Genome-wide association study identifies multiple susceptibility loci for diffuse large B cell lymphoma (original) (raw)

Accession codes

Accessions

Gene Expression Omnibus

References

1. Siegel, R., Naishadham, D. & Jemal, A. Cancer statistics, 2013. CA Cancer J. Clin. 63, 11–30 (2013).
   Article PubMed Google Scholar
2. Flowers, C.R., Sinha, R. & Vose, J.M. Improving outcomes for patients with diffuse large B-cell lymphoma. CA Cancer J. Clin. 60, 393–408 (2010).
   PubMed Google Scholar
3. Wang, S.S. et al. Family history of hematopoietic malignancies and risk of non-Hodgkin lymphoma (NHL): a pooled analysis of 10,211 cases and 11,905 controls from the International Lymphoma Epidemiology Consortium (InterLymph). Blood 109, 3479–3488 (2007).
   Article CAS PubMed PubMed Central Google Scholar
4. Goldin, L.R., Bjorkholm, M., Kristinsson, S.Y., Turesson, I. & Landgren, O. Highly increased familial risks for specific lymphoma subtypes. Br. J. Haematol. 146, 91–94 (2009).
   Article PubMed PubMed Central Google Scholar
5. Skibola, C.F. et al. Tumor necrosis factor (TNF) and lymphotoxin-α (LTA) polymorphisms and risk of non-Hodgkin lymphoma in the InterLymph Consortium. Am. J. Epidemiol. 171, 267–276 (2010).
   Article PubMed PubMed Central Google Scholar
6. Skibola, C.F. et al. Genetic variants at 6p21.33 are associated with susceptibility to follicular lymphoma. Nat. Genet. 41, 873–875 (2009).
   Article CAS PubMed PubMed Central Google Scholar
7. Conde, L. et al. Genome-wide association study of follicular lymphoma identifies a risk locus at 6p21.32. Nat. Genet. 42, 661–664 (2010).
   Article CAS PubMed PubMed Central Google Scholar
8. Smedby, K.E. et al. GWAS of follicular lymphoma reveals allelic heterogeneity at 6p21.32 and suggests shared genetic susceptibility with diffuse large B-cell lymphoma. PLoS Genet. 7, e1001378 (2011).
   Article CAS PubMed PubMed Central Google Scholar
9. Vijai, J. et al. Susceptibility loci associated with specific and shared subtypes of lymphoid malignancies. PLoS Genet. 9, e1003220 (2013).
   Article CAS PubMed PubMed Central Google Scholar
10. Tan, D.E. et al. Genome-wide association study of B cell non-Hodgkin lymphoma identifies 3q27 as a susceptibility locus in the Chinese population. Nat. Genet. 45, 804–807 (2013).
    Article CAS PubMed Google Scholar
11. Wang, Z. et al. Improved imputation of common and uncommon SNPs with a new reference set. Nat. Genet. 44, 6–7 (2012).
    Article CAS Google Scholar
12. Abecasis, G.R. et al. A map of human genome variation from population-scale sequencing. Nature 467, 1061–1073 (2010).
    Article PubMed Google Scholar
13. Howie, B.N., Donnelly, P. & Marchini, J. A flexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet. 5, e1000529 (2009).
    Article PubMed PubMed Central Google Scholar
14. Wang, S.S. et al. Human leukocyte antigen class I and II alleles in non-Hodgkin lymphoma etiology. Blood 115, 4820–4823 (2010).
    Article CAS PubMed PubMed Central Google Scholar
15. Ward, L.D. & Kellis, M. HaploReg: a resource for exploring chromatin states, conservation, and regulatory motif alterations within sets of genetically linked variants. Nucleic Acids Res. 40, D930–D934 (2012).
    Article CAS PubMed Google Scholar
16. Barenboim, M. & Manke, T. ChroMoS: an integrated web tool for SNP classification, prioritization and functional interpretation. Bioinformatics 29, 2197–2198 (2013).
    Article CAS PubMed PubMed Central Google Scholar
17. Ernst, J. et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473, 43–49 (2011).
    Article CAS PubMed PubMed Central Google Scholar
18. Mukerji, J., Olivieri, K.C., Misra, V., Agopian, K.A. & Gabuzda, D. Proteomic analysis of HIV-1 Nef cellular binding partners reveals a role for exocyst complex proteins in mediating enhancement of intercellular nanotube formation. Retrovirology 9, 33 (2012).
    Article CAS PubMed PubMed Central Google Scholar
