Genome-wide analyses characterize shared heritability among cancers and identify novel cancer susceptibility regions.


Journal

Journal of the National Cancer Institute
ISSN: 1460-2105
Titre abrégé: J Natl Cancer Inst
Pays: United States
ID NLM: 7503089

Informations de publication

Date de publication:
08 06 2023
Historique:
received: 15 06 2022
revised: 07 11 2022
accepted: 14 02 2023
medline: 9 6 2023
pubmed: 18 3 2023
entrez: 17 3 2023
Statut: ppublish

Résumé

The shared inherited genetic contribution to risk of different cancers is not fully known. In this study, we leverage results from 12 cancer genome-wide association studies (GWAS) to quantify pairwise genome-wide genetic correlations across cancers and identify novel cancer susceptibility loci. We collected GWAS summary statistics for 12 solid cancers based on 376 759 participants with cancer and 532 864 participants without cancer of European ancestry. The included cancer types were breast, colorectal, endometrial, esophageal, glioma, head and neck, lung, melanoma, ovarian, pancreatic, prostate, and renal cancers. We conducted cross-cancer GWAS and transcriptome-wide association studies to discover novel cancer susceptibility loci. Finally, we assessed the extent of variant-specific pleiotropy among cancers at known and newly identified cancer susceptibility loci. We observed widespread but modest genome-wide genetic correlations across cancers. In cross-cancer GWAS and transcriptome-wide association studies, we identified 15 novel cancer susceptibility loci. Additionally, we identified multiple variants at 77 distinct loci with strong evidence of being associated with at least 2 cancer types by testing for pleiotropy at known cancer susceptibility loci. Overall, these results suggest that some genetic risk variants are shared among cancers, though much of cancer heritability is cancer-specific and thus tissue-specific. The increase in statistical power associated with larger sample sizes in cross-disease analysis allows for the identification of novel susceptibility regions. Future studies incorporating data on multiple cancer types are likely to identify additional regions associated with the risk of multiple cancer types.

Sections du résumé

BACKGROUND
The shared inherited genetic contribution to risk of different cancers is not fully known. In this study, we leverage results from 12 cancer genome-wide association studies (GWAS) to quantify pairwise genome-wide genetic correlations across cancers and identify novel cancer susceptibility loci.
METHODS
We collected GWAS summary statistics for 12 solid cancers based on 376 759 participants with cancer and 532 864 participants without cancer of European ancestry. The included cancer types were breast, colorectal, endometrial, esophageal, glioma, head and neck, lung, melanoma, ovarian, pancreatic, prostate, and renal cancers. We conducted cross-cancer GWAS and transcriptome-wide association studies to discover novel cancer susceptibility loci. Finally, we assessed the extent of variant-specific pleiotropy among cancers at known and newly identified cancer susceptibility loci.
RESULTS
We observed widespread but modest genome-wide genetic correlations across cancers. In cross-cancer GWAS and transcriptome-wide association studies, we identified 15 novel cancer susceptibility loci. Additionally, we identified multiple variants at 77 distinct loci with strong evidence of being associated with at least 2 cancer types by testing for pleiotropy at known cancer susceptibility loci.
CONCLUSIONS
Overall, these results suggest that some genetic risk variants are shared among cancers, though much of cancer heritability is cancer-specific and thus tissue-specific. The increase in statistical power associated with larger sample sizes in cross-disease analysis allows for the identification of novel susceptibility regions. Future studies incorporating data on multiple cancer types are likely to identify additional regions associated with the risk of multiple cancer types.

Identifiants

pubmed: 36929942
pii: 7079819
doi: 10.1093/jnci/djad043
pmc: PMC10248849
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

