A growing number of loci within the human leukocyte antigen (HLA) region have been implicated in non-Hodgkin lymphoma (NHL) etiology. Here, we test a complementary hypothesis of "heterozygote advantage" regarding the role of HLA and NHL, whereby HLA diversity is beneficial and homozygous HLA loci are associated with increased disease risk. HLA alleles at class I and II loci were imputed from genome-wide association studies (GWAS) using SNP2HLA for 3,617 diffuse large B-cell lymphomas (DLBCL), 2,686 follicular lymphomas (FL), 2,878 chronic lymphocytic leukemia/small lymphocytic lymphomas (CLL/SLL), 741 marginal zone lymphomas (MZL), and 8,753 controls of European descent. Both DLBCL and MZL risk were elevated with homozygosity at class I HLA-B and -C loci (OR DLBCL = 1.31, 95% CI = 1.06-1.60; OR MZL = 1.45, 95% CI = 1.12-1.89) and class II HLA-DRB1 locus (OR DLBCL = 2.10, 95% CI = 1.24-3.55; OR MZL = 2.10, 95% CI = 0.99-4.45). Increased FL risk was observed with the overall increase in number of homozygous HLA class II loci (P trend < 0.0001, FDR = 0.0005). These results support a role for HLA zygosity in NHL etiology and suggests that distinct immune pathways may underly the etiology of the different NHL subtypes.Significance: HLA gene diversity reduces risk for non-Hodgkin lymphoma. Cancer Res; 78(14); 4086-96. ©2018 AACR.

Bill Lyons Informatics Centre UCL Cancer Institute University College London London United Kingdom

Braun School of Public Health and Community Medicine Hadassah Hebrew University Medical Center Jerusalem Israel

Cancer and Inflammation Program Leidos Biomedical Research Inc Frederick National Laboratory for Cancer Research Frederick Maryland and Ragon Institute of MGH MIT and Harvard Cambridge Massachusetts

Cancer Control Research British Columbia Cancer Agency Vancouver British Columbia Canada School of Population and Public Health University of British Columbia Vancouver British Columbia Canada

Cancer Epidemiology and Intelligence Division Cancer Council Victoria Melbourne Australia

Cancer Epidemiology and Intelligence Division Cancer Council Victoria Melbourne Australia Centre for Epidemiology and Biostatistics Melbourne School of Population and Global Health University of Melbourne Melbourne Victoria Australia

Cancer Epidemiology Unit University of Oxford Oxford United Kingdom

Cancer Research Center of Lyon INSERM UMR1052 Center Léon Bérard Lyon France

Center of Oncological Prevention Piemonte and Unit of Medical Statistics and Epidemiology Department Translational Medicine University of Piemonte Orientale Novara Italy

Centre for Big Data Research in Health The University of New South Wales Sydney New South Wales Australia

Centre for Chronic Immunodeficiency University Medical Center Freiburg Freiburg Baden Württemberg Germany

Channing Division of Network Medicine Department of Medicine Brigham and Women's Hospital and Harvard Medical School Boston Massachusetts

Department of Biomedical Physiology and Kinesiology Simon Fraser University Burnaby British Columbia Canada Genome Sciences Centre BC Cancer Agency Vancouver British Columbia Canada

Department of Biomedical Science University of Cagliari Monserrato Cagliari Italy

Department of Cancer Epidemiology and Genetics Masaryk Memorial Cancer Institute MF MU Brno Czech Republic

Department of Epidemiology and Biostatistics School of Public Health Imperial College London London United Kingdom

Department of Epidemiology and Biostatistics University of California San Francisco San Francisco California

Department of Epidemiology Harvard T H Chan School of Public Health Boston Massachusetts Department of Biostatistics Harvard T H Chan School of Public Health Boston Massachusetts

Department of Epidemiology Research Division of Health Surveillance and Research Statens Serum Institut Copenhagen Denmark Department of Hematology Rishospitalet Copenhagen Denmark

Department of Epidemiology Research Division of Health Surveillance and Research Statens Serum Institut Copenhagen Denmark Department of Medicine Stanford University School of Medicine Stanford Calfornia

Department of Epidemiology School of Public Health Brown University Providence Rhode Island

Department of Family Medicine and Public Health Sciences Wayne State University Detroit Michigan

Department of Health Sciences Research Mayo Clinic Rochester Minnesota

Department of Health Sciences University of York York United Kingdom

Department of Hematology and Medical Oncology Emory University School of Medicine Atlanta Georgia

