Global effects of the CSR-1 RNA interference pathway on the transcriptional landscape

RNAi pathways inhibit gene expression at the transcriptional and post-transcriptional level. Genome-wide analyses of nascent RNA transcripts in nematodes now suggest that the CSR-1 RNAi pathway helps maintain the directionality of active transcription and propagate the distinction between transcript...

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Published in	Nature structural & molecular biology Vol. 21; no. 4; pp. 358 - 365
Main Authors	Cecere, Germano, Hoersch, Sebastian, O'Keeffe, Sean, Sachidanandam, Ravi, Grishok, Alla
Format	Journal Article
Language	English
Published	New York Nature Publishing Group US 01.04.2014 Nature Publishing Group
Subjects	38 38/15 45 45/91 631/337/505 64 64/11 Animals Biochemistry Biochemistry, Molecular Biology Biological Microscopy Caenorhabditis elegans Caenorhabditis elegans - metabolism Caenorhabditis elegans Proteins Caenorhabditis elegans Proteins - metabolism Caenorhabditis elegans Proteins - physiology Chromatin Chromatin - metabolism Chromatin Assembly and Disassembly Gene expression Gene Expression Regulation Genetic aspects Genetic research Genetic transcription Genomics Histones Histones - metabolism Life Sciences Membrane Biology Protein Structure Ribonucleic acid RNA RNA Interference RNA, Small Interfering Signal transduction Transcription, Genetic
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Abstract	RNAi pathways inhibit gene expression at the transcriptional and post-transcriptional level. Genome-wide analyses of nascent RNA transcripts in nematodes now suggest that the CSR-1 RNAi pathway helps maintain the directionality of active transcription and propagate the distinction between transcriptionally active and silent genomic regions. Argonaute proteins and their small RNA cofactors short interfering RNAs are known to inhibit gene expression at the transcriptional and post-transcriptional levels. In Caenorhabditis elegans , the Argonaute CSR-1 binds thousands of endogenous siRNAs (endo-siRNAs) that are antisense to germline transcripts. However, its role in gene expression regulation remains controversial. Here we used genome-wide profiling of nascent RNA transcripts and found that the CSR-1 RNA interference pathway promoted sense-oriented RNA polymerase II transcription. Moreover, a loss of CSR-1 function resulted in global increase in antisense transcription and ectopic transcription of silent chromatin domains, which led to reduced chromatin incorporation of centromere-specific histone H3. On the basis of these findings, we propose that the CSR-1 pathway helps maintain the directionality of active transcription, thereby propagating the distinction between transcriptionally active and silent genomic regions.
AbstractList	Argonaute proteins and their small RNA cofactors short interfering RNAs are known to inhibit gene expression at the transcriptional and post-transcriptional levels. In Caenorhabditis elegans, the Argonaute CSR-1 binds thousands of endogenous siRNAs (endo-siRNAs) that are antisense to germline transcripts. However, its role in gene expression regulation remains controversial. Here we used genome-wide profiling of nascent RNA transcripts and found that the CSR-1 RNA interference pathway promoted sense-oriented RNA polymerase II transcription. Moreover, a loss of CSR-1 function resulted in global increase in antisense transcription and ectopic transcription of silent chromatin domains, which led to reduced chromatin incorporation of centromere-specific histone H3. On the basis of these findings, we propose that the CSR-1 pathway helps maintain the directionality of active transcription, thereby propagating the distinction between transcriptionally active and silent genomic regions. Argonaute proteins and their small RNA co-factors short interfering RNAs (siRNAs) are known to inhibit gene expression at the transcriptional and post-transcriptional levels. In Caenorhabditis elegans , the Argonaute CSR-1 binds thousands of endogenous siRNAs (endo-siRNAs) antisense to germline transcripts and associates with chromatin in a siRNA-dependent manner. However, its role in gene expression regulation remains controversial. Here, we used a genome-wide profiling of nascent RNA transcripts to demonstrate that the CSR-1 RNAi pathway promotes sense-oriented Pol II transcription. Moreover, a loss of CSR-1 function resulted in global increase in antisense transcription and ectopic transcription of silent chromatin domains, which led to reduced chromatin incorporation of centromere-specific histone H3. Based on these findings, we propose that the CSR-1 pathway has a role in maintaining the directionality of active transcription thereby propagating the distinction between transcriptionally active and silent genomic regions. RNAi pathways inhibit gene expression at the transcriptional and post-transcriptional level. Genome-wide analyses of nascent RNA transcripts in nematodes now suggest that the CSR-1 RNAi pathway helps maintain the directionality of active transcription and propagate the distinction between transcriptionally active and silent genomic regions. Argonaute proteins and their small RNA cofactors short interfering RNAs are known to inhibit gene expression at the transcriptional and post-transcriptional levels. In Caenorhabditis elegans , the Argonaute CSR-1 binds thousands of endogenous siRNAs (endo-siRNAs) that are antisense to germline transcripts. However, its role in gene expression regulation remains controversial. Here we used genome-wide profiling of nascent RNA transcripts and found that the CSR-1 RNA interference pathway promoted sense-oriented RNA polymerase II transcription. Moreover, a loss of CSR-1 function resulted in global increase in antisense transcription and ectopic transcription of silent chromatin domains, which led to reduced chromatin incorporation of centromere-specific histone H3. On the basis of these findings, we