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PMID: 26647970 Published · epublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

A comprehensive assessment of somatic mutation detection in cancer using whole-genome sequencing.

Nature communications ·Vol. 6 ·2015-12-09 ·Pages 10001

Alioto TS, Buchhalter I, Derdak S, Hutter B, Eldridge MD, Hovig E, Heisler LE, Beck TA, Simpson JT, Tonon L, Sertier AS, Patch AM, Jäger N, Ginsbach P, Drews R, Paramasivam N, Kabbe R, Chotewutmontri S, Diessl N, Previti C, Schmidt S, Brors B, Feuerbach L, Heinold M, Gröbner S, Korshunov A, Tarpey PS, Butler AP, Hinton J, Jones D, Menzies A, Raine K, Shepherd R, Stebbings L, Teague JW, Ribeca P, Giner FC, Beltran S, Raineri E, Dabad M, Heath SC, Gut M, Denroche RE, Harding NJ, Yamaguchi TN, Fujimoto A, Nakagawa H, Quesada V, Valdés-Mas R, Nakken S, Vodák D, Bower L, Lynch AG, Anderson CL, Waddell N, Pearson JV, Grimmond SM, Peto M, Spellman P, He M, Kandoth C, Lee S, Zhang J, Létourneau L, Ma S, Seth S, Torrents D, Xi L, Wheeler DA, López-Otín C, Campo E, Campbell PJ, Boutros PC, Puente XS, Gerhard DS, Pfister SM, McPherson JD, Hudson TJ, Schlesner M, Lichter P, Eils R, Jones DT, Gut IG

Abstract

As whole-genome sequencing for cancer genome analysis becomes a clinical tool, a full understanding of the variables affecting sequencing analysis output is required. Here using tumour-normal sample pairs from two different types of cancer, chronic lymphocytic leukaemia and medulloblastoma, we conduct a benchmarking exercise within the context of the International Cancer Genome Consortium. We compare sequencing methods, analysis pipelines and validation methods. We show that using PCR-free methods and increasing sequencing depth to ∼ 100 × shows benefits, as long as the tumour:control coverage ratio remains balanced. We observe widely varying mutation call rates and low concordance among analysis pipelines, reflecting the artefact-prone nature of the raw data and lack of standards for dealing with the artefacts. However, we show that, using the benchmark mutation set we have created, many issues are in fact easy to remedy and have an immediate positive impact on mutation detection accuracy.

