Nature Genetics

, volume 52 , issue 6 , pages 572-581

Genome-wide association study identifies 32 novel breast cancer susceptibility loci from overall and subtype-specific analyses

Haoyu Zhang ^{1, 2}

Thomas U. Ahearn ³

Julie Lecarpentier ³

Daniel R. Barnes ⁴

Jonathan Beesley ²

Guanghao Qi ⁵

Xia Jiang ⁴

Tracy A Omara ²

Zhao Ni ⁶

Manjeet K. Bolla ³

ALISON DUNNING ⁶

Joe Dennis ⁶

Qin Wang ⁷

Zumuruda Abu Ful ⁸

Kristiina Aittomäki ⁹

I Andrulis ¹⁰

Hoda Anton-Culver ¹¹

Volker Arndt ¹²

Kristan J Aronson ¹³

Banu K Arun ^{14, 15}

Paul L. Auer ¹⁶

Jacopo Azzollini ¹⁷

Daniel Barrowdale ¹⁸

Heiko Becher ¹⁹

Matthias W. Beckmann ²⁰

Sabine Behrens ²¹

Javier Benitez ²²

Marina Bermisheva ²³

Katarzyna Bialkowska ^{24, 25, 26}

Ana Blanco ^{27, 28}

Carl Blomqvist ^{29, 30, 31}

Natalia V. Bogdanova ^{32, 33, 34, 35}

Stig Egil Bojesen ³⁶

Bernardo Bonanni ³⁶

Bondavalli Davide ³⁷

Ake Borg ^{38, 39, 40}

H. Brauch ^{11, 40, 41}

Hermann Brenner ⁴²

Ignacio Briceno ⁴³

Annegien Broeks ⁴⁴

Sara Y. Brucker ⁴⁵

Thomas Brüning ^{46, 47}

Barbara Burwinkel ⁴⁸

Saundra S. Buys ⁴⁹

Helen Byers ⁵⁰

Trinidad Caldes ⁵¹

Maria A Caligo ³⁶

Mariarosaria Calvello ^{20, 52}

Daniele Campa ⁵³

Jose E. Castelao ^{20, 54}

Jenny Chang-Claude ¹

STEPHEN CHANOCK ⁵⁵

Melissa Christiaens ³¹

Hans Christiansen ⁵⁶

Wendy K. Chung ⁵⁷

Kathleen Claes ⁵⁸

Christine L. Clarke ⁴³

Sten Cornelissen ⁵⁹

Fergus J Couch ⁶⁰

Angela Cox ⁶¹

Simon S Cross ⁶²

Kamila Czene ⁶³

Mary B. Daly ⁶⁴

Peter Devilee ⁶⁵

Orland Diez ⁶⁶

Susan M. Domchek ³⁰

T. DorkDork ⁶⁷

Miriam V. Dwek ⁶⁸

Diana M Eccles ⁶⁹

A.B. Ekici ^{49, 70}

D. Gareth Evans ^{19, 71}

Peter A. Fasching ⁷²

Jonine Figueroa ⁷³

Lenka Foretova ⁷⁴

Florentia Fostira ⁷⁵

Eitan Friedman ¹⁷

Debra Frost ^{76, 77}

Manuela Gago-Dominguez ⁷⁸

Susan M. Gapstur ⁷⁹

Judy Garber ⁵⁰

Jose Angel García-Saenz ⁷⁸

Mia M Gaudet ⁸⁰

Simon A. Gayther ^{81, 82, 83}

G. R. Giles ⁸⁴

Andrew K. Godwin ^{85, 86, 87}

Mark S. Goldberg ⁸⁸

David E. Goldgar ³⁵

Anna González-Neira ⁸⁹

Mark H. Greene ²³

Jacek Gronwald ⁹⁰

Pascal Guénel ⁹¹

Lothar Häberle ⁹²

Eric Hahnen ⁹³

Christopher A. Haiman ⁹⁴

Christopher R Hake ^{62, 95}

Per Hall ⁹⁶

Ute Hamann ^{97, 98}

Elaine Harkness ⁹⁹

Bernadette A.M. Heemskerk-Gerritsen ³⁰

Peter Hillemanns ¹⁰⁰

Frans B.L. Hogervorst ¹⁰¹

Bernd Holleczek ⁹⁹

Antoinette Hollestelle ⁹⁹

Maartje J. Hooning ¹

Robert N Hoover ⁸²

John L. Hopper ¹⁰²

Anthony Howell ¹⁹

Hanna Huebner ¹⁰³

Peter Richard Hulick ¹⁰⁴

Evgeny N Imyanitov ¹⁰⁵

Claudine Isaacs ¹⁰⁶

Louise Izatt ⁹⁹

Agnes Jager ¹⁰⁷

Milena Jakimovska Özdemir ^{23, 108}

Anna Jakubowska ¹⁰⁹

Paul M. James ^{110, 111}

Ramunas Janavicius ¹¹²

Wolfgang Janni ¹¹³

Esther M. John ¹¹⁴

Michael E Jones ²⁰

Audrey Jung ²⁰

Rudolf Kaaks ^{20, 115}

Pooja Middha ¹¹⁶

Beth Y. Karlan ⁴³

Renske Keeman ¹¹⁷

Sofia Khan ^{22, 118}

Elza Khusnutdinova ¹¹⁹

Cari M. Kitahara ¹²⁰

Yon-Dschun Ko ⁷⁴

I. Konstantopoulou ¹²¹

Linetta B. Koppert ¹

Stella Koutros ^{122, 123}

Vessela N. Kristensen ¹²⁴

Anne-Vibeke Laenkholm ^{125, 126}

Diether Lambrechts ^{127, 128}