propose that the CSR-1 pathway helps maintain the directionality of active transcription, thereby propagating the distinction between transcriptionally active and silent genomic regions. Argonaute proteins and their small RNA cofactors short interfering RNAs are known to inhibit gene expression at the transcriptional and post-transcriptional levels. In Caenorhabditis elegans, the Argonaute CSR-1 binds thousands of endogenous siRNAs (endo-siRNAs) that are antisense to germline transcripts. However, its role in gene expression regulation remains controversial. Here we used genome-wide profiling of nascent RNA transcripts and found that the CSR-1 RNA interference pathway promoted sense-oriented RNA polymerase II transcription. Moreover, a loss of CSR-1 function resulted in global increase in antisense transcription and ectopic transcription of silent chromatin domains, which led to reduced chromatin incorporation of centromere-specific histone H3. On the basis of these findings, we propose that the CSR-1 pathway helps maintain the directionality of active transcription, thereby propagating the distinction between transcriptionally active and silent genomic regions. [PUBLICATION ABSTRACT] Argonaute proteins and their small RNA cofactors short interfering RNAs are known to inhibit gene expression at the transcriptional and post-transcriptional levels. In Caenorhabditis elegans, the Argonaute CSR-1 binds thousands of endogenous siRNAs (endo-siRNAs) that are antisense to germline transcripts. However, its role in gene expression regulation remains controversial. Here we used genome-wide profiling of nascent RNA transcripts and found that the CSR-1 RNA interference pathway promoted sense-oriented RNA polymerase II transcription. Moreover, a loss of CSR-1 function resulted in global increase in antisense transcription and ectopic transcription of silent chromatin domains, which led to reduced chromatin incorporation of centromere-specific histone H3. On the basis of these findings, we propose that the CSR-1 pathway helps maintain the directionality of active transcription, thereby propagating the distinction between transcriptionally active and silent genomic regions.Argonaute proteins and their small RNA cofactors short interfering RNAs are known to inhibit gene expression at the transcriptional and post-transcriptional levels. In Caenorhabditis elegans, the Argonaute CSR-1 binds thousands of endogenous siRNAs (endo-siRNAs) that are antisense to germline transcripts. However, its role in gene expression regulation remains controversial. Here we used genome-wide profiling of nascent RNA transcripts and found that the CSR-1 RNA interference pathway promoted sense-oriented RNA polymerase II transcription. Moreover, a loss of CSR-1 function resulted in global increase in antisense transcription and ectopic transcription of silent chromatin domains, which led to reduced chromatin incorporation of centromere-specific histone H3. On the basis of these findings, we propose that the CSR-1 pathway helps maintain the directionality of active transcription, thereby propagating the distinction between transcriptionally active and silent genomic regions.
Audience	Academic
Author	Cecere, Germano O'Keeffe, Sean Sachidanandam, Ravi Hoersch, Sebastian Grishok, Alla
AuthorAffiliation	2 David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA 1 Department of Biochemistry and Molecular Biophysics, Columbia University, New York, NY, USA 3 Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA
AuthorAffiliation_xml	– name: 1 Department of Biochemistry and Molecular Biophysics, Columbia University, New York, NY, USA – name: 2 David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA – name: 3 Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA
Author_xml	– sequence: 1 givenname: Germano surname: Cecere fullname: Cecere, Germano organization: Department of Biochemistry and Molecular Biophysics, Columbia University – sequence: 2 givenname: Sebastian surname: Hoersch fullname: Hoersch, Sebastian organization: David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology – sequence: 3 givenname: Sean surname: O'Keeffe fullname: O'Keeffe, Sean organization: Department of Biochemistry and Molecular Biophysics, Columbia University – sequence: 4 givenname: Ravi surname: Sachidanandam fullname: Sachidanandam, Ravi organization: Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai – sequence: 5 givenname: Alla surname: Grishok fullname: Grishok, Alla email: ag2691@columbia.edu organization: Department of Biochemistry and Molecular Biophysics, Columbia University
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Snippet	RNAi pathways inhibit gene expression at the transcriptional and post-transcriptional level. Genome-wide analyses of nascent RNA transcripts in nematodes now... Argonaute proteins and their small RNA cofactors short interfering RNAs are known to inhibit gene expression at the transcriptional and post-transcriptional... Argonaute proteins and their small RNA co-factors short interfering RNAs (siRNAs) are known to inhibit gene expression at the transcriptional and...
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SubjectTerms	38 38/15 45 45/91 631/337/505 64 64/11 Animals Biochemistry Biochemistry, Molecular Biology Biological Microscopy Caenorhabditis elegans Caenorhabditis elegans - metabolism Caenorhabditis elegans Proteins Caenorhabditis elegans Proteins - metabolism Caenorhabditis elegans Proteins - physiology Chromatin Chromatin - metabolism Chromatin Assembly and Disassembly Gene expression Gene Expression Regulation Genetic aspects Genetic research Genetic transcription Genomics Histones Histones - metabolism Life Sciences Membrane Biology Protein Structure Ribonucleic acid RNA RNA Interference RNA, Small Interfering Signal transduction Transcription, Genetic
Title	Global effects of the CSR-1 RNA interference pathway on the transcriptional landscape
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