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Meta-analysis of five genome-wide association studies identifies multiple new loci associated with testicular germ cell tumor

Nature Genetics volume 49, pages 1141–1147 (2017)Cite this article

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Abstract

The international Testicular Cancer Consortium (TECAC) combined five published genome-wide association studies of testicular germ cell tumor (TGCT; 3,558 cases and 13,970 controls) to identify new susceptibility loci. We conducted a fixed-effects meta-analysis, including, to our knowledge, the first analysis of the X chromosome. Eight new loci mapping to 2q14.2, 3q26.2, 4q35.2, 7q36.3, 10q26.13, 15q21.3, 15q22.31, and Xq28 achieved genome-wide significance (P < 5 × 10−8). Most loci harbor biologically plausible candidate genes. We refined previously reported associations at 9p24.3 and 19p12 by identifying one and three additional independent SNPs, respectively. In aggregate, the 39 independent markers identified to date explain 37% of father-to-son familial risk, 8% of which can be attributed to the 12 new signals reported here. Our findings substantially increase the number of known TGCT susceptibility alleles, move the field closer to a comprehensive understanding of the underlying genetic architecture of TGCT, and provide further clues to the etiology of TGCT.

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Figure 1: All identified SNP markers associated with TGCT susceptibility to date.
Figure 2: Genetic association between SNP markers and TGCT risk for regions with multiple independent signals.

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Acknowledgements

The content of this publication does not necessarily reflect the views or policies of the Department of Health and Human Services nor does the mention of trade names, commercial products, or organizations indicate endorsement by the US government. We thank B. Weathers for her coordination of TECAC, J. Pluta for biostatistical assistance, and K. D'Andrea for expert assistance with SNP genotyping. We thank D.R. Stewart and J.T. Loud for critical support of the NCI Clinical Genetics Branch Familial Testicular Cancer Project (NCI 02-C-0178; NCT-00039598). We also thank all previous contributors to the GWAS analyzed in this study, including N. Weinhold, D. Edsgärd, H. Leffers, and A. Juul, N.E. Skakkebæk, and S. Brunak from the Danish study.

The Testicular Cancer Consortium is supported by National Institutes of Health grant U01CA164947 to K.L.N., P.A.K., and S.M.S. A portion of this work was supported by the Intramural Research Program of the National Cancer Institute and by support services contract HHSN26120130003C with IMS, Inc. The Penn GWAS (Penn) was supported by the Abramson Cancer Center at the University of Pennsylvania and National Institute of Health grant CA114478 to K.L.N. and P.A.K. The UK testicular cancer study was supported by the Institute of Cancer Research, Cancer Research UK, and made use of control data generated by the Wellcome Trust Case Control Consortium 2 (WTCCC2). C.T. is supported by the Movember Foundation. K.L. is supported by a PhD fellowship from Cancer Research UK. L.C.P. is supported by the National Institutes of Health (T32-GM008638). The contribution from the University of Leeds was funded by Cancer Research UK (C588/A19167). The Norwegian/Swedish study was supported by the Norwegian Cancer Society (grants 418975–71081–PR-2006-0387 and PK01-2007-0375); the Nordic Cancer Union (grant S-12/07), and the Swedish Cancer Society (grants 2008/708, 2010/808, 2011/484, and CAN2012/823). The Danish GWAS was supported by the Villum Kann Rasmussen Foundation, a NABIIT grant from the Danish Strategic Research Council, the Novo Nordisk Foundation, the Danish Cancer Society, and the Danish and Swedish Childhood Cancer Foundation.

Author information

Author notes

  1. Zhaoming Wang & Lorenzo Richiardi

    Present address: Department of Computational Biology, St. Jude Children's Research Hospital, Memphis, Tennessee, USA

  2. Peter A Kanetsky, Katherine L Nathanson and Rolf Skotheim: These authors jointly directed this work.

Authors and Affiliations

  1. Division of Cancer Epidemiology and Genetics, US Department of Health and Human Services, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, USA

    Zhaoming Wang, Katherine A McGlynn, Charles C Chung, Mark H Greene, Stephen J Chanock, Katherine A McGlynn, Mark H Greene & Stephen J Chanock

  2. Department of Growth and Reproduction, Copenhagen University Hospital (Rigshospitalet), Copenhagen, Denmark

    Ewa Rajpert-De Meyts, Marlene D Dalgaard & Ewa Rajpert-De Meyts

  3. Section of Epidemiology and Biostatistics, Leeds Institute of Cancer and Pathology, University of Leeds, Leeds, UK

    D Timothy Bishop & D Timothy Bishop

  4. Department of Bio and Health Informatics, Technical University of Denmark, Kongens Lyngby, Denmark

    Marlene D Dalgaard, Ramneek Gupta, Kasper Nielsen & Ramneek Gupta

  5. Cancer Registry of Norway, Oslo, Norway

    Tom Grotmol & Tom Grotmol

  6. Faculty of Health Sciences, Oslo and Akershus University College of Applied Sciences, Oslo, Norway

    Trine B Haugen & Trine B Haugen

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

    Robert Karlsson, Fredrik Wiklund & Fredrik Wiklund

  8. Division of Genetics and Epidemiology, Institute of Cancer Research, London, UK

    Kevin Litchfield, Clare Turnbull & Clare Turnbull

  9. Department of Biostatistics and Epidemiology, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Nandita Mitra

  10. Department of Medicine, Division of Translational Medicine and Human Genetics, Perelman School of Medicine at the University of Pennsylvania, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Louise C Pyle, Katherine L Nathanson & Katherine L Nathanson

