Meta-analysis of genome-wide association studies discovers multiple loci for chronic lymphocytic leukemia

Sonja I. Berndt (), Nicola J. Camp, Christine F. Skibola, Joseph Vijai, Zhaoming Wang, Jian Gu, Alexandra Nieters, Rachel S. Kelly, Karin E. Smedby, Alain Monnereau, Wendy Cozen, Angela Cox, Sophia S. Wang, Qing Lan, Lauren R. Teras, Moara Machado, Meredith Yeager, Angela R. Brooks-Wilson, Patricia Hartge, Mark P. Purdue, Brenda M. Birmann, Claire M. Vajdic, Pierluigi Cocco, Yawei Zhang, Graham G. Giles, Anne Zeleniuch-Jacquotte, Charles Lawrence, Rebecca Montalvan, Laurie Burdett, Amy Hutchinson, Yuanqing Ye, Timothy G. Call, Tait D. Shanafelt, Anne J. Novak, Neil E. Kay, Mark Liebow, Julie M. Cunningham, Cristine Allmer, Henrik Hjalgrim, Hans-Olov Adami, Mads Melbye, Bengt Glimelius, Ellen T. Chang, Martha Glenn, Karen Curtin, Lisa A. Cannon-Albright, W Ryan Diver, Brian K. Link, George J. Weiner, Lucia Conde, Paige M. Bracci, Jacques Riby, Donna K. Arnett, Degui Zhi, Justin M. Leach, Elizabeth A. Holly, Rebecca D. Jackson, Lesley F. Tinker, Yolanda Benavente, Núria Sala, Delphine Casabonne, Nikolaus Becker, Paolo Boffetta, Paul Brennan, Lenka Foretova, Marc Maynadie, James McKay, Anthony Staines, Kari G. Chaffee, Sara J. Achenbach, Celine M. Vachon, Lynn R. Goldin, Sara S. Strom, Jose F. Leis, J. Brice Weinberg, Neil E. Caporaso, Aaron D. Norman, Anneclaire J. De Roos, Lindsay M. Morton, Richard K. Severson, Elio Riboli, Paolo Vineis, Rudolph Kaaks, Giovanna Masala, Elisabete Weiderpass, María- Dolores Chirlaque, Roel C. H. Vermeulen, Ruth C. Travis, Melissa C. Southey, Roger L. Milne, Demetrius Albanes, Jarmo Virtamo, Stephanie Weinstein, Jacqueline Clavel, Tongzhang Zheng, Theodore R. Holford, Danylo J. Villano, Ann Maria, John J. Spinelli, Randy D. Gascoyne, Joseph M. Connors, Kimberly A. Bertrand, Edward Giovannucci, Peter Kraft, Anne Kricker, Jenny Turner, Maria Grazia Ennas, Giovanni M. Ferri, Lucia Miligi, Liming Liang, Baoshan Ma, Jinyan Huang, Simon Crouch, Ju-Hyun Park, Nilanjan Chatterjee, Kari E. North, John A. Snowden, Josh Wright, Joseph F. Fraumeni, Kenneth Offit, Xifeng Wu, Silvia de Sanjose, James R. Cerhan, Stephen J. Chanock, Nathaniel Rothman and Susan L. Slager
Additional contact information
Sonja I. Berndt: National Cancer Institute
Nicola J. Camp: Huntsman Cancer Institute and University of Utah School of Medicine
Christine F. Skibola: School of Public Health and Comprehensive Cancer Center, University of Alabama at Birmingham
Joseph Vijai: Memorial Sloan Kettering Cancer Center
Zhaoming Wang: Cancer Genomics Research Laboratory, National Cancer Institute
Jian Gu: MD Anderson Cancer Center
Alexandra Nieters: Center for Chronic Immunodeficiency, University Medical Center Freiburg
Rachel S. Kelly: Harvard School of Public Health
Karin E. Smedby: Solna, Karolinska Institutet, Karolinska University Hospital
Alain Monnereau: Epidemiology of Childhood and Adolescent Cancers Group, INSERM, Center of Research in Epidemiology and Statistics Sorbonne Paris Cité (CRESS)
Wendy Cozen: USC Keck School of Medicine, University of Southern California
Angela Cox: University of Sheffield
Sophia S. Wang: City of Hope Beckman Research Institute
Qing Lan: National Cancer Institute
Lauren R. Teras: Epidemiology Research Program, American Cancer Society
Moara Machado: National Cancer Institute
Meredith Yeager: Cancer Genomics Research Laboratory, National Cancer Institute
Angela R. Brooks-Wilson: Genome Sciences Centre, BC Cancer Agency
Patricia Hartge: National Cancer Institute
Mark P. Purdue: Ontario Health Study
