This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Google Scholar
Right arrow Articles by Tomar, R. S.
Right arrow Articles by Reese, J. C.
PubMed
Right arrow PubMed Citation
Right arrow Articles by Tomar, R. S.
Right arrow Articles by Reese, J. C.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, June 2009, p. 3255-3265, Vol. 29, No. 12
0270-7306/09/$08.00+0     doi:10.1128/MCB.01741-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

A Novel Mechanism of Antagonism between ATP-Dependent Chromatin Remodeling Complexes Regulates RNR3 Expression{triangledown}

Raghuvir S. Tomar,{dagger} James N. Psathas, Hesheng Zhang, Zhengjian Zhang,{ddagger} and Joseph C. Reese*

Department of Biochemistry and Molecular Biology, Center for Eukaryotic Gene Regulation, Pennsylvania State University, University Park, Pennsylvania 16802

Received 13 November 2008/ Returned for modification 11 December 2008/ Accepted 24 March 2009

Gene expression depends upon the antagonistic actions of chromatin remodeling complexes. While this has been studied extensively for the enzymes that covalently modify the tails of histones, the mechanism of how ATP-dependent remodeling complexes antagonize each other to maintain the proper level of gene activity is not known. The gene encoding a large subunit of ribonucleotide reductase, RNR3, is regulated by ISW2 and SWI/SNF, complexes that repress and activate transcription, respectively. Here, we studied the functional interactions of these two complexes at RNR3. Deletion of ISW2 causes constitutive recruitment of SWI/SNF, and conditional reexpression of ISW2 causes the repositioning of nucleosomes and reduced SWI/SNF occupancy at RNR3. Thus, ISW2 is required for restriction of access of SWI/SNF to the RNR3 promoter under the uninduced condition. Interestingly, the binding of sequence-specific DNA binding factors and the general transcription machinery are unaffected by the status of ISW2, suggesting that disruption of nucleosome positioning does not cause a nonspecific increase in cross-linking of all factors to RNR3. We provide evidence that ISW2 does not act on SWI/SNF directly but excludes its occupancy by positioning nucleosomes over the promoter. Genetic disruption of nucleosome positioning by other means led to a similar phenotype, linking repressed chromatin structure to SWI/SNF exclusion. Thus, incorporation of promoters into a repressive chromatin structure is essential for prevention of the opportunistic actions of nucleosome-disrupting activities in vivo, providing a novel mechanism for maintaining tight control of gene expression.

* Corresponding author. Mailing address: Pennsylvania State University, Department of Biochemistry and Molecular Biology, 203 Althouse Laboratory, University Park, PA 16802. Phone: (814) 865-1976. Fax: (814) 863-7024. E-mail: Jcr8{at}psu.edu

{triangledown} Published ahead of print on 6 April 2009.

{dagger} Present address: Indian Institute of Science Education and Research, Bhopal, India.

{ddagger} Present address: University of California—Berkeley, Department of Molecular & Cell Biology, 16 Barker Hall, No. 3204, Berkeley, CA 94720-3204.

Molecular and Cellular Biology, June 2009, p. 3255-3265, Vol. 29, No. 12
0270-7306/09/$08.00+0     doi:10.1128/MCB.01741-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Psathas, J. N., Zheng, S., Tan, S., Reese, J. C. (2009). Set2-Dependent K36 Methylation Is Regulated by Novel Intratail Interactions within H3. Mol. Cell. Biol. 29: 6413-6426 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»