19. Mantovani, A. & Balkwill, F. RalB signaling: a bridge between inflammation and cancer. Cell 127, 42–44 (2006).
    Article CAS PubMed Google Scholar
20. Bodemann, B.O. & White, M.A. Ral GTPases and cancer: linchpin support of the tumorigenic platform. Nat. Rev. Cancer 8, 133–140 (2008).
    Article CAS PubMed Google Scholar
21. Issaq, S.H., Lim, K.H. & Counter, C.M. Sec5 and Exo84 foster oncogenic Ras-mediated tumorigenesis. Mol. Cancer Res. 8, 223–231 (2010).
    Article CAS PubMed PubMed Central Google Scholar
22. Kashatus, D.F. Ral GTPases in tumorigenesis: emerging from the shadows. Exp. Cell Res. 319, 2337–2342 (2013).
    Article CAS PubMed PubMed Central Google Scholar
23. Di Bernardo, M.C. et al. A genome-wide association study identifies six susceptibility loci for chronic lymphocytic leukemia. Nat. Genet. 40, 1204–1210 (2008).
    Article CAS PubMed Google Scholar
24. Berndt, S.I. et al. Genome-wide association study identifies multiple risk loci for chronic lymphocytic leukemia. Nat. Genet. 45, 868–876 (2013).
    Article CAS PubMed PubMed Central Google Scholar
25. Wang, S.S. et al. Common gene variants in the tumor necrosis factor (TNF) and TNF receptor superfamilies and NF-κB transcription factors and non-Hodgkin lymphoma risk. PLoS ONE 4, e5360 (2009).
    Article PubMed PubMed Central Google Scholar
26. Wacholder, S., Yeager, M. & Liao, L.M. Invited commentary: more surprises from a gene desert. Am. J. Epidemiol. 175, 488–491 (2012).
    Article PubMed PubMed Central Google Scholar
27. Crowther-Swanepoel, D. et al. Common variants at 2q37.3, 8q24.21, 15q21.3 and 16q24.1 influence chronic lymphocytic leukemia risk. Nat. Genet. 42, 132–136 (2010).
    Article CAS PubMed PubMed Central Google Scholar
28. Enciso-Mora, V. et al. A genome-wide association study of Hodgkin's lymphoma identifies new susceptibility loci at 2p16.1 (REL), 8q24.21 and 10p14 (GATA3). Nat. Genet. 42, 1126–1130 (2010).
    Article CAS PubMed PubMed Central Google Scholar
29. Graham, M. & Adams, J.M. Chromosome 8 breakpoint far 3′ of the c-myc oncogene in a Burkitt's lymphoma 2;8 variant translocation is equivalent to the murine pvt-1 locus. EMBO J. 5, 2845–2851 (1986).
    Article CAS PubMed PubMed Central Google Scholar
30. Love, C. et al. The genetic landscape of mutations in Burkitt lymphoma. Nat. Genet. 44, 1321–1325 (2012).
    Article CAS PubMed PubMed Central Google Scholar
31. Savage, K.J. et al. MYC gene rearrangements are associated with a poor prognosis in diffuse large B-cell lymphoma patients treated with R-CHOP chemotherapy. Blood 114, 3533–3537 (2009).
    Article CAS PubMed Google Scholar
32. Pasqualucci, L. et al. Analysis of the coding genome of diffuse large B-cell lymphoma. Nat. Genet. 43, 830–837 (2011).
    Article CAS PubMed PubMed Central Google Scholar
33. Oñate, S.A., Tsai, S.Y., Tsai, M.J. & O'Malley, B.W. Sequence and characterization of a coactivator for the steroid hormone receptor superfamily. Science 270, 1354–1357 (1995).
    Article PubMed Google Scholar
34. Novokhatska, O. et al. Adaptor proteins intersectin 1 and 2 bind similar proline-rich ligands but are differentially recognized by SH2 domain–containing proteins. PLoS ONE 8, e70546 (2013).
    Article CAS PubMed PubMed Central Google Scholar
35. McGavin, M.K. et al. The intersectin 2 adaptor links Wiskott Aldrich Syndrome protein (WASp)-mediated actin polymerization to T cell antigen receptor endocytosis. J. Exp. Med. 194, 1777–1787 (2001).
    Article CAS PubMed PubMed Central Google Scholar
36. Jia, X. et al. Imputing amino acid polymorphisms in human leukocyte antigens. PLoS ONE 8, e64683 (2013).
    Article CAS PubMed PubMed Central Google Scholar
37. Howell, W.M. HLA and disease: guilt by association. Int. J. Immunogenet. 41, 1–12 (2014).
    Article CAS PubMed Google Scholar
38. Klitz, W., Aldrich, C.L., Fildes, N., Horning, S.J. & Begovich, A.B. Localization of predisposition to Hodgkin disease in the HLA class II region. Am. J. Hum. Genet. 54, 497–505 (1994).
    CAS PubMed PubMed Central Google Scholar
