Role of an ING1 Growth Regulator in Transcriptional Activation and Targeted Histone Acetylation by the NuA4 Complex

doi:10.1128/MCB.21.22.7629-7640.2001

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Molecular and Cellular Biology, November 2001, p. 7629-7640, Vol. 21, No. 22
0270-7306/01/$04.00+0 DOI: 10.1128/MCB.21.22.7629-7640.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Role of an ING1 Growth Regulator in Transcriptional Activation and Targeted Histone Acetylation by the NuA4 Complex

Amine Nourani,¹ Yannick Doyon,¹ Rhea T. Utley,¹ Stéphane Allard,¹ William S. Lane,² and Jacques Côté¹^,^*

Laval University Cancer Research Center, Hôtel-Dieu de Québec, Quebec City, Quebec G1R 2J6, Canada,¹ and Harvard Microchemistry Facility, Harvard University, Cambridge, Massachusetts 02138²

Received 12 March 2001/Returned for modification 7 May 2001/Accepted 10 August 2001

The yeast NuA4 complex is a histone H4 and H2A acetyltransferase involved in transcription regulation and essential for cellcycle progression. We identify here a novel subunit of the complex,Yng2p, a plant homeodomain (PHD)-finger protein homologous tohuman p33/ING1, which has tumor suppressor activity and is essentialfor p53 function. Mass spectrometry, immunoblotting, and immunoprecipitationexperiments confirm the stable stoichiometric association of thisprotein with purified NuA4. Yeast cells harboring a deletion ofthe YNG2 gene show severe growth phenotype and have gene-specifictranscription defects. NuA4 complex purified from the mutant strainis low in abundance and shows weak histone acetyltransferase activity.We demonstrate conservation of function by the requirement ofYng2p for p53 to function as a transcriptional activator in yeast.Accordingly, p53 interacts with NuA4 in vitro and in vivo, aninteraction reminiscent of the p53-ING1 physical link in humancells. The growth defect of $Delta$ yng2 cells can be rescued by theN-terminal part of the protein, lacking the PHD-finger. WhileYng2 PHD-finger is not required for p53 interaction, it is necessaryfor full expression of the p53-responsive gene and other NuA4target genes. Transcriptional activation by p53 in vivo is associatedwith targeted NuA4-dependent histone H4 hyperacetylation, whilehistone H3 acetylation levels remain unchanged. These resultsemphasize the essential role of the NuA4 complex in the controlof cell proliferation through gene-specific transcription regulation.They also suggest that regulation of mammalian cell proliferationby p53-dependent transcriptional activation functions throughrecruitment of an ING1-containing histone acetyltransferasecomplex.

^* Corresponding author. Mailing address: Laval University Cancer Research Center, Hôtel-Dieu de Québec (CHUQ), 9 McMahon Street,Quebec City, Quebec G1R 2J6, Canada. Phone: (418) 691-5545. Fax:(418) 691-5439. E-mail: jacques.cote{at}crhdq.ulaval.ca.

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