Letter | Published:

Identification of seven new prostate cancer susceptibility loci through a genome-wide association study

Nature Genetics volume 41, pages 11161121 (2009) | Download Citation

Abstract

Prostate cancer (PrCa) is the most frequently diagnosed cancer in males in developed countries. To identify common PrCa susceptibility alleles, we previously conducted a genome-wide association study in which 541,129 SNPs were genotyped in 1,854 PrCa cases with clinically detected disease and in 1,894 controls. We have now extended the study to evaluate promising associations in a second stage in which we genotyped 43,671 SNPs in 3,650 PrCa cases and 3,940 controls and in a third stage involving an additional 16,229 cases and 14,821 controls from 21 studies. In addition to replicating previous associations, we identified seven new prostate cancer susceptibility loci on chromosomes 2, 4, 8, 11 and 22 (with P = 1.6 × 10−8 to P = 2.7 × 10−33).

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Acknowledgements

These are detailed in the Supplementary Note.

Other members of The UK Genetic Prostate Cancer Study Collaborators/British Association of Urological Surgeons' Section of Oncology, The UK ProtecT Study Collaborators and The PRACTICAL Consortium (membership lists provided in the Supplementary Note) collected clinical samples and provided data management.

Author information

Author notes

    • Ali Amin Al Olama
    • , Graham G Giles
    • , Michelle Guy
    • , Gianluca Severi
    • , Kenneth Muir
    • , John L Hopper
    • , Brian E Henderson
    • , Christopher A Haiman
    • , Johanna Schleutker
    • , Freddie C Hamdy
    • , David E Neal
    • , Jenny L Donovan
    • , Janet L Stanford
    • , Elaine A Ostrander
    • , Sue A Ingles
    • , Esther M John
    • , Stephen N Thibodeau
    • , Daniel Schaid
    • , Jong Y Park
    • , Amanda Spurdle
    • , Judith Clements
    • , Joanne L Dickinson
    • , Christiane Maier
    • , Walther Vogel
    • , Thilo Dörk
    • , Timothy R Rebbeck
    • , Kathleen A Cooney
    • , Lisa Cannon-Albright
    • , Pierre O Chappuis
    • , Pierre Hutter
    • , Maurice Zeegers
    • , Radka Kaneva
    • , Hong-Wei Zhang
    • , Yong-Jie Lu
    • , William D Foulkes
    •  & Dallas R English

    These authors contributed equally to this work.

Affiliations

  1. The Institute of Cancer Research, Sutton, Surrey, UK.

    • Rosalind A Eeles
    • , Zsofia Kote-Jarai
    • , Michelle Guy
    • , Daniel A Leongamornlert
    • , Malgorzata Tymrakiewicz
    • , Amanda L Hall
    • , Lynne T O'Brien
    • , Rosemary A Wilkinson
    • , Edward J Saunders
    • , Elizabeth C Page
    • , Emma J Sawyer
    • , Stephen M Edwards
    • , David P Dearnaley
    • , Alan Horwich
    • , Robert A Huddart
    • , Vincent S Khoo
    • , Christopher C Parker
    •  & Colin S Cooper
  2. The Royal Marsden National Health Service Foundation Trust, Sutton, Surrey and London, UK.

    • Rosalind A Eeles
    • , Audrey T Ardern-Jones
    • , Amanda L Hall
    • , Elizabeth C Page
    • , David P Dearnaley
    • , Alan Horwich
    • , Robert A Huddart
    • , Vincent S Khoo
    • , Christopher C Parker
    • , Nicholas Van As
    • , Christopher J Woodhouse
    • , Alan Thompson
    • , Tim Christmas
    •  & Chris Ogden
  3. Cancer Research UK Genetic Epidemiology Unit, Department of Public Health and Primary Care, University of Cambridge, Strangeways Laboratory, Cambridge, UK.

    • Ali Amin Al Olama
    • , Jonathan Morrison
    •  & Douglas F Easton
  4. Cancer Epidemiology Centre, The Cancer Council Victoria, Carlton, Victoria, Australia.

    • Graham G Giles
    •  & Gianluca Severi
  5. Centre for Molecular, Environmental, Genetic and Analytic Epidemiology, The University of Melbourne, Carlton, Victoria, Australia.

    • Graham G Giles
    • , Gianluca Severi
    • , John L Hopper
    •  & Dallas R English
  6. University of Nottingham Medical School, Queens Medical Centre, Nottingham, UK.

    • Kenneth Muir
    • , Artitaya Lophatananon
    •  & Jo-Fen Liu
  7. Department of Preventive Medicine, Keck School of Medicine, University of Southern California/Norris Comprehensive Cancer Center, Los Angeles, California, USA.

    • Brian E Henderson
    •  & Christopher A Haiman
  8. Institute of Medical Technology, University of Tampere and Tampere University Hospital, Tampere, Finland.

    • Johanna Schleutker
    •  & Tiina Wahlfors
  9. Nuffield Department of Surgery, University of Oxford, Oxford, UK.

