Genetic Analysis of Lung Cancer and the Germline Impact on Somatic Mutation Burden.


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 08 2022
Historique:
accepted: 13 04 2022
received: 13 10 2021
revised: 31 01 2022
pubmed: 6 5 2022
medline: 11 8 2022
entrez: 5 5 2022
Statut: ppublish

Résumé

Germline genetic variation contributes to lung cancer (LC) susceptibility. Previous genome-wide association studies (GWAS) have implicated susceptibility loci involved in smoking behaviors and DNA repair genes, but further work is required to identify susceptibility variants. To identify LC susceptibility loci, a family history-based genome-wide association by proxy (GWAx) of LC (48 843 European proxy LC patients, 195 387 controls) was combined with a previous LC GWAS (29 266 patients, 56 450 controls) by meta-analysis. Colocalization was used to explore candidate genes and overlap with existing traits at discovered susceptibility loci. Polygenic risk scores (PRS) were tested within an independent validation cohort (1 666 LC patients vs 6 664 controls) using variants selected from the LC susceptibility loci and a novel selection approach using published GWAS summary statistics. Finally, the effects of the LC PRS on somatic mutational burden were explored in patients whose tumor resections have been profiled by exome (n = 685) and genome sequencing (n = 61). Statistical tests were 2-sided. The GWAx-GWAS meta-analysis identified 8 novel LC loci. Colocalization implicated DNA repair genes (CHEK1), metabolic genes (CYP1A1), and smoking propensity genes (CHRNA4 and CHRNB2). PRS analysis demonstrated that these variants, as well as subgenome-wide significant variants related to expression quantitative trait loci and/or smoking propensity, assisted in LC genetic risk prediction (odds ratio = 1.37, 95% confidence interval = 1.29 to 1.45; P < .001). Patients with higher genetic PRS loads of smoking-related variants tended to have higher mutation burdens in their lung tumors. This study has expanded the number of LC susceptibility loci and provided insights into the molecular mechanisms by which these susceptibility variants contribute to LC development.

Sections du résumé

BACKGROUND
Germline genetic variation contributes to lung cancer (LC) susceptibility. Previous genome-wide association studies (GWAS) have implicated susceptibility loci involved in smoking behaviors and DNA repair genes, but further work is required to identify susceptibility variants.
METHODS
To identify LC susceptibility loci, a family history-based genome-wide association by proxy (GWAx) of LC (48 843 European proxy LC patients, 195 387 controls) was combined with a previous LC GWAS (29 266 patients, 56 450 controls) by meta-analysis. Colocalization was used to explore candidate genes and overlap with existing traits at discovered susceptibility loci. Polygenic risk scores (PRS) were tested within an independent validation cohort (1 666 LC patients vs 6 664 controls) using variants selected from the LC susceptibility loci and a novel selection approach using published GWAS summary statistics. Finally, the effects of the LC PRS on somatic mutational burden were explored in patients whose tumor resections have been profiled by exome (n = 685) and genome sequencing (n = 61). Statistical tests were 2-sided.
RESULTS
The GWAx-GWAS meta-analysis identified 8 novel LC loci. Colocalization implicated DNA repair genes (CHEK1), metabolic genes (CYP1A1), and smoking propensity genes (CHRNA4 and CHRNB2). PRS analysis demonstrated that these variants, as well as subgenome-wide significant variants related to expression quantitative trait loci and/or smoking propensity, assisted in LC genetic risk prediction (odds ratio = 1.37, 95% confidence interval = 1.29 to 1.45; P < .001). Patients with higher genetic PRS loads of smoking-related variants tended to have higher mutation burdens in their lung tumors.
CONCLUSIONS
This study has expanded the number of LC susceptibility loci and provided insights into the molecular mechanisms by which these susceptibility variants contribute to LC development.

Identifiants

pubmed: 35511172
pii: 6576636
doi: 10.1093/jnci/djac087
pmc: PMC9360465
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1159-1166

Subventions

Organisme : NCI NIH HHS
ID : U19 CA203654
Pays : United States
Organisme : NCI NIH HHS
ID : R03 CA256222
Pays : United States
Organisme : NCI NIH HHS
ID : K99 CA246076
Pays : United States
Organisme : Medical Research Council
ID : MR/T043202/1
Pays : United Kingdom
Organisme : Cancer Research UK
ID : C18281/A29019
Pays : United Kingdom

Informations de copyright

© The Author(s) 2022. Published by Oxford University Press.

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Auteurs

Aurélie A G Gabriel (AAG)

Genomic Epidemiology Branch, International Agency for Research on Cancer/World Health Organization (IARC/WHO), Lyon, France.