39. Price, P. et al. The genetic basis for the association of the 8.1 ancestral haplotype (A1, B8, DR3) with multiple immunopathological diseases. Immunol. Rev. 167, 257–274 (1999).
    Article CAS PubMed Google Scholar
40. Kumar, V. et al. Common variants on 14q32 and 13q12 are associated with DLBCL susceptibility. J. Hum. Genet. 56, 436–439 (2011).
    Article CAS PubMed Google Scholar
41. Yang, J. et al. Common SNPs explain a large proportion of the heritability for human height. Nat. Genet. 42, 565–569 (2010).
    Article CAS PubMed PubMed Central Google Scholar
42. Morton, L.M. et al. Proposed classification of lymphoid neoplasms for epidemiologic research from the Pathology Working Group of the International Lymphoma Epidemiology Consortium (InterLymph). Blood 110, 695–708 (2007).
    Article CAS PubMed PubMed Central Google Scholar
43. Turner, J.J. et al. InterLymph hierarchical classification of lymphoid neoplasms for epidemiologic research based on the WHO classification (2008): update and future directions. Blood 116, e90–e98 (2010).
    Article CAS PubMed PubMed Central Google Scholar
44. Swerdlow, S., Campo, E. & Harris, N. World Health Organization Classification of Tumours of Haematopoietic and Lymphoid Tissues (IARC Press, Lyon, France, 2008).
45. Pritchard, J.K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).
    CAS PubMed PubMed Central Google Scholar
46. Price, A.L. et al. Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 38, 904–909 (2006).
    Article CAS PubMed Google Scholar
47. Schumacher, F.R. et al. Genome-wide association study identifies new prostate cancer susceptibility loci. Hum. Mol. Genet. 20, 3867–3875 (2011).
    Article CAS PubMed PubMed Central Google Scholar
48. Siddiq, A. et al. A meta-analysis of genome-wide association studies of breast cancer identifies two novel susceptibility loci at 6q14 and 20q11. Hum. Mol. Genet. 21, 5373–5384 (2012).
    Article CAS PubMed PubMed Central Google Scholar
49. Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).
    CAS PubMed PubMed Central Google Scholar
50. Dixon, A.L. et al. A genome-wide association study of global gene expression. Nat. Genet. 39, 1202–1207 (2007).
    Article CAS PubMed Google Scholar
51. Cheung, V.G. et al. Polymorphic _cis_- and _trans_-regulation of human gene expression. PLoS Biol. 8, e1000480 (2010).
    Article PubMed PubMed Central Google Scholar
52. Lee, S.H., Wray, N.R., Goddard, M.E. & Visscher, P.M. Estimating missing heritability for disease from genome-wide association studies. Am. J. Hum. Genet. 88, 294–305 (2011).
    Article PubMed PubMed Central Google Scholar
53. Yang, J., Lee, S.H., Goddard, M.E. & Visscher, P.M. GCTA: a tool for genome-wide complex trait analysis. Am. J. Hum. Genet. 88, 76–82 (2011).
    CAS PubMed PubMed Central Google Scholar
54. Howlader, N. et al. SEER Cancer Statistics Review, 1975–2010. National Cancer Institute http://seer.cancer.gov/csr/1975_2010/ (2013).
55. Fearnhead, P. SequenceLDhot: detecting recombination hotspots. Bioinformatics 22, 3061–3066 (2006).
    Article CAS PubMed Google Scholar
56. Fearnhead, P., Harding, R.M., Schneider, J.A., Myers, S. & Donnelly, P. Application of coalescent methods to reveal fine-scale rate variation and recombination hotspots. Genetics 167, 2067–2081 (2004).
    Article CAS PubMed PubMed Central Google Scholar
57. Li, N. & Stephens, M. Modeling linkage disequilibrium and identifying recombination hotspots using single-nucleotide polymorphism data. Genetics 165, 2213–2233 (2003).
    CAS PubMed PubMed Central Google Scholar
58. Crawford, D.C., et al. Evidence for substantial fine-scale variation in recombination rates across the human genome. Nat. Genet. 36, 700–706 (2004).
    Article CAS PubMed Google Scholar
59. Luna, A. & Nicodemus, K.K. snp.plotter: an R-based SNP/haplotype association and linkage disequilibrium plotting package. Bioinformatics 23, 774–776 (2007).
    Article CAS PubMed Google Scholar