Department of Hematology Rishospitalet Copenhagen Denmark

Department of Histopathology Douglass Hanly Moir Pathology Sydney Australia Faculty of Medicine and Health Sciences Macquarie University Sydney Australia

Department of Immunology CHU Henri Mondor Créteil France

Department of Immunology CHU Henri Mondor Créteil France INSERM U 955 CHU Henri Mondor Créteil France

Department of Immunology Genetics and Pathology Uppsala University Uppsala Sweden

Department of Internal Medicine Carver College of Medicine The University of Iowa Iowa City Iowa

Department of Internal Medicine Huntsman Cancer Institute University of Utah School of Medicine Salt Lake City Utah

Department of Laboratory Medicine and Pathology Mayo Clinic Rochester Minnesota

Department of Medical Epidemiology and Biostatistics Karolinska Institutet Stockholm Sweden

Department of Medicine Memorial Sloan Kettering Cancer Center New York City New York

Department of Medicine Solna unit of clinical epidemiology Karolinska Institutet Stockholm Sweden Hematology Center Karolinska University Hospital Stockholm Sweden

Department of Obstetrics and Gynecology New York University School of Medicine New York City New York Department of Environmental Medicine New York University School of Medicine New York City New York Perlmutter Cancer Center NYU Langone Medical Center New York City New York

Department of Pathology City of Hope Duarte California

Department of Pathology School of Medicine and the UAB Comprehensive Cancer Center The University of Alabama at Birmingham Birmingham Alabama

Department of Population Sciences Beckman Research Institute and the City of Hope Duarte California

Department of Public Health Clinical and Molecular Medicine University of Cagliari Cagliari Italy

Department of Surgery Yale School of Medicine New Haven Connecticut Department of Environmental Health Sciences Yale School of Public Health New Haven

Division of Cancer Epidemiology and Genetics NCI Bethesda Maryland

Division of Clinical Epidemiology German Cancer Research Centre Heidelberg Baden Württemberg Germany

Division of Environmental Health Sciences School of Public Health University of California Berkeley Berkeley California

Division of Hematology S Francesco Hospital Nuoro Italy

Epidemiology of Childhood and Adolescent Cancers Group Inserm Center of Research in Epidemiology and Statistics Sorbonne Paris Cité Paris France Université Paris Descartes Paris France

Epidemiology Research Program American Cancer Society Atlanta Georgia

Fred Hutchinson Cancer Research Center and School of Public Health and Community Medicine University of Washington Seattle Washington

Genetic Epidemiology Laboratory Department of Pathology University of Melbourne Melbourne Victoria Australia

Institute for Risk Assessment Sciences Utrecht University Utrecht the Netherlands Julius Center for Health Sciences and Primary Care University Medical Center Utrecht Utrecht the Netherlands

International Agency for Research on Cancer Lyon France

Laboratoire de Biologie Moléculaire de la Cellule UMR 5239 Centre National de la Recherche Scientifique Pierre benite Cedex France Department of Hematology Hospices Civils De Lyon Centre Hospitalier Lyon Sud and Université Claude Bernard Lyon France

Norris Comprehensive Cancer Center Keck School of Medicine of USC Departments of Preventive Medicine and Pathology University of Southern California Los Angeles Calfornia

Registry of Hematological Malignancies of Cote d'Or INSERM UMR1231 University of Burgundy and Dijon University Hospital Dijon France

School of Nursing and Human Sciences Dublin City University Dublin Ireland

School of Public Health Imperial College London London United Kingdom

Sydney School of Public Health The University of Sydney Sydney Australia

The Tisch Cancer Institute Icahn School of Medicine at Mount Sinai New York City New York

Unit of Infections and Cancer Cancer Epidemiology Research Programme Institut Català d' Oncologia IDIBELL 08908 L'Hospitalet de Llobregat Barcelona Spain CIBER Epidemiología y Salud Pública Madrid Spain

Université Paris Descartes Paris France Laboratoire de Biologie Moléculaire de la Cellule UMR 5239 Centre National de la Recherche Scientifique Pierre benite Cedex France

Université Paris Descartes Paris France Université Paris Descartes Paris France Registre des hémopathies malignes de la Gironde Institut Bergonié University of Bordeaux Inserm Team EPICENE UMR 1219 France

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$a Wang, Sophia S $u Department of Population Sciences, Beckman Research Institute and the City of Hope, Duarte, California. sowang@coh.org.