    • Freddie C Hamdy
  10. Surgical Oncology (Uro-Oncology), University of Cambridge, Cambridge, UK and Cancer Research UK Cambridge Research Institute, Li Ka Shing Centre, Cambridge, UK.

    • David E Neal
  11. Department of Social Medicine, University of Bristol, Canynge Hall, Bristol, UK.

    • Jenny L Donovan
    •  & Sarah J Lewis
  12. Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington, USA.

    • Janet L Stanford
    • , Liesel M FitzGerald
    •  & Joseph S Koopmeiners
  13. Department of Epidemiology, School of Public Health and Community Medicine, University of Washington, Seattle, Washington, USA.

    • Janet L Stanford
  14. National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland, USA.

    • Elaine A Ostrander
    • , Danielle M Karyadi
    •  & Erika M Kwon
  15. Department of Preventive Medicine, University of Southern California Keck School of Medicine, Los Angeles, California, USA.

    • Sue A Ingles
    • , Mariana C Stern
    • , Roman Corral
    • , Amit D Joshi
    •  & Ahva Shahabi
  16. Northern California Cancer Center, Fremont, California, USA and Stanford University School of Medicine, Stanford, California, USA.

    • Esther M John
  17. Mayo Clinic, Rochester, Minnesota, USA.

    • Stephen N Thibodeau
    • , Daniel Schaid
    •  & Shannon K McDonnell
  18. Division of Cancer Prevention and Control, H. Lee Moffitt Cancer Center, Tampa, Florida, USA.

    • Jong Y Park
    • , Thomas A Sellers
    •  & Julio Pow-Sang
  19. Molecular Cancer Epidemiology Laboratory, Queensland Institute of Medical Research, Brisbane, Australia.

    • Amanda Spurdle
    •  & Felicity Lose
  20. Australian Prostate Cancer Research Centre-Queensland, Institute of Health and Biomedical Innovation and Schools of Life Science and Public Health, Queensland University of Technology, Brisbane, Australia.

    • Judith Clements
    • , Jyotsna Batra
    • , Mary Anne Kedda
    •  & Felicity Lose
  21. Menzies Research Institute, University of Tasmania, Hobart, Tasmania, Australia.

    • Joanne L Dickinson
    • , Liesel M FitzGerald
    • , Andrea Polanowski
    •  & Briony Patterson
  22. Institut für Humangenetik, Ulm, Germany.

    • Christiane Maier
    • , Walther Vogel
    •  & Manuel Luedeke
  23. Clinics of Obstetrics and Gynaecology, Hannover Medical School, Hannover, Germany.

    • Thilo Dörk
  24. Center for Clinical Epidemiology and Biostatistics and Abramson Cancer Center, University of Pennsylvania, Philadelphia, Philadelphia, USA.

    • Timothy R Rebbeck
    •  & Klara Stefflova
  25. Departments of Internal Medicine and Urology, University of Michigan Medical School, Ann Arbor, Michigan, USA.

    • Kathleen A Cooney
    •  & Anna M Ray
  26. Genetic Epidemiology, Department of Biomedical Informatics, University of Utah School of Medicine, Salt Lake City, Utah, USA.

    • Lisa Cannon-Albright
    •  & Jim Farnham
  27. Division of Genetic Medicine and Division of Oncology, University Hospitals of Geneva, Geneva, Switzerland.

    • Pierre O Chappuis
  28. Division of Medical Genetics, Institut Central des Hôpitaux Valaisans, Sion, Switzerland.

    • Pierre Hutter
  29. Unit of Genetic Epidemiology, Department of Public Health, Epidemiology and Biostatistics, School of Medicine, University of Birmingham, UK.

    • Maurice Zeegers
    •  & Humera Khan
  30. Department of Complex Genetics, Cluster of Genetics and Cell Biology, Nutrition and Toxicology Research Institute, Maastricht University Medical Centre, The Netherlands.

    • Maurice Zeegers
  31. Molecular Medicine Center and Department of Chemistry and Biochemistry, Medical University of Sofia, Sofia, Bulgaria.

    • Radka Kaneva
    •  & Atanaska Mitkova
  32. Epidemiology Department, Second Military Medical University, Shanghai, China.

    • Hong-Wei Zhang
    •  & Guangwen Cao
  33. Molecular Oncology and Imaging, Institute of Cancer, Barts and The London School of Medicine and Dentistry, Queen Mary, University of London, Charterhouse Square, London, UK.

    • Yong-Jie Lu
  34. Program in Cancer Genetics, McGill University, Montreal, Quebec, Canada.

    • William D Foulkes
  35. Genetic Epidemiology Laboratory, Department of Pathology, The University of Melbourne, Parkville, Victoria, Australia.

    • Melissa C Southey
  36. Chulabhorn Cancer Research Centre, Bangkok, Thailand.

    • Artitaya Lophatananon
  37. Epidemiology Program, Cancer Research Center, University of Hawaii, Honolulu, Hawaii, USA.