Brenda M. Birmann: Brigham and Women’s Hospital and Harvard Medical School
Claire M. Vajdic: Centre for Big Data Research in Health, University of New South Wales
Pierluigi Cocco: Clinical and Molecular Medicine, University of Cagliari
Yawei Zhang: Yale School of Public Health
Graham G. Giles: Cancer Epidemiology Centre, Cancer Council Victoria
Anne Zeleniuch-Jacquotte: New York University School of Medicine
Charles Lawrence: Westat
Rebecca Montalvan: Westat
Laurie Burdett: Cancer Genomics Research Laboratory, National Cancer Institute
Amy Hutchinson: Cancer Genomics Research Laboratory, National Cancer Institute
Yuanqing Ye: MD Anderson Cancer Center
Timothy G. Call: Mayo Clinic
Tait D. Shanafelt: Mayo Clinic
Anne J. Novak: Mayo Clinic
Neil E. Kay: Mayo Clinic
Mark Liebow: Mayo Clinic
Julie M. Cunningham: Mayo Clinic
Cristine Allmer: Mayo Clinic
Henrik Hjalgrim: Statens Serum Institut
Hans-Olov Adami: Harvard School of Public Health
Mads Melbye: Statens Serum Institut
Bengt Glimelius: Genetics and Pathology, Uppsala University
Ellen T. Chang: Center for Epidemiology and Computational Biology, Health Sciences, Exponent, Inc.
Martha Glenn: Huntsman Cancer Institute
Karen Curtin: University of Utah School of Medicine
Lisa A. Cannon-Albright: University of Utah School of Medicine
W Ryan Diver: Epidemiology Research Program, American Cancer Society
Brian K. Link: Carver College of Medicine, The University of Iowa
George J. Weiner: Carver College of Medicine, The University of Iowa
Lucia Conde: School of Public Health and Comprehensive Cancer Center, University of Alabama at Birmingham
Paige M. Bracci: University of California San Francisco
Jacques Riby: School of Public Health and Comprehensive Cancer Center, University of Alabama at Birmingham
Donna K. Arnett: School of Public Health and Comprehensive Cancer Center, University of Alabama at Birmingham
Degui Zhi: University of Alabama at Birmingham
Justin M. Leach: University of Alabama at Birmingham
Elizabeth A. Holly: University of California San Francisco
Rebecca D. Jackson: Diabetes and Metabolism, The Ohio State University
Lesley F. Tinker: Fred Hutchinson Cancer Research Center
Yolanda Benavente: Cancer Epidemiology Research Programme, Catalan Institute of Oncology-IDIBELL, L’Hospitalet de Llobregat
Núria Sala: Unit of Nutrition, Environment and Cancer, Cancer Epidemiology Research Program, Catalan Institute of Oncology-IDIBELL, L’Hospitalet de Llobregat
Delphine Casabonne: Unit of Infections and Cancer (UNIC), Cancer Epidemiology Research Programme, Institut Catala d’Oncologia, IDIBELL, 08908L’Hospitalet de Llobregat
Nikolaus Becker: German Cancer Research Center (DKFZ)
Paolo Boffetta: The Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai
Paul Brennan: International Agency for Research on Cancer (IARC)
Lenka Foretova: Masaryk Memorial Cancer Institute and MF MU
Marc Maynadie: EA 4184, Registre des Hémopathies Malignes de Côte d’Or, University of Burgundy and Dijon University Hospital
James McKay: International Agency for Research on Cancer (IARC)
Anthony Staines: School of Nursing and Human Sciences, Dublin City University
Kari G. Chaffee: Mayo Clinic
Sara J. Achenbach: Mayo Clinic
Celine M. Vachon: Mayo Clinic
Lynn R. Goldin: National Cancer Institute
Sara S. Strom: MD Anderson Cancer Center
Jose F. Leis: Mayo Clinic
J. Brice Weinberg: Duke University and VA Medical Centers
Neil E. Caporaso: National Cancer Institute
Aaron D. Norman: Mayo Clinic
Anneclaire J. De Roos: Fred Hutchinson Cancer Research Center
Lindsay M. Morton: National Cancer Institute
Richard K. Severson: Wayne State University
Elio Riboli: School of Public Health, Imperial College London