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$a HLA Class I and II Diversity Contributes to the Etiologic Heterogeneity of Non-Hodgkin Lymphoma Subtypes / $c SS. Wang, M. Carrington, SI. Berndt, SL. Slager, PM. Bracci, J. Voutsinas, JR. Cerhan, KE. Smedby, H. Hjalgrim, J. Vijai, LM. Morton, R. Vermeulen, O. Paltiel, CM. Vajdic, MS. Linet, A. Nieters, S. de Sanjose, W. Cozen, EE. Brown, J. Turner, JJ. Spinelli, T. Zheng, BM. Birmann, CR. Flowers, N. Becker, EA. Holly, E. Kane, D. Weisenburger, M. Maynadie, P. Cocco, D. Albanes, SJ. Weinstein, LR. Teras, WR. Diver, SJ. Lax, RC. Travis, R. Kaaks, E. Riboli, Y. Benavente, P. Brennan, J. McKay, MH. Delfau-Larue, BK. Link, C. Magnani, MG. Ennas, G. Latte, AL. Feldman, NW. Doo, GG. Giles, MC. Southey, RL. Milne, K. Offit, J. Musinsky, AA. Arslan, MP. Purdue, HO. Adami, M. Melbye, B. Glimelius, L. Conde, NJ. Camp, M. Glenn, K. Curtin, J. Clavel, A. Monnereau, DG. Cox, H. Ghesquières, G. Salles, P. Bofetta, L. Foretova, A. Staines, S. Davis, RK. Severson, Q. Lan, A. Brooks-Wilson, MT. Smith, E. Roman, A. Kricker, Y. Zhang, P. Kraft, SJ. Chanock, N. Rothman, P. Hartge, CF. Skibola,

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$a A growing number of loci within the human leukocyte antigen (HLA) region have been implicated in non-Hodgkin lymphoma (NHL) etiology. Here, we test a complementary hypothesis of "heterozygote advantage" regarding the role of HLA and NHL, whereby HLA diversity is beneficial and homozygous HLA loci are associated with increased disease risk. HLA alleles at class I and II loci were imputed from genome-wide association studies (GWAS) using SNP2HLA for 3,617 diffuse large B-cell lymphomas (DLBCL), 2,686 follicular lymphomas (FL), 2,878 chronic lymphocytic leukemia/small lymphocytic lymphomas (CLL/SLL), 741 marginal zone lymphomas (MZL), and 8,753 controls of European descent. Both DLBCL and MZL risk were elevated with homozygosity at class I HLA-B and -C loci (OR DLBCL = 1.31, 95% CI = 1.06-1.60; OR MZL = 1.45, 95% CI = 1.12-1.89) and class II HLA-DRB1 locus (OR DLBCL = 2.10, 95% CI = 1.24-3.55; OR MZL = 2.10, 95% CI = 0.99-4.45). Increased FL risk was observed with the overall increase in number of homozygous HLA class II loci (P trend < 0.0001, FDR = 0.0005). These results support a role for HLA zygosity in NHL etiology and suggests that distinct immune pathways may underly the etiology of the different NHL subtypes.Significance: HLA gene diversity reduces risk for non-Hodgkin lymphoma. Cancer Res; 78(14); 4086-96. ©2018 AACR.

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700    1_

$a Berndt, Sonja I $u Division of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.

700    1_

$a Slager, Susan L $u Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota.

700    1_

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700    1_

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700    1_

$a Cerhan, James R $u Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota.

700    1_

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700    1_

$a Hjalgrim, Henrik $u Department of Epidemiology Research, Division of Health Surveillance and Research, Statens Serum Institut, Copenhagen, Denmark. Department of Hematology, Rishospitalet, Copenhagen, Denmark.

700    1_

$a Vijai, Joseph $u Department of Medicine, Memorial Sloan Kettering Cancer Center, New York City, New York.

700    1_

$a Morton, Lindsay M $u Division of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.

700    1_

$a Vermeulen, Roel $u Institute for Risk Assessment Sciences, Utrecht University, Utrecht, the Netherlands. Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, the Netherlands.

700    1_

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700    1_

$a Vajdic, Claire M $u Centre for Big Data Research in Health, The University of New South Wales, Sydney, New South Wales, Australia.

700    1_

$a Linet, Martha S $u Division of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.

700    1_

$a Nieters, Alexandra $u Centre for Chronic Immunodeficiency, University Medical Center Freiburg, Freiburg, Baden-Württemberg, Germany.

700    1_

$a de Sanjose, Silvia $u Unit of Infections and Cancer, Cancer Epidemiology Research Programme, Institut Català d' Oncologia, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain. CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.

700    1_

$a Cozen, Wendy $u Norris Comprehensive Cancer Center, Keck School of Medicine of USC, Departments of Preventive Medicine and Pathology, University of Southern California, Los Angeles, Calfornia.

