Uncovering the Contribution of Moderate-Penetrance Susceptibility Genes to Breast Cancer by Whole-Exome Sequencing and Targeted Enrichment Sequencing of Candidate Genes in Women of European Ancestry.

breast cancer genetic susceptibility moderate-penetrance genes whole-exome sequencing

Journal

Cancers
ISSN: 2072-6694
Titre abrégé: Cancers (Basel)
Pays: Switzerland
ID NLM: 101526829

Informations de publication

Date de publication:
11 Jul 2022
Historique:
received: 12 04 2022
revised: 29 06 2022
accepted: 01 07 2022
entrez: 27 7 2022
pubmed: 28 7 2022
medline: 28 7 2022
Statut: epublish

Résumé

Rare variants in at least 10 genes, including BRCA1, BRCA2, PALB2, ATM, and CHEK2, are associated with increased risk of breast cancer; however, these variants, in combination with common variants identified through genome-wide association studies, explain only a fraction of the familial aggregation of the disease. To identify further susceptibility genes, we performed a two-stage whole-exome sequencing study. In the discovery stage, samples from 1528 breast cancer cases enriched for breast cancer susceptibility and 3733 geographically matched unaffected controls were sequenced. Using five different filtering and gene prioritization strategies, 198 genes were selected for further validation. These genes, and a panel of 32 known or suspected breast cancer susceptibility genes, were assessed in a validation set of 6211 cases and 6019 controls for their association with risk of breast cancer overall, and by estrogen receptor (ER) disease subtypes, using gene burden tests applied to loss-of-function and rare missense variants. Twenty genes showed nominal evidence of association (p-value < 0.05) with either overall or subtype-specific breast cancer. Our study had the statistical power to detect susceptibility genes with effect sizes similar to ATM, CHEK2, and PALB2, however, it was underpowered to identify genes in which susceptibility variants are rarer or confer smaller effect sizes. Larger sample sizes would be required in order to identify such genes.

Identifiants

pubmed: 35884425
pii: cancers14143363
doi: 10.3390/cancers14143363
pmc: PMC9317824
pii:
doi:

Types de publication

Journal Article

Langues

eng

Subventions

Organisme : Government of Canada through Genome Canada (#13529) and the Canadian Institutes of Health Research (#155865), the Ministère de l'Économie et de l'Innovation du Québec through Genome Québec, the Quebec Breast Cancer Foundation, the CHU de Quebec Foundation
ID : 13529
Organisme : NIGMS NIH HHS
ID : P41 GM103504
Pays : United States
Organisme : NIGMS NIH HHS
ID : P41 GM103504
Pays : United States
Organisme : Ministère de l'Économie, de la Science et de l'Innovation du Québec
ID : PSR-SIIRI-949
Organisme : NHGRI NIH HHS
ID : R01 HG009979
Pays : United States
Organisme : the Government of Canada through Genome Canada and the Canadian Institutes of Health Re-search (GPH-129344), the Ministère de l'Économie, de la Science et de l'Innovation du Québec through Genome Quebec, and the Quebec Breast Cancer Foundation
ID : GPH-129344

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Auteurs

Martine Dumont (M)

Genomics Center, CHU de Québec-Université Laval Research Center, 2705 Laurier Boulevard, Quebec City, QC GIV 4G2, Canada.

Nana Weber-Lassalle (N)

Center for Familial Breast and Ovarian Cancer, Center for Integrated Oncology (CIO), Faculty of Medicine and University Hospital Cologne, University of Cologne, 50937 Cologne, Germany.

Charles Joly-Beauparlant (C)

Genomics Center, CHU de Québec-Université Laval Research Center, 2705 Laurier Boulevard, Quebec City, QC GIV 4G2, Canada.

Corinna Ernst (C)

Center for Familial Breast and Ovarian Cancer, Center for Integrated Oncology (CIO), Faculty of Medicine and University Hospital Cologne, University of Cologne, 50937 Cologne, Germany.