Download references

Acknowledgements

We thank C. Allmer, E. Angelucci, A. Bigelow, S. Buehler, K. Butterbach, A. Chabrier, J.M. Conners, M. Corines, M. Cornelis, K. Corsano, H. Dykes, L. Ershler, A. Gabbas, R.P. Gallagher, R.D. Gascoyne, P. Hui, L. Irish, L. Jacobus, L. Klareskog, A.S. Lai, J. Lunde, M. McAdams, R. Montalvan, L. Padyukov, M. Rais, T. Rattle, L. Rigacci, K. Snyder, G. Specchia, M. Stagner, G. Thomas, C. Tornow, G. Wood and M. Yang. The overall GWAS project was supported by the Intramural Program of the US National Institutes of Health/National Cancer Institute. A list of support provided to individual studies appears in the Supplementary Note.

Author information

Author notes

1. James R Cerhan, Sonja I Berndt, Joseph Vijai, Hervé Ghesquières, James McKay, Sophia S Wang and Zhaoming Wang: These authors contributed equally to this work.
2. Xifeng Wu, Silvia de Sanjose, Karin E Smedby, Gilles Salles, Christine F Skibola, Nathaniel Rothman and Stephen J Chanock: These authors jointly directed this work.

Authors and Affiliations

1. Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota, USA
   James R Cerhan & Susan L Slager
2. Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Maryland, USA
   Sonja I Berndt, Qing Lan, Mark P Purdue, Demetrius Albanes, Patricia Hartge, Lindsay M Morton, Stephanie Weinstein, Joshua Sampson, Charles C Chung, Nilanjan Chatterjee, Joseph F Fraumeni Jr, Nathaniel Rothman & Stephen J Chanock
3. Department of Medicine, Memorial Sloan-Kettering Cancer Center, New York, New York, USA
   Joseph Vijai, Kenneth Offit, Andrew Zelenetz, Robert J Klein & Danylo J Villano
4. Department of Hematology, Centre Léon Bérard, Lyon, France
   Hervé Ghesquières
5. Laboratoire de Biologie Moléculaire de la Cellule, UMR 5239, CNRS, Pierre-Benite, France
   Hervé Ghesquières & Gilles Salles
6. Genetic Cancer Susceptibility Group, Section of Genetics, International Agency for Research on Cancer, Lyon, France
   James McKay
7. Department of Cancer Etiology, City of Hope Beckman Research Institute, Duarte, California, USA
   Sophia S Wang
8. Division of Cancer Epidemiology and Genetics, Cancer Genomics Research Laboratory, National Cancer Institute, Gaithersburg, Maryland, USA
   Zhaoming Wang, Meredith Yeager, Laurie Burdett & Amy Hutchinson
9. Department of Epidemiology, School of Public Health and Comprehensive Cancer Center, Birmingham, Alabama, USA
   Lucia Conde, Jacques Riby & Christine F Skibola
10. Division of Environmental Health Sciences, University of California Berkeley School of Public Health, Berkeley, California, USA
    Lucia Conde, Jacques Riby, Martyn T Smith & Christine F Skibola
11. Department of Medical Genetics and of Epidemiology, University Medical Center Utrecht, Utrecht, the Netherlands
    Paul I W de Bakker
12. Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, the Netherlands
    Paul I W de Bakker & Roel C H Vermeulen
13. Center for Chronic Immunodeficiency, University Medical Center Freiburg, Freiburg, Germany
    Alexandra Nieters
14. Cancer Research Center of Lyon, Centre Léon Bérard, Lyon, France.,
    David Cox & Amelie S Veron
15. Environmental Epidemiology of Cancer Group, INSERM, Centre for Research in Epidemiology and Population Health (CESP), Villejuif, France
    Alain Monnereau & Jacqueline Clavel
16. UMRS 1018, Université Paris Sud, Villejuif, France
    Alain Monnereau & Jacqueline Clavel
17. Registre des Hémopathies Malignes de la Gironde, Institut Bergonié, Bordeaux, France
    Alain Monnereau
18. Winship Cancer Institute, Emory University School of Medicine, Atlanta, Georgia, USA
    Christopher R Flowers
19. Department of Environmental and Occupational Health, Drexel University School of Public Health, Philadelphia, Pennsylvania, USA
    Anneclaire J De Roos
20. Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington, USA
    Anneclaire J De Roos & Lesley F Tinker
21. Genome Sciences Centre, BC Cancer Agency, Vancouver, British Columbia, Canada
    Angela R Brooks-Wilson
22. Department of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, British Columbia, Canada
    Angela R Brooks-Wilson
23. Human Genetics Foundation, Turin, Italy