712-732

Subventions

Organisme : NCI NIH HHS
ID : U01 CA182883
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA015704
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH101782
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA164930
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA206110
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA015083
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH090951
Pays : United States
Organisme : NIEHS NIH HHS
ID : T32 ES013678
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH101820
Pays : United States
Organisme : NIDA NIH HHS
ID : R01 DA006227
Pays : United States
Organisme : Cancer Research UK
ID : 25514
Pays : United Kingdom
Organisme : NIH HHS
ID : U01 CA167551
Pays : United States
Organisme : NIH HHS
ID : T32 ES013678
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH101810
Pays : United States
Organisme : NIH HHS
ID : S10 OD028685
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH101819
Pays : United States
Organisme : Cancer Research UK
ID : 29017
Pays : United Kingdom
Organisme : NIH HHS
ID : U01 CA122839
Pays : United States
Organisme : NIH HHS
ID : U19 CA148065
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH090936
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA261339
Pays : United States
Organisme : NHLBI NIH HHS
ID : HHSN268201200008C
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA242218
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA167551
Pays : United States
Organisme : Cancer Research UK
ID : C1287/A10118
Pays : United Kingdom
Organisme : NIMH NIH HHS
ID : R01 MH101825
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH090948
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH090941
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA194393
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH101822
Pays : United States
Organisme : CCR NIH HHS
ID : HHSN261200800001C
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH090937
Pays : United States
Organisme : NHLBI NIH HHS
ID : HHSN268201200008I
Pays : United States
Organisme : Cancer Research UK
ID : 4584
Pays : United Kingdom
Organisme : NIA NIH HHS
ID : U01 AG18033
Pays : United States
Organisme : NHLBI NIH HHS
ID : HHSN268201000029C
Pays : United States
Organisme : NCI NIH HHS
ID : HHSN261200800001E
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH101814
Pays : United States
Organisme : NIH HHS
ID : R01 CA189184
Pays : United States
Organisme : NCI NIH HHS
ID : U19 CA148107
Pays : United States
Organisme : NIA NIH HHS
ID : U01 AG018033
Pays : United States

Informations de copyright

© The Author(s) 2023. Published by Oxford University Press. All rights reserved. For permissions, please email: journals.permissions@oup.com.

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Auteurs

Sara Lindström (S)

Department of Epidemiology, University of Washington, Seattle, WA, USA.
Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.

Lu Wang (L)

Department of Environmental and Occupational Health Sciences, University of Washington, Seattle, WA, USA.

Helian Feng (H)

Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA, USA.

Arunabha Majumdar (A)

Department of Pathology and Laboratory Medicine, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA.
Department of Mathematics, Indian Institute of Technology Hyderabad, Kandi, Telangana, India.

Sijia Huo (S)

Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA, USA.

James Macdonald (J)

Department of Environmental and Occupational Health Sciences, University of Washington, Seattle, WA, USA.

Tabitha Harrison (T)

Department of Epidemiology, University of Washington, Seattle, WA, USA.

Constance Turman (C)

Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA.

Hongjie Chen (H)

Department of Epidemiology, University of Washington, Seattle, WA, USA.

Nicholas Mancuso (N)

Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.

Theo Bammler (T)

Department of Environmental and Occupational Health Sciences, University of Washington, Seattle, WA, USA.

Steve Gallinger (S)

Lunenfeld Tanenbaum Research Institute, Mount Sinai Hospital, University of Toronto, Toronto, Ontario, Canada.

Stephen B Gruber (SB)

Department of Medical Oncology & Therapeutics Research, City of Hope National Medical Center, Duarte, CA, USA.

Marc J Gunter (MJ)

International Agency for Research on Cancer, World Health Organization, Lyon, France.

Loic Le Marchand (L)

University of Hawaii Cancer Center, Honolulu, HI, USA.

Victor Moreno (V)

Oncology Data Analytics Program, Catalan Institute of Oncology-IDIBELL, L'Hospitalet de Llobregat, Barcelona, Spain.
CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.
Department of Clinical Sciences, Faculty of Medicine, University of Barcelona, Barcelona, Spain.
ONCOBEL Program, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain.

Kenneth Offit (K)

Clinical Genetics Service, Department of Medicine, Memorial Sloan-Kettering Cancer Center, New York, NY, USA.
Department of Medicine, Weill Cornell Medical College, New York, NY, USA.

Immaculata De Vivo (I)

Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Harvard Radcliffe Institute, Cambridge, MA, USA.

Tracy A O'Mara (TA)

Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.

Amanda B Spurdle (AB)

Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.

Ian Tomlinson (I)

Cancer Research Centre, The University of Edinburgh, Edinburgh, UK.

Rebecca Fitzgerald (R)

MRC Cancer Unit, Hutchison-MRC Research Centre, University of Cambridge, Cambridge, UK.

Puya Gharahkhani (P)

Statistical Genetics, QIMR Berghofer Medical Research Institute, Brisbane, Australia.