Arnaud Droit (A)

Genomics Center, CHU de Québec-Université Laval Research Center, 2705 Laurier Boulevard, Quebec City, QC GIV 4G2, Canada.

Bing-Jian Feng (BJ)

Department of Dermatology, University of Utah, Salt Lake City, UT 84103, USA.
Huntsman Cancer Institute, University of Utah, Salt Lake City, UT 84112, USA.

Stéphane Dubois (S)

Genomics Center, CHU de Québec-Université Laval Research Center, 2705 Laurier Boulevard, Quebec City, QC GIV 4G2, Canada.

Annie-Claude Collin-Deschesnes (AC)

Genomics Center, CHU de Québec-Université Laval Research Center, 2705 Laurier Boulevard, Quebec City, QC GIV 4G2, Canada.

Penny Soucy (P)

Genomics Center, CHU de Québec-Université Laval Research Center, 2705 Laurier Boulevard, Quebec City, QC GIV 4G2, Canada.

Maxime Vallée (M)

Genomics Center, CHU de Québec-Université Laval Research Center, 2705 Laurier Boulevard, Quebec City, QC GIV 4G2, Canada.

Frédéric Fournier (F)

Genomics Center, CHU de Québec-Université Laval Research Center, 2705 Laurier Boulevard, Quebec City, QC GIV 4G2, Canada.

Audrey Lemaçon (A)

Genomics Center, CHU de Québec-Université Laval Research Center, 2705 Laurier Boulevard, Quebec City, QC GIV 4G2, Canada.

Muriel A Adank (MA)

Family Cancer Clinic, The Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, 1066 Amsterdam, The Netherlands.

Jamie Allen (J)

Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge CB1 8RN, UK.

Janine Altmüller (J)

Cologne Center for Genomics (CCG), Faculty of Medicine, University Hospital Cologne, University of Cologne, 50931 Cologne, Germany.

Norbert Arnold (N)

Institute of Clinical Molecular Biology, Department of Gynaecology and Obstetrics, University Hospital of Schleswig-Holstein, Campus Kiel, Christian-Albrechts University Kiel, 24105 Kiel, Germany.

Margreet G E M Ausems (MGEM)

Division Laboratories, Pharmacy and Biomedical Genetics, Department of Genetics, University Medical Center Utrecht, 3584 Utrecht, The Netherlands.

Riccardo Berutti (R)

Institute of Human Genetics, Technische Universität München, 81675 Munich, Germany.

Manjeet K Bolla (MK)

Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge CB1 8RN, UK.

Shelley Bull (S)

Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON M5G 1X5, Canada.
Dalla Lana School of Public Health, University of Toronto, Toronto, ON M5T 3M7, Canada.

Sara Carvalho (S)

Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge CB1 8RN, UK.

Sten Cornelissen (S)

Division of Molecular Pathology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, 1066 Amsterdam, The Netherlands.

Michael R Dufault (MR)

Precision Medicine and Computational Biology, Sanofi Genzyme, Cambridge, MA 02142, USA.

Alison M Dunning (AM)

Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge CB1 8RN, UK.

Christoph Engel (C)

Institute for Medical Informatics, Statistics and Epidemiology, University of Leipzig, 04107 Leipzig, Germany.

Andrea Gehrig (A)

Centre of Familial Breast and Ovarian Cancer, Department of Medical Genetics, Institute of Human Genetics, University of Würzburg, 97074 Würzburg, Germany.

Willemina R R Geurts-Giele (WRR)

Department of Clinical Genetics, Erasmus University Medical Center, 3015 Rotterdam, The Netherlands.

Christian Gieger (C)

Institute of Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Neuherberg, Germany.
Research Unit Molecular Epidemiology, Helmholtz Zentrum München, German Research Centre for Environmental Health, 85764 Neuherberg, Germany.

Jessica Green (J)

Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON M5G 1X5, Canada.
Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 1A8, Canada.