    Gianluca Severi & Paolo Vineis
24. Cancer Epidemiology Centre, Cancer Council Victoria, Melbourne, Victoria, Australia
    Gianluca Severi & Graham G Giles
25. Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Carlton, Victoria, Australia
    Gianluca Severi & Graham G Giles
26. Department of Epidemiology Research, Division of Health Surveillance and Research, Statens Serum Institut, Copenhagen, Denmark
    Mads Melbye & Henrik Hjalgrim
27. Department of Medicine, Stanford University School of Medicine, Stanford, California, USA
    Mads Melbye
28. Department of Epidemiology, MD Anderson Cancer Center, Houston, Texas, USA
    Jian Gu, Yuanqing Ye & Xifeng Wu
29. Division of Endocrinology, Diabetes and Metabolism, Ohio State University, Columbus, Ohio, USA
    Rebecca D Jackson
30. Department of Health Sciences, University of York, York, UK
    Eleanor Kane, Tracy Lightfoot, Simon Crouch, Alex Smith & Eve Roman
31. Epidemiology Research Program, American Cancer Society, Atlanta, Georgia, USA
    Lauren R Teras & W Ryan Diver
32. Prince of Wales Clinical School, University of New South Wales, Sydney, New South Wales, Australia
    Claire M Vajdic
33. Cancer Control Research, BC Cancer Agency, Vancouver, British Columbia, Canada
    John J Spinelli
34. School of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada
    John J Spinelli
35. Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, USA
    Rachel S Kelly, Kimberly A Bertrand, Hans-Olov Adami, Dimitrios Trichopoulos, Francine Laden, Edward Giovannucci, Peter Kraft, Jinyan Huang, Baoshan Ma & Liming Liang
36. Medical Research Council (MRC)–Public Health England (PHE) Centre for Environment and Health, School of Public Health, Imperial College London, London, UK
    Rachel S Kelly & Paolo Vineis
37. Department of Biomedical Science, University of Cagliari, Monserrato, Italy
    Mariagrazia Zucca
38. Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA
    Kimberly A Bertrand, Brenda M Birmann, Francine Laden & Edward Giovannucci
39. Department of Population Health, New York University School of Medicine, New York, New York, USA
    Anne Zeleniuch-Jacquotte
40. Cancer Institute, New York University School of Medicine, New York, New York, USA
    Anne Zeleniuch-Jacquotte
41. Health Studies Sector, Westat, Rockville, Maryland, USA
    Charles Lawrence
42. Department of Biostatistics, University of Alabama at Birmingham, Birmingham, Alabama, USA
    Degui Zhi
43. Department of Medicine, Mayo Clinic, Rochester, Minnesota, USA
    Thomas M Habermann, Anne J Novak, Mark Liebow, Carrie A Thompson, Stephen M Ansell & Thomas E Witzig
44. Department of Internal Medicine, Carver College of Medicine, The University of Iowa, Iowa City, Iowa, USA
    Brian K Link & George J Weiner
45. Department of Laboratory Medicine and Pathology, Memorial Sloan Kettering Cancer Center, New York, New York, USA
    Ahmet Dogan
46. Division of Biomedical Statistics and Informatics, Mayo Clinic, Jacksonville, Florida, USA
    Yan W Asmann
47. Centre National de Génotypage, Evry, France
    Diana Zelenika
48. Centre Heni Becquerel, Rouen, France
    Hervé Tilly
49. Department of Hematology, Centre Hospitalier Universitaire (CHU) Henri Mondor, Creteil, France
    Corinne Haioun
50. Department of Pathology, Necker Enfants Malades, Université Paris Descartes, Sorbonne Paris Cité, Paris, France
    Thierry Jo Molina
51. Department of Oncology and Pathology, Karolinska Institutet, Karolinska University Hospital Solna, Stockholm, Sweden
    Bengt Glimelius
52. Department of Radiology, Oncology and Radiation Science, Uppsala University, Uppsala, Sweden
    Bengt Glimelius
53. Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden
    Hans-Olov Adami
54. Department of Epidemiology and Biostatistics, University of California, San Francisco, San Francisco, California, USA
    Paige M Bracci & Elizabeth A Holly
55. Department of Preventive Medicine, University of Southern California Keck School of Medicine, University of Southern California, Los Angeles, California, USA
    Wendy Cozen
56. Norris Comprehensive Cancer Center, University of Southern California Keck School of Medicine, University of Southern California, Los Angeles, California, USA
