Common Susceptibility Loci for Male Breast Cancer.


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:
06 04 2021
Historique:
received: 12 11 2019
revised: 14 05 2020
accepted: 10 07 2020
pubmed: 14 8 2020
medline: 16 9 2021
entrez: 14 8 2020
Statut: ppublish

Résumé

The etiology of male breast cancer (MBC) is poorly understood. In particular, the extent to which the genetic basis of MBC differs from female breast cancer (FBC) is unknown. A previous genome-wide association study of MBC identified 2 predisposition loci for the disease, both of which were also associated with risk of FBC. We performed genome-wide single nucleotide polymorphism genotyping of European ancestry MBC case subjects and controls in 3 stages. Associations between directly genotyped and imputed single nucleotide polymorphisms with MBC were assessed using fixed-effects meta-analysis of 1380 cases and 3620 controls. Replication genotyping of 810 cases and 1026 controls was used to validate variants with P values less than 1 × 10-06. Genetic correlation with FBC was evaluated using linkage disequilibrium score regression, by comprehensively examining the associations of published FBC risk loci with risk of MBC and by assessing associations between a FBC polygenic risk score and MBC. All statistical tests were 2-sided. The genome-wide association study identified 3 novel MBC susceptibility loci that attained genome-wide statistical significance (P < 5 × 10-08). Genetic correlation analysis revealed a strong shared genetic basis with estrogen receptor-positive FBC. Men in the top quintile of genetic risk had a fourfold increased risk of breast cancer relative to those in the bottom quintile (odds ratio = 3.86, 95% confidence interval = 3.07 to 4.87, P = 2.08 × 10-30). These findings advance our understanding of the genetic basis of MBC, providing support for an overlapping genetic etiology with FBC and identifying a fourfold high-risk group of susceptible men.

Sections du résumé

BACKGROUND
The etiology of male breast cancer (MBC) is poorly understood. In particular, the extent to which the genetic basis of MBC differs from female breast cancer (FBC) is unknown. A previous genome-wide association study of MBC identified 2 predisposition loci for the disease, both of which were also associated with risk of FBC.
METHODS
We performed genome-wide single nucleotide polymorphism genotyping of European ancestry MBC case subjects and controls in 3 stages. Associations between directly genotyped and imputed single nucleotide polymorphisms with MBC were assessed using fixed-effects meta-analysis of 1380 cases and 3620 controls. Replication genotyping of 810 cases and 1026 controls was used to validate variants with P values less than 1 × 10-06. Genetic correlation with FBC was evaluated using linkage disequilibrium score regression, by comprehensively examining the associations of published FBC risk loci with risk of MBC and by assessing associations between a FBC polygenic risk score and MBC. All statistical tests were 2-sided.
RESULTS
The genome-wide association study identified 3 novel MBC susceptibility loci that attained genome-wide statistical significance (P < 5 × 10-08). Genetic correlation analysis revealed a strong shared genetic basis with estrogen receptor-positive FBC. Men in the top quintile of genetic risk had a fourfold increased risk of breast cancer relative to those in the bottom quintile (odds ratio = 3.86, 95% confidence interval = 3.07 to 4.87, P = 2.08 × 10-30).
CONCLUSIONS
These findings advance our understanding of the genetic basis of MBC, providing support for an overlapping genetic etiology with FBC and identifying a fourfold high-risk group of susceptible men.

Identifiants

pubmed: 32785646
pii: 5885091
doi: 10.1093/jnci/djaa101
pmc: PMC8023850
doi:

Substances chimiques

Receptors, Estrogen 0

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

453-461

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : NCI NIH HHS
ID : R01 CA074415
Pays : United States
Organisme : Medical Research Council
ID : G0000934
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 068545/Z/02
Pays : United Kingdom
Organisme : Cancer Research UK
ID : CA8197/A10865
Pays : United Kingdom
Organisme : Cancer Research UK
ID : C588/A10589
Pays : United Kingdom

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press.

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Auteurs

Sarah Maguire (S)

The Patrick G Johnston Centre for Cancer Research, Queen's University Belfast, Belfast, UK.
The Breast Cancer Now Toby Robins Research Centre, The Institute of Cancer Research, London, UK.

Eleni Perraki (E)

The Breast Cancer Now Toby Robins Research Centre, The Institute of Cancer Research, London, UK.

Katarzyna Tomczyk (K)

The Breast Cancer Now Toby Robins Research Centre, The Institute of Cancer Research, London, UK.

Michael E Jones (ME)

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

Olivia Fletcher (O)

The Breast Cancer Now Toby Robins Research Centre, The Institute of Cancer Research, London, UK.

Matthew Pugh (M)

The Breast Cancer Now Toby Robins Research Centre, The Institute of Cancer Research, London, UK.

Timothy Winter (T)

The Patrick G Johnston Centre for Cancer Research, Queen's University Belfast, Belfast, UK.

Kyle Thompson (K)

The Patrick G Johnston Centre for Cancer Research, Queen's University Belfast, Belfast, UK.