700    1_

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700    1_

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700    1_

$a Spinelli, John J $u Cancer Control Research, British Columbia Cancer Agency, Vancouver, British Columbia, Canada. School of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada.

700    1_

$a Zheng, Tongzhang $u Department of Epidemiology, School of Public Health, Brown University, Providence, Rhode Island.

700    1_

$a Birmann, Brenda M $u Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.

700    1_

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700    1_

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700    1_

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700    1_

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700    1_

$a Weisenburger, Dennis $u Department of Pathology, City of Hope, Duarte, California.

700    1_

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700    1_

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700    1_

$a Albanes, Demetrius $u Division of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.

700    1_

$a Weinstein, Stephanie J $u Division of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.

700    1_

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700    1_

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700    1_

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700    1_

$a Travis, Ruth C $u Cancer Epidemiology Unit, University of Oxford, Oxford, United Kingdom.

700    1_

$a Kaaks, Rudolph $u Division of Clinical Epidemiology, German Cancer Research Centre, Heidelberg, Baden-Württemberg, Germany.

700    1_

$a Riboli, Elio $u School of Public Health, Imperial College London, London, United Kingdom.

700    1_

$a Benavente, Yolanda $u Unit of Infections and Cancer, Cancer Epidemiology Research Programme, Institut Català d' Oncologia, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain. CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.

700    1_

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700    1_

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700    1_

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700    1_

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700    1_

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700    1_

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700    1_

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700    1_

$a Feldman, Andrew L $u Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, Minnesota.

700    1_

$a Doo, Nicole Wong $u Cancer Epidemiology & Intelligence Division, Cancer Council Victoria, Melbourne, Australia.

700    1_

$a Giles, Graham G $u Cancer Epidemiology & Intelligence Division, Cancer Council Victoria, Melbourne, Australia. Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Melbourne, Victoria, Australia.

700    1_

$a Southey, Melissa C $u Genetic Epidemiology Laboratory, Department of Pathology, University of Melbourne, Melbourne, Victoria, Australia.

700    1_

$a Milne, Roger L $u Cancer Epidemiology & Intelligence Division, Cancer Council Victoria, Melbourne, Australia. Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Melbourne, Victoria, Australia.

700    1_

$a Offit, Kenneth $u Department of Hematology, Rishospitalet, Copenhagen, Denmark.

700    1_

$a Musinsky, Jacob $u Department of Hematology, Rishospitalet, Copenhagen, Denmark.

700    1_

$a Arslan, Alan A $u Department of Obstetrics and Gynecology, New York University School of Medicine, New York City, New York. Department of Environmental Medicine, New York University School of Medicine, New York City, New York. Perlmutter Cancer Center, NYU Langone Medical Center, New York City, New York.

700    1_

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700    1_

$a Adami, Hans-Olov $u Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.

700    1_

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700    1_

$a Glimelius, Bengt $u Department of Immunology, Genetics and Pathology, Uppsala University, Uppsala, Sweden.

700    1_

$a Conde, Lucia $u Bill Lyons Informatics Centre, UCL Cancer Institute, University College London, London, United Kingdom.

700    1_

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700    1_

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700    1_

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700    1_

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700    1_

$a Cox, David G $u Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom; Cancer Research Center of Lyon, INSERM UMR1052, Center Léon Bérard, Lyon, France.

700    1_

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700    1_

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700    1_

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700    1_

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700    1_

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700    1_

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700    1_

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700    1_

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700    1_

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700    1_

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700    1_

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700    1_

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700    1_

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$a Chanock, Stephen J $u Division of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.

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700    1_

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$a UM1 CA186107 $p NCI NIH HHS $2 United States

GRA    __

$a U01 CA049449 $p NCI NIH HHS $2 United States

GRA    __

$a K08 CA134919 $p NCI NIH HHS $2 United States

GRA    __

$a P30 ES000260 $p NIEHS NIH HHS $2 United States

GRA    __

$a UM1 CA167552 $p NCI NIH HHS $2 United States

GRA    __

$a R21 CA165923 $p NCI NIH HHS $2 United States

GRA    __

$a R01 CA098122 $p NCI NIH HHS $2 United States

GRA    __

$a N01 PC065064 $p NCI NIH HHS $2 United States

GRA    __

$a P50 CA097274 $p NCI NIH HHS $2 United States

GRA    __

$a P30 CA033572 $p NCI NIH HHS $2 United States

GRA    __

$a HHSN261200800001E $p NCI NIH HHS $2 United States

LZP    __

$a Pubmed-20191007