A Large Fraction of Extragenic RNA Pol II Transcription Sites Overlap Enhancers

Mammalian genomes are pervasively transcribed outside mapped protein-coding genes. One class of extragenic transcription products is represented by long non-coding RNAs (lncRNAs), some of which result from Pol_II transcription of bona-fide RNA genes. Whether all lncRNAs described insofar are product...

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Published in:	PLoS biology Vol. 8; no. 5; p. e1000384
Main Authors:	De Santa, Francesca, Barozzi, Iros, Mietton, Flore, Ghisletti, Serena, Polletti, Sara, Tusi, Betsabeh Khoramian, Muller, Heiko, Ragoussis, Jiannis, Wei, Chia-Lin, Natoli, Gioacchino
Format:	Journal Article
Language:	English
Published:	United States Public Library of Science 01.05.2010 Public Library of Science (PLoS)
Subjects:	Animals Binding Sites Binding sites (Biochemistry) Cell Biology/Gene Expression Cell Biology/Leukocyte Signaling and Gene Expression Experiments Female Fractions Gene Expression Regulation Genetic transcription Genetics Genetics and Genomics/Epigenetics Genomes Genomics Humans Immunology/Innate Immunity Lipopolysaccharides - immunology Macrophage Activation - immunology Mice Molecular Biology/Histone Modification Noise Physiological aspects Promoter Regions, Genetic - genetics Proteins Regulatory Sequences, Nucleic Acid RNA polymerase RNA Polymerase II - genetics RNA Polymerase II - metabolism RNA polymerases RNA, Untranslated - genetics Signatures Transcription, Genetic Italy United Kingdom Singapore Promoter Regions, Genetic Humans RNA, Untranslated Regulatory Sequences, Nucleic Acid Gene Expression Regulation Lipopolysaccharides Macrophage Activation Animals Female Transcription, Genetic Mice Binding Sites RNA Polymerase II
ISSN:	1545-7885, 1544-9173, 1545-7885
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Abstract	Mammalian genomes are pervasively transcribed outside mapped protein-coding genes. One class of extragenic transcription products is represented by long non-coding RNAs (lncRNAs), some of which result from Pol_II transcription of bona-fide RNA genes. Whether all lncRNAs described insofar are products of RNA genes, however, is still unclear. Here we have characterized transcription sites located outside protein-coding genes in a highly regulated response, macrophage activation by endotoxin. Using chromatin signatures, we could unambiguously classify extragenic Pol_II binding sites as belonging to either canonical RNA genes or transcribed enhancers. Unexpectedly, 70% of extragenic Pol_II peaks were associated with genomic regions with a canonical chromatin signature of enhancers. Enhancer-associated extragenic transcription was frequently adjacent to inducible inflammatory genes, was regulated in response to endotoxin stimulation, and generated very low abundance transcripts. Moreover, transcribed enhancers were under purifying selection and contained binding sites for inflammatory transcription factors, thus suggesting their functionality. These data demonstrate that a large fraction of extragenic Pol_II transcription sites can be ascribed to cis-regulatory genomic regions. Discrimination between lncRNAs generated by canonical RNA genes and products of transcribed enhancers will provide a framework for experimental approaches to lncRNAs and help complete the annotation of mammalian genomes.
AbstractList	Mammalian genomes are pervasively transcribed outside mapped protein-coding genes. One class of extragenic transcription products is represented by long non-coding RNAs (lncRNAs), some of which result from Pol_II transcription of bona-fide RNA genes. Whether all lncRNAs described insofar are products of RNA genes, however, is still unclear. Here we have characterized transcription sites located outside protein-coding genes in a highly regulated response, macrophage activation by endotoxin. Using chromatin signatures, we could unambiguously classify extragenic Pol_II binding sites as belonging to either canonical RNA genes or transcribed enhancers. Unexpectedly, 70% of extragenic Pol_II peaks were associated with genomic regions with a canonical chromatin signature of enhancers. Enhancer-associated extragenic transcription was frequently adjacent to inducible inflammatory genes, was regulated in response to endotoxin stimulation, and generated very low abundance transcripts. Moreover, transcribed enhancers were under purifying selection and contained binding sites for inflammatory transcription factors, thus suggesting their functionality. These data demonstrate that a large fraction of extragenic Pol_II transcription sites can be ascribed to cis-regulatory genomic regions. Discrimination between lncRNAs generated by canonical RNA genes and products of transcribed enhancers will provide a framework for experimental approaches to lncRNAs and help complete the annotation of mammalian genomes. Mammalian genomes are pervasively transcribed outside mapped protein-coding genes. One class of extragenic transcription products is represented by long non-coding RNAs (lncRNAs), some of which result from Pol_II transcription of bona-fide RNA genes. Whether all lncRNAs described insofar are products of RNA genes, however, is still unclear. Here we have characterized transcription sites located outside protein-coding genes in a highly regulated response, macrophage activation by endotoxin. Using chromatin signatures, we could unambiguously classify extragenic Pol_II binding sites as belonging to either canonical RNA genes or transcribed enhancers. Unexpectedly, 70% of extragenic Pol_II peaks were associated with genomic regions with a canonical chromatin signature of enhancers. Enhancer-associated extragenic transcription was frequently adjacent to inducible inflammatory genes, was regulated in response to endotoxin stimulation, and generated very low abundance transcripts. Moreover, transcribed enhancers were under purifying selection and contained binding sites for inflammatory transcription factors, thus suggesting their functionality. These data demonstrate that a large fraction of extragenic Pol_II transcription sites can be ascribed to cis-regulatory genomic regions. Discrimination between lncRNAs generated by canonical RNA genes and products of transcribed enhancers will provide