Purified chromatin rings, excised from the PHO5 locus of Saccharomyces cerevisiae in transcriptionally repressed and activated states, were remodeled with RSC and ATP. Nucleosomes were translocated, and those originating on the promoter of repressed rings were removed, whereas those originating on the open reading frame (ORF) were retained. Treatment of the repressed rings with histone deacetylase diminished the removal of promoter nucleosomes. These findings point to a principle of promoter chromatin remodeling for transcription, namely that promoter specificity resides primarily in the nucleosomes rather than in the remodeling complex that acts upon them.
Subscribe to Journal
Get full journal access for 1 year
only $18.75 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Lorch, Y., LaPointe, J.W. & Kornberg, R.D. Nucleosomes inhibit the initiation of transcription but allow chain elongation with the displacement of histones. Cell 49, 203–210 (1987).
Knezetic, J.A. & Luse, D.S. The presence of nucleosomes on a DNA template prevents initiation by RNA polymerase II in vitro. Cell 45, 95–104 (1986).
Han, M. & Grunstein, M. Nucleosome loss activates yeast downstream promoters in vivo. Cell 55, 1137–1145 (1988).
Elgin, S.C. The formation and function of DNase I hypersensitive sites in the process of gene activation. J. Biol. Chem. 263, 19259–19262 (1988).
McGhee, J.D., Wood, W.I., Dolan, M., Engel, J.D. & Felsenfeld, G. A 200 base pair region at the 5′ end of the chicken adult beta-globin gene is accessible to nuclease digestion. Cell 27, 45–55 (1981).
Paranjape, S.M., Kamakaka, R.T. & Kadonaga, J.T. Role of chromatin structure in the regulation of transcription by RNA polymerase II. Annu. Rev. Biochem. 63, 265–297 (1994).
Almer, A., Rudolph, H., Hinnen, A. & Horz, W. Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements. EMBO J. 5, 2689–2696 (1986).
Reinke, H. & Horz, W. Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter. Mol. Cell 11, 1599–1607 (2003).
Boeger, H., Griesenbeck, J., Strattan, J.S. & Kornberg, R.D. Nucleosomes unfold completely at a transcriptionally active promoter. Mol. Cell 11, 1587–1598 (2003).
Boeger, H., Griesenbeck, J. & Kornberg, R.D. Nucleosome retention and the stochastic nature of promoter chromatin remodeling for transcription. Cell 133, 716–726 (2008).
Bernstein, B.E., Liu, C.L., Humphrey, E.L., Perlstein, E.O. & Schreiber, S.L. Global nucleosome occupancy in yeast. Genome Biol. 5, R62 (2004).
Lee, C.K., Shibata, Y., Rao, B., Strahl, B.D. & Lieb, J.D. Evidence for nucleosome depletion at active regulatory regions genome-wide. Nat. Genet. 36, 900–905 (2004).
Cairns, B.R. et al. RSC, an essential, abundant chromatin-remodeling complex. Cell 87, 1249–1260 (1996).
Sudarsanam, P. & Winston, F. The Swi/Snf family nucleosome-remodeling complexes and transcriptional control. Trends Genet. 16, 345–351 (2000).
Cairns, B.R., Kim, Y.J., Sayre, M.H., Laurent, B.C. & Kornberg, R.D. A multi-subunit complex containing the SWI1/ADR6, SWI2/SNF2, SWI3, SNF5, and SNF6 gene products isolated from yeast. Proc. Natl. Acad. Sci. USA 91, 1950–1954 (1994).
Peterson, C.L., Dingwall, A. & Scott, M.P. Five SWI/SNF gene products are components of a large multisubunit complex required for transcriptional enhancement. Proc. Natl. Acad. Sci. USA 91, 2905–2908 (1994).
Côté, J., Quinn, J., Workman, J.L. & Peterson, C.L. Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. Science 265, 53–60 (1994).
Kwon, H., Imbalzano, A.N., Khavari, P.A., Kingston, R.E. & Green, M.R. Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex. Nature 370, 477–481 (1994).
