Widespread Expansion of Protein Interaction Capabilities by Alternative Splicing

While alternative splicing is known to diversify the functional characteristics of some genes, the extent to which protein isoforms globally contribute to functional complexity on a proteomic scale remains unknown. To address this systematically, we cloned full-length open reading frames of alternat...

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Published in	Cell Vol. 164; no. 4; pp. 805 - 817
Main Authors	Yang, Xinping, Coulombe-Huntington, Jasmin, Kang, Shuli, Sheynkman, Gloria M., Hao, Tong, Richardson, Aaron, Sun, Song, Yang, Fan, Shen, Yun A., Murray, Ryan R., Spirohn, Kerstin, Begg, Bridget E., Duran-Frigola, Miquel, MacWilliams, Andrew, Pevzner, Samuel J., Zhong, Quan, Wanamaker, Shelly A., Tam, Stanley, Ghamsari, Lila, Sahni, Nidhi, Yi, Song, Rodriguez, Maria D., Balcha, Dawit, Tan, Guihong, Costanzo, Michael, Andrews, Brenda, Boone, Charles, Zhou, Xianghong J., Salehi-Ashtiani, Kourosh, Charloteaux, Benoit, Chen, Alyce A., Calderwood, Michael A., Aloy, Patrick, Roth, Frederick P., Hill, David E., Iakoucheva, Lilia M., Xia, Yu, Vidal, Marc
Format	Journal Article Web Resource
Language	English
Published	United States Elsevier Inc 11.02.2016 Cell Press
Subjects	Alternative Splicing Animals Cloning, Molecular Evolution, Molecular functional properties genes Genetics & genetic processes Génétique & processus génétiques Humans Life sciences Models, Molecular Open Reading Frames Protein Interaction Domains and Motifs Protein Interaction Maps protein isoforms Protein Isoforms - metabolism protein-protein interactions proteins Proteome - analysis Proteome - metabolism Proteome/analysis/metabolism proteomics Sciences du vivant
Online Access	Get full text
ISSN	0092-8674 1097-4172 1097-4172
DOI	10.1016/j.cell.2016.01.029

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Abstract	While alternative splicing is known to diversify the functional characteristics of some genes, the extent to which protein isoforms globally contribute to functional complexity on a proteomic scale remains unknown. To address this systematically, we cloned full-length open reading frames of alternatively spliced transcripts for a large number of human genes and used protein-protein interaction profiling to functionally compare hundreds of protein isoform pairs. The majority of isoform pairs share less than 50% of their interactions. In the global context of interactome network maps, alternative isoforms tend to behave like distinct proteins rather than minor variants of each other. Interaction partners specific to alternative isoforms tend to be expressed in a highly tissue-specific manner and belong to distinct functional modules. Our strategy, applicable to other functional characteristics, reveals a widespread expansion of protein interaction capabilities through alternative splicing and suggests that many alternative “isoforms” are functionally divergent (i.e., “functional alloforms”). [Display omitted] •Alternative splicing can produce isoforms with vastly different interaction profiles•These differences can be as great as those between proteins encoded by different genes•Isoform-specific partners exhibit distinct expression and functional characteristics Alternatively spliced isoforms of proteins exhibit strikingly different interaction profiles and thus, in the context of global interactome networks, appear to behave as if encoded by distinct genes rather than as minor variants of each other.
AbstractList	While alternative splicing is known to diversify the functional characteristics of some genes, the extent to which protein isoforms globally contribute to functional complexity on a proteomic scale remains unknown. To address this systematically, we cloned full-length open reading frames of alternatively spliced transcripts for a large number of human genes and used protein-protein interaction profiling to functionally compare hundreds of protein isoform pairs. The majority of isoform pairs share less than 50% of their interactions. In the global context of interactome network maps, alternative isoforms tend to behave like distinct proteins rather than minor variants of each other. Interaction partners specific to alternative isoforms tend to be expressed in a highly tissue-specific manner and belong to distinct functional modules. Our strategy, applicable to other functional characteristics, reveals a widespread expansion of protein interaction capabilities through alternative splicing and suggests that many alternative "isoforms'' are functionally divergent (i.e., "functional alloforms''). While alternative splicing is known to diversify the functional characteristics of some genes, the extent to which protein isoforms globally contribute to functional complexity on a proteomic scale remains unknown. To address this systematically, we cloned full-length open reading frames of alternatively spliced transcripts for a large number of human genes and used protein-protein interaction profiling to functionally compare hundreds of protein isoform pairs. The majority of isoform pairs share less than 50% of their interactions. In the global context of interactome network maps, alternative isoforms tend to behave like distinct proteins rather than minor variants of each other. Interaction partners specific to alternative isoforms tend to be expressed in a highly tissue-specific manner and belong to distinct functional modules. Our strategy, applicable