A Landscape of Driver Mutations in Melanoma
Despite recent insights into melanoma genetics, systematic surveys for driver mutations are challenged by an abundance of passenger mutations caused by carcinogenic UV light exposure. We developed a permutation-based framework to address this challenge, employing mutation data from intronic sequence...
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| Published in | Cell Vol. 150; no. 2; pp. 251 - 263 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
20.07.2012
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Despite recent insights into melanoma genetics, systematic surveys for driver mutations are challenged by an abundance of passenger mutations caused by carcinogenic UV light exposure. We developed a permutation-based framework to address this challenge, employing mutation data from intronic sequences to control for passenger mutational load on a per gene basis. Analysis of large-scale melanoma exome data by this approach discovered six novel melanoma genes (PPP6C, RAC1, SNX31, TACC1, STK19, and ARID2), three of which—RAC1, PPP6C, and STK19—harbored recurrent and potentially targetable mutations. Integration with chromosomal copy number data contextualized the landscape of driver mutations, providing oncogenic insights in BRAF- and NRAS-driven melanoma as well as those without known NRAS/BRAF mutations. The landscape also clarified a mutational basis for RB and p53 pathway deregulation in this malignancy. Finally, the spectrum of driver mutations provided unequivocal genomic evidence for a direct mutagenic role of UV light in melanoma pathogenesis.
[Display omitted]
► Landscape of driver mutations by exon sequencing of 121 melanoma tumor/normal pairs ► Method for detecting genes with driver mutations in high-mutation-rate setting ► PPP6C, RAC1, SNX31, TACC1, STK19, and ARID2 are significantly mutated melanoma genes ► Signature spectrum of UV mutagenesis accounts for 46% of driver mutations found
A statistical approach for analyzing exome sequencing data differentiates between driver mutations and the abundant passenger mutations found in melanoma due to UV light exposure. Analysis of whole-exome sequence data from 121 tumors identifies six new melanoma genes and defines a landscape of driver mutations in this challenging malignancy. |
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| AbstractList | Despite recent insights into melanoma genetics, systematic surveys for driver mutations are challenged by an abundance of passenger mutations caused by carcinogenic ultraviolet (UV) light exposure. We developed a permutation-based framework to address this challenge, employing mutation data from intronic sequences to control for passenger mutational load on a per gene basis. Analysis of large-scale melanoma exome data by this approach discovered six novel melanoma genes (
PPP6C
,
RAC1
,
SNX31
,
TACC1
,
STK19
and
ARID2
), three of which -
RAC1
,
PPP6C
and
STK19
- harbored recurrent and potentially targetable mutations. Integration with chromosomal copy number data contextualized the landscape of driver mutations, providing oncogenic insights in BRAF- and NRAS-driven melanoma as well as those without known
NRAS
/
BRAF
mutations. The landscape also clarified a mutational basis for RB and p53 pathway deregulation in this malignancy. Finally, the spectrum of driver mutations provided unequivocal genomic evidence for a direct mutagenic role of UV light in melanoma pathogenesis. Despite recent insights into melanoma genetics, systematic surveys for driver mutations are challenged by an abundance of passenger mutations caused by carcinogenic UV light exposure. We developed a permutation-based framework to address this challenge, employing mutation data from intronic sequences to control for passenger mutational load on a per gene basis. Analysis of large-scale melanoma exome data by this approach discovered six novel melanoma genes (PPP6C, RAC1, SNX31, TACC1, STK19, and ARID2), three of which—RAC1, PPP6C, and STK19—harbored recurrent and potentially targetable mutations. Integration with chromosomal copy number data contextualized the landscape of driver mutations, providing oncogenic insights in BRAF- and NRAS-driven melanoma as well as those without known NRAS/BRAF mutations. The landscape also clarified a mutational basis for RB and p53 pathway deregulation in this malignancy. Finally, the spectrum of driver mutations provided unequivocal genomic evidence for a direct mutagenic role of UV light in melanoma pathogenesis. Despite recent insights into melanoma genetics, systematic surveys for driver mutations are challenged by an abundance of passenger mutations caused by carcinogenic UV light exposure. We developed a permutation-based framework to address this challenge, employing mutation data from intronic sequences to control for passenger mutational load on a per gene basis. Analysis of large-scale melanoma exome data by this approach discovered six novel melanoma genes (PPP6C, RAC1, SNX31, TACC1, STK19, and ARID2), three of which—RAC1, PPP6C, and STK19—harbored recurrent and potentially targetable mutations. Integration with chromosomal copy number data contextualized the landscape of driver mutations, providing oncogenic insights in BRAF- and NRAS-driven melanoma as well as those without known NRAS/BRAF mutations. The landscape also clarified a mutational basis for RB and p53 pathway deregulation in this malignancy. Finally, the