    Wendy Cozen
57. Department of Family Medicine and Public Health Sciences, Wayne State University, Detroit, Michigan, USA
    Richard K Severson
58. Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA
    Kari E North
59. Carolina Center for Genome Sciences, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA
    Kari E North
60. Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany
    Nikolaus Becker & Rudolph Kaaks
61. Unit of Infections and Cancer (UNIC), Cancer Epidemiology Research Programme, Institut Catala d'Oncologia, Bellvitge Biomedical Research Institute (IDIBELL), Barcelona, Spain
    Yolanda Benavente & Silvia de Sanjose
62. Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain
    Yolanda Benavente & Silvia de Sanjose
63. Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, New York, USA
    Paolo Boffetta
64. Group of Genetic Epidemiology, Section of Genetics, International Agency for Research on Cancer, Lyon, France
    Paul Brennan
65. Department of Cancer Epidemiology and Genetics, Masaryk Memorial Cancer Institute and Masaryk University, Brno, Czech Republic
    Lenka Foretova
66. Registre des Hémopathies Malignes de Côte d'Or, University of Burgundy and Dijon University Hospital, Dijon, France
    Marc Maynadie
67. School of Nursing and Human Sciences, Dublin City University, Dublin, Ireland
    Anthony Staines
68. Department of Environmental Health Sciences, Yale School of Public Health, New Haven, Connecticut, USA
    Tongzhang Zheng & Yawei Zhang
69. Department of Biostatistics, Yale School of Public Health, New Haven, Connecticut, USA
    Theodore R Holford
70. Sydney School of Public Health, University of Sydney, Sydney, New South Wales, Australia
    Anne Kricker
71. Pathology, Australian School of Advanced Medicine, Macquarie University, Sydney, New South Wales, Australia
    Jenny Turner
72. Department of Histopathology, Douglass Hanly Moir Pathology, Macquarie Park, New South Wales, Australia
    Jenny Turner
73. Department of Pathology, University of Melbourne, Parkville, Victoria, Australia
    Melissa C Southey
74. Department of Chronic Disease Prevention, National Institute for Health and Welfare, Helsinki, Finland
    Jarmo Virtamo
75. School of Public Health, Imperial College London, London, UK
    Elio Riboli
76. Bureau of Epidemiologic Research, Academy of Athens, Athens, Greece
    Dimitrios Trichopoulos
77. Hellenic Health Foundation, Athens, Greece
    Dimitrios Trichopoulos
78. Institute for Risk Assessment Sciences, Utrecht University, Utrecht, the Netherlands
    Roel C H Vermeulen
79. Department of Epidemiology, German Institute for Human Nutrition, Potsdam, Germany
    Heiner Boeing
80. Danish Cancer Society Research Center, Copenhagen, Denmark
    Anne Tjonneland
81. Hematology Unit, Ospedale Oncologico di Riferimento Regionale A. Businco, Cagliari, Italy.,
    Emanuele Angelucci
82. Department of Surgery and Translational Medicine, Section of Anatomo-Pathology, University of Florence, Florence, Italy
    Simonetta Di Lollo
83. Department of Public Health, Clinical and Molecular Medicine, University of Cagliari, Monserrato, Italy
    Marco Rais
84. Department of Environmental Health, Harvard School of Public Health, Boston, Massachusetts, USA
    Francine Laden
85. Department of Nutrition, Harvard School of Public Health, Boston, Massachusetts, USA
    Edward Giovannucci
86. Department of Biostatistics, Harvard School of Public Health, Boston, Massachusetts, USA
    Peter Kraft & Liming Liang
87. College of Information Science and Technology, Dalian Maritime University, Dalian, China
    Baoshan Ma
88. Department of Health Studies, University of Chicago, Chicago, Illinois, USA
    Brian C H Chiu
89. Dongguk University–Seoul, Seoul, South Korea
    Ju-Hyun Park
90. Department of Pathology, City of Hope National Medical Center, Duarte, California, USA
    Dennis D Weisenburger
91. Department of Medicine Solna, Karolinska Institutet, Stockholm, Sweden
    Karin E Smedby
92. Department of Hematology, Hospices Civils de Lyon, Pierre-Benite, France
    Gilles Salles
93. Department of Hematology, Université Lyon 1, Pierre-Benite, France
    Gilles Salles