to other functional characteristics, reveals a widespread expansion of protein interaction capabilities through alternative splicing and suggests that many alternative “isoforms” are functionally divergent (i.e., “functional alloforms”). [Display omitted] •Alternative splicing can produce isoforms with vastly different interaction profiles•These differences can be as great as those between proteins encoded by different genes•Isoform-specific partners exhibit distinct expression and functional characteristics Alternatively spliced isoforms of proteins exhibit strikingly different interaction profiles and thus, in the context of global interactome networks, appear to behave as if encoded by distinct genes rather than as minor variants of each other. While alternative splicing is known to diversify the functional characteristics of some genes, the extent to which protein isoforms globally contribute to functional complexity on a proteomic scale remains unknown. To address this systematically, we cloned full-length open reading frames of alternatively spliced transcripts for a large number of human genes and used protein-protein interaction profiling to functionally compare hundreds of protein isoform pairs. The majority of isoform pairs share less than 50% of their interactions. In the global context of interactome network maps, alternative isoforms tend to behave like distinct proteins rather than minor variants of each other. Interaction partners specific to alternative isoforms tend to be expressed in a highly tissue-specific manner and belong to distinct functional modules. Our strategy, applicable to other functional characteristics, reveals a widespread expansion of protein interaction capabilities through alternative splicing and suggests that many alternative ‘isoforms’ are functionally divergent (i.e., ‘functional alloforms’). eTOC Blurb Alternatively-spliced isoforms of proteins exhibit strikingly different interaction profiles and thus in the context of global interactome networks appear to behave as if encoded by distinct genes, rather than as minor variants of each other. While alternative splicing is known to diversify the functional characteristics of some genes, the extent to which protein isoforms globally contribute to functional complexity on a proteomic scale remains unknown. To address this systematically, we cloned full-length open reading frames of alternatively spliced transcripts for a large number of human genes and used protein-protein interaction profiling to functionally compare hundreds of protein isoform pairs. The majority of isoform pairs share less than 50% of their interactions. In the global context of interactome network maps, alternative isoforms tend to behave like distinct proteins rather than minor variants of each other. Interaction partners specific to alternative isoforms tend to be expressed in a highly tissue-specific manner and belong to distinct functional modules. Our strategy, applicable to other functional characteristics, reveals a widespread expansion of protein interaction capabilities through alternative splicing and suggests that many alternative "isoforms" are functionally divergent (i.e., "functional alloforms").While alternative splicing is known to diversify the functional characteristics of some genes, the extent to which protein isoforms globally contribute to functional complexity on a proteomic scale remains unknown. To address this systematically, we cloned full-length open reading frames of alternatively spliced transcripts for a large number of human genes and used protein-protein interaction profiling to functionally compare hundreds of protein isoform pairs. The majority of isoform pairs share less than 50% of their interactions. In the global context of interactome network maps, alternative isoforms tend to behave like distinct proteins rather than minor variants of each other. Interaction partners specific to alternative isoforms tend to be expressed in a highly tissue-specific manner and belong to distinct functional modules. Our strategy, applicable to other functional characteristics, reveals a widespread expansion of protein interaction capabilities through alternative splicing and suggests that many alternative "isoforms" are functionally divergent (i.e., "functional alloforms").
Author	Richardson, Aaron Wanamaker, Shelly A. Boone, Charles Yang, Xinping Spirohn, Kerstin Sun, Song Charloteaux, Benoit Zhou, Xianghong J. Aloy, Patrick Hao, Tong Duran-Frigola, Miquel Xia, Yu Kang, Shuli Rodriguez, Maria D. Pevzner, Samuel J. Sahni, Nidhi Sheynkman, Gloria M. Tan, Guihong Chen, Alyce A. Roth, Frederick P. Iakoucheva, Lilia M. Salehi-Ashtiani, Kourosh Murray, Ryan R. Costanzo, Michael Andrews, Brenda MacWilliams, Andrew Vidal, Marc Begg, Bridget E. Shen, Yun A. Yi, Song Ghamsari, Lila Hill, David E. Balcha, Dawit Zhong, Quan Yang, Fan Calderwood, Michael A. Coulombe-Huntington, Jasmin Tam, Stanley
AuthorAffiliation	6 Department of Psychiatry, University of California, San Diego, La Jolla, CA 92093, USA 11 Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology, Barcelona 08028, Catalonia, Spain 9 Lunenfeld-Tanenbaum Research Institute, Mt. Sinai Hospital, Toronto, ON M5G 1X5, Canada 5 Department of Bioengineering, McGill University, Montreal, QC H3A 0C3, Canada 8 Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 3E1, Canada 1 Genomic Analysis of Network Perturbations Center of Excellence in Genomic Science (CEGS), Dana-Farber Cancer Institute, Boston, MA 02215, USA 3 Department of Genetics, Harvard Medical School, Boston, MA 02115, USA 2 Center for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, USA 15 Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona 08010, Catalonia, Spain 7 Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada 16 Canadia