MeSH Terms
Genome, Human High-Throughput Nucleotide Sequencing/methods Humans Leukemia, Lymphoid/genetics Medulloblastoma/genetics Mutation
Authors & Affiliations
83 authors, click to expand affiliations / ORCID
Alioto Tyler S ORCID
CNAG-CRG, Centre for Genomic Regulation, Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain. | Universitat Pompeu Fabra (UPF), 08002 Barcelona, Spain.
Buchhalter Ivo ORCID
Division of Theoretical Bioinformatics, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg 69120, Germany. | Division of Applied Bioinformatics, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg 69120, Germany.
Derdak Sophia
CNAG-CRG, Centre for Genomic Regulation, Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain. | Universitat Pompeu Fabra (UPF), 08002 Barcelona, Spain.
Hutter Barbara ORCID
Division of Applied Bioinformatics, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg 69120, Germany.
Eldridge Matthew D
Cancer Research UK Cambridge Institute, University of Cambridge, Li Ka Shing Centre, Robinson Way, Cambridge CB2 0RE, UK.
Hovig Eivind ORCID
Department of Tumor Biology, Institute for Cancer Research, Oslo University Hospital, 0424 Oslo, Norway. | Department of Informatics, University of Oslo, 0373 Oslo, Norway.
Heisler Lawrence E
Ontario Institute for Cancer Research, 661 University Avenue, Suite 510, Toronto, Ontario, Canada M5G 0A3.
Beck Timothy A
Ontario Institute for Cancer Research, 661 University Avenue, Suite 510, Toronto, Ontario, Canada M5G 0A3.
Simpson Jared T
Ontario Institute for Cancer Research, 661 University Avenue, Suite 510, Toronto, Ontario, Canada M5G 0A3.
Tonon Laurie
Synergie Lyon Cancer Foundation, Centre Léon Bérard, Cheney C, 28 rue Laennec, Lyon 69373, France.
Sertier Anne-Sophie
Synergie Lyon Cancer Foundation, Centre Léon Bérard, Cheney C, 28 rue Laennec, Lyon 69373, France.
Patch Ann-Marie ORCID
Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia. | QIMR Berghofer Medical Research Institute, Brisbane, Queensland 4006, Australia.
Jäger Natalie
Division of Theoretical Bioinformatics, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg 69120, Germany. | Department of Genetics, Stanford University, Mail Stop-5120, Stanford, California 94305-5120, USA.
Ginsbach Philip
Division of Theoretical Bioinformatics, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg 69120, Germany.
Drews Ruben ORCID
Division of Theoretical Bioinformatics, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg 69120, Germany.
Paramasivam Nagarajan
Division of Theoretical Bioinformatics, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg 69120, Germany.
Kabbe Rolf
Division of Theoretical Bioinformatics, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg 69120, Germany.
Chotewutmontri Sasithorn
Genome and Proteome Core Facility, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg, 69120 Germany.
Diessl Nicolle
Genome and Proteome Core Facility, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg, 69120 Germany.
Previti Christopher
Genome and Proteome Core Facility, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg, 69120 Germany.
Schmidt Sabine
Genome and Proteome Core Facility, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg, 69120 Germany.
Brors Benedikt
Division of Applied Bioinformatics, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg 69120, Germany.
Feuerbach Lars
Division of Applied Bioinformatics, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg 69120, Germany.
Heinold Michael
Division of Applied Bioinformatics, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg 69120, Germany.
Gröbner Susanne
Department of Pediatric Hematology and Oncology, Heidelberg University Hospital, Im Neuenheimer Feld 430, Heidelberg 69120, Germany.
Korshunov Andrey
Department of Neuropathology, Heidelberg University Hospital, Im Neuenheimer Feld 224, Heidelberg 69120, Germany.
Tarpey Patrick S
Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK.
Butler Adam P
Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK.
Hinton Jonathan
Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK.
Jones David
Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK.
Menzies Andrew
Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK.
Raine Keiran ORCID
Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK.
Shepherd Rebecca
Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK.
Stebbings Lucy
Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK.
Teague Jon W
Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK.
Ribeca Paolo ORCID
CNAG-CRG, Centre for Genomic Regulation, Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain. | Universitat Pompeu Fabra (UPF), 08002 Barcelona, Spain.
Giner Francesc Castro ORCID
CNAG-CRG, Centre for Genomic Regulation, Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain. | Universitat Pompeu Fabra (UPF), 08002 Barcelona, Spain.
Beltran Sergi
CNAG-CRG, Centre for Genomic Regulation, Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain. | Universitat Pompeu Fabra (UPF), 08002 Barcelona, Spain.
Raineri Emanuele
CNAG-CRG, Centre for Genomic Regulation, Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain. | Universitat Pompeu Fabra (UPF), 08002 Barcelona, Spain.
Dabad Marc
CNAG-CRG, Centre for Genomic Regulation, Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain. | Universitat Pompeu Fabra (UPF), 08002 Barcelona, Spain.
Heath Simon C ORCID
CNAG-CRG, Centre for Genomic Regulation, Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain. | Universitat Pompeu Fabra (UPF), 08002 Barcelona, Spain.
Gut Marta
CNAG-CRG, Centre for Genomic Regulation, Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain. | Universitat Pompeu Fabra (UPF), 08002 Barcelona, Spain.
Denroche Robert E ORCID
Ontario Institute for Cancer Research, 661 University Avenue, Suite 510, Toronto, Ontario, Canada M5G 0A3.
Harding Nicholas J
Ontario Institute for Cancer Research, 661 University Avenue, Suite 510, Toronto, Ontario, Canada M5G 0A3.
Yamaguchi Takafumi N ORCID
Ontario Institute for Cancer Research, 661 University Avenue, Suite 510, Toronto, Ontario, Canada M5G 0A3.
Fujimoto Akihiro