Karl Hackmann (K)

Institute for Clinical Genetics, Faculty of Medicine Carl Gustav Carus, Technische Universität Dresden, 01307 Dresden, Germany.

Mohamed Helmy (M)

The Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada.
Bioinformatics Institute (BII), Agency for Science, Technology and Research (A*STAR), Singapore 138632, Singapore.
Department of Computer Science, Lakehead University, Thunder Bay, ON P7B 5E1, Canada.

Julia Hentschel (J)

Institute of Human Genetics, University Leipzig, 04103 Leipzig, Germany.

Frans B L Hogervorst (FBL)

Family Cancer Clinic, The Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, 1066 Amsterdam, The Netherlands.

Antoinette Hollestelle (A)

Department of Medical Oncology, Erasmus MC Cancer Institute, 3015 Rotterdam, The Netherlands.

Maartje J Hooning (MJ)

Department of Medical Oncology, Erasmus MC Cancer Institute, 3015 Rotterdam, The Netherlands.

Judit Horváth (J)

Institute of Human Genetics, University of Münster, 48149 Münster, Germany.

M Arfan Ikram (MA)

Department of Epidemiology, Erasmus MC University Medical Center, 3015 Rotterdam, The Netherlands.

Silke Kaulfuß (S)

Institute of Human Genetics, University Medical Center Göttingen, 37075 Göttingen, Germany.

Renske Keeman (R)

Division of Molecular Pathology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, 1066 Amsterdam, The Netherlands.

Da Kuang (D)

Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 1A8, Canada.
The Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada.

Craig Luccarini (C)

Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge CB1 8RN, UK.

Wolfgang Maier (W)

German Center for Neurodegenerative Diseases (DZNE), Department of Neurodegenerative Diseases and Geriatric Psychiatry, Medical Faculty, University Hospital Bonn, 53127 Bonn, Germany.

John W M Martens (JWM)

Department of Medical Oncology, Erasmus MC Cancer Institute, 3015 Rotterdam, The Netherlands.

Dieter Niederacher (D)

Department of Gynecology and Obstetrics, University Hospital Düsseldorf, Heinrich-Heine University Düsseldorf, 40225 Düsseldorf, Germany.

Peter Nürnberg (P)

Center for Molecular Medicine Cologne (CMMC), Cologne Center for Genomics (CCG), Faculty of Medicine, University Hospital Cologne, University of Cologne, 50931 Cologne, Germany.

Claus-Eric Ott (CE)

Institute of Medical Genetics and Human Genetics, Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin and Berlin Institute of Health, 13353 Berlin, Germany.

Annette Peters (A)

Institute of Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Neuherberg, Germany.
Department of Epidemiology, Institute for Medical Information Processing, Biometry and Epidemiology, Medical Faculty, Ludwig-Maximilians-Universität München, 80539 Munich, Germany.

Paul D P Pharoah (PDP)

Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge CB1 8RN, UK.
Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge CB1 8RN, UK.

Alfredo Ramirez (A)

Division for Neurogenetics and Molecular Psychiatry, Medical Faculty, University of Cologne, 50937 Cologne, Germany.

Juliane Ramser (J)

Division of Gynaecology and Obstetrics, Klinikum Rechts der Isar der Technischen Universität München, 81675 Munich, Germany.

Steffi Riedel-Heller (S)

Institute of Social Medicine, Occupational Health and Public Health, Faculty of Medicine, University of Leipzig, 04103 Leipzig, Germany.

Gunnar Schmidt (G)

Institute of Human Genetics, Hannover Medical School, 30625 Hannover, Germany.

Mitul Shah (M)

Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge CB1 8RN, UK.

Martin Scherer (M)

Department of Primary Medical Care, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.

Antje Stäbler (A)

Institute of Medical Genetics and Applied Genomics, University of Tübingen, 72076 Tübingen, Germany.

Tim M Strom (TM)

Institute of Human Genetics, Technische Universität München, 81675 Munich, Germany.