a framework for experimental approaches to lncRNAs and help complete the annotation of mammalian genomes. A substantial fraction of extragenic Pol II transcription sites coincides with transcriptional enhancers, which may be relevant for functional annotation of mammalian genomes. Mammalian genomes are pervasively transcribed outside mapped protein-coding genes. One class of extragenic transcription products is represented by long non-coding RNAs (lncRNAs), some of which result from Pol_II transcription of bona-fide RNA genes. Whether all lncRNAs described insofar are products of RNA genes, however, is still unclear. Here we have characterized transcription sites located outside protein-coding genes in a highly regulated response, macrophage activation by endotoxin. Using chromatin signatures, we could unambiguously classify extragenic Pol_II binding sites as belonging to either canonical RNA genes or transcribed enhancers. Unexpectedly, 70% of extragenic Pol_II peaks were associated with genomic regions with a canonical chromatin signature of enhancers. Enhancer-associated extragenic transcription was frequently adjacent to inducible inflammatory genes, was regulated in response to endotoxin stimulation, and generated very low abundance transcripts. Moreover, transcribed enhancers were under purifying selection and contained binding sites for inflammatory transcription factors, thus suggesting their functionality. These data demonstrate that a large fraction of extragenic Pol_II transcription sites can be ascribed to cis-regulatory genomic regions. Discrimination between lncRNAs generated by canonical RNA genes and products of transcribed enhancers will provide a framework for experimental approaches to lncRNAs and help complete the annotation of mammalian genomes. Mammalian genomes contain vast intergenic regions that are extensively transcribed and generate various types of short and long non-coding RNAs (ncRNAs). Although in some cases specific functions have been assigned to intergenic transcripts, the functional significance of this transcriptional output remains largely unknown, and the possibility exists that part of this transcription reflects noise generated by random collisions of the transcriptional machinery with the genome to generate meaningless transcription. In this study we used chromatin signatures to characterize extragenic transcription sites targeted by RNA Polymerase II (RNA Pol II) in a highly regulated response—endotoxin activation of macrophages. We found that a significant portion of extragenic transcription sites are associated with the chromatin signature characteristic of enhancers. Consistent with their chromatin signature, we found that these extragenic transcription sites are under purifying selection and contain binding sites for inflammatory transcription factors, as well as for PU.1, a hematopoietic transcription factor that marks enhancers in macrophages. Moreover, much of this extragenic transcription is regulated by stimulation. We also identified hundreds of transcribed regions with a signature of canonical RNA genes. Our data indicate that extragenic transcription sites can be efficiently classified using chromatin signatures, which will be relevant for functional annotation of mammalian genomes. Mammalian genomes are pervasively transcribed outside mapped protein-coding genes. One class of extragenic transcription products is represented by long non-coding RNAs (lncRNAs), some of which result from Pol_II transcription of bona-fide RNA genes. Whether all lncRNAs described insofar are products of RNA genes, however, is still unclear. Here we have characterized transcription sites located outside protein-coding genes in a highly regulated response, macrophage activation by endotoxin. Using chromatin signatures, we could unambiguously classify extragenic Pol_II binding sites as belonging to either canonical RNA genes or transcribed enhancers. Unexpectedly, 70% of extragenic Pol_II peaks were associated with genomic regions with a canonical chromatin signature of enhancers. Enhancer-associated extragenic transcription was frequently adjacent to inducible inflammatory genes, was regulated in response to endotoxin stimulation, and generated very low abundance transcripts. Moreover, transcribed enhancers were under purifying selection and contained binding sites for inflammatory transcription factors, thus suggesting their functionality. These data demonstrate that a large fraction of extragenic Pol_II transcription sites can be ascribed to cis-regulatory genomic regions. Discrimination between lncRNAs generated by canonical RNA genes and products of transcribed enhancers will provide a framework for experimental approaches to lncRNAs and help complete the annotation of mammalian genomes.Mammalian genomes are pervasively transcribed outside mapped protein-coding genes. One class of extragenic transcription products is represented by long non-coding RNAs (lncRNAs), some of which result from Pol_II transcription of bona-fide RNA genes. Whether all lncRNAs described insofar are products of RNA genes, however, is still unclear. Here we have characterized transcription sites located outside protein-coding genes in a highly regulated response, macrophage activation by endotoxin. Using chromatin signatures, we could unambiguously classify extragenic Pol_II binding sites as belonging to either canonical RNA genes or transcribed enhancers. Unexpectedly, 70% of extragenic Pol_II peaks were associated with genomic regions with a canonical chromatin signature of enhancers. Enhancer-associated extragenic transcription was frequently adjacent to inducible inflammatory genes, was regulated in response to endotoxin stimulation, and generated very low abundance transcripts. Moreover, transcribed enhancers were under purifying selection and contained binding sites for inflammatory transcription factors, thus suggesting their functionality. These data demonstrate that a large fraction of extragenic Pol_II transcription sites can be ascribed to cis-regulatory genomic regions. Discrimination between lncRNAs generated by canonical RNA genes and products of transcribed enhancers will provide a framework for experimental approaches to lncRNAs and help complete the annotation of mammalian genomes.
