Evidence for transcript networks composed of chimeric RNAs in human cells

Sarah Djebali; Julien Lagarde; Philipp Kapranov; Vincent Lacroix; Christelle Borel; Jonathan M Mudge; Cédric Howald; Sylvain Foissac; Catherine Ucla; Jacqueline Chrast; Paolo Ribeca; David Martin; Ryan R Murray; Xinping Yang; Lila Ghamsari; Chenwei Lin; Ian Bell; Erica Dumais; Jorg Drenkow; Michael L Tress; Josep Lluís Gelpí; Modesto Orozco; Alfonso Valencia; Nynke L van Berkum; Bryan R Lajoie; Marc Vidal; John Stamatoyannopoulos; Philippe Batut; Alex Dobin; Jennifer Harrow; Tim Hubbard; Job Dekker; Adam Frankish; Kourosh Salehi-Ashtiani; Alexandre Reymond; Stylianos E Antonarakis; Roderic Guigó; Thomas R Gingeras

doi:10.1371/journal.pone.0028213

Evidence for transcript networks composed of chimeric RNAs in human cells

Sarah Djebali, Julien Lagarde, Philipp Kapranov, Vincent Lacroix, Christelle Borel, Jonathan M Mudge, Cédric Howald, Sylvain Foissac, Catherine Ucla, Jacqueline Chrast, Paolo Ribeca, David Martin, Ryan R Murray, Xinping Yang, Lila Ghamsari, Chenwei Lin, Ian Bell, Erica Dumais, Jorg Drenkow, Michael L TressJosep Lluís Gelpí, Modesto Orozco, Alfonso Valencia, Nynke L van Berkum, Bryan R Lajoie, Marc Vidal, John Stamatoyannopoulos, Philippe Batut, Alex Dobin, Jennifer Harrow, Tim Hubbard, Job Dekker, Adam Frankish, Kourosh Salehi-Ashtiani, Alexandre Reymond, Stylianos E Antonarakis, Roderic Guigó, Thomas R Gingeras

Medical & Molecular Genetics

CRG Centre for Genomic Regulation

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

55 Citations (Scopus)

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.

Original language	English
Article number	e28213
Pages (from-to)	N/A
Number of pages	22
Journal	PLoS ONE
Volume	7
Issue number	1
DOIs	https://doi.org/10.1371/journal.pone.0028213
Publication status	Published - 4 Jan 2012

Keywords

Algorithms
Cells
Chimerin Proteins
Chromosomes, Human, Pair 1
Female
Gene Expression Profiling
Gene Regulatory Networks
Humans
Male
Microarray Analysis
Models, Biological
Nucleic Acid Amplification Techniques
RNA
RNA Isoforms
Transcription, Genetic
Transcriptome
Validation Studies as Topic

Access to Document

10.1371/journal.pone.0028213

Cite this

Djebali, S., Lagarde, J., Kapranov, P., Lacroix, V., Borel, C., Mudge, J. M., Howald, C., Foissac, S., Ucla, C., Chrast, J., Ribeca, P., Martin, D., Murray, R. R., Yang, X., Ghamsari, L., Lin, C., Bell, I., Dumais, E., Drenkow, J., ... Gingeras, T. R. (2012). Evidence for transcript networks composed of chimeric RNAs in human cells. PLoS ONE, 7(1), N/A. Article e28213. https://doi.org/10.1371/journal.pone.0028213

@article{5273485fdae5431eaa9c803c3ca5da8a,

title = "Evidence for transcript networks composed of chimeric RNAs in human cells",

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.",

keywords = "Algorithms, Cells, Chimerin Proteins, Chromosomes, Human, Pair 1, Female, Gene Expression Profiling, Gene Regulatory Networks, Humans, Male, Microarray Analysis, Models, Biological, Nucleic Acid Amplification Techniques, RNA, RNA Isoforms, Transcription, Genetic, Transcriptome, Validation Studies as Topic",

