ArticleCancer research2018
HLA Class I and II Diversity Contributes to the Etiologic Heterogeneity of Non-Hodgkin Lymphoma Subtypes.
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Article in Cancer research, 2018. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 25 papers.
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Who cites it
25 citing papers in PubMed, 41 citations in OpenAlex.
- Polygenic Risk, Agent Orange Exposure, and Lymphoid Neoplasms in the Veterans Affairs Million Veteran Program.JAMA network open · 2025Article
- HLA Genetic Diversity and Chronic Hepatitis B Virus Infection: Effect of Heterozygosity Advantage.Medical sciences (Basel, Switzerland) · 2024Article
- Impact of HLA class I functional divergence on HIV control.Science (New York, N.Y.) · 2024Article
- Homozygosity in any HLA locus is a risk factor for specific antibody production: the taboo concept 2.0.Frontiers in immunology · 2024Article
- Gene targeted and immune therapies for nodal and gastrointestinal follicular lymphomas.World journal of gastroenterology · 2023Review
- Epidemiology and etiology of diffuse large B-cell lymphoma.Seminars in hematology · 2023Article
- Heterozygote advantage at HLA class I and II loci and reduced risk of colorectal cancer.Frontiers in immunology · 2023Article
- Article
- Etiology of non-Hodgkin lymphoma: A review from epidemiologic studies.Journal of the National Cancer Center · 2022Review
- Phenome of coeliac disease vs. inflammatory bowel disease.Scientific reports · 2022Article
- HLA Homozygosity and Likelihood of Sensitization in Kidney Transplant Candidates.Transplantation direct · 2022Article
- HLA Zygosity Increases Risk of Hepatitis B Virus-Associated Hepatocellular Carcinoma.The Journal of infectious diseases · 2021Article
- Germline HLA-B evolutionary divergence influences the efficacy of immune checkpoint blockade therapy in gastrointestinal cancer.Genome medicine · 2021Article
- Genetic mechanisms of HLA-I loss and immune escape in diffuse large B cell lymphoma.Proceedings of the National Academy of Sciences of the United States of America · 2021Article
- Epidemiology of Marginal Zone Lymphoma.Annals of lymphoma · 2021Article
- Patterns of Human Leukocyte Antigen Class I and Class II Associations and Cancer.Cancer research · 2021Article
- Article
- Establishment of tumor inflammasome clusters with distinct immunogenomic landscape aids immunotherapy.Theranostics · 2021Article
- Association Between Human Leukocyte Antigen Class I and II Diversity and Non-virus-associated Solid Tumors.Frontiers in genetics · 2021Article
- Genome-wide homozygosity and risk of four non-Hodgkin lymphoma subtypes.Journal of translational genetics and genomics · 2021Article
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Authors and funding
83 authors at 20 institutions in 14 countries.
Sophia S WangDepartment of Population Sciences, Beckman Research Institute and the City of Hope, Duarte, California. sowang@coh.org.
Mary CarringtonCancer 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.
Sonja I BerndtDivision of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.
Susan L SlagerDepartment of Health Sciences Research, Mayo Clinic, Rochester, Minnesota.
Paige M BracciDepartment of Epidemiology and Biostatistics, University of California-San Francisco, San Francisco, California.
Jenna VoutsinasDepartment of Population Sciences, Beckman Research Institute and the City of Hope, Duarte, California.
James R CerhanDepartment of Health Sciences Research, Mayo Clinic, Rochester, Minnesota.
Karin E SmedbyDepartment of Medicine Solna, unit of clinical epidemiology, Karolinska Institutet, Stockholm, Sweden.
Henrik HjalgrimDepartment of Epidemiology Research, Division of Health Surveillance and Research, Statens Serum Institut, Copenhagen, Denmark.
Joseph VijaiDepartment of Medicine, Memorial Sloan Kettering Cancer Center, New York City, New York.
Lindsay M MortonDivision of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.
Roel VermeulenInstitute for Risk Assessment Sciences, Utrecht University, Utrecht, the Netherlands.
Ora PaltielBraun School of Public Health and Community Medicine, Hadassah-Hebrew University Medical Center, Jerusalem, Israel.
