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Association analysis of 9,560 prostate cancer cases from the International Consortium of Prostate Cancer Genetics confirms the role of reported prostate cancer associated SNPs for familial disease

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Abstract

Previous GWAS studies have reported significant associations between various common SNPs and prostate cancer risk using cases unselected for family history. How these variants influence risk in familial prostate cancer is not well studied. Here, we analyzed 25 previously reported SNPs across 14 loci from prior prostate cancer GWAS. The International Consortium for Prostate Cancer Genetics (ICPCG) previously validated some of these using a family-based association method (FBAT). However, this approach suffered reduced power due to the conditional statistics implemented in FBAT. Here, we use a case–control design with an empirical analysis strategy to analyze the ICPCG resource for association between these 25 SNPs and familial prostate cancer risk. Fourteen sites contributed 12,506 samples (9,560 prostate cancer cases, 3,368 with aggressive disease, and 2,946 controls from 2,283 pedigrees). We performed association analysis with Genie software which accounts for relationships. We analyzed all familial prostate cancer cases and the subset of aggressive cases. For the familial prostate cancer phenotype, 20 of the 25 SNPs were at least nominally associated with prostate cancer and 16 remained significant after multiple testing correction (p ≤ 1E −3) occurring on chromosomal bands 6q25, 7p15, 8q24, 10q11, 11q13, 17q12, 17q24, and Xp11. For aggressive disease, 16 of the SNPs had at least nominal evidence and 8 were statistically significant including 2p15. The results indicate that the majority of common, low-risk alleles identified in GWAS studies for all prostate cancer also contribute risk for familial prostate cancer, and that some may contribute risk to aggressive disease.

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Acknowledgments

Partial support for L.A.C.A. and for all data sets with in the Utah Population Database (UPDB) was provided by Huntsman Cancer Institute, University of Utah and the Huntsman Cancer Institute’s Cancer Center Support grant, P30 CA42014 from National Cancer Institute. Research was supported by the Utah Cancer Registry, which is funded by Contract No. HHSN261201000026C from the National Cancer Institute’s SEER Program with additional support from the Utah State Department of Health and the University of Utah. A subcontract from Johns Hopkins University with funds provided by grant R01 CA89600 from the NIH National Cancer Institute (to L.A. Cannon Albright). The International Consortium for Prostate Cancer Genetics has provided access to genotyping for this study (U01CA089600). RE is supported by Cancer Research UK and Prostate Action (now Prostate Cancer UK) and National Institute of Health Research support to the Biomedical Research Centre at The Institute of Cancer Research and Royal Marsden NHS Foundation Trust. Robert Stephenson generously donated funds for the data analysis aspects of this project.

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Authors and Affiliations

  1. Division of Genetic Epidemiology, Department of Medicine, University of Utah School of Medicine, Salt Lake City, UT, USA

    Craig C. Teerlink, Nicola J. Camp & Lisa A. Cannon-Albright

  2. George E. Wahlen Department of Veterans Affairs Medical Center, Salt Lake City, UT, USA

    Lisa A. Cannon-Albright

  3. Mayo Clinic ICPCG Group, Rochester, MN, USA

    Stephen N. Thibodeau, Shannon K. McDonnell & Daniel J. Schaid

  4. Department of Lab Medicine and Pathology, Mayo Clinic, Rochester, MN, 55905, USA

    Stephen N. Thibodeau

  5. Department of Health Sciences Research, Mayo Clinic, Rochester, MN, 55905, USA

    Shannon K. McDonnell & Daniel J. Schaid

  6. University of Ulm ICPCG Group, Ulm, Germany

    Antje Rinckleb, Christiane Maier & Walther Vogel

  7. Department of Urology, University of Ulm, Ulm, Germany

    Antje Rinckleb, Christiane Maier & Walther Vogel

  8. Institute for Human Genetics, University of Ulm, Ulm, Germany

    Antje Rinckleb & Christiane Maier

  9. CeRePP ICPCG Group, Hopital Tenon, Assistance Publique-Hopitaux de Paris, 75020, Paris, France

    Geraldine Cancel-Tassin, Christophe Egrot & Olivier Cussenot

  10. ACTANE Consortium ICPCG Group, Surrey, UK

    William D. Foulkes, Graham G. Giles, John L. Hopper, Gianluca Severi, Ros Eeles, Douglas Easton, Zsofia Kote-Jarai & Michelle Guy

  11. Program in Cancer Genetics, McGill University, Montreal, QC, H3T 1E2, Canada

    William D. Foulkes

  12. Cancer Epidemiology Centre, Cancer Council Victoria, Carlton, VIC, 3053, Australia

    Graham G. Giles & Gianluca Severi

  13. Centre for Molecular, Environmental, Genetic, and Analytic Epidemiology, The University of Melbourne, Melbourne, VIC, 3010, Australia