spectrum of driver mutations provided unequivocal genomic evidence for a direct mutagenic role of UV light in melanoma pathogenesis. [Display omitted] ► Landscape of driver mutations by exon sequencing of 121 melanoma tumor/normal pairs ► Method for detecting genes with driver mutations in high-mutation-rate setting ► PPP6C, RAC1, SNX31, TACC1, STK19, and ARID2 are significantly mutated melanoma genes ► Signature spectrum of UV mutagenesis accounts for 46% of driver mutations found A statistical approach for analyzing exome sequencing data differentiates between driver mutations and the abundant passenger mutations found in melanoma due to UV light exposure. Analysis of whole-exome sequence data from 121 tumors identifies six new melanoma genes and defines a landscape of driver mutations in this challenging malignancy. |
| Author | Kryukov, Gregory V. Ladbury, John E. Winckler, Wendy Hodis, Eran Chong, Kelly Chen, Guo Li, Liren Chin, Lynda Arold, Stefan T. Davies, Michael A. Watson, Ian R. Imielinski, Marcin Place, Chelsea Schadendorf, Dirk Ramos, Alex H. Auclair, Daniel Wagle, Nikhil Stemke-Hale, Katherine Gershenwald, Jeffrey E. Sivachenko, Andrey Lawrence, Michael S. Saksena, Gordon Morton, Donald L. Onofrio, Robert C. Noble, Michael Lander, Eric S. Cibulskis, Kristian Voet, Douglas Wargo, Jennifer Hoon, Dave S.B. Wagner, Stephan N. Meyerson, Matthew Stransky, Nicolas DiCara, Daniel Garraway, Levi A. Ardlie, Kristin Getz, Gad Nickerson, Elizabeth Theurillat, Jean-Philippe Gabriel, Stacey B. |
| AuthorAffiliation | 3 Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA 4 Department of Biochemistry and Molecular Biology and Center for Biomolecular Structure and Function, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA 18 Whitehead Institute for Biomedical Research, 9 Cambridge Center, Cambridge, MA 02142, USA 16 Division of Immunology, Allergy and Infectious Diseases, Department of Dermatology, Medical University of Vienna and CeMM-Research, Center for Molecular Medicine of the Austrian Academy of Sciences, 1090 Vienna, Austria 14 Department of Molecular Oncology, John Wayne Cancer Institute, Santa Monica, CA 90404, USA 17 Department of Dermatology, University Hospital Essen, 45122 Essen, Germany 7 Department of Surgical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA 11 Center for Cancer Genome Discovery, Dana-Farber Cancer Institute, Boston, MA 02115, USA 9 Institute for Applied Cancer Scie |
| AuthorAffiliation_xml | – name: 1 The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – name: 7 Department of Surgical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – name: 17 Department of Dermatology, University Hospital Essen, 45122 Essen, Germany – name: 14 Department of Molecular Oncology, John Wayne Cancer Institute, Santa Monica, CA 90404, USA – name: 16 Division of Immunology, Allergy and Infectious Diseases, Department of Dermatology, Medical University of Vienna and CeMM-Research, Center for Molecular Medicine of the Austrian Academy of Sciences, 1090 Vienna, Austria – name: 8 Department of Cancer Biology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – name: 9 Institute for Applied Cancer Science, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – name: 5 Department of Systems Biology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – name: 18 Whitehead Institute for Biomedical Research, 9 Cambridge Center, Cambridge, MA 02142, USA – name: 10 Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02115, USA – name: 6 Department of Melanoma Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – name: 11 Center for Cancer Genome Discovery, Dana-Farber Cancer Institute, Boston, MA 02115, USA – name: 15 Melanoma Department, John Wayne Cancer Institute, Santa Monica, CA 90404, USA – name: 2 Harvard Medical School, Boston, MA 02115, USA – name: 12 Division of Genetics, Brigham and Women’s Hospital, Boston, MA 02115, USA – name: 13 Department of Surgery, Massachusetts General Hospital, Boston, MA 02114, USA – name: 3 Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – name: 4 Department of Biochemistry and Molecular Biology and Center for Biomolecular Structure and Function, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA |
| Author_xml | – sequence: 1 givenname: Eran surname: Hodis fullname: Hodis, Eran organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 2 givenname: Ian R. surname: Watson fullname: Watson, Ian R. organization: Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 3 givenname: Gregory V. surname: Kryukov fullname: Kryukov, Gregory V. organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 4 givenname: Stefan T. surname: Arold fullname: Arold, Stefan T. organization: Department of Biochemistry and Molecular Biology and Center for Biomolecular Structure and Function, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 5 givenname: Marcin surname: Imielinski fullname: Imielinski, Marcin organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 6 givenname: Jean-Philippe surname: Theurillat fullname: Theurillat, Jean-Philippe organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 7 givenname: Elizabeth surname: Nickerson fullname: Nickerson, Elizabeth organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 8 givenname: Daniel surname: Auclair fullname: Auclair, Daniel organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 9 givenname: Liren surname: Li fullname: Li, Liren organization: Department of