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Molecular and Cellular Biology, September 2009, p. 4994-5007, Vol. 29, No. 18
0270-7306/09/$08.00+0     doi:10.1128/MCB.01858-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Cooperation between the INO80 Complex and Histone Chaperones Determines Adaptation of Stress Gene Transcription in the Yeast Saccharomyces cerevisiae{triangledown} ,{dagger}

Eva Klopf,1,{ddagger} Ludmila Paskova,1,{ddagger} Carme Solé,2 Gloria Mas,2 Andriy Petryshyn,1 Francesc Posas,2 Ulrike Wintersberger,1 Gustav Ammerer,1 and Christoph Schüller1*

Department of Biochemistry and Cell Biology, Max F. Perutz Laboratories, University of Vienna, A-1030 Vienna, Austria,1 Cell Signaling Unit, Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, Parc de Recerca Biomèdica de Barcelona, Barcelona, Spain2

Received 5 December 2008/ Returned for modification 20 January 2009/ Accepted 7 July 2009

In yeast, environmental stresses provoke sudden and dramatic increases in gene expression at stress-inducible loci. Stress gene transcription is accompanied by the transient eviction of histones from the promoter and the transcribed regions of these genes. We found that mutants defective in subunits of the INO80 complex, as well as in several histone chaperone systems, exhibit extended expression windows that can be correlated with a distinct delay in histone redeposition during adaptation. Surprisingly, Ino80 became associated with the ORFs of stress genes in a stress-specific way, suggesting a direct function in the repression during adaptation. This recruitment required elongation by RNA polymerase (Pol) II but none of the histone modifications that are usually associated with active transcription, such as H3 K4/K36 methylation. A mutant lacking the Asf1-associated H3K56 acetyltransferase Rtt109 or Asf1 itself also showed enhanced stress-induced transcript levels. Genetic data, however, suggest that Asf1 and Rtt109 function in parallel with INO80 to restore histone homeostasis, whereas Spt6 seems to have a function that overlaps that of the chromatin remodeler. Thus, chromatin remodeling by INO80 in cooperation with Spt6 determines the shape of the expression profile under acute stress conditions, possibly by an elongation-dependent mechanism.


* Corresponding author. Mailing address: University of Vienna, MFPL, Department of Biochemistry and Cell Biology, Bohr-Gasse 9/5, A-1030 Vienna, Austria. Phone: 43-1-4277-52815. Fax: 43-1-4277-9528. E-mail: Christoph.Schueller{at}univie.ac.at

{triangledown} Published ahead of print on 20 July 2009.

{dagger} Supplemental material for this article may be found at http://mcb.asm.org/.

{ddagger} These authors contributed equally to this work.


Molecular and Cellular Biology, September 2009, p. 4994-5007, Vol. 29, No. 18
0270-7306/09/$08.00+0     doi:10.1128/MCB.01858-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.