins physically interacted with GATA proteins, and the basic domain of HRT was critical for physical association as well as transcriptional inhibition. These results suggest that HRT proteins may regulate specific sets of cardiac genes by modulating the function of GATA proteins and other cardiac transcriptional activators in a signal-dependent manner.

Received for publication, August 27, 2004 , and in revised form, October 6, 2004.

* 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.

c These authors contributed equally.

d Fellows of the National Institutes of Health Medical Scientist Training Program.

e An NICHD/National Institutes of Health fellow of the Pediatric Scientist Development Program.

f Supported by a fellowship from the Japan Heart Foundation and by Kumamoto University Institute of Molecular Embryology and Genetics.

h Supported by the Donald W. Reynolds Center for Clinical Cardiovascular Research.

i Supported by grants from the National Institutes of Health, the Donald W. Reynolds Center for Clinical Cardiovascular Research, and the Robert A. Welch Foundation.

j To whom correspondence may be address: 6000 Harry Hines Blvd., Dallas, TX 75390-9148. E-mail: Deepak.Srivastava{at}UTSouthwestern.edu. k To whom correspondence may be addressed: 6000 Harry Hines Blvd., Dallas, TX 75390-9148. E-mail: Osamu.Nakagawa{at}UTSouthwestern.edu.


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