Claire M VajdicCentre for Big Data Research in Health, The University of New South Wales, Sydney, New South Wales, Australia.
Martha S LinetDivision of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.
Alexandra NietersCentre for Chronic Immunodeficiency, University Medical Center Freiburg, Freiburg, Baden-Württemberg, Germany.
Silvia de SanjoseUnit of Infections and Cancer, Cancer Epidemiology Research Programme, Institut Català d' Oncologia, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain.
Wendy CozenNorris Comprehensive Cancer Center, Keck School of Medicine of USC, Departments of Preventive Medicine and Pathology, University of Southern California, Los Angeles, Calfornia.
Elizabeth E BrownDepartment of Pathology, School of Medicine and the UAB Comprehensive Cancer Center, The University of Alabama at Birmingham, Birmingham, Alabama.
Jennifer TurnerDepartment of Histopathology, Douglass Hanly Moir Pathology, Sydney, Australia.ORCID 0000-0001-5550-3375
John J SpinelliCancer Control Research, British Columbia Cancer Agency, Vancouver, British Columbia, Canada.
Tongzhang ZhengDepartment of Epidemiology, School of Public Health, Brown University, Providence, Rhode Island.
Brenda M BirmannChanning Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.
Christopher R FlowersDepartment of Hematology and Medical Oncology, Emory University School of Medicine, Atlanta, Georgia.
Nikolaus BeckerDivision of Clinical Epidemiology, German Cancer Research Centre, Heidelberg, Baden-Württemberg, Germany.
Elizabeth A HollyDepartment of Epidemiology and Biostatistics, University of California-San Francisco, San Francisco, California.
Eleanor KaneDepartment of Health Sciences, University of York, York, United Kingdom.
Dennis WeisenburgerDepartment of Pathology, City of Hope, Duarte, California.
Marc MaynadieRegistry of Hematological Malignancies of Cote d'Or, INSERM UMR1231, University of Burgundy and Dijon University Hospital, Dijon, France.
Pierluigi CoccoDepartment of Public Health, Clinical and Molecular Medicine, University of Cagliari, Cagliari, Italy.
Demetrius AlbanesDivision of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.
Stephanie J WeinsteinDivision of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.ORCID 0000-0002-3834-1535
Lauren R TerasEpidemiology Research Program, American Cancer Society, Atlanta, Georgia.
W Ryan DiverEpidemiology Research Program, American Cancer Society, Atlanta, Georgia.
Stephanie J LaxDepartment of Health Sciences, University of York, York, United Kingdom.
Ruth C TravisCancer Epidemiology Unit, University of Oxford, Oxford, United Kingdom.
Rudolph KaaksDivision of Clinical Epidemiology, German Cancer Research Centre, Heidelberg, Baden-Württemberg, Germany.
Elio RiboliSchool of Public Health, Imperial College London, London, United Kingdom.
Yolanda BenaventeUnit of Infections and Cancer, Cancer Epidemiology Research Programme, Institut Català d' Oncologia, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain.
Paul BrennanInternational Agency for Research on Cancer, Lyon, France.
James McKayDepartment of Immunology, CHU Henri Mondor, Créteil, France.
Marie-Hélène Delfau-LarueDepartment of Immunology, CHU Henri Mondor, Créteil, France.
Brian K LinkDepartment of Internal Medicine, Carver College of Medicine, The University of Iowa, Iowa City, Iowa.
Corrado MagnaniCenter of Oncological Prevention (CPO) Piemonte and Unit of Medical Statistics and Epidemiology, Department Translational Medicine, University of Piemonte Orientale, Novara, Italy.
Maria Grazia EnnasDepartment of Biomedical Science, University of Cagliari, Monserrato, Cagliari, Italy.
Giancarlo LatteDivision of Hematology, S. Francesco Hospital, Nuoro, Italy.
Andrew L FeldmanDepartment of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, Minnesota.
Nicole Wong DooCancer Epidemiology & Intelligence Division, Cancer Council Victoria, Melbourne, Australia.
Graham G GilesCancer Epidemiology & Intelligence Division, Cancer Council Victoria, Melbourne, Australia.
