Different Requirements of the SWI/SNF Complex for Robust Nucleosome Displacement at Promoters of Heat Shock Factor and Msn2- and Msn4-Regulated Heat Shock Genes

Abstract

The stress response in yeast cells is regulated by at least two classes of transcription activators—HSF and Msn2/4, which differentially affect promoter chromatin remodeling. We demonstrate that the deletion of SNF2, an ATPase activity-containing subunit of the chromatin remodeling SWI/SNF complex, eliminates histone displacement, RNA polymerase II recruitment, and heat shock factor (HSF) binding at the HSP12 promoter while delaying these processes at the HSP82 and SSA4 promoters. Out of the three promoters, the double deletion of MSN2 and MSN4 eliminates both chromatin remodeling and HSF binding only at the HSP12 promoter, suggesting that Msn2/4 activators are primary determinants of chromatin disassembly at the HSP12 promoter. Unexpectedly, during heat shock the level of Msn2/4 at the HSP12 promoter declines. This is likely a result of promoter-targeted Msn2/4 degradation associated with transcription complex assembly. While histone displacement kinetic profiles bear clear promoter specificity, the kinetic profiles of recovery from heat shock for all analyzed genes display an equal or even higher nucleosome return rate, which is to some extent delayed by the deletion of SNF2.

ACKNOWLEDGMENTS

We thank David Gross for discussion of unpublished data, Jocelyn Krebs, Robin Miskimins, and Robert Noiva for critical reading of the manuscript and helpful suggestions, and Fred Winston, Jessica Tyler, Kevin Morano, and David Gross for plasmids and yeast strains.

This work was supported by grants awarded to A.M.E. from NSF (MCB-0352042) and from NIH (P20 RR016479) from the INBRE Program of the National Center for Research Resources.