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A meta-analysis of 87,040 individuals identifies 23 new susceptibility loci for prostate cancer.

Nat. Genet.2014 Oct;46(10):1103-9. Epub 2014 Sep 14
Ali Amin Al Olama 1 , Zsofia Kote-Jarai 2 , Sonja I Berndt 3 , David V Conti 4 , Fredrick Schumacher 4 , Ying Han 5 , Sara Benlloch 6 , Dennis J Hazelett 4 , Zhaoming Wang 7 , Ed Saunders 8 , Daniel Leongamornlert 8 , Sara Lindstrom 9 , Sara Jugurnauth-Little 8 , Tokhir Dadaev 8 , Malgorzata Tymrakiewicz 8 , Daniel O Stram 4 , Kristin Rand 5 , Peggy Wan 5 , Alex Stram 5 , Xin Sheng 5 , Loreall C Pooler 5 , Karen Park 5 , Lucy Xia 5 , Jonathan Tyrer 6 , Laurence N Kolonel 10 , Loic Le Marchand 10 , Robert N Hoover 3 , Mitchell J Machiela 3 , Merideth Yeager 3 , Laurie Burdette 3 , Charles C Chung 3 , Amy Hutchinson 3 , Kai Yu 3 , Chee Goh 8 , Mahbubl Ahmed 8 , Koveela Govindasami 8 , Michelle Guy 8 , Teuvo L J Tammela 11 , Anssi Auvinen 12 , Tiina Wahlfors 13 , Johanna Schleutker 14 , Tapio Visakorpi 15 , Katri A Leinonen 15 , Jianfeng Xu 16 , Markus Aly 17 , Jenny Donovan 18 , Ruth C Travis 19 , Tim J Key 19 , Afshan Siddiq 20 , Federico Canzian 21 , Kay-Tee Khaw 22 , Atsushi Takahashi 23 , Michiaki Kubo 24 , Paul Pharoah 25 , Nora Pashayan 25 , Maren Weischer 26 , Borge G Nordestgaard 27 , Sune F Nielsen 27 , Peter Klarskov 28 , Martin Andreas Røder 29 , Peter Iversen 29 , Stephen N Thibodeau 30 , Shannon K McDonnell 30 , Daniel J Schaid 30 , Janet L Stanford 31 , Suzanne Kolb 32 , Sarah Holt 33 , Beatrice Knudsen 34 , Antonio Hurtado Coll 35 , Susan M Gapstur 36 , W Ryan Diver 36 , Victoria L Stevens 36 , Christiane Maier 37 , Manuel Luedeke 37 , Kathleen Herkommer 38 , Antje E Rinckleb 37 , Sara S Strom 39 , Curtis Pettaway 40 , Edward D Yeboah 41 , Yao Tettey 41 , Richard B Biritwum 41 , Andrew A Adjei 41 , Evelyn Tay 41 , Ann Truelove 42 , Shelley Niwa 42 , Anand P Chokkalingam 43 , Lisa Cannon-Albright 44 , Cezary Cybulski 45 , Dominika Wokołorczyk 45 , Wojciech Kluźniak 45 , Jong Park 46 , Thomas Sellers 46 , Hui-Yi Lin 47 , William B Isaacs 48 , Alan W Partin 48 , Hermann Brenner 49 , Aida Karina Dieffenbach 49 , Christa Stegmaier 50 , Constance Chen 9 , Edward L Giovannucci 51 , Jing Ma 52 , Meir Stampfer 53 , Kathryn L Penney 54 , Lorelei Mucci 54 , Esther M John 55 , Sue A Ingles 4 , Rick A Kittles 56 , Adam B Murphy 57 , Hardev Pandha 58 , Agnieszka Michael 58 , Andrzej M Kierzek 58 , William Blot 59 , Lisa B Signorello 54 , Wei Zheng 60 , Demetrius Albanes 61 , Jarmo Virtamo 62 , Stephanie Weinstein 61 , Barbara Nemesure 63 , John Carpten 64 , Cristina Leske 63 , Suh-Yuh Wu 63 , Anselm Hennis 65 , Adam S Kibel 66 , Benjamin A Rybicki 67 , Christine Neslund-Dudas 67 , Ann W Hsing 55 , Lisa Chu 55 , Phyllis J Goodman 68 , Eric A Klein 69 , S Lilly Zheng 16 , Jyotsna Batra 70 , Judith Clements 70 , Amanda Spurdle 71 , Manuel R Teixeira 72 , Paula Paulo 73 , Sofia Maia 73 , Chavdar Slavov 74 , Radka Kaneva 75 , Vanio Mitev 75 , John S Witte 76 , Graham Casey 4 , Elizabeth M Gillanders 77 , Daniella Seminara 77 , Elio Riboli 78 , Freddie C Hamdy 79 , Gerhard A Coetzee 4 , Qiyuan Li 80 , Matthew L Freedman 80 , David J Hunter 9 , Kenneth Muir 81 , Henrik Gronberg 82 , David E Neal 83 , Melissa Southey 84 , Graham G Giles 85 , Gianluca Severi 86 , Breast and Prostate Cancer Cohort Consortium (BPC3) , PRACTICAL (Prostate Cancer Association Group to Investigate Cancer-Associated Alterations in the Genome) Consortium , COGS (Collaborative Oncological Gene-environment Study) Consortium , GAME-ON/ELLIPSE Consortium , Michael B Cook 87 , Hidewaki Nakagawa 88 , Fredrik Wiklund 89 , Peter Kraft 90 , Stephen J Chanock 87 , Brian E Henderson 91 , Douglas F Easton 1 , Rosalind A Eeles 92 , Christopher A Haiman 91
Ali Amin Al Olama 1 , Zsofia Kote-Jarai 2 , Sonja I Berndt 3 , David V Conti 4 , Fredrick Schumacher 4 , Ying Han 5 , Sara Benlloch 6 , Dennis J Hazelett 4 , Zhaoming Wang 7 , Ed Saunders 8 , Daniel Leongamornlert 8 , Sara Lindstrom 9 , Sara Jugurnauth-Little 8 , Tokhir Dadaev 8 , Malgorzata Tymrakiewicz 8 , Daniel O Stram 4 , Kristin Rand 5 , Peggy Wan 5 , Alex Stram 5 , Xin Sheng 5 , Loreall C Pooler 5 , Karen Park 5 , Lucy Xia 5 , Jonathan Tyrer 6 , Laurence N Kolonel 10 , Loic Le Marchand 10 , Robert N Hoover 3 , Mitchell J Machiela 3 , Merideth Yeager 3 , Laurie Burdette 3 , Charles C Chung 3 , Amy Hutchinson 3 , Kai Yu 3 , Chee Goh 8 , Mahbubl Ahmed 8 , Koveela Govindasami 8 , Michelle Guy 8 , Teuvo L J Tammela 11 , Anssi Auvinen 12 , Tiina Wahlfors 13 , Johanna Schleutker 14 , Tapio Visakorpi 15 , Katri A Leinonen 15 , Jianfeng Xu 16 , Markus Aly 17 , Jenny Donovan 18 , Ruth C Travis 19 , Tim J Key 19 , Afshan Siddiq 20 , Federico Canzian 21 , Kay-Tee Khaw 22 , Atsushi Takahashi 23 , Michiaki Kubo 24 , Paul Pharoah 25 , Nora Pashayan 25 , Maren Weischer 26 , Borge G Nordestgaard 27 , Sune F Nielsen 27 , Peter Klarskov 28 , Martin Andreas Røder 29 , Peter Iversen 29 , Stephen N Thibodeau 30 , Shannon K McDonnell 30 , Daniel J Schaid 30 , Janet L Stanford 31 , Suzanne Kolb 32 , Sarah Holt 33 , Beatrice Knudsen 34 , Antonio Hurtado Coll 35 , Susan M Gapstur 36 , W Ryan Diver 36 , Victoria L Stevens 36 , Christiane Maier 37 , Manuel Luedeke 37 , Kathleen Herkommer 38 , Antje E Rinckleb 37 , Sara S Strom 39 , Curtis Pettaway 40 , Edward D Yeboah 41 , Yao Tettey 41 , Richard B Biritwum 41 , Andrew A Adjei 41 , Evelyn Tay 41 , Ann Truelove 42 , Shelley Niwa 42 , Anand P Chokkalingam 43 , Lisa Cannon-Albright 44 , Cezary Cybulski 45 , Dominika Wokołorczyk 45 , Wojciech Kluźniak 45 , Jong Park 46 , Thomas Sellers 46 , Hui-Yi Lin 47 , William B Isaacs 48 , Alan W Partin 48 , Hermann Brenner 49 , Aida Karina Dieffenbach 49 , Christa Stegmaier 50 , Constance Chen 9 , Edward L Giovannucci 51 , Jing Ma 52 , Meir Stampfer 53 , Kathryn L Penney 54 , Lorelei Mucci 54 , Esther M John 55 , Sue A Ingles 4 , Rick A Kittles 56 , Adam B Murphy 57 , Hardev Pandha 58 , Agnieszka Michael 58 , Andrzej M Kierzek 58 , William Blot 59 , Lisa B Signorello 54 , Wei Zheng 60 , Demetrius Albanes 61 , Jarmo Virtamo 62 , Stephanie Weinstein 61 , Barbara Nemesure 63 , John Carpten 64 , Cristina Leske 63 , Suh-Yuh Wu 63 , Anselm Hennis 65 , Adam S Kibel 66 , Benjamin A Rybicki 67 , Christine Neslund-Dudas 67 , Ann W Hsing 55 , Lisa Chu 55 , Phyllis J Goodman 68 , Eric A Klein 69 , S Lilly Zheng 16 , Jyotsna Batra 70 , Judith Clements 70 , Amanda Spurdle 71 , Manuel R