Evidence for Transcript Networks Composed of Chimeric RNAs in Human Cells

The classic organization of a gene structure has followed the Jacob and Monod bacterial gene model proposed more than 50 years ago. Since then, empirical determinations of the complexity of the transcriptomes found in yeast to human has blurred the definition and physical boundaries of genes. Using...

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Published inPloS one Vol. 7; no. 1; pp. e28213 - 22
Main Authors Djebali, Sarah, Lagarde, Julien, Kapranov, Philipp, Lacroix, Vincent, Borel, Christelle, Mudge, Jonathan M., Howald, Cédric, Foissac, Sylvain, Ucla, Catherine, Chrast, Jacqueline, Ribeca, Paolo, Martin, David, Murray, Ryan R., Yang, Xinping, Ghamsari, Lila, Lin, Chenwei, Bell, Ian, Dumais, Erica, Drenkow, Jorg, Tress, Michael L., Gelpí, Josep Lluís, Orozco, Modesto, Valencia, Alfonso, van Berkum, Nynke L., Lajoie, Bryan R., Vidal, Marc, Stamatoyannopoulos, John, Batut, Philippe, Dobin, Alex, Harrow, Jennifer, Hubbard, Tim, Dekker, Job, Frankish, Adam, Salehi-Ashtiani, Kourosh, Reymond, Alexandre, Antonarakis, Stylianos E., Guigó, Roderic, Gingeras, Thomas R.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 04.01.2012
Public Library of Science (PLoS)
Subjects
Algorithms
Analysis
Annotations
Biochemistry
Biochemistry, Molecular Biology
Bioinformatics
Biological evolution
Biology
Boundaries
Cancer
Cells (Biology)
Cells - metabolism
Chimerin Proteins - chemistry
Chimerin Proteins - genetics
Chromosomes
Chromosomes, Human, Pair 1 - genetics
Cloning
Computer Science
Empirical analysis
Encyclopedias
Exons
Female
Gene expression
Gene Expression Profiling
Gene mapping
Gene Regulatory Networks - genetics
Gene Regulatory Networks - physiology
Genes
Genetic aspects
Genetic transcription
Genetics
Genomes
Genomics
Genètica molecular
Humans
Laboratories
Life Sciences
Male
Mathematics
Medical research
Medical schools
Microarray Analysis - methods
Models, Biological
Molecular genetics
Molecular Networks
Nucleic Acid Amplification Techniques - methods
Other
Pharmacology
Phylogeny
Physicians
Proteomics
Quantitative Methods
Ribonucleic acid
RNA
RNA - genetics
RNA - physiology
RNA Isoforms - chemistry
RNA Isoforms - genetics
RNA Isoforms - metabolism
Supercomputers
Transcripció genètica
Transcription
Transcription (Genetics)
Transcription, Genetic - genetics
Transcriptome - physiology
Validation Studies as Topic
Yeast
New York
United Kingdom > UK
United States > US
Massachusetts
California
United Arab Emirates
Switzerland
Abu Dhabi United Arab Emirates
Spain
Online AccessGet full text
ISSN1932-6203
1932-6203
DOI10.1371/journal.pone.0028213

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Abstract The classic organization of a gene structure has followed the Jacob and Monod bacterial gene model proposed more than 50 years ago. Since then, empirical determinations of the complexity of the transcriptomes found in yeast to human has blurred the definition and physical boundaries of genes. Using multiple analysis approaches we have characterized individual gene boundaries mapping on human chromosomes 21 and 22. Analyses of the locations of the 5' and 3' transcriptional termini of 492 protein coding genes revealed that for 85% of these genes the boundaries extend beyond the current annotated termini, most often connecting with exons of transcripts from other well annotated genes. The biological and evolutionary importance of these chimeric transcripts is underscored by (1) the non-random interconnections of genes involved, (2) the greater phylogenetic depth of the genes involved in many chimeric interactions, (3) the coordination of the expression of connected genes and (4) the close in vivo and three dimensional proximity of the genomic regions being transcribed and contributing to parts of the chimeric RNAs. The non-random nature of the connection of the genes involved suggest that chimeric transcripts should not be studied in isolation, but together, as an RNA network.
