Breakpoint analysis of transcriptional and genomic profiles uncovers novel gene fusions spanning multiple human cancer types

Gene fusions, like BCR/ABL1 in chronic myelogenous leukemia, have long been recognized in hematologic and mesenchymal malignancies. The recent finding of gene fusions in prostate and lung cancers has motivated the search for pathogenic gene fusions in other malignancies. Here, we developed a "b...

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Published inPLoS genetics Vol. 9; no. 4; p. e1003464
Main Authors Giacomini, Craig P, Sun, Steven, Varma, Sushama, Shain, A Hunter, Giacomini, Marilyn M, Balagtas, Jay, Sweeney, Robert T, Lai, Everett, Del Vecchio, Catherine A, Forster, Andrew D, Clarke, Nicole, Montgomery, Kelli D, Zhu, Shirley, Wong, Albert J, van de Rijn, Matt, West, Robert B, Pollack, Jonathan R
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.04.2013
Public Library of Science (PLoS)
Subjects
Biology
Breast cancer
Cancer
Colorectal cancer
Deoxyribonucleic acid
DNA
Gene Fusion
Genes
Genetic aspects
Genetic transcription
Genomes
Genomics
Humans
Leukemia
Leukemia, Myelogenous, Chronic, BCR-ABL Positive - genetics
Medical research
Medicine
Melanoma
Oncogene Proteins, Fusion - genetics
Physiology, Pathological
Prostate cancer
Protein-Tyrosine Kinases - genetics
Proteins
Proto-Oncogene Proteins - genetics
Stomach cancer
United States
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Abstract Gene fusions, like BCR/ABL1 in chronic myelogenous leukemia, have long been recognized in hematologic and mesenchymal malignancies. The recent finding of gene fusions in prostate and lung cancers has motivated the search for pathogenic gene fusions in other malignancies. Here, we developed a "breakpoint analysis" pipeline to discover candidate gene fusions by tell-tale transcript level or genomic DNA copy number transitions occurring within genes. Mining data from 974 diverse cancer samples, we identified 198 candidate fusions involving annotated cancer genes. From these, we validated and further characterized novel gene fusions involving ROS1 tyrosine kinase in angiosarcoma (CEP85L/ROS1), SLC1A2 glutamate transporter in colon cancer (APIP/SLC1A2), RAF1 kinase in pancreatic cancer (ATG7/RAF1) and anaplastic astrocytoma (BCL6/RAF1), EWSR1 in melanoma (EWSR1/CREM), CDK6 kinase in T-cell acute lymphoblastic leukemia (FAM133B/CDK6), and CLTC in breast cancer (CLTC/VMP1). Notably, while these fusions involved known cancer genes, all occurred with novel fusion partners and in previously unreported cancer types. Moreover, several constituted druggable targets (including kinases), with therapeutic implications for their respective malignancies. Lastly, breakpoint analysis identified new cell line models for known rearrangements, including EGFRvIII and FIP1L1/PDGFRA. Taken together, we provide a robust approach for gene fusion discovery, and our results highlight a more widespread role of fusion genes in cancer pathogenesis.
AbstractList Gene fusions, like BCR/ABL1 in chronic myelogenous leukemia, have long been recognized in hematologic and mesenchymal malignancies. The recent finding of gene fusions in prostate and lung cancers has motivated the search for pathogenic gene fusions in other malignancies. Here, we developed a "breakpoint analysis" pipeline to discover candidate gene fusions by tell-tale transcript level or genomic DNA copy number transitions occurring within genes. Mining data from 974 diverse cancer samples, we identified 198 candidate fusions involving annotated cancer genes. From these, we validated and further characterized novel gene fusions involving ROS1 tyrosine kinase in angiosarcoma (CEP85L/ROS1), SLC1A2 glutamate transporter in colon cancer (APIP/SLC1A2), RAF1 kinase in pancreatic cancer (ATG7/RAF1) and anaplastic astrocytoma (BCL6/RAF1), EWSR1 in melanoma (EWSR1/CREM), CDK6 kinase in T-cell acute lymphoblastic leukemia (FAM133B/CDK6), and CLTC in breast cancer (CLTC/VMP1). Notably, while these fusions involved known cancer genes, all occurred with novel fusion partners and in previously unreported cancer types. Moreover, several constituted druggable targets (including kinases), with therapeutic implications for their respective malignancies. Lastly, breakpoint analysis identified new cell line models for known rearrangements, including EGFRvIII and FIP1L1/PDGFRA. Taken together, we provide a robust approach for gene fusion discovery, and our results highlight a more widespread role of fusion genes in cancer pathogenesis.