Melissa C SoutheyGenetic Epidemiology Laboratory, Department of Pathology, University of Melbourne, Melbourne, Victoria, Australia.
Roger L MilneCancer Epidemiology & Intelligence Division, Cancer Council Victoria, Melbourne, Australia.
Kenneth OffitDepartment of Hematology, Rishospitalet, Copenhagen, Denmark.
Jacob MusinskyDepartment of Hematology, Rishospitalet, Copenhagen, Denmark.
Alan A ArslanDepartment of Obstetrics and Gynecology, New York University School of Medicine, New York City, New York.
Mark P PurdueDivision of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.
Hans-Olov AdamiDepartment of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
Mads MelbyeDepartment of Epidemiology Research, Division of Health Surveillance and Research, Statens Serum Institut, Copenhagen, Denmark.
Bengt GlimeliusDepartment of Immunology, Genetics and Pathology, Uppsala University, Uppsala, Sweden.
Lucia CondeBill Lyons Informatics Centre, UCL Cancer Institute, University College London, London, United Kingdom.
Nicola J CampDepartment of Internal Medicine, Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, Utah.
Martha GlennDepartment of Internal Medicine, Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, Utah.
Karen CurtinDepartment of Internal Medicine, Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, Utah.
Jacqueline ClavelEpidemiology of Childhood and Adolescent Cancers Group, Inserm, Center of Research in Epidemiology and Statistics Sorbonne Paris Cité (CRESS), Paris, France.
Alain MonnereauUniversité Paris Descartes, Paris, France.
David G CoxDepartment 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.
Hervé GhesquièresUniversité Paris Descartes, Paris, France.
Gilles SallesLaboratoire de Biologie Moléculaire de la Cellule UMR 5239, Centre National de la Recherche Scientifique, Pierre benite Cedex, France.
Paulo BofettaThe Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York City, New York.
Lenka ForetovaDepartment of Cancer Epidemiology and Genetics, Masaryk Memorial Cancer Institute, MF MU, Brno, Czech Republic.
Anthony StainesSchool of Nursing and Human Sciences, Dublin City University, Dublin, Ireland.
Scott DavisFred Hutchinson Cancer Research Center and School of Public Health and Community Medicine, University of Washington, Seattle, Washington.
Richard K SeversonDepartment of Family Medicine and Public Health Sciences, Wayne State University, Detroit, Michigan.
Qing LanDivision of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.
Angela Brooks-WilsonDepartment of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, British Columbia, Canada.
Martyn T SmithDivision of Environmental Health Sciences, School of Public Health, University of California, Berkeley, Berkeley, California.
Eve RomanDepartment of Health Sciences, University of York, York, United Kingdom.
Anne KrickerSydney School of Public Health, The University of Sydney, Sydney, Australia.
Yawei ZhangDepartment of Surgery, Yale School of Medicine, New Haven, Connecticut.
Peter KraftDepartment of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
Stephen J ChanockDivision of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.
Nathaniel RothmanDivision of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.
Patricia HartgeDivision of Cancer Epidemiology and Genetics, NCI, Bethesda, Maryland.
Christine F SkibolaDepartment of Hematology and Medical Oncology, Emory University School of Medicine, Atlanta, Georgia.