AbstractList The classic organization of a gene structure has followed the Jacob and Monod bacterial gene model proposed more than 50 years ago. Since then, empirical determinations of the complexity of the transcriptomes found in yeast to human has blurred the definition and physical boundaries of genes. Using multiple analysis approaches we have characterized individual gene boundaries mapping on human chromosomes 21 and 22. Analyses of the locations of the 5' and 3' transcriptional termini of 492 protein coding genes revealed that for 85% of these genes the boundaries extend beyond the current annotated termini, most often connecting with exons of transcripts from other well annotated genes. The biological and evolutionary importance of these chimeric transcripts is underscored by (1) the non-random interconnections of genes involved, (2) the greater phylogenetic depth of the genes involved in many chimeric interactions, (3) the coordination of the expression of connected genes and (4) the close in vivo and three dimensional proximity of the genomic regions being transcribed and contributing to parts of the chimeric RNAs. The non-random nature of the connection of the genes involved suggest that chimeric transcripts should not be studied in isolation, but together, as an RNA network.The classic organization of a gene structure has followed the Jacob and Monod bacterial gene model proposed more than 50 years ago. Since then, empirical determinations of the complexity of the transcriptomes found in yeast to human has blurred the definition and physical boundaries of genes. Using multiple analysis approaches we have characterized individual gene boundaries mapping on human chromosomes 21 and 22. Analyses of the locations of the 5' and 3' transcriptional termini of 492 protein coding genes revealed that for 85% of these genes the boundaries extend beyond the current annotated termini, most often connecting with exons of transcripts from other well annotated genes. The biological and evolutionary importance of these chimeric transcripts is underscored by (1) the non-random interconnections of genes involved, (2) the greater phylogenetic depth of the genes involved in many chimeric interactions, (3) the coordination of the expression of connected genes and (4) the close in vivo and three dimensional proximity of the genomic regions being transcribed and contributing to parts of the chimeric RNAs. The non-random nature of the connection of the genes involved suggest that chimeric transcripts should not be studied in isolation, but together, as an RNA network.
The classic organization of a gene structure has followed the Jacob and Monod bacterial gene model proposed more than 50 years ago. Since then, empirical determinations of the complexity of the transcriptomes found in yeast to human has blurred the definition and physical boundaries of genes. Using multiple analysis approaches we have characterized individual gene boundaries mapping on human chromosomes 21 and 22. Analyses of the locations of the 5′ and 3′ transcriptional termini of 492 protein coding genes revealed that for 85% of these genes the boundaries extend beyond the current annotated termini, most often connecting with exons of transcripts from other well annotated genes. The biological and evolutionary importance of these chimeric transcripts is underscored by (1) the non-random interconnections of genes involved, (2) the greater phylogenetic depth of the genes involved in many chimeric interactions, (3) the coordination of the expression of connected genes and (4) the close in vivo and three dimensional proximity of the genomic regions being transcribed and contributing to parts of the chimeric RNAs. The non-random nature of the connection of the genes involved suggest that chimeric transcripts should not be studied in isolation, but together, as an RNA network.
The classic organization of a gene structure has followed the Jacob and Monod bacterial gene model proposed more than 50 years ago. Since then, empirical determinations of the complexity of the transcriptomes found in yeast to human has blurred the definition and physical boundaries of genes. Using multiple analysis approaches we have characterized individual gene boundaries mapping on human chromosomes 21 and 22. Analyses of the locations of the 5′ and 3′ transcriptional termini of 492 protein coding genes revealed that for 85% of these genes the boundaries extend beyond the current annotated termini, most often connecting with exons of transcripts from other well annotated genes. The biological and evolutionary importance of these chimeric transcripts is underscored by (1) the non-random interconnections of genes involved, (2) the greater phylogenetic depth of the genes involved in many chimeric interactions, (3) the coordination of the expression of connected genes and (4) the close in vivo and three dimensional proximity of the genomic regions being transcribed and contributing to parts of the chimeric RNAs. The non-random nature of the connection of the genes involved suggest that chimeric transcripts should not be studied in isolation, but together, as an RNA network.
The classic organization of a gene structure has followed the Jacob and Monod bacterial gene model proposed more than 50 years ago. Since then, empirical determinations of the complexity of the transcriptomes found in yeast to human has blurred the definition and physical boundaries of genes. Using multiple analysis approaches we have characterized individual gene boundaries mapping on human chromosomes 21 and 22. Analyses of the locations of the 59 and 39 transcriptional termini of 492 protein coding genes revealed that for 85% of these genes the boundaries extend beyond the current annotated termini, most often connecting with exons of transcripts from other well annotated genes. The biological and evolutionary importance of these chimeric transcripts is underscored by (1) the non-random interconnections of genes involved, (2) the greater phylogenetic depth of the genes involved in many chimeric interactions, (3) the coordination of the expression of connected genes and (4) the close in vivo and three dimensional proximity of the genomic regions being transcribed and contributing to parts of the chimeric RNAs. The non-random nature of the connection of the genes involved suggest that chimeric transcripts should not be studied in isolation, but together, as an RNA network.
Audience Academic
Author Reymond, Alexandre
Lajoie, Bryan R.
Orozco, Modesto
Antonarakis, Stylianos E.
Foissac, Sylvain
Lagarde, Julien
Stamatoyannopoulos, John
Dumais, Erica
Yang, Xinping
Borel, Christelle
Valencia, Alfonso
van Berkum, Nynke L.
