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Genome-wide association study identifies three loci associated with melanoma risk

Nature Genetics volume 41, pages 920–925 (2009)Cite this article

Abstract

We report a genome-wide association study of melanoma conducted by the GenoMEL consortium based on 317K tagging SNPs for 1,650 selected cases and 4,336 controls, with replication in an additional two cohorts (1,149 selected cases and 964 controls from GenoMEL, and a population-based case-control study in Leeds of 1,163 cases and 903 controls). The genome-wide screen identified five loci with genotyped or imputed SNPs reaching P < 5 × 10−7. Three of these loci were replicated: 16q24 encompassing MC1R (combined P = 2.54 × 10−27 for rs258322), 11q14-q21 encompassing TYR (P = 2.41 × 10−14 for rs1393350) and 9p21 adjacent to MTAP and flanking CDKN2A (P = 4.03 × 10−7 for rs7023329). MC1R and TYR are associated with pigmentation, freckling and cutaneous sun sensitivity, well-recognized melanoma risk factors. Common variants within the 9p21 locus have not previously been associated with melanoma. Despite wide variation in allele frequency, these genetic variants show notable homogeneity of effect across populations of European ancestry living at different latitudes and show independent association to disease risk.

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Figure 1: Results of Cochran-Armitage (CA) trend test for all SNPs passing quality control reported as −log10 P values.
Figure 2: Stratified CA trend tests.
Figure 3: Forest plot of associations by geography and case category.

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Acknowledgements

The study was funded by the European Commission under the 6th Framework Programme, contract no: LSHC-CT-2006-018702, by Cancer Research UK Programme Award (C588/A4994) and by US National Institutes of Health R01 ROI CA83115. Work at CNG was supported by the Ministère de l'Enseignement Supérieur et de la Recherche and Institut National du Cancer (INCa).

This study was also supported by the following: research grant no. C-20070050 from the Israel Cancer Association, the Intramural Research Program of the NIH, National Cancer Institute, Division of Cancer Epidemiology and Genetics, and by National Cancer Institute grants RO1 CA5558 to M.T.L. Grants 03/0019 and 06/0265 from Fondo de Investigaciones Sanitarias; grant RO-1 CA 83115 (fund 538226 from National Cancer Institute); Francisco Cuellar from CONACYT, Mexico, 2007 Italian Ministry of Health DGRST.4/4235-P1.9.A.B to G.B.-S., the Swedish Cancer Society, Kamprad Foundation, Lund Hospital Fund, National Institutes of Health (#CA88363), The Swedish Cancer Society (Grant No: 4860-B06-04XBC), The Swedish Research Council (Grant No: K2006-74X-20141-01-3) and the Radiumhemmet Research Funds. Grants from Institut National du Cancer (INCa-PL016) and Ligue Nationale contre le Cancer (PRE2005.LNCC/FD) to F.D., PHRC2007 (AOM-07-195) to M.-F.A. and F.D., grant from Institut National du Cancer (Melanoma Network RS Number 13) to B.B.-deP. This work was developed in the Melanoma Unit of Hospital Clinic I Provincial de Barcelona, IDIBAPS. Ascertainment and data collection in Sydney and the Australian Melanoma Family Study (AMFS) was supported by NHMRC grants 107359, 200071 and 402761 and grants from Cancer Councils of NSW, Victoria and Queensland and the Cancer Institute NSW. J.H. is an Australia Fellow of the NHMRC. This work was supported by the Intramural Program at the National Human Genome Research Institute, National Institutes of Health. Funding was provided by NIH National Cancer Institute grant RO1 CA102422 (to L.A.C.-A.).

The Principal Investigators of Q-MEGA would like to thank D. Statham, M. de Nooyer, I. Gardner and B. Haddon for project management; A. Henders, M. Campbell and M. Stark for managing sample processing and preparation; D. Smyth and H. Beeby for data management and J. Palmer and J. Simmons for ascertainment of clinical records. We also thank the numerous interviewers who collected questionnaire data. Most of all we thank the individuals with melanoma and their families for their cooperation.