Teixeira 72 , Paula Paulo 73 , Sofia Maia 73 , Chavdar Slavov 74 , Radka Kaneva 75 , Vanio Mitev 75 , John S Witte 76 , Graham Casey 4 , Elizabeth M Gillanders 77 , Daniella Seminara 77 , Elio Riboli 78 , Freddie C Hamdy 79 , Gerhard A Coetzee 4 , Qiyuan Li 80 , Matthew L Freedman 80 , David J Hunter 9 , Kenneth Muir 81 , Henrik Gronberg 82 , David E Neal 83 , Melissa Southey 84 , Graham G Giles 85 , Gianluca Severi 86 , Breast and Prostate Cancer Cohort Consortium (BPC3) , PRACTICAL (Prostate Cancer Association Group to Investigate Cancer-Associated Alterations in the Genome) Consortium , COGS (Collaborative Oncological Gene-environment Study) Consortium , GAME-ON/ELLIPSE Consortium , Michael B Cook 87 , Hidewaki Nakagawa 88 , Fredrik Wiklund 89 , Peter Kraft 90 , Stephen J Chanock 87 , Brian E Henderson 91 , Douglas F Easton 1 , Rosalind A Eeles 92 , Christopher A Haiman 91
+ et al

[No authors listed]

Author information
  • 1 1] Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK. [2].
  • 2 1] Institute of Cancer Research, London, UK. [2].
  • 3 Division of Cancer Epidemiology and Genetics, National Cancer Institute, US National Institute of Health, Bethesda, Maryland, USA.
  • 4 1] Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California, USA. [2] Norris Comprehensive Cancer Center, University of Southern California, Los Angeles, California, USA.
  • 5 Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
  • 6 Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
  • 7 1] Division of Cancer Epidemiology and Genetics, National Cancer Institute, US National Institute of Health, Bethesda, Maryland, USA. [2] Cancer Genomics Research Laboratory, National Cancer Institute, Division of Cancer Epidemiology and Genetics, SAIC-Frederick, Inc., Frederick, Maryland, USA.
  • 8 Institute of Cancer Research, London, UK.
  • 9 Program in Genetic Epidemiology and Statistical Genetics, Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, USA.
  • 10 Epidemiology Program, University of Hawaii Cancer Center, Honolulu, Hawaii, USA.
  • 11 Department of Urology, Tampere University Hospital and Medical School, University of Tampere, Tampere, Finland.
  • 12 Department of Epidemiology, School of Health Sciences, University of Tampere, Tampere, Finland.
  • 13 BioMediTech, University of Tampere and FimLab Laboratories, Tampere, Finland.
  • 14 1] BioMediTech, University of Tampere and FimLab Laboratories, Tampere, Finland. [2] Department of Medical Biochemistry, Institute of Biomedicine, University of Turku, Turku, Finland.
  • 15 Institute of Biomedical Technology/BioMediTech, University of Tampere and Tampere University Hospital, Tampere, Finland.
  • 16 Center for Cancer Genomics, Wake Forest School of Medicine, Winston-Salem, North Carolina, USA.
  • 17 1] Department of Medical Epidemiology and Biostatistics, Karolinska Institute, Stockholm, Sweden. [2] Department of Clinical Sciences at Danderyds Hospital, Stockholm, Sweden.
  • 18 School of Social and Community Medicine, University of Bristol, Bristol, UK.
  • 19 Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, UK.
  • 20 Department of Genomics of Common Disease, School of Public Health, Imperial College London, London, UK.