Cancer Genetics (United States) · USHuntsman Cancer Institute · USInserm · FRThe University of Melbourne · AUUniversity of York · GBAmerican Cancer Society · USBC Cancer Agency · CACity of Hope · USDélégation Paris 5 · FREmory University · USGerman Cancer Research Center · DEInstitut Català d'Oncologia · ESMayo Clinic in Florida · USRigshospitalet · DKStatens Serum Institut · DKUniversité Claude Bernard Lyon 1 · FRUniversity of Cagliari · ITUniversity of California, San Francisco · USAssociazione Istituzione Libera Università Nuorese · ITBerkeley Public Health Division · US
Funding
X-RAY CRYSTALLOGRAPHYP30CA008748 · NCI · SLOAN-KETTERING INSTITUTE FOR CANCER RES · PI Hongbiao Carl Lekaye · 1985 to 2026
$347.4MWomen's Cancer ProgramP30CA015083 · NCI · MAYO CLINIC ROCHESTER · PI AKHILESH PANDEY · 1985 to 2026
$151.3MTransgenic Mouse FacilityP30CA033572 · NCI · CITY OF HOPE/BECKMAN RESEARCH INSTITUTE · PI XIWEI WU · 1985 to 2026
$86.3MVaccine FacilityP30CA016087 · NCI · NEW YORK UNIVERSITY SCHOOL OF MEDICINE · PI ANIRBAN MAITRA · 1985 to 2026
$83.1MStatistical MethodsP01CA087969 · NCI · BRIGHAM AND WOMEN'S HOSPITAL · PI ROSNER, BERNARD A · 2000 to 2019
$77.8MUTAH REGIONAL CANCER CENTERP30CA042014 · NCI · UTAH STATE HIGHER EDUCATION SYSTEM--UNIVERSITY OF UTAH · PI KATHARINE S ULLMAN · 1986 to 2026
$72.6MViral VectorP30CA086862 · NCI · UNIVERSITY OF IOWA · PI Christopher K Laubenthal · 2000 to 2026
$70.0MThe Role of Monocytes in non-Hodgkin LymphomaP50CA097274 · NCI · UNIVERSITY OF IOWA · PI LENTZ, STEVEN R · 2002 to 2021
$45.7MMayo Clinic Center for Translational Science ActivitiesUL1TR000135 · NCATS · MAYO CLINIC ROCHESTER · PI KHOSLA, SUNDEEP · 2012 to 2015
$41.2MRESEARCH IN ENVIRONMENTAL HEALTH SCIENCES (CENTER GRANT)P30ES000260 · NIEHS · NEW YORK UNIVERSITY SCHOOL OF MEDICINE · PI ZELIKOFF, JUDITH TERRY · 1985 to 2020
$26.1MCALIFORNIA'S PARTICIPATION IN THE NATIONAL CANCER PREVENTION AND CONTRO PROGRAMU58DP000807 · DP · PUBLIC HEALTH INSTITUTE · PI SNIPES, KURT P · 2007 to 2011
$22.5MLong Term Multidisciplinary Study of Cancer in Women: The Nurses Health StudyUM1CA186107 · NCI · BRIGHAM AND WOMEN'S HOSPITAL · PI ELIASSEN, A. HEATHER, STAMPFER, MEIR · 2014 to 2023
$22.3MCancer Research UKNCCDPHP CDC HHS U58 DP000807NCI NIH HHS K08 CA134919NCI NIH HHS N01 CO012400NCI NIH HHS N01 PC065064NCI NIH HHS N01 PC067008NCI NIH HHS N01 PC067009NCI NIH HHS N01 PC067010NCI NIH HHS P01 CA087969NCI NIH HHS P30 CA008748NCI NIH HHS P30 CA015083NCI NIH HHS P30 CA016087NCI NIH HHS P30 CA033572NCI NIH HHS P30 CA042014NCI NIH HHS P30 CA086862NCI NIH HHS P50 CA097274NCI NIH HHS R01 CA049449NCI NIH HHS R01 CA062006NCI NIH HHS R01 CA092153NCI NIH HHS R01 CA098122NCI NIH HHS R01 CA098661NCI NIH HHS R01 CA134674NCI NIH HHS R01 CA148690NCI NIH HHS R01 CA149445NCI NIH HHS R01 CA154643NCI NIH HHS R01 CA200703NCI NIH HHS R03 CA179558NCI NIH HHS R21 CA165923NCI NIH HHS U01 CA049449NCI NIH HHS U01 CA118444NCI NIH HHS U01 CA167552NCI NIH HHS UM1 CA167552NCI NIH HHS UM1 CA186107NHGRI NIH HHS U01 HG007033NIEHS NIH HHS P30 ES000260World Health Organization 001
Abstract
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 (
Indexed as
Case-Control StudiesFemaleGenetic HeterogeneityGenome-Wide Association StudyHeterozygoteHistocompatibility Antigens Class IHistocompatibility Antigens Class IIHumansLymphoma, Non-HodgkinMaleProspective StudiesHistocompatibility Antigens Class IHistocompatibility Antigens Class II
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