RIKEN Center for Integrative Medical Sciences, 4-6-1 Shirokanedai, Minato-ku, Tokyo 108-8639, Japan.
Nakagawa Hidewaki
RIKEN Center for Integrative Medical Sciences, 4-6-1 Shirokanedai, Minato-ku, Tokyo 108-8639, Japan.
Quesada Víctor
Universidad de Oviedo-IUOPA, C/Fernando Bongera s/n, 33006 Oviedo, Spain.
Valdés-Mas Rafael
Universidad de Oviedo-IUOPA, C/Fernando Bongera s/n, 33006 Oviedo, Spain.
Nakken Sigve
Department of Tumor Biology, Institute for Cancer Research, Oslo University Hospital, 0424 Oslo, Norway.
Vodák Daniel
Department of Tumor Biology, Institute for Cancer Research, Oslo University Hospital, 0424 Oslo, Norway. | The Bioinformatics Core Facility, Institute for Cancer Genetics and Informatics, Oslo University Hospital, 0310 Oslo, Norway.
Bower Lawrence
Cancer Research UK Cambridge Institute, University of Cambridge, Li Ka Shing Centre, Robinson Way, Cambridge CB2 0RE, UK.
Lynch Andrew G
Cancer Research UK Cambridge Institute, University of Cambridge, Li Ka Shing Centre, Robinson Way, Cambridge CB2 0RE, UK.
Anderson Charlotte L
Cancer Research UK Cambridge Institute, University of Cambridge, Li Ka Shing Centre, Robinson Way, Cambridge CB2 0RE, UK. | Victorian Life Sciences Computation Initiative, The University of Melbourne, Melbourne, Victoria 3053, Australia.
Waddell Nicola
Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia. | QIMR Berghofer Medical Research Institute, Brisbane, Queensland 4006, Australia.
Pearson John V
Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia. | QIMR Berghofer Medical Research Institute, Brisbane, Queensland 4006, Australia.
Grimmond Sean M
Queensland Centre for Medical Genomics, Institute for Molecular Bioscience, University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia. | WolfsonWohl Cancer Research Centre, Institute of Cancer Sciences, University of Glasgow, Glasgow, Scotland G61 1QH, UK.
Peto Myron
Knight Cancer Institute, Oregon Health and Science University, Portland, Oregon 97239-3098, USA.
Spellman Paul
Knight Cancer Institute, Oregon Health and Science University, Portland, Oregon 97239-3098, USA.
He Minghui
BGI-Shenzhen, Shenzhen 518083, China.
Kandoth Cyriac
The Genome Institute, Washington University, St Louis, Missouri 63108, USA.
Lee Semin
Harvard Medical School, Boston, Massachusetts 02115, USA.
Zhang John
Harvard Medical School, Boston, Massachusetts 02115, USA. | MD Anderson Cancer Center, Houston, Texas 77030, USA.
Létourneau Louis
McGill University, Montreal, Quebec, Canada QC H3A 0G4.
Ma Singer
Center for Biomolecular Science and Engineering, University of California, Santa Cruz, California 95064, USA.
Seth Sahil ORCID
MD Anderson Cancer Center, Houston, Texas 77030, USA.
Torrents David
IRB-BSC Joint Research Program on Computational Biology, Barcelona Supercomputing Center, 08034 Barcelona, Spain.
Xi Liu
Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.
Wheeler David A
Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.
López-Otín Carlos
Universidad de Oviedo-IUOPA, C/Fernando Bongera s/n, 33006 Oviedo, Spain.
Campo Elías
Hematopathology Unit, Department of Pathology, Hospital Clinic, University of Barcelona, Institut d'Investigacions Biomèdiques August Pi i Sunyer, 08036 Barcelona, Spain.
Campbell Peter J
Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK.
Boutros Paul C ORCID
Synergie Lyon Cancer Foundation, Centre Léon Bérard, Cheney C, 28 rue Laennec, Lyon 69373, France. | Department of Medical Biophysics, University of Toronto, Toronto, Ontario, Canada M5G 1L7.
Puente Xose S
Universidad de Oviedo-IUOPA, C/Fernando Bongera s/n, 33006 Oviedo, Spain.
Gerhard Daniela S
National Cancer Institute, Office of Cancer Genomics, 31 Center Drive, 10A07, Bethesda, Maryland 20892-2580, USA.
Pfister Stefan M
Department of Pediatric Hematology and Oncology, Heidelberg University Hospital, Im Neuenheimer Feld 430, Heidelberg 69120, Germany. | Division of Pediatric Neurooncology, German Cancer Research Center (DKFZ), Im Neuenheimer Feld 280, Heidelberg 69120, Germany.
McPherson John D
Ontario Institute for Cancer Research, 661 University Avenue, Suite 510, Toronto, Ontario, Canada M5G 0A3. | Department of Medical Biophysics, University of Toronto, Toronto, Ontario, Canada M5G 1L7.
Hudson Thomas J ORCID
Ontario Institute for Cancer Research, 661 University Avenue, Suite 510, Toronto, Ontario, Canada M5G 0A3. | Department of Medical Biophysics, University of Toronto, Toronto, Ontario, Canada M5G 1L7. | Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada M5S 1A8.
Schlesner Matthias
Division of Theoretical Bioinformatics, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg 69120, Germany.
Lichter Peter
Division of Molecular Genetics, German Cancer Research Center (DKFZ), Im Neuenheimer Feld 280, Heidelberg 69120,Germany. | Heidelberg Center for Personalised Oncology (DKFZ-HIPO), German Cancer Research Center (DKFZ), Heidelberg, Germany.
Eils Roland
Division of Theoretical Bioinformatics, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg 69120, Germany. | Heidelberg Center for Personalised Oncology (DKFZ-HIPO), German Cancer Research Center (DKFZ), Heidelberg, Germany. | Institute of Pharmacy and Molecular Biotechnology, University of Heidelberg, Heidelberg 69120, Germany. | Bioquant Center, University of Heidelberg, Im Neuenheimer Feld 267, Heidelberg 69120, Germany.
Jones David T W
Division of Pediatric Neurooncology, German Cancer Research Center (DKFZ), Im Neuenheimer Feld 280, Heidelberg 69120, Germany.
Gut Ivo G ORCID
CNAG-CRG, Centre for Genomic Regulation, Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain. | Universitat Pompeu Fabra (UPF), 08002 Barcelona, Spain.
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Article Info
Journal
Nature communications
Abbr.
Nat Commun
ISSN
2041-1723
DOI
10.1038/ncomms10001
Published
2015-12-09
Epub
2015-00-09
Pages
10001
Language
English
Region
England
NLM ID
101528555
PMCID
PMC4682041
Subset
IM
Grants
Canadian Institutes of Health Research · Canada
Cancer Research UK · United Kingdom
External Links
PubMed source DOI: 10.1038/ncomms10001 PMC Full Text View journal details
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