  • 21 Genomic Epidemiology Group, German Cancer Research Center (DKFZ), Heidelberg, Germany.
  • 22 Clinical Gerontology Unit, University of Cambridge, Cambridge, UK.
  • 23 Laboratory for Statistical Analysis, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
  • 24 Laboratory for Genotyping Development, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
  • 25 Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.
  • 26 Department of Clinical Biochemistry, Herlev Hospital, Copenhagen University Hospital, Herlev, Denmark.
  • 27 1] Department of Clinical Biochemistry, Herlev Hospital, Copenhagen University Hospital, Herlev, Denmark. [2] Faculty of Healthy and Medical Sciences, University of Copenhagen, Herlev, Denmark.
  • 28 Department of Urology, Herlev Hospital, Copenhagen University Hospital, Herlev, Denmark.
  • 29 Copenhagen Prostate Cancer Center, Department of Urology, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
  • 30 Mayo Clinic, Rochester, Minnesota, USA.
  • 31 1] Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington, USA. [2] Department of Epidemiology, School of Public Health, University of Washington, Seattle, Washington, USA.
  • 32 Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington, USA.
  • 33 Fred Hutchinson Cancer Research Center, Seattle, Washington, USA.
  • 34 Translational Pathology, Cedars-Sinai, Los Angeles, California, USA.
  • 35 Prostate Center, Vancouver, British Columbia, Canada.
  • 36 Epidemiology Research Program, American Cancer Society, Atlanta, Georgia, USA.
  • 37 Department of Urology, University Hospital Ulm, Ulm, Germany.
  • 38 Department of Urology, Klinikum Rechts der Isar der Technischen Universität München, Munich, Germany.
  • 39 Department of Epidemiology, University of Texas MD Anderson Cancer Center, Houston, Texas, USA.
  • 40 Department of Urology, University of Texas MD Anderson Cancer Center, Houston, Texas, USA.
  • 41 1] University of Ghana Medical School, Accra, Ghana. [2] Korle Bu Teaching Hospital, Accra, Ghana.
  • 42 Westat, Rockville, Maryland, USA.
  • 43 School of Public Health, University of California, Berkeley, Berkeley, California, USA.
  • 44 1] Division of Genetic Epidemiology, Department of Medicine, University of Utah School of Medicine, Salt Lake City, Utah, USA. [2] George E. Wahlen Department of Veterans Affairs Medical Center, Salt Lake City, Utah, USA.
  • 45 International Hereditary Cancer Center, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland.
  • 46 Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, Florida, USA.
  • 47 Department of Biostatistics and Bioinformatics, Moffitt Cancer Center, Tampa, Florida, USA.
  • 48 James Buchanan Brady Urological Institute, Johns Hopkins Hospital and Medical Institution, Baltimore, Maryland, USA.
  • 49 1] Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany. [2] German Cancer Consortium, Heidelberg, Germany.
  • 50 Saarland Cancer Registry, Saarbrücken, Germany.
  • 51 1] Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, USA. [2] Department of Nutrition, Harvard School of Public Health, Boston, Massachusetts, USA.
  • 52 Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.
  • 53 1] Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, USA. [2] Department of Nutrition, Harvard School of Public Health, Boston, Massachusetts, USA. [3] Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.
  • 54 1] Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, USA. [2] Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.
  • 55 1] Cancer Prevention Institute of California, Fremont, California, USA. [2] Stanford Cancer Institute, Stanford University School of Medicine, Stanford, California, USA.
  • 56 Department of Medicine, University of Illinois at Chicago, Chicago, Illinois, USA.
  • 57 Department of Urology, Northwestern University, Chicago, Illinois, USA.
  • 58 Faculty of Health and Medical Sciences, University of Surrey, Guildford, UK.
  • 59 1] International Epidemiology Institute, Rockville, Maryland, USA. [2] Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt University School of Medicine, Nashville, Tennessee, USA.
  • 60 Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt University School of Medicine, Nashville, Tennessee, USA.
  • 61 Nutritional Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, US National Institute of Health, Bethesda, Maryland, USA.
  • 62 Department of Chronic Disease Prevention, National Institute for Health and Welfare, Helsinki, Finland.
  • 63 Department of Preventive Medicine, Stony Brook University, Stony Brook, New York, USA.
  • 64 Translational Genomics Research Institute, Phoenix, Arizona, USA.
  • 65 1] Department of Preventive Medicine, Stony Brook University, Stony Brook, New York, USA. [2] Chronic Disease Research Centre, University of the West Indies, Bridgetown, Barbados.