Lorch, Y., Cairns, B.R., Zhang, M. & Kornberg, R.D. Activated RSC-nucleosome complex and persistently altered form of the nucleosome. Cell 94, 29–34 (1998).
Saha, A., Wittmeyer, J. & Cairns, B.R. Chromatin remodeling through directional DNA translocation from an internal nucleosomal site. Nat. Struct. Mol. Biol. 12, 747–755 (2005).
Zofall, M., Persinger, J., Kassabov, S.R. & Bartholomew, B. Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome. Nat. Struct. Mol. Biol. 13, 339–346 (2006).
Chaban, Y. et al. Structure of a RSC-nucleosome complex and insights into chromatin remodeling. Nat. Struct. Mol. Biol. 15, 1272–1277 (2008).
Lorch, Y., Maier-Davis, B. & Kornberg, R.D. Mechanism of chromatin remodeling. Proc. Natl. Acad. Sci. USA 107, 3458–3462 (2010).
Griesenbeck, J., Boeger, H., Strattan, J.S. & Kornberg, R.D. Affinity purification of specific chromatin segments from chromosomal loci in yeast. Mol. Cell. Biol. 23, 9275–9282 (2003).
Svaren, J. & Horz, W. Transcription factors vs nucleosomes: regulation of the PHO5 promoter in yeast. Trends Biochem. Sci. 22, 93–97 (1997).
Lorch, Y., Maier-Davis, B. & Kornberg, R.D. Chromatin remodeling by nucleosome disassembly in vitro. Proc. Natl. Acad. Sci. USA 103, 3090–3093 (2006).
Boeger, H., Griesenbeck, J., Strattan, J.S. & Kornberg, R.D. Removal of promoter nucleosomes by disassembly rather than sliding in vivo. Mol. Cell 14, 667–673 (2004).
Clapier, C.R. & Cairns, B.R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78, 273–304 (2009).
Floer, M. et al. A RSC/nucleosome complex determines chromatin architecture and facilitates activator binding. Cell 141, 407–418 (2010).
Badis, G. et al. A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Mol. Cell 32, 878–887 (2008).
Barbaric, S. et al. Redundancy of chromatin remodeling pathways for the induction of the yeast PHO5 promoter in vivo. J. Biol. Chem. 282, 27610–27621 (2007).
Zhang, H., Roberts, D.N. & Cairns, B.R. Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell 123, 219–231 (2005).
Albert, I. et al. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 446, 572–576 (2007).
Cairns, B.R. Chromatin remodeling: insights and intrigue from single-molecule studies. Nat. Struct. Mol. Biol. 14, 989–996 (2007).
Moreira, J.M. & Holmberg, S. Transcriptional repression of the yeast CHA1 gene requires the chromatin-remodeling complex RSC. EMBO J. 18, 2836–2844 (1999).
Depew, D.E. & Wang, J.C. Conformational fluctuations of DNA helix. Proc. Natl. Acad. Sci. USA 72, 4275–4279 (1975).
This research was supported by US National Institutes of Health grant GM36659 (R.D.K).
The authors declare no competing financial interests.
About this article
Cite this article
Lorch, Y., Griesenbeck, J., Boeger, H. et al. Selective removal of promoter nucleosomes by the RSC chromatin-remodeling complex. Nat Struct Mol Biol 18, 881–885 (2011). https://doi.org/10.1038/nsmb.2072
The Structural Basis for Specific Recognition of H3K14 Acetylation by Sth1 in the RSC Chromatin Remodeling Complex
Dynamics of Chromatin and Transcription during Transient Depletion of the RSC Chromatin Remodeling Complex
Cell Reports (2019)
Genome-wide reconstitution of chromatin transactions reveals that RSC preferentially disrupts H2AZ-containing nucleosomes
Genome Research (2019)
Coupling of replisome movement with nucleosome dynamics can contribute to the parent–daughter information transfer
Nucleic Acids Research (2018)
Actin-related proteins regulate the RSC chromatin remodeler by weakening intramolecular interactions of the Sth1 ATPase
Communications Biology (2018)