Genomic Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 10 givenname: Chelsea surname: Place fullname: Place, Chelsea organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02115, USA – sequence: 11 givenname: Daniel surname: DiCara fullname: DiCara, Daniel organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 12 givenname: Alex H. surname: Ramos fullname: Ramos, Alex H. organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 13 givenname: Michael S. surname: Lawrence fullname: Lawrence, Michael S. organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 14 givenname: Kristian surname: Cibulskis fullname: Cibulskis, Kristian organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 15 givenname: Andrey surname: Sivachenko fullname: Sivachenko, Andrey organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 16 givenname: Douglas surname: Voet fullname: Voet, Douglas organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 17 givenname: Gordon surname: Saksena fullname: Saksena, Gordon organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 18 givenname: Nicolas surname: Stransky fullname: Stransky, Nicolas organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 19 givenname: Robert C. surname: Onofrio fullname: Onofrio, Robert C. organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 20 givenname: Wendy surname: Winckler fullname: Winckler, Wendy organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 21 givenname: Kristin surname: Ardlie fullname: Ardlie, Kristin organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 22 givenname: Nikhil surname: Wagle fullname: Wagle, Nikhil organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 23 givenname: Jennifer surname: Wargo fullname: Wargo, Jennifer organization: Department of Surgery, Massachusetts General Hospital, Boston, MA 02114, USA – sequence: 24 givenname: Kelly surname: Chong fullname: Chong, Kelly organization: Department of Molecular Oncology, John Wayne Cancer Institute, Santa Monica, CA 90404, USA – sequence: 25 givenname: Donald L. surname: Morton fullname: Morton, Donald L. organization: Melanoma Department, John Wayne Cancer Institute, Santa Monica, CA 90404, USA – sequence: 26 givenname: Katherine surname: Stemke-Hale fullname: Stemke-Hale, Katherine organization: Department of Systems Biology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 27 givenname: Guo surname: Chen fullname: Chen, Guo organization: Department of Melanoma Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 28 givenname: Michael surname: Noble fullname: Noble, Michael organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 29 givenname: Matthew surname: Meyerson fullname: Meyerson, Matthew organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 30 givenname: John E. surname: Ladbury fullname: Ladbury, John E. organization: Department of Biochemistry and Molecular Biology and Center for Biomolecular Structure and Function, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 31 givenname: Michael A. surname: Davies fullname: Davies, Michael A. organization: Department of Systems Biology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 32 givenname: Jeffrey E. surname: Gershenwald fullname: Gershenwald, Jeffrey E. organization: Department of Surgical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 33 givenname: Stephan N. surname: Wagner fullname: Wagner, Stephan N. organization: Division of Immunology, Allergy and Infectious Diseases, Department of Dermatology, Medical University of Vienna and CeMM-Research Center for Molecular Medicine of the Austrian Academy of Sciences, 1090 Vienna, Austria – sequence: 34 givenname: Dave S.B. surname: Hoon fullname: Hoon, Dave S.B. organization: Department of Molecular Oncology, John Wayne Cancer Institute, Santa Monica, CA 90404, USA – sequence: 35 givenname: Dirk surname: Schadendorf fullname: Schadendorf, Dirk organization: Department of Dermatology, University Hospital Essen, 45122 Essen, Germany – sequence: 36 givenname: Eric S. surname: Lander fullname: Lander, Eric S. organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 37 givenname: Stacey B. surname: Gabriel fullname: Gabriel, Stacey B. organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 38 givenname: Gad surname: Getz fullname: Getz, Gad organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 39 givenname: Levi A. surname: Garraway fullname: Garraway, Levi A. email: levi_garraway@dfci.harvard.edu organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – sequence: 40 givenname: Lynda surname: Chin fullname: Chin, Lynda email: lchin@mdanderson.org organization: The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22817889$$D View this record in MEDLINE/PubMed |
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| Notes | http://dx.doi.org/10.1016/j.cell.2012.06.024 These authors contributed equally to this work |
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| SubjectTerms | Amino Acid Sequence carcinogenicity Cells, Cultured Exome genes Genome-Wide Association Study Humans Melanocytes - metabolism melanoma Melanoma - genetics Models, Molecular Molecular Sequence Data Mutagenesis mutagenicity mutation pathogenesis Proto-Oncogene Proteins B-raf - genetics rac1 GTP-Binding Protein - genetics Sequence Alignment surveys ultraviolet radiation Ultraviolet Rays |
| Title | A Landscape of Driver Mutations in Melanoma |
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