    • Laurence N Kolonel
    •  & Loic Le Marchand
  38. Department of Urology, Tampere University Hospital and Medical School, University of Tampere, Tampere, Finland.

    • Teuvo L Tammela
  39. Tampere School of Public Health, University of Tampere, Tampere, Finland.

    • Anssi Auvinen
  40. Institute for Cancer Studies, University of Sheffield, Sheffield, UK.

    • Angela Cox
  41. Department of Biostatistics, School of Public Health and Community Medicine, University of Washington, Seattle, Washington, USA.

    • Joseph S Koopmeiners
  42. Viertel Centre for Research in Cancer Control, Cancer Council Queensland, Brisbane, Australia.

    • Suzanne Chambers
    •  & Joanne Aitken
  43. School of Population Health, University of Queensland, Brisbane, Australia.

    • Joanne Aitken
  44. University of Queensland, Department of Surgery, Royal Brisbane and Women's Hospital, Brisbane, Australia.

    • R A (Frank) Gardiner
  45. Clinics of Urology and Urological Oncology, Hannover Medical School, Hannover, Germany.

    • Jürgen Serth
  46. Department of Radiation Oncology, Hannover Medical School, Hannover, Germany.

    • Andreas Meyer
  47. Department of Genetics, University of North Carolina, Chapel Hill, North Carolina, USA.

    • Ethan M Lange
  48. Department of Urology, Alexandrovska University Hospital, Medical University of Sofia, Sofia, Bulgaria.

    • Chavdar Slavov

Consortia

  1. The UK Genetic Prostate Cancer Study Collaborators/British Association of Urological Surgeons' Section of Oncology

    Membership list provided in the Supplementary Note.

  2. The UK ProtecT Study Collaborators

    Membership list provided in the Supplementary Note.

  3. The PRACTICAL Consortium

    Full list of participants is provided in the Supplementary Note.

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Contributions

R.A.E. and D.F.E. designed the study, wrote the paper and are joint principal investigators (PIs) on the GWAS. R.A.E. is PI of the UKGPCS and project managed this study. Z.K.-J. coordinated the PRACTICAL genotyping and M.G. coordinated the administration. Z.K.-J., S.M.E., D.A.L., M.T., E.J.S. and C.S.C. coordinated sample collation, provided molecular advice and performed molecular work on UK samples. A.A.A.O. and D.F.E. performed the analyses; J.M. provided database and bioinformatic support for Illumina data. G.G.G., J.L.H. and D.R.E. are PIs of the Australian studies; M.C.S. led the Australian genotyping. G.S. coordinated the Australian studies. K.M. and R.A.E. are joint PIs of the PCRF study; A.L. and J.-F.L. coordinated sample collection. B.E.H. and C.A.H. lead the MEC consortium. J.S. is PI of the Tampere study; T.W. and T.L.T. coordinated sample collation, provided molecular advice and performed molecular work. F.C.H., D.E.N. and J.L.D. are joint PIs of ProtecT; S.J.L. helped with control matching for the UK. J.L.S. is PI of the Fred Hutchinson study, and E.A.O. is PI of the NHGRI genotyping for PROGRESS; L.M.F. and J.S.K. coordinated data collation. S.A.I. is PI of the USC study, E.M.J. is PI of the NC_CCPC study, S.N.T. and D.S. are PIs of the Mayo Clinic study and S.J.Mc. coordinated data collation. J.Y.P. is PI of the Moffit study, J.C. is PI of the Queensland study, A.S. led the Queensland genotyping, J.L.D. is PI of the Tasprac study, W.V. is PI of the Ulm study and C.M. led the genotyping. T.D. is PI of the Hannover study, T.R.R. is PI of the UPenn study, K.A.C. is PI of the FMHS study, L.C.A. is PI of the Utah study, P.O.C. and P.H. are PIs of the Valais study and W.D.F. led the molecular work. M.Z. is PI of the BiPAS study, R.K. is PI of the PCMUS study. G.C. is PI of the CHSH, H.-W.Z. led the genotyping and Y-J.L. provided study set up advice to the CHSH. A.T.A.-J., A.L.H., L.T.O., R.A.W., E.C.P., E.J.S., D.P.D., A.H., R.A.H., V.S.K., C.C.P., N.V.A., C.J.W., A.T., T.C., C.O., L.N.K., L.L.M., A.A., A.C., D.M.K., E.M.K., M.C.S., R.C., A.D.J., A.S., T.A.S., J.P.-S., S.C., J.A., R.A.G., J.B., M.A.K., F.L., A.P., B.P., J.S., A.M., M.L., K.L., A.M.R., E.M.L., J.F., H.K., C.S., K.S. and A.M. identified and collected clinical material, processed samples, undertook genotyping and collated data.

Corresponding author

Correspondence to Rosalind A Eeles.

Supplementary information

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    Supplementary Text and Figures

    Supplementary Figures 1 and 2, Supplementary Tables 1–13 and Supplementary Note

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Publication history

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Published

DOI

https://doi.org/10.1038/ng.450

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    •  & Ulrike Peters

    Nature Genetics (2019)