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Originally published In Press as doi:10.1074/jbc.M211460200 on December 23, 2002

J. Biol. Chem., Vol. 278, Issue 15, 13431-13441, April 11, 2003
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DNA-dependent Acetylation of p53 by the Transcription Coactivator p300*

David DornanDagger §, Harumi ShimizuDagger , Neil D. Perkins||, and Ted R. HuppDagger **

From the Dagger  Cancer Research UK Laboratories, Department of Molecular & Cellular Pathology,  School of Life Sciences, University of Dundee, Dundee DD1 9SY, Scotland, United Kingdom

Reconstitution of the stages in the assembly of the p300·p53 transcription complex has identified a novel type of DNA-dependent regulation of p300-catalyzed acetylation. Phosphorylation at the CHK2 site (Ser20) in the N-terminal activation domain of p53 stabilized p300 binding. The phosphopeptide binding activity of p300 was mapped in vitro to two domains: the C-terminal IBiD domain and the N-terminal IHD domain (IBiD homology domain). The IHD or IBiD minidomains can bind to the p53 activation domain in vivo as determined using the mammalian two-hybrid VP16-GAL4 luciferase reporter assay. The IHD and IBiD minidomains of p300 also functioned as dominant negative inhibitors of p53-dependent transcription in vivo. Upon examining the affects of p300 binding on substrate acetylation, we found that the p53 consensus site DNA promotes a striking increase in p53 acetylation in vitro. Co-transfection into cells of the p53 gene and plasmid DNA containing the consensus DNA binding site of p53 activated DNA-dependent acetylation of p53 in vivo. The phosphopeptide binding activity of p300 is critical for DNA-dependent acetylation, as p53 acetylation was inhibited by phospho-Ser20 peptides. Consensus site DNA-dependent acetylation of p53 stabilized the p300·p53 protein complex, whereas basal acetylation of p53 by p300 in the presence of nonspecific DNA resulted in p300 dissociation. These data identify at least three distinct stages in the assembly of a p300·p53 complex: 1) p300 docking to the activation domain of p53 via the IBiD and/or IHD domains; 2) DNA-dependent acetylation of p53; and 3) stabilization of the p300·p53AC complex after acetylation. The ability of DNA to act as an allosteric ligand to activate substrate acetylation identifies a conformational constraint that can be placed on the p300-acetylation reaction that is likely to be an amplification signal and influence protein-protein contacts at a promoter.

* 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.

§ Recipient of a BBSRC PhD studentship. Current address: Dept. of Molecular Oncology, Genentech Inc., 1 DNA Way, South San Francisco, CA 94080.

|| Supported by a Royal Society University Fellowship.

** Supported by a Program Grant from the Cancer Research UK and a Career Establishment Grant from the UK Medical Research Council. To whom correspondence should be addressed. Tel.: 44-0-1382-496430; Fax: 44-0-1382-633952; E-mail: t.r.hupp@dundee.ac.uk.

Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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