The RSC Complex Localizes to Coding Sequences to Regulate Pol II and Histone Occupancy

Marla M. Spain; Suraiya A. Ansari; Rakesh Pathak; Michael J. Palumbo; Randall H. Morse; Chhabi K. Govind

doi:10.1016/j.molcel.2014.10.002

The RSC Complex Localizes to Coding Sequences to Regulate Pol II and Histone Occupancy

Marla M. Spain, Suraiya A. Ansari, Rakesh Pathak, Michael J. Palumbo, Randall H. Morse, Chhabi K. Govind

Research output: Contribution to journal › Article › peer-review

31 Citations (Scopus)

Abstract

ATP-dependent chromatin remodelers regulate chromatin structure during multiple stages of transcription. We report that RSC, an essential chromatin remodeler, is recruited to the open reading frames (ORFs) of actively transcribed genes genome wide, suggesting a role for RSC in regulating transcription elongation. Consistent with such a role, Pol II occupancy in the ORFs of weakly transcribed genes is drastically reduced upon depletion of the RSC catalytic subunit Sth1. RSC inactivation also reduced histone H3 occupancy across transcribed regions. Remarkably, the strongest effects on Pol II and H3 occupancy were confined to the genes displaying the greatest RSC ORF enrichment. Additionally, RSC recruitment to the ORF requires the activities of the SAGA and NuA4 HAT complexes and is aided by the activities of the Pol II CTD Ser2 kinases Bur1 and Ctk1. Overall, our findings strongly implicate ORF-associated RSC in governing Pol II function and in maintaining chromatin structure over transcribed regions.

Original language	English
Pages (from-to)	653-666
Number of pages	14
Journal	Molecular Cell
Volume	56
Issue number	5
DOIs	https://doi.org/10.1016/j.molcel.2014.10.002
Publication status	Published - Dec 4 2014
Externally published	Yes

ASJC Scopus subject areas

Molecular Biology
Cell Biology

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10.1016/j.molcel.2014.10.002

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title = "The RSC Complex Localizes to Coding Sequences to Regulate Pol II and Histone Occupancy",

abstract = "ATP-dependent chromatin remodelers regulate chromatin structure during multiple stages of transcription. We report that RSC, an essential chromatin remodeler, is recruited to the open reading frames (ORFs) of actively transcribed genes genome wide, suggesting a role for RSC in regulating transcription elongation. Consistent with such a role, Pol II occupancy in the ORFs of weakly transcribed genes is drastically reduced upon depletion of the RSC catalytic subunit Sth1. RSC inactivation also reduced histone H3 occupancy across transcribed regions. Remarkably, the strongest effects on Pol II and H3 occupancy were confined to the genes displaying the greatest RSC ORF enrichment. Additionally, RSC recruitment to the ORF requires the activities of the SAGA and NuA4 HAT complexes and is aided by the activities of the Pol II CTD Ser2 kinases Bur1 and Ctk1. Overall, our findings strongly implicate ORF-associated RSC in governing Pol II function and in maintaining chromatin structure over transcribed regions.",

author = "Spain, {Marla M.} and Ansari, {Suraiya A.} and Rakesh Pathak and Palumbo, {Michael J.} and Morse, {Randall H.} and Govind, {Chhabi K.}",

note = "Funding Information: We thank Alan Hinnebusch for bur1as/ctk1Δ and Francois Robert for kin28as/bur2Δ. We also thank Swaminathan Venkatesh for sharing R and PERL scripts for the analysis of the genomic data. We acknowledge assistance from the Wadsworth Center Bioinformatics and Microarray Core Facilities. This work is supported by a grant to C.K.G. from The National Institutes of Health (NIH, GM095514) and by a grant from The National Science Foundation to R.H.M. (MCB0949722). Publisher Copyright: {\textcopyright} 2014 Elsevier Inc.",

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AU - Spain, Marla M.

AU - Ansari, Suraiya A.

AU - Pathak, Rakesh

AU - Palumbo, Michael J.

AU - Morse, Randall H.

AU - Govind, Chhabi K.

N1 - Funding Information: We thank Alan Hinnebusch for bur1as/ctk1Δ and Francois Robert for kin28as/bur2Δ. We also thank Swaminathan Venkatesh for sharing R and PERL scripts for the analysis of the genomic data. We acknowledge assistance from the Wadsworth Center Bioinformatics and Microarray Core Facilities. This work is supported by a grant to C.K.G. from The National Institutes of Health (NIH, GM095514) and by a grant from The National Science Foundation to R.H.M. (MCB0949722). Publisher Copyright: © 2014 Elsevier Inc.

PY - 2014/12/4

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N2 - ATP-dependent chromatin remodelers regulate chromatin structure during multiple stages of transcription. We report that RSC, an essential chromatin remodeler, is recruited to the open reading frames (ORFs) of actively transcribed genes genome wide, suggesting a role for RSC in regulating transcription elongation. Consistent with such a role, Pol II occupancy in the ORFs of weakly transcribed genes is drastically reduced upon depletion of the RSC catalytic subunit Sth1. RSC inactivation also reduced histone H3 occupancy across transcribed regions. Remarkably, the strongest effects on Pol II and H3 occupancy were confined to the genes displaying the greatest RSC ORF enrichment. Additionally, RSC recruitment to the ORF requires the activities of the SAGA and NuA4 HAT complexes and is aided by the activities of the Pol II CTD Ser2 kinases Bur1 and Ctk1. Overall, our findings strongly implicate ORF-associated RSC in governing Pol II function and in maintaining chromatin structure over transcribed regions.

AB - ATP-dependent chromatin remodelers regulate chromatin structure during multiple stages of transcription. We report that RSC, an essential chromatin remodeler, is recruited to the open reading frames (ORFs) of actively transcribed genes genome wide, suggesting a role for RSC in regulating transcription elongation. Consistent with such a role, Pol II occupancy in the ORFs of weakly transcribed genes is drastically reduced upon depletion of the RSC catalytic subunit Sth1. RSC inactivation also reduced histone H3 occupancy across transcribed regions. Remarkably, the strongest effects on Pol II and H3 occupancy were confined to the genes displaying the greatest RSC ORF enrichment. Additionally, RSC recruitment to the ORF requires the activities of the SAGA and NuA4 HAT complexes and is aided by the activities of the Pol II CTD Ser2 kinases Bur1 and Ctk1. Overall, our findings strongly implicate ORF-associated RSC in governing Pol II function and in maintaining chromatin structure over transcribed regions.

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The RSC Complex Localizes to Coding Sequences to Regulate Pol II and Histone Occupancy

Abstract

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