The Sydney and AMFS investigators are grateful to all members of the recruitment, data collection and laboratory team, especially C. Watts, R. Dalziell, K. Mahendran, G. St. George and C. Agha-Hamilton and AMFS coordinators J. Maskiell, M. Ferguson and J. Jettan.

This study makes use of data generated by the Wellcome Trust Case Control Consortium. A full list of the investigators who contributed to the generation of the data are available from the Wellcome Trust website. Funding for the project was provided by the Wellcome Trust under award 076113.

The authors thank the EGEA cooperative group for having given access to data on the EGEA (Epidemiological study on the Genetics and Environment of Asthma) study. Biological specimens of the French Family study group were obtained from IGR Biobank.

The authors are grateful for the contributions of P.A. Van Belle to the work of GenoMEL. The authors would also like to thank D. Seminara.

Author information

Authors and Affiliations

  1. Section of Epidemiology and Biostatistics, Leeds Institute of Molecular Medicine, Cancer Research UK Clinical Centre at Leeds, St James's University Hospital, Leeds, UK

    D Timothy Bishop, Mark M Iles, Mark Harland, John C Taylor, Juliette Randerson-Moor, Jennifer H Barrett & Julia A Newton Bishop

  2. INSERM, U946, Fondation Jean-Dausset–CEPH, Paris, 75010, France

    Florence Demenais & Eve Corda

  3. Fondation Jean Dausset-CEPH, Paris, 75010, France

    Eve Corda & G Mark Lathrop

  4. Viertel Centre for Research in Cancer Control, The Cancer Council, Queensland, Spring Hill, Brisbane, Australia

    Joanne F Aitken

  5. AP-HP, Hôpital Cochin, Service de Dermatologie, Faculté Paris 5, Paris, France

    Marie-Francoise Avril

  6. Department of Dermatology, Sheba Medical Center, Tel Hashomer, Sackler Faculty of Medicine, Tel Aviv University, Israel

    Esther Azizi & Gilli Galore-Haskel

  7. Department of Clinical Genetics, Center of Human and Clinical Genetics, Leiden University Medical Center, Leiden, The Netherlands

    Bert Bakker & Marjan Weiss

  8. Department of Oncology, Biology and Genetics, University of Genoa, Genova, Italy

    Giovanna Bianchi-Scarrà & Paola Ghiorzo

  9. Service de Génétique et FRE 2939 CNRS, Institut de Cancérologie Gustave Roussy, Villejuif, France

    Brigitte Bressac-de Paillerets

  10. Dermatology Unit, Maurizio Bufalini Hospital, Cesena, Italy

    Donato Calista

  11. Genetic Epidemiology, Biomedical Informatics, University of Utah, Salt Lake City, Utah, USA

    Lisa A Cannon-Albright

  12. ServiceXS, Plesmanlaan 1d, Leiden, 2333 BZ, The Netherlands

    Thomas Chin-A-Woeng & Wilbert van Workum

  13. International Hereditary Cancer Center, Pomeranian Medical University, Szczecin, Poland

    Tadeusz Dębniak & Jan Lubiński

  14. Commissariat à l'énergie Atomique, Institut de Génomique, Centre National de Génotypage, Evry, France

    Ivo Gut, Diana Zelenika, Anne Boland & G Mark Lathrop

  15. Department of Oncology-Pathology, Karolinska Institutet, Stockholm, Sweden

    Johan Hansson & Veronica Höiom

  16. Institute of Oncology Ljubljana, Zaloska 2, Ljubljana, Slovenia

    Marko Hočevar & Srdjan Novakovic

  17. Centre for Molecular, Environmental, Genetic and Analytic (MEGA) Epidemiology, School of Population Health, University of Melbourne, Melbourne, Australia