    Graham G. Giles, John L. Hopper & Gianluca Severi

  14. The Institute of Cancer Research, Sutton, Surrey, SM2 5NG, UK

    Ros Eeles, Zsofia Kote-Jarai & Michelle Guy

  15. Strangeways Laboratory, Worts Causeway, Cambridge, CB1 8RN, UK

    Douglas Easton

  16. University of Michigan ICPCG Group, Ann Arbor, MI, USA

    Kathleen A. Cooney, Anna M. Ray, Kimberly A. Zuhlke & Ethan M. Lange

  17. Department of Urology, University of Michigan Medical School, Ann Arbor, MI, 48109, USA

    Kathleen A. Cooney, Anna M. Ray & Kimberly A. Zuhlke

  18. Department of Internal Medicine, University of Michigan Medical School, Ann Arbor, MI, 48109, USA

    Kathleen A. Cooney, Anna M. Ray & Kimberly A. Zuhlke

  19. Department of Genetics, University of North Carolina, Chapel Hill, NC, 27599, USA

    Ethan M. Lange

  20. Department of Biostatistics, University of North Carolina, Chapel Hill, NC, 27599, USA

    Ethan M. Lange

  21. FHCRC/NHGRI ICPCG Group, Seattle, WA, USA

    Liesel M. FitzGerald, Janet L. Stanford & Elaine A. Ostrander

  22. Division of Public Health Sciences, Fred Hutchinson Cancer Research Center (FHCRC), Seattle, WA, 98195, USA

    Liesel M. FitzGerald & Janet L. Stanford

  23. Cancer Genetics Branch, National Human Genome Research Institute (NHGRI), National Institutes of Health (NIH), Bethesda, MD, 20892, USA

    Elaine A. Ostrander

  24. Department of Urology, Johns Hopkins University ICPCG Group, Johns Hopkins Medical Institutions, Baltimore, MD, 21287, USA

    Kathleen E. Wiley, Sarah D. Isaacs, Patrick C. Walsh & William B. Isaacs

  25. University of Tampere ICPCG Group, Tampere, Finland

    Tiina Wahlfors, Teuvo Tammela & Johanna Schleutker

  26. Institute of Biomedical Technology, University of Tampere, BioMediTech, Tampere, 33520, Finland

    Tiina Wahlfors

  27. Centre for Laboratory Medicine, Tampere University Hospital, Tampere, 33520, Finland

    Tiina Wahlfors

  28. Department of Urology, University of Tampere and Tampere University Hospital, Tampere, 33520, Finland

    Teuvo Tammela

  29. Department of Medical Biochemistry and Genetics, University of Turku, Turku, 20520, Finland

    Johanna Schleutker

  30. University of Umeå ICPCG Group, Umeå, Sweden

    Fredrik Wiklund, Henrik Grönberg & Monica Emanuelsson

  31. Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden

    Fredrik Wiklund & Henrik Grönberg

  32. Oncologic Centre, Umeå University, 90187, Umeå, Sweden

    Monica Emanuelsson

  33. Integrated Cancer Genomics Division, TGen, Phoenix, AZ, 85004, USA

    John Carpten

  34. Inherited Disease Research Branch, National Human Genome Research Institute (NHGRI), National Institutes of Health (NIH), Bethesda, MD, 20892, USA

    Joan Bailey-Wilson

  35. Stanford University ICPCG Group, Palo Alto, CA, USA

    Alice S. Whittemore, Ingrid Oakley-Girvan & Chih-Lin Hsieh

  36. Department of Health Research and Policy, Stanford School of Medicine, Stanford, CA, 94305, USA

    Alice S. Whittemore

  37. Cancer Prevention Institute of California, 2201 Walnut Ave Suite 300, Fremont, CA, 94538, USA

    Ingrid Oakley-Girvan

  38. Stanford Cancer Institute and Department of Health Research and Policy, Stanford School of Medicine, Palo Alto, CA, USA

    Ingrid Oakley-Girvan

  39. Department of Urology, University of Southern California, Los Angeles, CA, 90089, USA

    Chih-Lin Hsieh

  40. Department of Biochemistry and Molecular Biology, University of Southern California, Los Angeles, CA, 90089, USA

    Chih-Lin Hsieh

  41. Northwestern University ICPCG Group, Northwestern University Feinberg School of Medicine, Chicago, IL, 60611, USA

    William J. Catalona & S. Lilly Zheng

  42. Data Coordinating Center for the ICPCG and Center for Human Genomics, Wake Forest University School of Medicine, Winston-Salem, NC, 27157, USA

    Guangfu Jin, Lingyi Lu & Jianfeng Xu

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  1. Craig C. Teerlink
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  2. Stephen N. Thibodeau
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  3. Shannon K. McDonnell
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  40. Chih-Lin Hsieh
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  41. William J. Catalona
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  42. S. Lilly Zheng
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  43. Guangfu Jin
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  44. Lingyi Lu
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  45. Jianfeng Xu
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  46. Nicola J. Camp
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  47. Lisa A. Cannon-Albright
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Consortia

International Consortium for Prostate Cancer Genetics

Corresponding author

Correspondence to Craig C. Teerlink.

Additional information

Nicola Camp and Lisa Cannon-Albright contributed equally to the manuscript.

Electronic supplementary material

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Supplementary material 1 (DOC 43 kb)

439_2013_1384_MOESM2_ESM.pdf

Supplemental Fig. 1 Forrest plots showing odds ratios (dot) and 95 % confidence intervals (lines) for all sites (labeled Z (meta)), and each individual site for the analysis of all prostate cancer (PDF 45 kb)

439_2013_1384_MOESM3_ESM.pdf

Supplemental Fig. 2 Forrest plots showing odds ratios (dot) and 95 % confidence intervals (lines) for all sites (labeled Z (meta)), and each individual site for the analysis of aggressive prostate cancer (PDF 47 kb)

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Teerlink, C.C., Thibodeau, S.N., McDonnell, S.K. et al. Association analysis of 9,560 prostate cancer cases from the International Consortium of Prostate Cancer Genetics confirms the role of reported prostate cancer associated SNPs for familial disease. Hum Genet 133, 347–356 (2014). https://doi.org/10.1007/s00439-013-1384-2

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  • DOI: https://doi.org/10.1007/s00439-013-1384-2

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