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Research Article

GWAS of Follicular Lymphoma Reveals Allelic Heterogeneity at 6p21.32 and Suggests Shared Genetic Susceptibility with Diffuse Large B-cell Lymphoma

  • Karin E. Smedby equal contributor,

    equal contributor Contributed equally to this work with: Karin E. Smedby, Jia Nee Foo

    Affiliation: Department of Medicine, Clinical Epidemiology Unit, Karolinska Institutet, Stockholm, Sweden

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  • Jia Nee Foo equal contributor,

    equal contributor Contributed equally to this work with: Karin E. Smedby, Jia Nee Foo

    Affiliation: Human Genetics, Genome Institute of Singapore, A*STAR, Singapore, Singapore

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  • Christine F. Skibola ,

    Affiliation: Division of Environmental Health Sciences, School of Public Health, University of California Berkeley, Berkeley, California, United States of America

    ‡ These authors also contributed equally to this work.

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  • Hatef Darabi ,

    Affiliation: Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden

    ‡ These authors also contributed equally to this work.

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  • Lucia Conde,

    Affiliation: Division of Environmental Health Sciences, School of Public Health, University of California Berkeley, Berkeley, California, United States of America

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  • Henrik Hjalgrim,

    Affiliation: Department of Epidemiology Research, Statens Serum Institut, Copenhagen, Denmark

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  • Vikrant Kumar,

    Affiliation: Human Genetics, Genome Institute of Singapore, A*STAR, Singapore, Singapore

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  • Ellen T. Chang,

    Affiliations: Cancer Prevention Institute of California, Fremont, California, United States of America, Division of Epidemiology, Department of Health Research and Policy, Stanford University School of Medicine, Stanford, California, United States of America

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  • Nathaniel Rothman,

    Affiliation: Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, United States of America

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  • James R. Cerhan,

    Affiliation: College of Medicine, Mayo Clinic, Rochester, Minnesota, United States of America

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  • Angela R. Brooks-Wilson,

    Affiliations: British Columbia Cancer Research Center, British Columbia Cancer Agency, Vancouver, Canada, Department of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, Canada

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  • Emil Rehnberg,

    Affiliation: Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden

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  • Ishak D. Irwan,

    Affiliation: Human Genetics, Genome Institute of Singapore, A*STAR, Singapore, Singapore

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  • Lars P. Ryder,

    Affiliation: Department of Clinical Immunology, University Hospital of Copenhagen, Copenhagen, Denmark

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  • Peter N. Brown,

    Affiliation: Department of Haematology, Copenhagen University Hospital, Copenhagen, Denmark

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  • Paige M. Bracci,

    Affiliation: Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, California, United States of America

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  • Luz Agana,

    Affiliation: Division of Environmental Health Sciences, School of Public Health, University of California Berkeley, Berkeley, California, United States of America

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  • Jacques Riby,

    Affiliation: Division of Environmental Health Sciences, School of Public Health, University of California Berkeley, Berkeley, California, United States of America

    X
  • Wendy Cozen,

    Affiliation: Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California, United States of America

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  • Scott Davis,

    Affiliations: Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America, University of Washington, Seattle, Washington, United States of America

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  • Patricia Hartge,

    Affiliation: Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, United States of America

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  • Lindsay M. Morton,

    Affiliation: Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, United States of America

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  • Richard K. Severson,

    Affiliations: Department of Family Medicine and Public Health Sciences, Wayne State University, Detroit, Michigan, United States of America, Karmanos Cancer Institute, Detroit, Michigan, United States of America

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  • Sophia S. Wang,

    Affiliations: Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, United States of America, Division of Etiology, Beckman Research Institute and the City of Hope, Duarte, California, United States of America

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  • Susan L. Slager,

    Affiliation: College of Medicine, Mayo Clinic, Rochester, Minnesota, United States of America

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  • Zachary S. Fredericksen,

    Affiliation: College of Medicine, Mayo Clinic, Rochester, Minnesota, United States of America

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  • Anne J. Novak,

    Affiliation: College of Medicine, Mayo Clinic, Rochester, Minnesota, United States of America