Audience	Academic
Author	Barozzi, Iros De Santa, Francesca Ghisletti, Serena Wei, Chia-Lin Mietton, Flore Polletti, Sara Ragoussis, Jiannis Tusi, Betsabeh Khoramian Muller, Heiko Natoli, Gioacchino
AuthorAffiliation	1 Department of Experimental Oncology, European Institute of Oncology (IEO) Campus IFOM-IEO, Milan, Italy 2 Genomics Laboratory, Wellcome Trust Centre for Human Genetics (WTCHG), University of Oxford, Oxford, United Kingdom 3 Genome Technology and Biology Group, Genome Institute of Singapore, Singapore University of Queensland, Australia
AuthorAffiliation_xml	– name: 3 Genome Technology and Biology Group, Genome Institute of Singapore, Singapore – name: University of Queensland, Australia – name: 2 Genomics Laboratory, Wellcome Trust Centre for Human Genetics (WTCHG), University of Oxford, Oxford, United Kingdom – name: 1 Department of Experimental Oncology, European Institute of Oncology (IEO) Campus IFOM-IEO, Milan, Italy
Author_xml	– sequence: 1 givenname: Francesca surname: De Santa fullname: De Santa, Francesca – sequence: 2 givenname: Iros surname: Barozzi fullname: Barozzi, Iros – sequence: 3 givenname: Flore surname: Mietton fullname: Mietton, Flore – sequence: 4 givenname: Serena surname: Ghisletti fullname: Ghisletti, Serena – sequence: 5 givenname: Sara surname: Polletti fullname: Polletti, Sara – sequence: 6 givenname: Betsabeh Khoramian surname: Tusi fullname: Tusi, Betsabeh Khoramian – sequence: 7 givenname: Heiko surname: Muller fullname: Muller, Heiko – sequence: 8 givenname: Jiannis surname: Ragoussis fullname: Ragoussis, Jiannis – sequence: 9 givenname: Chia-Lin surname: Wei fullname: Wei, Chia-Lin – sequence: 10 givenname: Gioacchino surname: Natoli fullname: Natoli, Gioacchino
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/20485488$$D View this record in MEDLINE/PubMed
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ContentType	Journal Article
Copyright	COPYRIGHT 2010 Public Library of Science De Santa et al. 2010 2010 De Santa et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, et al. (2010) A Large Fraction of Extragenic RNA Pol II Transcription Sites Overlap Enhancers. PLoS Biol 8(5): e1000384. doi:10.1371/journal.pbio.1000384
Copyright_xml	– notice: COPYRIGHT 2010 Public Library of Science – notice: De Santa et al. 2010 – notice: 2010 De Santa et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, et al. (2010) A Large Fraction of Extragenic RNA Pol II Transcription Sites Overlap Enhancers. PLoS Biol 8(5): e1000384. doi:10.1371/journal.pbio.1000384
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Keywords	Promoter Regions, Genetic Humans RNA, Untranslated Regulatory Sequences, Nucleic Acid Gene Expression Regulation Lipopolysaccharides Macrophage Activation Animals Female Transcription, Genetic Mice Binding Sites RNA Polymerase II
Language	English
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: FDS IB GN. Performed the experiments: FDS FM SG SP BKT. Analyzed the data: FDS IB FM SG SP HM GN. Contributed reagents/materials/analysis tools: JR CLW. Wrote the paper: GN.
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Snippet	Mammalian genomes are pervasively transcribed outside mapped protein-coding genes. One class of extragenic transcription products is represented by long... A substantial fraction of extragenic Pol II transcription sites coincides with transcriptional enhancers, which may be relevant for functional annotation of... Mammalian genomes are pervasively transcribed outside mapped protein-coding genes. One class of extragenic transcription products is represented by long...
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SubjectTerms	Animals Binding Sites Binding sites (Biochemistry) Cell Biology/Gene Expression Cell Biology/Leukocyte Signaling and Gene Expression Experiments Female Fractions Gene Expression Regulation Genetic transcription Genetics Genetics and Genomics/Epigenetics Genomes Genomics Humans Immunology/Innate Immunity Lipopolysaccharides - immunology Macrophage Activation - immunology Mice Molecular Biology/Histone Modification Noise Physiological aspects Promoter Regions, Genetic - genetics Proteins Regulatory Sequences, Nucleic Acid RNA polymerase RNA Polymerase II - genetics RNA Polymerase II - metabolism RNA polymerases RNA, Untranslated - genetics Signatures Transcription, Genetic
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Title	A Large Fraction of Extragenic RNA Pol II Transcription Sites Overlap Enhancers
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