Christian Sutter (C)

Institute of Human Genetics, University Hospital Heidelberg, 69120 Heidelberg, Germany.

Holger Thiele (H)

Cologne Center for Genomics (CCG), Faculty of Medicine, University Hospital Cologne, University of Cologne, 50931 Cologne, Germany.

Christi J van Asperen (CJ)

Department of Clinical Genetics, Leiden University Medical Center, 2333 Leiden, The Netherlands.

Lizet van der Kolk (L)

Family Cancer Clinic, The Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, 1066 Amsterdam, The Netherlands.

Rob B van der Luijt (RB)

Department of Clinical Genetics, Leiden University Medical Center, 2333 Leiden, The Netherlands.
Department of Medical Genetics, University Medical Center, 3584 Utrecht, The Netherlands.

Alexander E Volk (AE)

Institute of Human Genetics, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.

Michael Wagner (M)

Department of Neurodegenerative Diseases and Geriatric Psychiatry, University Hospital Bonn, 53127 Bonn, Germany.

Quinten Waisfisz (Q)

Department of Human Genetics, Amsterdam UMC, Vrije Universiteit Amsterdam, 1081 Amsterdam, The Netherlands.

Qin Wang (Q)

Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge CB1 8RN, UK.

Shan Wang-Gohrke (S)

Department of Gynaecology and Obstetrics, University of Ulm, 89081 Ulm, Germany.

Bernhard H F Weber (BHF)

Institute of Human Genetics, Regensburg University, 93053 Regensburg, Germany.
Institute of Clinical Human Genetics, University Hospital Regensburg, 93053 Regensburg, Germany.

Peter Devilee (P)

Department of Pathology, Department of Human Genetics, Leiden University Medical Center, 2333 Leiden, The Netherlands.

Sean Tavtigian (S)

Huntsman Cancer Institute, University of Utah, Salt Lake City, UT 84112, USA.
Department of Oncological Sciences, University of Utah School of Medicine, Salt Lake City, UT 84132, USA.

Gary D Bader (GD)

Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON M5G 1X5, Canada.
Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 1A8, Canada.
The Donnelly Centre, University of Toronto, Toronto, ON M5S 3E1, Canada.
Department of Computer Science, University of Toronto, Toronto, ON M5S 3E1, Canada.
Princess Margaret Research Institute, University Health Network, Toronto, ON M5G 0A3, Canada.

Alfons Meindl (A)

Division of Gynaecology and Obstetrics, Klinikum Rechts der Isar der Technischen Universität München, 81675 Munich, Germany.

David E Goldgar (DE)

Department of Dermatology, University of Utah, Salt Lake City, UT 84103, USA.
Huntsman Cancer Institute, University of Utah, Salt Lake City, UT 84112, USA.

Irene L Andrulis (IL)

Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON M5G 1X5, Canada.
Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 1A8, Canada.

Rita K Schmutzler (RK)

Center for Familial Breast and Ovarian Cancer, Center for Integrated Oncology (CIO), Faculty of Medicine and University Hospital Cologne, University of Cologne, 50937 Cologne, Germany.

Douglas F Easton (DF)

Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge CB1 8RN, UK.
Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge CB1 8RN, UK.

Marjanka K Schmidt (MK)

Division of Molecular Pathology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, 1066 Amsterdam, The Netherlands.
Division of Psychosocial Research and Epidemiology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, 1066 Amsterdam, The Netherlands.

Eric Hahnen (E)

Center for Familial Breast and Ovarian Cancer, Center for Integrated Oncology (CIO), Faculty of Medicine and University Hospital Cologne, University of Cologne, 50937 Cologne, Germany.

Jacques Simard (J)

Genomics Center, CHU de Québec-Université Laval Research Center, 2705 Laurier Boulevard, Quebec City, QC GIV 4G2, Canada.
Department of Molecular Medicine, Faculty of Medicine, Université Laval, Quebec, QC G1V 0A6, Canada.

Classifications MeSH