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  • Neil E. Kay,

    Affiliation: College of Medicine, Mayo Clinic, Rochester, Minnesota, United States of America

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  • Thomas M. Habermann,

    Affiliation: College of Medicine, Mayo Clinic, Rochester, Minnesota, United States of America

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  • Bruce Armstrong,

    Affiliation: Sydney School of Public Health, The University of Sydney, Sydney, Australia

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  • Anne Kricker,

    Affiliation: Sydney School of Public Health, The University of Sydney, Sydney, Australia

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  • Sam Milliken,

    Affiliation: Department of Haematology, St. Vincent's Hospital, Sydney, Australia

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  • Mark P. Purdue,

    Affiliation: Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, United States of America

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  • Claire M. Vajdic,

    Affiliation: University of New South Wales Cancer Research Center, Prince of Wales Clinical School, Sydney, Australia

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  • Peter Boyle,

    Affiliation: International Prevention Research Institute, Lyon, France

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  • Qing Lan,

    Affiliation: Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, United States of America

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  • Shelia H. Zahm,

    Affiliation: Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, United States of America

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  • Yawei Zhang,

    Affiliation: School of Public Health, Yale University, New Haven, Connecticut, United States of America

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  • Tongzhang Zheng,

    Affiliation: School of Public Health, Yale University, New Haven, Connecticut, United States of America

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  • Stephen Leach,

    Affiliation: Canada's Michael Smith Genome Sciences Centre, British Columbia Cancer Agency, Vancouver, Canada

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  • John J. Spinelli,

    Affiliations: British Columbia Cancer Research Center, British Columbia Cancer Agency, Vancouver, Canada, School of Population and Public Health, University of British Columbia, Vancouver, Canada

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  • Martyn T. Smith,

    Affiliation: Division of Environmental Health Sciences, School of Public Health, University of California Berkeley, Berkeley, California, United States of America

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  • Stephen J. Chanock,

    Affiliation: Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, United States of America

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  • Leonid Padyukov,

    Affiliation: Rheumatology Unit, Department of Medicine, Karolinska Institutet and Karolinska University Hospital Solna, Stockholm, Sweden

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  • Lars Alfredsson,

    Affiliation: Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden

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  • Lars Klareskog,

    Affiliation: Rheumatology Unit, Department of Medicine, Karolinska Institutet and Karolinska University Hospital Solna, Stockholm, Sweden

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  • Bengt Glimelius,

    Affiliations: Department of Pathology and Oncology, Karolinska Institutet, Stockholm, Sweden, Department of Radiology, Oncology, and Radiation Sciences, Uppsala University, Uppsala, Sweden

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  • Mads Melbye,

    Affiliation: Department of Epidemiology Research, Statens Serum Institut, Copenhagen, Denmark

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  • Edison T. Liu,

    Affiliation: Human Genetics, Genome Institute of Singapore, A*STAR, Singapore, Singapore

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  • Hans-Olov Adami,

    Affiliations: Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden, Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, United States of America

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  • Keith Humphreys ,

    Affiliation: Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden

    These authors also contributed equally to this work.

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  • Jianjun Liu mail

    liuj3@gis.a-star.edu.sg

    Affiliation: Human Genetics, Genome Institute of Singapore, A*STAR, Singapore, Singapore

    These authors also contributed equally to this work.