Frankish, Adam
Lin, Chenwei
Ucla, Catherine
Kapranov, Philipp
Drenkow, Jorg
Djebali, Sarah
Mudge, Jonathan M.
Bell, Ian
Tress, Michael L.
Gingeras, Thomas R.
Dobin, Alex
Martin, David
Salehi-Ashtiani, Kourosh
Vidal, Marc
Guigó, Roderic
Murray, Ryan R.
Lacroix, Vincent
Harrow, Jennifer
Ghamsari, Lila
Batut, Philippe
Dekker, Job
Ribeca, Paolo
Gelpí, Josep Lluís
Hubbard, Tim
Howald, Cédric
Chrast, Jacqueline
AuthorAffiliation 10 Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, Massachusetts, United States of America
2 Affymetrix Inc., Santa Clara, California, United States of America
9 Institute of Research in Biomedicine and Barcelona Supercomputer Center, Joint Program on Computational Biology. Parc Científic de Barcelona, Universitat de Barcelona, Facultat de Biologia, Barcelona, Catalonia, Spain
1 Bioinformatics and Genomics, Centre for Genomic Regulation and Universitat Pompeu Fabra, Barcelona, Catalonia, Spain
5 The Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland
3 Department of Genetic Medicine and Development, University of Geneva Medical School, University Hospitals of Geneva, Geneva, Switzerland
11 University of Washington, Seattle, Washington, United States of America
8 Structural Biology and Biocomputing Programme, Spanish National Cancer Research Centre, Madrid, Spain
6 Center for Cancer Systems Biology and Depa
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– name: 9 Institute of Research in Biomedicine and Barcelona Supercomputer Center, Joint Program on Computational Biology. Parc Científic de Barcelona, Universitat de Barcelona, Facultat de Biologia, Barcelona, Catalonia, Spain
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/22238572$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2012 Public Library of Science
2012 Djebali et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
cc-by (c) Djebali, S. et al., 2012 info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by/3.0/es
Distributed under a Creative Commons Attribution 4.0 International License
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Copyright_xml – notice: COPYRIGHT 2012 Public Library of Science
– notice: 2012 Djebali et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: cc-by (c) Djebali, S. et al., 2012 info:eu-repo/semantics/openAccess <a href="http://creativecommons.org/licenses/by/3.0/es">http://creativecommons.org/licenses/by/3.0/es</a>
– notice: Distributed under a Creative Commons Attribution 4.0 International License
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Current address: Integromics, S.L., Grisolía, Tres Cantos, Madrid, Spain
Conceived and designed the experiments: TG RG SA AR KS-A J.Dekker SD JL SF MV JS. Performed the experiments: PK CB CH CU JC RM XY LG CL IB ED J.Drenkow NvB PB. Analyzed the data: SD JL VL JM SF PR DM MT JLG BL AD AF MO AV JH TH. Contributed reagents/materials/analysis tools: PK CB CH CL. Wrote the paper: TG RG SD VL JL.
Current address: Helicos BioSciences Corporation, Cambridge, Massachusetts, United States of America
Current address: Université Lyon 1, CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, INRIA BAMBOO, Villeurbanne, France
ORCID 0000-0002-4235-8524
0000-0002-0599-1267
0000-0002-0290-7445
0000-0002-3257-9876
0000-0003-3391-5410
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Snippet The classic organization of a gene structure has followed the Jacob and Monod bacterial gene model proposed more than 50 years ago. Since then, empirical...
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SubjectTerms Algorithms
Analysis
Annotations
Biochemistry
Biochemistry, Molecular Biology
Bioinformatics
Biological evolution
Biology
Boundaries
Cancer
Cells (Biology)
Cells - metabolism
Chimerin Proteins - chemistry
Chimerin Proteins - genetics
Chromosomes
Chromosomes, Human, Pair 1 - genetics
Cloning
Computer Science
Empirical analysis
Encyclopedias
Exons
Female
Gene expression
Gene Expression Profiling
Gene mapping
Gene Regulatory Networks - genetics
Gene Regulatory Networks - physiology
Genes
Genetic aspects
Genetic transcription
Genetics
Genomes
Genomics
Genètica molecular
Humans
Laboratories
Life Sciences
Male
Mathematics
Medical research
Medical schools
Microarray Analysis - methods
Models, Biological
Molecular genetics
Molecular Networks
Nucleic Acid Amplification Techniques - methods
Other
Pharmacology
Phylogeny
Physicians
Proteomics
Quantitative Methods
Ribonucleic acid
RNA
RNA - genetics
RNA - physiology
RNA Isoforms - chemistry
RNA Isoforms - genetics
RNA Isoforms - metabolism
Supercomputers
Transcripció genètica
Transcription
Transcription (Genetics)
Transcription, Genetic - genetics
Transcriptome - physiology
Validation Studies as Topic
Yeast
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Title Evidence for Transcript Networks Composed of Chimeric RNAs in Human Cells
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