Rosie Cooke (R)

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

Alison Trainer (A)

Parkville Familial Cancer Clinic, Sir Peter MacCallum Department of Oncology, University of Melbourne and Royal Melbourne Hospital, East Melbourne, Victoria, Australia.

Paul James (P)

Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
Sir Peter MacCallum Department of Oncology, The University of Melbourne, Melbourne, Victoria, Australia.

Stig Bojesen (S)

Department of Clinical Biochemistry, Herlev Hospital, Copenhagen University Hospital, Herlev, Denmark.
The Copenhagen General Population Study, Herlev and Gentofte Hospital, Copenhagen University Hospital, Denmark.
Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.

Henrik Flyger (H)

Department of Breast Surgery, Herlev and Gentofte Hospital, Copenhagen University Hospital, Copenhagen, Denmark.

Heli Nevanlinna (H)

Department of Obstetrics and Gynecology, University of Helsinki and Helsinki University Hospital, Helsinki, Finland.

Johanna Mattson (J)

Department of Oncology, University of Helsinki and Helsinki University Hospital, Helsinki, Finland.

Eitan Friedman (E)

The Susanne Levy Gertner Oncogenetics Unit, Sheba Medical Centre, Tel Aviv, Israel.
The Sackler School of Medicine, Tel-Aviv University, Tel Aviv, Israel.

Yael Laitman (Y)

The Susanne Levy Gertner Oncogenetics Unit, Sheba Medical Centre, Tel Aviv, Israel.
The Sackler School of Medicine, Tel-Aviv University, Tel Aviv, Israel.

Domenico Palli (D)

Cancer Risk Factors and Life-Style Epidemiology Unit, Institute for Cancer Research, Prevention and Clinical Network-ISPRO, Florence, Italy.

Giovanna Masala (G)

Cancer Risk Factors and Life-Style Epidemiology Unit, Institute for Cancer Research, Prevention and Clinical Network-ISPRO, Florence, Italy.

Ines Zanna (I)

Cancer Risk Factors and Life-Style Epidemiology Unit, Institute for Cancer Research, Prevention and Clinical Network-ISPRO, Florence, Italy.

Laura Ottini (L)

Department of Molecular Medicine, Sapienza University of Rome, Rome, Italy.

Valentina Silvestri (V)

Department of Molecular Medicine, Sapienza University of Rome, Rome, Italy.

Antoinette Hollestelle (A)

Department of Medical Oncology, Familial Cancer Clinic, Erasmus MC Cancer Institute, Rotterdam, the Netherlands.

Maartje J Hooning (MJ)

Department of Medical Oncology, Familial Cancer Clinic, Erasmus MC Cancer Institute, Rotterdam, the Netherlands.

Srdjan Novaković (S)

Department of Molecular Diagnostics, Institute of Oncology Ljubljana, Ljubljana, Slovenia.

Mateja Krajc (M)

Institute of Oncology Ljubljana, Cancer Genetics Clinic, Epidemiology and Cancer Registry, Ljubljana, Slovenia.

Manuela Gago-Dominguez (M)

Genomic Medicine Group, Galician Foundation of Genomic Medicine, Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Complejo Hospitalario Universitario de Santiago (CHUS), Servicio Galego de Saúde (SERGAS), Santiago de Compostela, Spain.
Instituto de Investigación Sanitaria Galicia Sur (IISGS), Xerencia de Xestion Integrada de Vigo-SERGAS, Oncology and Genetics Unit, Vigo, Spain.

Jose Esteban Castelao (JE)

Genetic Oncology Unit, Complexo Hospitalario Universitario de Vigo (CHUVI), SERGAS, Vigo, Spain.

Hakan Olsson (H)

Division of Oncology, Department of Clinical Sciences, Lund, Lund University and Skåne University Hospital, Lund, Sweden.

Ingrid Hedenfalk (I)

Division of Oncology, Department of Clinical Sciences, Lund, Lund University and Skåne University Hospital, Lund, Sweden.

Emmanouil Saloustros (E)

Department of Oncology, University Hospital of Larissa, Larissa, Greece.

Vasilios Georgoulias (V)

Department of Medical Oncology, University General Hospital of Heraklion, Heraklion, Greece.

Douglas F Easton (DF)

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

Paul Pharoah (P)

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

Alison M Dunning (AM)

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

D Timothy Bishop (DT)

Division of Immunology, Leeds Institute of Medical Research at St James's, University of Leeds, Leeds, UK.

Susan L Neuhausen (SL)

Department of Population Sciences, Beckman Research Institute of City of Hope, Duarte, CA, USA.

Linda Steele (L)

Department of Population Sciences, Beckman Research Institute of City of Hope, Duarte, CA, USA.

Alan Ashworth (A)

UCSF Helen Diller Family Comprehensive Cancer Centre, San Francisco, CA, USA.

Montserrat Garcia Closas (M)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MA, USA.

Richard Houlston (R)

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

Anthony Swerdlow (A)

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

Nick Orr (N)

The Patrick G Johnston Centre for Cancer Research, Queen's University Belfast, Belfast, UK.
The Breast Cancer Now Toby Robins Research Centre, The Institute of Cancer Research, London, UK.

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