Ines Gockel (I)

Department of Visceral, Transplant, Thoracic and Vascular Surgery, University Hospital of Leipzig, Leipzig, Germany.

Janusz Jankowski (J)

Institute for Clinical Trials, University College London, Holborn, UK.
University of the South Pacific, Suva, Fiji.

Stuart Macgregor (S)

Statistical Genetics, QIMR Berghofer Medical Research Institute, Brisbane, Australia.

Johannes Schumacher (J)

Center for Human Genetics, University Hospital of Marburg, Marburg, Germany.

Jill Barnholtz-Sloan (J)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
Trans-Divisional Research Program, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Melissa L Bondy (ML)

Department of Epidemiology and Population Health, Stanford University, Palo Alto, CA, USA.

Richard S Houlston (RS)

Division of Genetics and Epidemiology, The Institute of Cancer Research, London, UK.

Robert B Jenkins (RB)

Department of Laboratory Medicine and Pathology, Mayo Clinic Comprehensive Cancer Center, Mayo Clinic, Rochester, MN, USA.

Beatrice Melin (B)

Department of Radiation Sciences, Umeå University, Umeå, Sweden.

Margaret Wrensch (M)

Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA, USA.

Paul Brennan (P)

International Agency for Research on Cancer, World Health Organization, Lyon, France.

David C Christiani (DC)

Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
Department of Environmental Health, Harvard T.H. Chan School of Public Health, Boston, MA, USA.

Mattias Johansson (M)

International Agency for Research on Cancer, World Health Organization, Lyon, France.

James Mckay (J)

International Agency for Research on Cancer, World Health Organization, Lyon, France.

Melinda C Aldrich (MC)

Department of Thoracic Surgery, Division of Epidemiology, Vanderbilt University Medical Center, Nashville, TN, USA.

Christopher I Amos (CI)

Institute for Clinical and Translational Research, Baylor College of Medicine, Houston, TX, USA.

Maria Teresa Landi (MT)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Adonina Tardon (A)

University Institute of Oncology of the Principality of Asturias (IUOPA), University of Oviedo and Spanish Consortium for Research on Epidemiology and Public Health (CIBERESP), Oviedo, Spain.

D Timothy Bishop (DT)

Leeds Institute for Data Analytics, University of Leeds, Leeds, UK.

Florence Demenais (F)

Université Paris Cité, Institut National de la Santé et de la Recherche Médicale (INSERM), UMR-1124, Paris, France.

Alisa M Goldstein (AM)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Mark M Iles (MM)

Leeds Institute for Data Analytics, University of Leeds, Leeds, UK.

Peter A Kanetsky (PA)

Department of Cancer Epidemiology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA.

Matthew H Law (MH)

Statistical Genetics, QIMR Berghofer Medical Research Institute, Brisbane, Australia.
School of Biomedical Sciences, Faculty of Health, and Institute of Health and Biomedical Innovation, Queensland University of Technology, Kelvin Grove, Queensland, Australia.

Laufey T Amundadottir (LT)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Rachael Stolzenberg-Solomon (R)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Brian M Wolpin (BM)

Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA, USA.

Alison Klein (A)

Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins School of Medicine, Baltimore, MD, USA.
Department of Pathology, Sol Goldman Pancreatic Cancer Research Center, Johns Hopkins School of Medicine, Baltimore, MD, USA.

Gloria Petersen (G)

Department of Quantitative Health Science, Mayo Clinic, Rochester, MN, USA.

Harvey Risch (H)

Yale School of Public Health, Chronic Disease Epidemiology, New Haven, CT, USA.

Stephen J Chanock (SJ)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Mark P Purdue (MP)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Ghislaine Scelo (G)

International Agency for Research on Cancer, World Health Organization, Lyon, France.

Paul Pharoah (P)

Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.

Siddhartha Kar (S)

Medical Research Council Integrative Epidemiology Unit, Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, UK.

Rayjean J Hung (RJ)

Prosserman Centre for Population Health Research, Lunenfeld-Tanenbuaum Research Institute, Sinai Health System, Toronto, ON, Canada.

Bogdan Pasaniuc (B)

Department of Pathology and Laboratory Medicine, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA.
Department of Human Genetics, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA.
Department of Computational Medicine, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA.

Peter Kraft (P)

Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA.

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