Susanna C. Larsson ¹²⁹

Pierre Laurent-Puig ¹³⁰

Conxi Lázaro ¹³¹

Emilija Lazarova ⁷

Flavio Lejbkowicz ⁶

Goska Leslie ¹³²

Fabienne Lesueur ^{133, 134}

Annika Lindblom ¹³⁵

Jolanta Lissowska ^{38, 136}

Wing-Yee Lo ⁸⁹

Jennifer T. Loud ²³

Jan Lubinski ²³

Alicja Lukomska ^{81, 82}

Robert J. MacInnis ^{137, 138, 139}

Mannermaa Arto ⁹⁶

Mehdi Manoochehri ¹⁶

Siranoush Manoukian ^{95, 140}

Sara Margolin ^{77, 141}

Maria Elena Martinez ¹⁴²

Laura Matricardi ⁶

Lesley Mcguffog ¹⁴³

Catriona A. McLean ¹⁴⁴

Noura Mebirouk ¹⁴⁵

Alfons Meindl ¹⁴⁶

Usha Menon ¹⁴⁷

Austin Miller ¹¹⁸

Elvira Mingazheva ¹⁴²

Marco Montagna ^{148, 149}

Anna-Marie Mulligan ¹²⁹

Claire Mulot ¹¹⁷

Taru A. Muranen ⁶⁶

Katherine L. Nathanson ¹⁵⁰

Susan L. Neuhausen ¹¹⁷

Heli Nevanlinna ⁵⁵

Patrick Neven ^{49, 70}

William G. Newman ¹⁵¹

Finn C. NIELSEN ¹⁵²

Liene Ņikitina Zaķe ^{77, 153}

Jesse Nodora ¹⁵⁴

Kenneth Offit ¹⁵⁵

Edith Olah ^{156, 157}

Olufunmilayo Olopade ^{158, 159}

Hakan Olsson ¹⁶⁰

Andreas Engert ¹⁶¹

Laura Papi ¹⁵⁵

János Papp ³⁰

Tjoung-Won Park-Simon ⁴

MICHAEL F. PARSONS ¹⁶

Bernard Peissel ¹⁶²

Ana Peixoto ¹⁶³

Beth N. Peshkin ¹⁶⁴

Paolo Peterlongo ^{6, 165}

Julian Peto ^{82, 166, 167}

Kelly Anne Phillips ¹⁴⁷

Marion Piedmonte ¹⁰⁷

Dijana Plaseska Karanfilska ²³

Karolina Prajzendanc ¹⁴

ROSS PRENTICE ¹¹⁸

Darya Prokofyeva ¹¹²

BRIGITTE RACK ¹⁶⁸

PAOLO RADICE ^{169, 170, 171}

Susan J. Ramus ¹⁷²

Johanna Rantala ^{96, 173}

Muhammad U. Rashid ⁷

G Rennert ⁷

Hedy S. Rennert ¹⁷⁴

Harvey A. Risch ^{175, 176}

Atocha Romero ¹⁷⁷

Matti A. Rookus ⁹¹

Matthias Rübner ¹⁷⁸

Thomas Rüdiger ¹⁷⁹

Emmanouil Saloustros ¹⁸⁰

Sarah Sampson ¹⁸¹

Dale P. Sandler ¹⁸²

Elinor J. Sawyer ¹⁸³

Maren T. Scheuner ⁹²

Rita K. Schmutzler ^{47, 184}

Andreas Schneeweiss ¹¹⁴

Minouk J. Schoemaker ¹¹

Ben Schöttker ³⁰

Peter Schürmann ¹⁸⁵

Leigha Senter ¹⁸⁶

PRIYANKA SHARMA ¹⁸⁷

Mark E. Sherman ¹⁸⁸

Xiao-Ou Shu ¹⁸⁹

Christian F. Singer ¹³¹

Snezhana Smichkoska ¹⁹⁰

PENNY SOUCY ⁸³

Melissa C. Southey ^{191, 192}

John J. Spinelli ^{82, 193}

Jennifer M. Stone ¹⁹⁴

Dominique Stoppa-Lyonnet ^{114, 195}

Anthony J. Swerdlow ¹⁹⁶

Csilla I. Szabo ^{5, 197, 198}

Rulla M. Tamimi ¹⁹⁹

William J Tapper ^{181, 200}

Jack A. Taylor ^{162, 176}

Manuel R. Teixeira ²⁰¹

Marybeth Terry ²⁰²

Mads Thomassen ²⁰³

Darcy L Thull ^{204, 205}

Marc Tischkowitz ²⁰⁶

Amanda E. Toland ²⁰⁷

Rob A.E.M. Tollenaar ^{208, 209}

IAN W. TOMLINSON ^{96, 210}

Diana Torres ²¹¹

Melissa A. Troester ⁹⁰

Thérèse Truong ²¹²

Nadine Tung ²¹³

Michael Untch ²¹⁴

Celine M Vachon ²¹⁵

Ans M.W. van den Ouweland ¹⁰⁰

Lizet E. van der Kolk ^{49, 70}

Elke M. van Veen ²¹⁶

Elizabeth J. Van Rensburg ^{24, 25, 26}

Ana Vega ⁹²

Barbara Wappenschmidt ²¹⁷

Clarice R. Weinberg ²¹⁸

Jeffrey Weitzel ⁵⁵

Hans Wildiers ^{219, 220, 221, 222}

Robert Winqvist ^{108, 127, 128}

Alicja Wolk ¹

Xiaohong R. Yang ⁷⁴

Drakoulis Yannoukakos ¹⁸⁸

Wei Zheng ²²³

Kristin K Zorn ^{81, 82, 83}

R W Milne ^{5, 198}

Peter Kraft ¹⁹⁰

Jacques Simard ^{3, 6}

P. O. D. PHAROAH ^{6, 224, 225}

Kyriaki Michailidou ⁶