AuthorAffiliation_xml	– name: 6 Department of Psychiatry, University of California, San Diego, La Jolla, CA 92093, USA – name: 4 Department of Obstetrics and Gynecology, Nanfang Hospital, Southern Medical University, Guangzhou 510515, China – name: 16 Canadian Institute for Advanced Research, Toronto, ON M5G 1Z8, Canada – name: 7 Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada – name: 13 Boston University School of Medicine, Boston, MA 02118, USA – name: 8 Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 3E1, Canada – name: 12 Department of Biomedical Engineering, Boston University, Boston, MA 02215, USA – name: 9 Lunenfeld-Tanenbaum Research Institute, Mt. Sinai Hospital, Toronto, ON M5G 1X5, Canada – name: 10 Department of Medical Biochemistry and Microbiology, Uppsala University, SE-75123 Uppsala, Sweden – name: 3 Department of Genetics, Harvard Medical School, Boston, MA 02115, USA – name: 14 Molecular and Computational Biology Program, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089, USA – name: 1 Genomic Analysis of Network Perturbations Center of Excellence in Genomic Science (CEGS), Dana-Farber Cancer Institute, Boston, MA 02215, USA – name: 11 Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology, Barcelona 08028, Catalonia, Spain – name: 5 Department of Bioengineering, McGill University, Montreal, QC H3A 0C3, Canada – name: 15 Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona 08010, Catalonia, Spain – name: 2 Center for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, USA
Author_xml	– sequence: 1 givenname: Xinping surname: Yang fullname: Yang, Xinping organization: Genomic Analysis of Network Perturbations Center of Excellence in Genomic Science (CEGS), Dana-Farber Cancer Institute, Boston, MA 02215, USA – sequence: 2 givenname: Jasmin surname: Coulombe-Huntington fullname: Coulombe-Huntington, Jasmin organization: Department of Bioengineering, McGill University, Montreal, QC H3A 0C3, Canada – sequence: 3 givenname: Shuli surname: Kang fullname: Kang, Shuli organization: Department of Psychiatry, University of California, San Diego, La Jolla, CA 92093, USA – sequence: 4 givenname: Gloria M. surname: Sheynkman fullname: Sheynkman, Gloria M. organization: Genomic Analysis of Network Perturbations Center of Excellence in Genomic Science (CEGS), Dana-Farber Cancer Institute, Boston, MA 02215, USA – sequence: 5 givenname: Tong surname: Hao fullname: Hao, Tong organization: Genomic Analysis of Network Perturbations Center of Excellence in Genomic Science 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fullname: Tan, Guihong organization: Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada – sequence: 25 givenname: Michael surname: Costanzo fullname: Costanzo, Michael organization: Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada – sequence: 26 givenname: Brenda surname: Andrews fullname: Andrews, Brenda organization: Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada – sequence: 27 givenname: Charles surname: Boone fullname: Boone, Charles organization: Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada – sequence: 28 givenname: Xianghong J. surname: Zhou fullname: Zhou, Xianghong J. organization: Molecular and Computational Biology Program, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089, USA – sequence: 29 givenname: Kourosh surname: Salehi-Ashtiani fullname: Salehi-Ashtiani, Kourosh organization: Center for Cancer Systems Biology (CCSB) and Department of Cancer 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marc_vidal@dfci.harvard.edu organization: Genomic Analysis of Network Perturbations Center of Excellence in Genomic Science (CEGS), Dana-Farber Cancer Institute, Boston, MA 02215, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/26871637$$D View this record in MEDLINE/PubMed https://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-280244$$DView record from Swedish Publication Index
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Snippet	While alternative splicing is known to diversify the functional characteristics of some genes, the extent to which protein isoforms globally contribute to...
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SubjectTerms	Alternative Splicing Animals Cloning, Molecular Evolution, Molecular functional properties genes Genetics & genetic processes Génétique & processus génétiques Humans Life sciences Models, Molecular Open Reading Frames Protein Interaction Domains and Motifs Protein Interaction Maps protein isoforms Protein Isoforms - metabolism protein-protein interactions proteins Proteome - analysis Proteome - metabolism Proteome/analysis/metabolism proteomics Sciences du vivant
Title	Widespread Expansion of Protein Interaction Capabilities by Alternative Splicing
URI	https://dx.doi.org/10.1016/j.cell.2016.01.029 https://www.ncbi.nlm.nih.gov/pubmed/26871637 https://www.proquest.com/docview/1765108457 https://www.proquest.com/docview/2000213325 http://orbi.ulg.ac.be/handle/2268/238832 https://pubmed.ncbi.nlm.nih.gov/PMC4882190 https://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-280244
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