    John L Hopper

  18. Department of Oncology, University Hospital Lund, Barngatan 2B, Lund, Sweden

    Christian Ingvar & Håkan Olsson

  19. Centre for Clinical Epidemiology & Biostatistics and Department of Biostatistics & Epidemiology, University of Pennsylvania, Philadephia, Pennsylvania, USA

    Peter A Kanetsky

  20. Westmead Institute for Cancer Research, University of Sydney at Westmead Millennium Institute and Melanoma Institute Australia, Westmead, Australia

    Richard F Kefford & Graham J Mann

  21. Division of Cancer Epidemiology and Genetics, Genetic Epidemiology Branch, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, USA

    Maria Teresa Landi & Alisa M Goldstein

  22. Department of Medical Genetics, University of Glasgow, UK

    Julie Lang

  23. Departments of Medical Genetics and of Public Health & Health Policy, 1 Lilybank Gardens, University of Glasgow, UK

    Rona Mackie

  24. Dermatology Department, Melanoma Unit, Hospital Clinic, IDIBAPS, Barcelona, Spain and CIBER de Enfermedades Raras, Barcelona, Spain

    Josep Malvehy & Susana Puig

  25. Queensland Institute of Medical Research, Herston, QLD, Australia

    Nicholas G Martin, Grant W Montgomery & Nicholas K Hayward

  26. Department of Dermatology, Leiden University Medical Centre, Leiden, The Netherlands

    Frans A van Nieuwpoort & Nelleke A Gruis

  27. Melanoma Genomics Laboratory, The Translational Genomics Research Institute (TGen), Phoenix, Arizona, USA

    Kevin M Brown

  28. Inherited Disease Research Branch, National Human Genome Research Institute, National Institutes of Health, Baltimore, Maryland, USA

    Elizabeth M Gillanders

  29. UMR U557 Inserm, U1125 Inra, Cnam, Paris 13, CRNH Idf, Bobigny, France

    Pilar Galan

  30. Department of Pathology and Laboratory Medicine, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, USA

    David E Elder

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  1. D Timothy Bishop
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Contributions

D.T.B. led the analysis group, contributed to the design of the study and was a member of the writing team; F.D. advised on analysis, contributed to the design of the study and was a member of the writing team; M.M.I. and J.H.B. advised on and carried out analyses, contributed to the design of the study and were members of the writing team; M.H. contributed to the design of the study and contributed genotyping information; J.C.T. and E.C. carried out analyses and were members of the writing team; J.R.-M., T.C-a-W. and D.Z. contributed to the interpretation of genotyping data; J.F.A., M.-F.A., D.C., G.G.-H., V.H., C.I., J.Lang, J.M., N.G.M., G.W.M. and S.N. contributed to the identification of suitable samples for the study; E.A., P.G., M.T.L. and R.M. contributed to the design of the study and contributed to the identification of suitable samples for the study; B.B. contributed to the design of the study and supervised the initial processing of samples; G.B.-S., B.B-deP., L.A.C.-A., T.D., I.G., J.H., M.H., J.L.H., R.F.K., J.Lubiński, G.J.M., F.A.vanN., H.O., S.P., W.vanW., K.M.B., P.G. and D.E.E. contributed to the design of the study; P.A.K., N.K.H. contributed to the design of the study, contributed to the interpretation of genotyping data and advised the analysis group; M.W. contributed to the design of the sample handling process; A.M.G. and E.M.G. advised on study design and statistical analysis; A.B. contributed genotyping information; N.A.G. contributed to the design of the study and was project deputy lead; G.M.L. contributed to the design of the study and the interpretation of genotyping data; J.A.N.B. led the study design group and was overall project leader.

Corresponding author

Correspondence to D Timothy Bishop.

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Bishop, D., Demenais, F., Iles, M. et al. Genome-wide association study identifies three loci associated with melanoma risk. Nat Genet 41, 920–925 (2009). https://doi.org/10.1038/ng.411

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