    X
  • Published: April 21, 2011
  • DOI: 10.1371/journal.pgen.1001378

About the Authors

Karin E. Smedby
Department of Medicine, Clinical Epidemiology Unit, Karolinska Institutet, Stockholm, Sweden
Jia Nee Foo, Vikrant Kumar, Ishak D. Irwan, Edison T. Liu, Jianjun Liu
Human Genetics, Genome Institute of Singapore, A*STAR, Singapore, Singapore
Christine F. Skibola, Lucia Conde, Luz Agana, Jacques Riby, Martyn T. Smith
Division of Environmental Health Sciences, School of Public Health, University of California Berkeley, Berkeley, California, United States of America
Hatef Darabi, Emil Rehnberg, Hans-Olov Adami, Keith Humphreys
Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden
Henrik Hjalgrim, Mads Melbye
Department of Epidemiology Research, Statens Serum Institut, Copenhagen, Denmark
Ellen T. Chang
Cancer Prevention Institute of California, Fremont, California, United States of America
Ellen T. Chang
Division of Epidemiology, Department of Health Research and Policy, Stanford University School of Medicine, Stanford, California, United States of America
Nathaniel Rothman, Patricia Hartge, Lindsay M. Morton, Sophia S. Wang, Mark P. Purdue, Qing Lan, Shelia H. Zahm, Stephen J. Chanock
Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, United States of America
James R. Cerhan, Susan L. Slager, Zachary S. Fredericksen, Anne J. Novak, Neil E. Kay, Thomas M. Habermann
College of Medicine, Mayo Clinic, Rochester, Minnesota, United States of America
Angela R. Brooks-Wilson, John J. Spinelli
British Columbia Cancer Research Center, British Columbia Cancer Agency, Vancouver, Canada
Angela R. Brooks-Wilson
Department of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, Canada
Lars P. Ryder
Department of Clinical Immunology, University Hospital of Copenhagen, Copenhagen, Denmark
Peter N. Brown
Department of Haematology, Copenhagen University Hospital, Copenhagen, Denmark
Paige M. Bracci
Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, California, United States of America
Wendy Cozen
Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California, United States of America
Scott Davis
Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America
Scott Davis
University of Washington, Seattle, Washington, United States of America
Richard K. Severson
Department of Family Medicine and Public Health Sciences, Wayne State University, Detroit, Michigan, United States of America
Richard K. Severson
Karmanos Cancer Institute, Detroit, Michigan, United States of America
Sophia S. Wang
Division of Etiology, Beckman Research Institute and the City of Hope, Duarte, California, United States of America
Bruce Armstrong, Anne Kricker
Sydney School of Public Health, The University of Sydney, Sydney, Australia
Sam Milliken
Department of Haematology, St. Vincent's Hospital, Sydney, Australia
Claire M. Vajdic
University of New South Wales Cancer Research Center, Prince of Wales Clinical School, Sydney, Australia
Peter Boyle
International Prevention Research Institute, Lyon, France
Yawei Zhang, Tongzhang Zheng
School of Public Health, Yale University, New Haven, Connecticut, United States of America
Stephen Leach
Canada's Michael Smith Genome Sciences Centre, British Columbia Cancer Agency, Vancouver, Canada
John J. Spinelli
School of Population and Public Health, University of British Columbia, Vancouver, Canada
Leonid Padyukov, Lars Klareskog
Rheumatology Unit, Department of Medicine, Karolinska Institutet and Karolinska University Hospital Solna, Stockholm, Sweden
Lars Alfredsson
Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden
Bengt Glimelius
Department of Pathology and Oncology, Karolinska Institutet, Stockholm, Sweden
Bengt Glimelius
Department of Radiology, Oncology, and Radiation Sciences, Uppsala University, Uppsala, Sweden
Hans-Olov Adami
Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, United States of America

Corresponding Author

Email: liuj3@gis.a-star.edu.sg

Competing Interests

The authors have declared that no competing interests exist.

Author Contributions

Conceived and designed the experiments: KES ETL HOA JL. Performed the experiments: IDI. Analyzed the data: KES JNF CFS HD LC VK ER KH JL. Contributed reagents/materials/analysis tools: KES CFS LC HH ETC NR JRC LPR PNB PMB LA JR WC SD PH LMM RKS SSW SLS ZSF AJN NEK TMH BA AK SM MPP CMV PB QL SHZ YZ TZ SL JJS MTS SJC LP LA LK BG MM ETL HOA JL. Wrote the paper: KES JNF KH JL. Critical revision of manuscript: CFS HD LC VK ETC IDI SJC. Genotyped samples and provided data from the BC study: ARBW. Provided data from the SF1 and SF2 GWAS studies: JR. Supervised the experiments: JL JNF.