  11. Division of Human Genetics and Metabolism, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA

    Louise C Pyle

  12. Fred Hutchinson Cancer Research Center, Seattle, Washington, USA

    Stephen M Schwartz & Stephen M Schwartz

  13. Institute for Systems Biology, Seattle, Washington, USA

    Vésteinn Thorsson

  14. Department of Biostatistics, Harvard School of Public Health, Harvard University, Boston, Massachusetts, USA

    Saran Vardhanabhuti

  15. Genomics England, London, UK

    Clare Turnbull & Clare Turnbull

  16. Department of Cancer Epidemiology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, Florida, USA

    Peter A Kanetsky & Peter A Kanetsky

  17. Abramson Cancer Center, Perelman School of Medicine at the University of Pennsylvania, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Katherine L Nathanson & Katherine L Nathanson

  18. Department of Medicine, Unit of Andrology and Reproductive Medicine, University of Padova, Padova, Italy

    Alberto Ferlin

  19. Medical Oncology, University Medical Center Groningen, Groningen, The Netherlands

    Jourik A Gietema

  20. Department of Clinical Preventive Medicine, Keck School of Medicine at the University of Southern California, University of Southern California, Los Angeles, California, USA

    Victoria Cortessis

  21. Department of Environmental Health, Harvard T.H. Chan School of Public Health, Harvard University, Boston, Massachusetts, USA

    Russ Hauser

  22. Department of Epidemiology, Division of OVP, Cancer Prevention and Population Sciences, University of Texas MD Anderson Cancer Center, Houston, Texas, USA

    Michelle Hildebrandt

  23. Radboud University Medical Centre, Radhoud Institute for Health Sciences, Nijmegen, Nijmegen, The Netherlands

    Lambertus A Kiemeney

  24. Institute of Human Genetics, University Medical Center Hamburg-Eppendorf, Hamburg, Germany

    Christian Kubisch & Davor Lessel

  25. deCODE Genetics, Reykjavik, Iceland

    Thorunn Rafnar

  26. Department of Biostatistics and Epidemiology, University of Turin, Turin, Italy

    Nandita Mitra

  27. Department of Molecular Oncology, Institute for Cancer Research, Oslo University Hospital, Oslo, Norway

    Rolf Skotheim

  28. Department of Epidemiology, Brown University, Providence, Rhode Island, USA

    Tongzhang Zheng

Authors
  1. Zhaoming Wang
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  2. Katherine A McGlynn
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Consortia

the Testicular Cancer Consortium

  • Katherine A McGlynn
  • , Ewa Rajpert-De Meyts
  • , D Timothy Bishop
  • , Mark H Greene
  • , Ramneek Gupta
  • , Tom Grotmol
  • , Trine B Haugen
  • , Stephen M Schwartz
  • , Fredrik Wiklund
  • , Clare Turnbull
  • , Stephen J Chanock
  • , Peter A Kanetsky
  • , Katherine L Nathanson
  • , Alberto Ferlin
  • , Jourik A Gietema
  • , Victoria Cortessis
  • , Russ Hauser
  • , Michelle Hildebrandt
  • , Lambertus A Kiemeney
  • , Christian Kubisch
  • , Davor Lessel
  • , Thorunn Rafnar
  • , Lorenzo Richiardi
  • , Rolf Skotheim
  •  & Tongzhang Zheng

Contributions

K.L.N. and P.A.K. supervised the overall study. K.A.M., E.R.-D.M., D.T.B., M.D.D., M.H.G., R.G., T.G., T.B.H., K.L., K.N., S.M.S., F.W., C.T., P.A.K., and K.L.N. contributed to recruitment and to study, data management. Z.W., K.A.M., E.R.-D.M., D.T.B., M.D.D., M.H.G., R.G., T.G., T.B.H., R.K., K.L., N.M., K.N., S.V., F.W., C.T., S.J.C., P.A.K., and K.L.N. contributed to genotyping or association analysis of individual studies. Z.W., C.C.C., L.C.P., V.T., S.J.C., P.A.K., and K.L.N. carried out the meta-analysis and the additional bioinformatics analyses, including using GTEx and TCGA TGCT data. Z.W., P.A.K., and K.L.N. drafted the initial manuscript, and all authors reviewed and contributed to the manuscript.

Corresponding author

Correspondence to Katherine L Nathanson.

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The authors declare no competing financial interests.

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Wang, Z., McGlynn, K., Rajpert-De Meyts, E. et al. Meta-analysis of five genome-wide association studies identifies multiple new loci associated with testicular germ cell tumor. Nat Genet 49, 1141–1147 (2017). https://doi.org/10.1038/ng.3879

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