Authors

1. James R Cerhan
2. Sonja I Berndt
3. Joseph Vijai
4. Hervé Ghesquières
5. James McKay
6. Sophia S Wang
7. Zhaoming Wang
8. Meredith Yeager
9. Lucia Conde
10. Paul I W de Bakker
11. Alexandra Nieters
12. David Cox
13. Laurie Burdett
14. Alain Monnereau
15. Christopher R Flowers
16. Anneclaire J De Roos
17. Angela R Brooks-Wilson
18. Qing Lan
19. Gianluca Severi
20. Mads Melbye
21. Jian Gu
22. Rebecca D Jackson
23. Eleanor Kane
24. Lauren R Teras
25. Mark P Purdue
26. Claire M Vajdic
27. John J Spinelli
28. Graham G Giles
29. Demetrius Albanes
30. Rachel S Kelly
31. Mariagrazia Zucca
32. Kimberly A Bertrand
33. Anne Zeleniuch-Jacquotte
34. Charles Lawrence
35. Amy Hutchinson
36. Degui Zhi
37. Thomas M Habermann
38. Brian K Link
39. Anne J Novak
40. Ahmet Dogan
41. Yan W Asmann
42. Mark Liebow
43. Carrie A Thompson
44. Stephen M Ansell
45. Thomas E Witzig
46. George J Weiner
47. Amelie S Veron
48. Diana Zelenika
49. Hervé Tilly
50. Corinne Haioun
51. Thierry Jo Molina
52. Henrik Hjalgrim
53. Bengt Glimelius
54. Hans-Olov Adami
55. Paige M Bracci
56. Jacques Riby
57. Martyn T Smith
58. Elizabeth A Holly
59. Wendy Cozen
60. Patricia Hartge
61. Lindsay M Morton
62. Richard K Severson
63. Lesley F Tinker
64. Kari E North
65. Nikolaus Becker
66. Yolanda Benavente
67. Paolo Boffetta
68. Paul Brennan
69. Lenka Foretova
70. Marc Maynadie
71. Anthony Staines
72. Tracy Lightfoot
73. Simon Crouch
74. Alex Smith
75. Eve Roman
76. W Ryan Diver
77. Kenneth Offit
78. Andrew Zelenetz
79. Robert J Klein
80. Danylo J Villano
81. Tongzhang Zheng
82. Yawei Zhang
83. Theodore R Holford
84. Anne Kricker
85. Jenny Turner
86. Melissa C Southey
87. Jacqueline Clavel
88. Jarmo Virtamo
89. Stephanie Weinstein
90. Elio Riboli
91. Paolo Vineis
92. Rudolph Kaaks
93. Dimitrios Trichopoulos
94. Roel C H Vermeulen
95. Heiner Boeing
96. Anne Tjonneland
97. Emanuele Angelucci
98. Simonetta Di Lollo
99. Marco Rais
100. Brenda M Birmann
101. Francine Laden
102. Edward Giovannucci
103. Peter Kraft
104. Jinyan Huang
105. Baoshan Ma
106. Yuanqing Ye
107. Brian C H Chiu
108. Joshua Sampson
109. Liming Liang
110. Ju-Hyun Park
111. Charles C Chung
112. Dennis D Weisenburger
113. Nilanjan Chatterjee
114. Joseph F Fraumeni Jr
115. Susan L Slager
116. Xifeng Wu
117. Silvia de Sanjose
118. Karin E Smedby
119. Gilles Salles
120. Christine F Skibola
121. Nathaniel Rothman
122. Stephen J Chanock