Joshua R Atkins (JR)

Genomic Epidemiology Branch, International Agency for Research on Cancer/World Health Organization (IARC/WHO), Lyon, France.

Ricardo C C Penha (RCC)

Genomic Epidemiology Branch, International Agency for Research on Cancer/World Health Organization (IARC/WHO), Lyon, France.

Karl Smith-Byrne (K)

Genomic Epidemiology Branch, International Agency for Research on Cancer/World Health Organization (IARC/WHO), Lyon, France.
Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, England.

Valerie Gaborieau (V)

Genomic Epidemiology Branch, International Agency for Research on Cancer/World Health Organization (IARC/WHO), Lyon, France.

Catherine Voegele (C)

Genomic Epidemiology Branch, International Agency for Research on Cancer/World Health Organization (IARC/WHO), Lyon, France.

Behnoush Abedi-Ardekani (B)

Genomic Epidemiology Branch, International Agency for Research on Cancer/World Health Organization (IARC/WHO), Lyon, France.

Maja Milojevic (M)

Genomic Epidemiology Branch, International Agency for Research on Cancer/World Health Organization (IARC/WHO), Lyon, France.

Robert Olaso (R)

Université Paris-Saclay, The French Alternative Energies and Atomic Energy Commission (CEA), Centre National de Recherche en Génomique Humaine (CNRGH), Evry, France.

Vincent Meyer (V)

Université Paris-Saclay, The French Alternative Energies and Atomic Energy Commission (CEA), Centre National de Recherche en Génomique Humaine (CNRGH), Evry, France.

Anne Boland (A)

Université Paris-Saclay, The French Alternative Energies and Atomic Energy Commission (CEA), Centre National de Recherche en Génomique Humaine (CNRGH), Evry, France.

Jean François Deleuze (JF)

Université Paris-Saclay, The French Alternative Energies and Atomic Energy Commission (CEA), Centre National de Recherche en Génomique Humaine (CNRGH), Evry, France.

David Zaridze (D)

Russian N.N. Blokhin Cancer Research Centre, Moscow, Russian Federation.

Anush Mukeriya (A)

Russian N.N. Blokhin Cancer Research Centre, Moscow, Russian Federation.

Beata Swiatkowska (B)

Department of Environmental Epidemiology, Nofer Institute of Occupational Medicine, Lodz, Poland.

Vladimir Janout (V)

Faculty of Medicine, Palacky University, Olomouc, Czech Republic.

Miriam Schejbalová (M)

First Faculty of Medicine, Charles University, Prague, Czech Republic.

Dana Mates (D)

National Institute of Public Health, Bucharest, Romania.

Jelena Stojšić (J)

Department of Thoracic Pathology, Service of Pathology, University Clinical Centre of Serbia, Belgrade, Serbia.

Miodrag Ognjanovic (M)

International Organisation for Cancer Prevention and Research, Belgrade, Serbia.

John S Witte (JS)

Department of Epidemiology & Biostatistics, University of California San Francisco, San Francisco, CA, USA.

Sara R Rashkin (SR)

Department of Epidemiology & Biostatistics, University of California San Francisco, San Francisco, CA, USA.
Department of Hematology, St. Jude Children's Research Hospital, Memphis, TN, USA.

Linda Kachuri (L)

Department of Epidemiology & Biostatistics, University of California San Francisco, San Francisco, CA, USA.

Rayjean J Hung (RJ)

Lunenfeld-Tanenbaum Research Institute, Sinai Health, Toronto, Canada.

Siddhartha Kar (S)

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

Paul Brennan (P)

Genomic Epidemiology Branch, International Agency for Research on Cancer/World Health Organization (IARC/WHO), Lyon, France.

Anne-Sophie Sertier (AS)

Fondation Synergie Lyon Cancer, Plateforme de bioinformatique Gilles Thomas, Lyon, France.

Anthony Ferrari (A)

Fondation Synergie Lyon Cancer, Plateforme de bioinformatique Gilles Thomas, Lyon, France.

Alain Viari (A)

Fondation Synergie Lyon Cancer, Plateforme de bioinformatique Gilles Thomas, Lyon, France.
Inria Centre de Recherche Grenoble Rhone-Alpes, Grenoble, France.

Mattias Johansson (M)

Genomic Epidemiology Branch, International Agency for Research on Cancer/World Health Organization (IARC/WHO), Lyon, France.

Christopher I Amos (CI)

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

Matthieu Foll (M)

Genomic Epidemiology Branch, International Agency for Research on Cancer/World Health Organization (IARC/WHO), Lyon, France.

James D McKay (JD)

Genomic Epidemiology Branch, International Agency for Research on Cancer/World Health Organization (IARC/WHO), Lyon, France.

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