  Gene fusions, like BCR/ABL1 in chronic myelogenous leukemia, have long been recognized in hematologic and mesenchymal malignancies. The recent finding of gene fusions in prostate and lung cancers has motivated the search for pathogenic gene fusions in other malignancies. Here, we developed a "breakpoint analysis" pipeline to discover candidate gene fusions by tell-tale transcript level or genomic DNA copy number transitions occurring within genes. Mining data from 974 diverse cancer samples, we identified 198 candidate fusions involving annotated cancer genes. From these, we validated and further characterized novel gene fusions involving ROS1 tyrosine kinase in angiosarcoma (CEP85L/ROS1), SLC1A2 glutamate transporter in colon cancer (APIP/SLC1A2), RAF1 kinase in pancreatic cancer (ATG7/RAF1) and anaplastic astrocytoma (BCL6/RAF1), EWSR1 in melanoma (EWSR1/CREM), CDK6 kinase in T-cell acute lymphoblastic leukemia (FAM133B/CDK6), and CLTC in breast cancer (CLTC/VMP1). Notably, while these fusions involved known cancer genes, all occurred with novel fusion partners and in previously unreported cancer types. Moreover, several constituted druggable targets (including kinases), with therapeutic implications for their respective malignancies. Lastly, breakpoint analysis identified new cell line models for known rearrangements, including EGFRvIII and FIP1L1/PDGFRA. Taken together, we provide a robust approach for gene fusion discovery, and our results highlight a more widespread role of fusion genes in cancer pathogenesis.
Gene fusions, like BCR/ABL1 in chronic myelogenous leukemia, have long been recognized in hematologic and mesenchymal malignancies. The recent finding of gene fusions in prostate and lung cancers has motivated the search for pathogenic gene fusions in other malignancies. Here, we developed a “breakpoint analysis” pipeline to discover candidate gene fusions by tell-tale transcript level or genomic DNA copy number transitions occurring within genes. Mining data from 974 diverse cancer samples, we identified 198 candidate fusions involving annotated cancer genes. From these, we validated and further characterized novel gene fusions involving ROS1 tyrosine kinase in angiosarcoma ( CEP85L/ROS1 ), SLC1A2 glutamate transporter in colon cancer ( APIP/SLC1A2 ), RAF1 kinase in pancreatic cancer ( ATG7/RAF1 ) and anaplastic astrocytoma ( BCL6/RAF1 ), EWSR1 in melanoma ( EWSR1/CREM ), CDK6 kinase in T-cell acute lymphoblastic leukemia ( FAM133B/CDK6 ), and CLTC in breast cancer ( CLTC/VMP1 ). Notably, while these fusions involved known cancer genes, all occurred with novel fusion partners and in previously unreported cancer types. Moreover, several constituted druggable targets (including kinases), with therapeutic implications for their respective malignancies. Lastly, breakpoint analysis identified new cell line models for known rearrangements, including EGFRvIII and FIP1L1/PDGFRA . Taken together, we provide a robust approach for gene fusion discovery, and our results highlight a more widespread role of fusion genes in cancer pathogenesis. Gene fusions represent an important class of cancer genes, created by rearrangements of the genome that bring together two different genes. Because they are unique to cancer cells, gene fusions are ideal diagnostic markers and therapeutic targets. While gene fusions were once thought restricted mainly to blood cancers, recent discoveries suggest they are more widespread. Here, we have developed an approach for mining DNA microarray data to detect the tell-tale signatures of gene fusions, as “breakpoints” occurring within the encoding DNA or expressed transcripts. We apply this approach to a large collection of nearly 1,000 human cancer specimens. From this analysis, we discover and verify twelve new gene fusions occurring in diverse cancer types. We verify that some of these rearrangements recur in other samples of the same cancer type (supporting a causal role) and that the cancers show dependency on the fusion for cancer cell growth. Notably, some of these fusions (e.g. CEP85L/ROS1 in angiosarcoma) represent the first for that cancer type and thus provide important new biological insight. Some are also good drug targets (including rearrangements of ROS1 , RAF1 , and CDK6 kinases), with clear implications for therapy.