Contributions

J.R.C., S.I.B., S.S.W., A.N., A.R.B.-W., Q.L., G. Severi, M. Melbye, L.R.T., M.P.P., C.L., B.M.B., S.L.S., S.d.S., K.E.S., C.F.S., N.R. and S.J.C. organized and designed the study. J.R.C., L.C., L.B., A.H., P.M.B., E.A.H., S.L.S., G. Salles, C.F.S., N.R. and S.J.C. conducted and supervised the genotyping of samples. J.R.C., S.I.B., J. Vijai, Z.W., M.Y., L.C., P.I.W.d.B., D.C., J.G., D. Zhi, Y.W.A., J.H., B.M., J.S., L.L., J.-H.P., C.C.C., N.C., S.d.S., K.E.S., C.F.S., N.R. and S.J.C. contributed to the design and execution of statistical analysis. J.R.C., S.I.B., J. Vijai, H.G., J.M., S.S.W., Z.W., M.Y., L.C., A.N., D.C., A.M., C.R.F., A.J.D.R., C.L., K.E.S., C.F.S., N.R. and S.J.C. wrote the first draft of the manuscript. J.R.C., J. Vijai, H.G., J.M., S.S.W., L.C., A.N., L.B., A.M., A.R.B.-W., Q.L., G. Severi, M. Melbye, J.G., R.D.J., E.K., L.R.T., M.P.P., C.M.V., J.J.S., G.G.G., D.A., R.S.K., M.Z., K.A.B., A.Z.-J., T.M.H., B.K.L., A.J.N., A.D., Y.W.A., M.L., C.A.T., S.M.A., T.E.W., G.J.W., A.S.V., D. Zelenika, H.T., C.H., T.J.M., H.H., B.G., H.-O.A., P.M.B., J.R., M.T.S., E.A.H., W.C., P.H., L.M.M., R.K.S., L.F.T., K.E.N., N.B., Y.B., P. Boffetta, P. Brennan, L.F., M. Maynadie, A. Staines, T.L., S.C., A. Smith, E. Roman, W.R.D., K.O., A.Z., R.J.K., D.J.V., T.Z., Y.Z., T.R.H., A.K., J.T., M.C.S., J.C., J. Virtamo, S.W., E. Riboli, P.V., R.K., D.T., R.C.H.V., H.B., A.T., E.A., S.D.L., M.R., B.M.B., F.L., E.G., P.K., Y.Y., B.C.H.C., D.D.W., N.C., J.F.F., S.L.S., X.W., S.d.S., K.E.S., G. Salles, C.F.S. and N.R. conducted the epidemiological studies and contributed samples to the GWAS and/or follow-up genotyping. All authors contributed to the writing of the manuscript.

Corresponding author

Correspondence toJames R Cerhan.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Integrated supplementary information

Supplementary information

Rights and permissions

About this article

Cite this article

Cerhan, J., Berndt, S., Vijai, J. et al. Genome-wide association study identifies multiple susceptibility loci for diffuse large B cell lymphoma.Nat Genet 46, 1233–1238 (2014). https://doi.org/10.1038/ng.3105

Download citation

• Received: 26 June 2014
• Accepted: 04 September 2014
• Published: 28 September 2014
• Issue date: November 2014
• DOI: https://doi.org/10.1038/ng.3105