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Molecular and Cellular Biology, October 2005, p. 8985-8999, Vol. 25, No. 20
0270-7306/05/$08.00+0     doi:10.1128/MCB.25.20.8985-8999.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Domain-Wide Displacement of Histones by Activated Heat Shock Factor Occurs Independently of Swi/Snf and Is Not Correlated with RNA Polymerase II Density

Jing Zhao, Jorge Herrera-Diaz, and David S. Gross*

Department of Biochemistry and Molecular Biology, Louisiana State University Health Sciences Center, Shreveport, Louisiana 71130-3932

Received 19 June 2005/ Returned for modification 8 July 2005/ Accepted 15 July 2005

We show that histone-DNA interactions are disrupted across entire yeast heat shock genes upon their transcriptional activation. At HSP82, nucleosomal disassembly spans a domain of ~3 kb, beginning upstream of the promoter and extending through the transcribed region. A kinetic analysis reveals that histone H4 loses contact with DNA within 45 s of thermal upshift. Nucleosomal reassembly, prompted by temperature downshift, is also rapid, detectable within 60 s. Prior to their eviction, promoter-associated histones are transiently hyperacetylated, while those in the coding region are not. An upstream activation sequence mutation that weakens the binding of heat shock factor obviates domain-wide remodeling, while deletion of the TATA box that nearly abolishes transcription is permissive to 5'-end remodeling. The Swi/Snf complex is rapidly recruited to HSP82 upon heat shock. Nonetheless, domain-wide remodeling occurs efficiently in Swi/Snf mutants despite a sixfold reduction in transcription; it is also seen in gcn5{Delta}, set1{Delta}, and paf1{Delta} mutants. Contrary to current models, we demonstrate that a high density of RNA polymerase (Pol) is insufficient to elicit histone displacement. This finding suggests that histone eviction is modulated by factors that are not linked to elongating Pol II. It further suggests that histone depletion plays a causal role in mediating vigorous transcription in vivo and is not merely a consequence of it.

* Corresponding author. Mailing address: Department of Biochemistry and Molecular Biology, Louisiana State University Health Sciences Center, Shreveport, LA 71130-3932. Phone: (318) 675-5027. Fax: (318) 675-5180. E-mail: dgross{at}lsuhsc.edu.

Molecular and Cellular Biology, October 2005, p. 8985-8999, Vol. 25, No. 20
0022-538X/05/$08.00+0     doi:10.1128/MCB.25.20.8985-8999.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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