Audience Academic
Author Montgomery, Kelli D
Shain, A Hunter
Lai, Everett
Giacomini, Marilyn M
Sweeney, Robert T
West, Robert B
Forster, Andrew D
van de Rijn, Matt
Pollack, Jonathan R
Sun, Steven
Balagtas, Jay
Zhu, Shirley
Giacomini, Craig P
Del Vecchio, Catherine A
Wong, Albert J
Varma, Sushama
Clarke, Nicole
AuthorAffiliation 1 Department of Pathology, Stanford University School of Medicine, Stanford, California, United States of America
4 Department of Neurosurgery, Stanford University School of Medicine, Stanford, California, United States of America
3 Department of Pediatrics, Stanford University School of Medicine, Stanford, California, United States of America
2 Department of Medicine, University of California San Francisco, San Francisco, California, United States of America
University of Washington, United States of America
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/23637631$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2013 Public Library of Science
2013 Giacomini et al 2013 Giacomini et al
2013 Giacomini 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: Giacomini CP, Sun S, Varma S, Shain AH, Giacomini MM, et al. (2013) Breakpoint Analysis of Transcriptional and Genomic Profiles Uncovers Novel Gene Fusions Spanning Multiple Human Cancer Types. PLoS Genet 9(4): e1003464. doi:10.1371/journal.pgen.1003464
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– notice: 2013 Giacomini 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: Giacomini CP, Sun S, Varma S, Shain AH, Giacomini MM, et al. (2013) Breakpoint Analysis of Transcriptional and Genomic Profiles Uncovers Novel Gene Fusions Spanning Multiple Human Cancer Types. PLoS Genet 9(4): e1003464. doi:10.1371/journal.pgen.1003464
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Conceived and designed the experiments: CPG JRP. Performed the experiments: CPG SV AHS MMG JB RTS CADV ADF NC KDM SZ. Analyzed the data: CPG SS SV AHS MMG JB RTS EL CADV ADF SZ AJW RBW JRP. Contributed reagents/materials/analysis tools: CPG AJW MvdR RBW JRP. Wrote the paper: CPG JRP.
The authors have declared that no competing interests exist.
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3636093/
PMID 23637631
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Snippet Gene fusions, like BCR/ABL1 in chronic myelogenous leukemia, have long been recognized in hematologic and mesenchymal malignancies. The recent finding of gene...
Gene fusions, like BCR/ABL1 in chronic myelogenous leukemia, have long been recognized in hematologic and mesenchymal malignancies. The recent finding of gene...
  Gene fusions, like BCR/ABL1 in chronic myelogenous leukemia, have long been recognized in hematologic and mesenchymal malignancies. The recent finding of...
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SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
StartPage e1003464
SubjectTerms Biology
Breast cancer
Cancer
Colorectal cancer
Deoxyribonucleic acid
DNA
Gene Fusion
Genes
Genetic aspects
Genetic transcription
Genomes
Genomics
Humans
Leukemia
Leukemia, Myelogenous, Chronic, BCR-ABL Positive - genetics
Medical research
Medicine
Melanoma
Oncogene Proteins, Fusion - genetics
Physiology, Pathological
Prostate cancer
Protein-Tyrosine Kinases - genetics
Proteins
Proto-Oncogene Proteins - genetics
Stomach cancer
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Title Breakpoint analysis of transcriptional and genomic profiles uncovers novel gene fusions spanning multiple human cancer types
URI https://www.ncbi.nlm.nih.gov/pubmed/23637631
https://search.proquest.com/docview/1348500121
https://pubmed.ncbi.nlm.nih.gov/PMC3636093
https://doaj.org/article/92ff14bb419441ca9049ba522a6d3f11
http://dx.doi.org/10.1371/journal.pgen.1003464
Volume 9
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