author = "Sarah Djebali and Julien Lagarde and Philipp Kapranov and Vincent Lacroix and Christelle Borel and Mudge, {Jonathan M} and C{\'e}dric Howald and Sylvain Foissac and Catherine Ucla and Jacqueline Chrast and Paolo Ribeca and David Martin and Murray, {Ryan R} and Xinping Yang and Lila Ghamsari and Chenwei Lin and Ian Bell and Erica Dumais and Jorg Drenkow and Tress, {Michael L} and Gelp{\'i}, {Josep Llu{\'i}s} and Modesto Orozco and Alfonso Valencia and {van Berkum}, {Nynke L} and Lajoie, {Bryan R} and Marc Vidal and John Stamatoyannopoulos and Philippe Batut and Alex Dobin and Jennifer Harrow and Tim Hubbard and Job Dekker and Adam Frankish and Kourosh Salehi-Ashtiani and Alexandre Reymond and Antonarakis, {Stylianos E} and Roderic Guig{\'o} and Gingeras, {Thomas R}",

year = "2012",

month = jan,

day = "4",

doi = "10.1371/journal.pone.0028213",

language = "English",

volume = "7",

pages = "N/A",

journal = "PLoS ONE",

issn = "1932-6203",

publisher = "Public Library of Science",

number = "1",

}

Djebali, S, Lagarde, J, Kapranov, P, Lacroix, V, Borel, C, Mudge, JM, Howald, C, Foissac, S, Ucla, C, Chrast, J, Ribeca, P, Martin, D, Murray, RR, Yang, X, Ghamsari, L, Lin, C, Bell, I, Dumais, E, Drenkow, J, Tress, ML, Gelpí, JL, Orozco, M, Valencia, A, van Berkum, NL, Lajoie, BR, Vidal, M, Stamatoyannopoulos, J, Batut, P, Dobin, A, Harrow, J, Hubbard, T, Dekker, J, Frankish, A, Salehi-Ashtiani, K, Reymond, A, Antonarakis, SE, Guigó, R & Gingeras, TR 2012, 'Evidence for transcript networks composed of chimeric RNAs in human cells', PLoS ONE, vol. 7, no. 1, e28213, pp. N/A. https://doi.org/10.1371/journal.pone.0028213

TY - JOUR

T1 - Evidence for transcript networks composed of chimeric RNAs in human cells

AU - Djebali, Sarah

AU - Lagarde, Julien

AU - Kapranov, Philipp

AU - Lacroix, Vincent

AU - Borel, Christelle

AU - Mudge, Jonathan M

AU - Howald, Cédric

AU - Foissac, Sylvain

AU - Ucla, Catherine

AU - Chrast, Jacqueline

AU - Ribeca, Paolo

AU - Martin, David

AU - Murray, Ryan R

AU - Yang, Xinping

AU - Ghamsari, Lila

AU - Lin, Chenwei

AU - Bell, Ian

AU - Dumais, Erica

AU - Drenkow, Jorg

AU - Tress, Michael L

AU - Gelpí, Josep Lluís

AU - Orozco, Modesto

AU - Valencia, Alfonso

AU - van Berkum, Nynke L

AU - Lajoie, Bryan R

AU - Vidal, Marc

AU - Stamatoyannopoulos, John

AU - Batut, Philippe

AU - Dobin, Alex

AU - Harrow, Jennifer

AU - Hubbard, Tim

AU - Dekker, Job

AU - Frankish, Adam

AU - Salehi-Ashtiani, Kourosh

AU - Reymond, Alexandre

AU - Antonarakis, Stylianos E

AU - Guigó, Roderic

AU - Gingeras, Thomas R

PY - 2012/1/4

Y1 - 2012/1/4

N2 - 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.

AB - 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.

KW - Algorithms

KW - Cells

KW - Chimerin Proteins

KW - Chromosomes, Human, Pair 1

KW - Female

KW - Gene Expression Profiling

KW - Gene Regulatory Networks

KW - Humans

KW - Male

KW - Microarray Analysis

KW - Models, Biological

KW - Nucleic Acid Amplification Techniques

KW - RNA

KW - RNA Isoforms

KW - Transcription, Genetic

KW - Transcriptome

KW - Validation Studies as Topic

U2 - 10.1371/journal.pone.0028213

DO - 10.1371/journal.pone.0028213

M3 - Article

C2 - 22238572

SN - 1932-6203

VL - 7

SP - N/A

JO - PLoS ONE

JF - PLoS ONE

IS - 1

M1 - e28213

ER -

Evidence for transcript networks composed of chimeric RNAs in human cells

Abstract

Keywords

Access to Document

Fingerprint

Cite this