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Molecular and Cellular Biology, October 2004, p. 8823-8833, Vol. 24, No. 20
0270-7306/04/$08.00+0     DOI: 10.1128/MCB.24.20.8823-8833.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Genome-Wide Analysis of the Relationship between Transcriptional Regulation by Rpd3p and the Histone H3 and H4 Amino Termini in Budding Yeast{dagger}

Nevin Sabet,1 Sam Volo,1 Cailin Yu,2 James P. Madigan,1 and Randall H. Morse1,2*

Wadsworth Center, New York State Department of Health,1 Department of Biomedical of Sciences, School of Public Health, State University of New York at Albany, Albany, New York2

Received 14 October 2003/ Returned for modification 14 January 2004/ Accepted 19 July 2004

The histone amino termini have emerged as key targets for a variety of modifying enzymes that function as transcriptional coactivators and corepressors. However, an important question that has remained largely unexplored is the extent to which specific histone amino termini are required for the activating and repressive functions of these enzymes, Here we address this issue by focusing on the prototypical histone deacetylase, Rpd3p, in the budding yeast Saccharomyces cerevisiae. We show that targeting Rpd3p to a reporter gene in this yeast can partially repress transcription when either the histone H3 or the histone H4 amino terminus is deleted, indicating that the "tails" are individually dispensable for repression by Rpd3p. In contrast, we find that the effect of rpd3 gene disruption on global gene expression is considerably reduced in either a histone H3{Delta}1-28 (H3 lacking the amino-terminal 28 amino acids) or a histone H4(K5,8,12,16Q) (H4 with lysine residues 5, 8, 12, and 16 changed to glutamine residues) background compared to the wild-type background, indicating a requirement for one or both of these histone tails in Rpd3p-mediated regulation for many genes. These results suggest that acetylation of either the H3 or the H4 amino terminus could suffice to allow the activation of such genes. We also examine the relationship between H3 tails and H4 tails in global gene expression and find substantial overlap among the gene sets regulated by these histone tails. We also show that the effects on genome-wide expression of deleting the H3 or H4 amino terminus are similar but not identical to the effects of mutating the lysine residues in these same regions. These results indicate that the gene regulatory potential of the H3 and H4 amino termini is substantially but not entirely contained in these modifiable lysine residues.

* Corresponding author. Mailing address: Wadsworth Center, Albany, NY 12201-2002. Phone: (518) 486-3116. Fax: (518) 474-3181. E-mail: randall.morse{at}wadsworth.org.

{dagger} This work is dedicated to the memory of Robert Simpson.

Molecular and Cellular Biology, October 2004, p. 8823-8833, Vol. 24, No. 20
0022-538X/04/$08.00+0     DOI: 10.1128/MCB.24.20.8823-8833.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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