  • 66 Division of Urologic Surgery, Brigham and Women's Hospital, Dana-Farber Cancer Institute, Boston, Massachusetts, USA.
  • 67 Department of Public Health Sciences, Henry Ford Hospital, Detroit, Michigan, USA.
  • 68 Southwest Oncology Group Statistical Center, Fred Hutchinson Cancer Research Center, Seattle, Washington, USA.
  • 69 Department of Urology, Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, Ohio, USA.
  • 70 Australian Prostate Cancer Research Centre-Queensland, Institute of Health and Biomedical Innovation and School of Biomedical Science, Queensland University of Technology, Translational Research Institute, Brisbane, Queensland, Australia.
  • 71 Molecular Cancer Epidemiology Laboratory, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
  • 72 1] Department of Genetics, Portuguese Oncology Institute, Porto, Portugal. [2] Biomedical Sciences Institute, University of Porto, Porto, Portugal.
  • 73 Department of Genetics, Portuguese Oncology Institute, Porto, Portugal.
  • 74 Department of Urology, Medical University-Sofia, Sofia, Bulgaria.
  • 75 Department of Medical Chemistry and Biochemistry, Molecular Medicine Center, Medical University-Sofia, Sofia, Bulgaria.
  • 76 1] Institute for Human Genetics, University of California, San Francisco, San Francisco, California, USA. [2] Department of Epidemiology and Biostatistics, University of California, San Francisco, San Francisco, California, USA.
  • 77 Division of Cancer Control and Population Sciences, National Cancer Institute, Bethesda, Maryland, USA.
  • 78 Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK.
  • 79 Nuffield Department of Surgical Sciences, University of Oxford, Oxford, UK.
  • 80 Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts, USA.
  • 81 1] Institute of Population Health, University of Manchester, Manchester, UK. [2] Warwick Medical School, University of Warwick, Coventry, UK.
  • 82 Department of Medical Epidemiology and Biostatistics, Karolinska Institute, Stockholm, Sweden.
  • 83 1] Cancer Research UK, Cambridge Research Institute, Li Ka Shing Centre, Cambridge, UK. [2] Department of Oncology, University of Cambridge, Addenbrooke's Hospital, Cambridge, UK.
  • 84 Genetic Epidemiology Laboratory, Department of Pathology, University of Melbourne, Parkville, Victoria, Australia.
  • 85 1] Cancer Epidemiology Centre, Cancer Council Victoria, Melbourne, Victoria, Australia. [2] Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Melbourne, Victoria, Australia.
  • 86 1] Cancer Epidemiology Centre, Cancer Council Victoria, Melbourne, Victoria, Australia. [2] Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Melbourne, Victoria, Australia. [3] Human Genetics Foundation, Torino, Italy.
  • 87 1] Division of Cancer Epidemiology and Genetics, National Cancer Institute, US National Institute of Health, Bethesda, Maryland, USA. [2].
  • 88 1] Laboratory for Genome Sequencing Analysis, RIKEN Center for Integrative Medical Sciences, Tokyo, Japan. [2].
  • 89 1] Department of Medical Epidemiology and Biostatistics, Karolinska Institute, Stockholm, Sweden. [2].
  • 90 1] Program in Genetic Epidemiology and Statistical Genetics, Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, USA. [2] Department of Biostatistics, Harvard School of Public Health, Boston, Massachusetts, USA. [3].
  • 91 1] Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California, USA. [2] Norris Comprehensive Cancer Center, University of Southern California, Los Angeles, California, USA. [3].
  • 92 1] Institute of Cancer Research, London, UK. [2] Royal Marsden National Health Service (NHS) Foundation Trust, London and Sutton, UK. [3].
全文

摘要

Genome-wide association studies (GWAS) have identified 76 variants associated with prostate cancer risk predominantly in populations of European ancestry. To identify additional susceptibility loci for this common cancer, we conducted a meta-analysis of > 10 million SNPs in 43,303 prostate cancer cases and 43,737 controls from studies in populations of European, African, Japanese and Latino ancestry. Twenty-three new susceptibility loci were identified at association P < 5 × 10(-8); 15 variants were identified among men of European ancestry, 7 were identified in multi-ancestry analyses and 1 was associated with early-onset prostate cancer. These 23 variants, in combination with known prostate cancer risk variants, explain 33% of the familial risk for this disease in European-ancestry populations. These findings provide new regions for investigation into the pathogenesis of prostate cancer and demonstrate the usefulness of combining ancestrally diverse populations to discover risk loci for disease.

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