Paolo Vineis: MRC-PHE Centre for Environment and Health, School of Public Health, Imperial College London
Rudolph Kaaks: German Cancer Research Center (DKFZ)
Giovanna Masala: Molecular and Nutritional Epidemiology Unit, Cancer Research and Prevention Institute (ISPO)
Elisabete Weiderpass: Karolinska Institutet
María- Dolores Chirlaque: CIBER de Epidemiología y Salud Pública (CIBERESP)
Roel C. H. Vermeulen: Institute for Risk Assessment Sciences, Utrecht University
Ruth C. Travis: Cancer Epidemiology Unit, University of Oxford
Melissa C. Southey: Genetic Epidemiology Laboratory, University of Melbourne
Roger L. Milne: Cancer Epidemiology Centre, Cancer Council Victoria
Demetrius Albanes: National Cancer Institute
Jarmo Virtamo: Chronic Disease Prevention Unit, National Institute for Health and Welfare
Stephanie Weinstein: National Cancer Institute
Jacqueline Clavel: Epidemiology of Childhood and Adolescent Cancers Group, INSERM, Center of Research in Epidemiology and Statistics Sorbonne Paris Cité (CRESS)
Tongzhang Zheng: Yale School of Public Health
Theodore R. Holford: Yale School of Public Health
Danylo J. Villano: Memorial Sloan Kettering Cancer Center
Ann Maria: Memorial Sloan Kettering Cancer Center
John J. Spinelli: Cancer Control Research, BC Cancer Agency
Randy D. Gascoyne: Center for Lymphoid Cancer, BC Cancer Agency
Joseph M. Connors: Center for Lymphoid Cancer, BC Cancer Agency
Kimberly A. Bertrand: Harvard School of Public Health
Edward Giovannucci: Harvard School of Public Health
Peter Kraft: Harvard School of Public Health
Anne Kricker: Sydney School of Public Health, The University of Sydney
Jenny Turner: Faculty of Medicine and Health Sciences, Macquarie University
Maria Grazia Ennas: University of Cagliari
Giovanni M. Ferri: University of Bari
Lucia Miligi: Environmental and Occupational Epidemiology Unit, Cancer Prevention and Research Institute (ISPO)
Liming Liang: Harvard School of Public Health
Baoshan Ma: Harvard School of Public Health
Jinyan Huang: Harvard School of Public Health
Simon Crouch: University of York
Ju-Hyun Park: Dongguk University
Nilanjan Chatterjee: National Cancer Institute
Kari E. North: University of North Carolina at Chapel Hill
John A. Snowden: University of Sheffield
Josh Wright: University of Sheffield
Joseph F. Fraumeni: National Cancer Institute
Kenneth Offit: Memorial Sloan Kettering Cancer Center
Xifeng Wu: MD Anderson Cancer Center
Silvia de Sanjose: Cancer Epidemiology Research Programme, Catalan Institute of Oncology-IDIBELL, L’Hospitalet de Llobregat
James R. Cerhan: Mayo Clinic
Stephen J. Chanock: National Cancer Institute
Nathaniel Rothman: National Cancer Institute
Susan L. Slager: Mayo Clinic

Nature Communications, 2016, vol. 7, issue 1, 1-9

Abstract: Abstract Chronic lymphocytic leukemia (CLL) is a common lymphoid malignancy with strong heritability. To further understand the genetic susceptibility for CLL and identify common loci associated with risk, we conducted a meta-analysis of four genome-wide association studies (GWAS) composed of 3,100 cases and 7,667 controls with follow-up replication in 1,958 cases and 5,530 controls. Here we report three new loci at 3p24.1 (rs9880772, EOMES, P=2.55 × 10−11), 6p25.2 (rs73718779, SERPINB6, P=1.97 × 10−8) and 3q28 (rs9815073, LPP, P=3.62 × 10−8), as well as a new independent SNP at the known 2q13 locus (rs9308731, BCL2L11, P=1.00 × 10−11) in the combined analysis. We find suggestive evidence (P

Date: 2016
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DOI: 10.1038/ncomms10933

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