Antonis C. Antoniou ^{43, 226}

Marjanka K. Schmidt ⁴

Georgia Chenevix-Trench ³

Douglas F. Easton ^{2, 227}

Nilanjan Chatterjee ¹

Hide authors affiliations Show authors affiliations: 227 affiliations

Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health (NIH), Department of Health and Human Services, Bethesda, USA |

Department of Biostatistics, Johns Hopkins Bloomberg School of Public Health, Baltimore, USA |

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

⁴

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

⁵

Program in Genetic Epidemiology and Statistical Genetics, Harvard T.H. Chan School of Public Health, Boston, USA |

⁶

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

⁷

Clalit National Cancer Control Center, Carmel Medical Center and Technion Faculty of Medicine, Haifa, Israel

Technion – Israel Institute of Technology

Carmel Medical Center

⁸

Department of Clinical Genetics, Helsinki University Hospital, University of Helsinki, Helsinki, Finland |

⁹

Fred A. Litwin Center for Cancer Genetics, Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada |

¹⁰

Department of Epidemiology, Genetic Epidemiology Research Institute, University of California, Irvine, Irvine, USA |

¹¹

Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany |

¹²

Department of Public Health Sciences and Cancer Research Institute, Queen’s University, Kingston, Canada |

¹³

Department of Breast Medical Oncology, University of Texas MD Anderson Cancer Center, Houston, USA |

¹⁴

Cancer Prevention Program, Fred Hutchinson Cancer Research Center, Seattle, USA |

¹⁵

Zilber School of Public Health, University of Wisconsin-Milwaukee, Milwaukee, USA |

¹⁶

Unit of Medical Genetics, Department of Medical Oncology and Hematology, Fondazione IRCCS Istituto Nazionale dei Tumori (INT), Milan, Italy |

¹⁷

Centre for Cancer Genetic Epidemiology, University of Cambridge, Cambridge, UK |

¹⁸

Institute of Medical Biometry and Epidemiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany |

¹⁹

Department of Gynecology and Obstetrics, Comprehensive Cancer Center ER-EMN, University Hospital Erlangen, Friedrich–Alexander University of Erlangen–Nuremberg, Erlangen, Germany |

²⁰

Division of Cancer Epidemiology, DKFZ, Heidelberg, Germany |

²¹

Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Valencia, Spain |

²²

Institute of Biochemistry and Genetics, Ufa Federal Research Centre of the Russian Academy of Sciences, Ufa, Russia

Institute of Biochemistry and Genetics of the Ufa Federal Research Center of the Russian Academy of Sciences

Ufa Federal Research Center of the Russian Academy of Sciences

²³

Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland |

²⁴

Molecular Medicine Unit, Fundación Pública Galega de Medicina Xenómica, Santiago de Compostela, Spain |

²⁵

Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Complejo Hospitalario Universitario de Santiago, Servicio Galego de Saude (SERGAS), Santiago de Compostela, Spain |

²⁶

CIBERER, Santiago de Compostela, Spain |

²⁷

Department of Oncology, Helsinki University Hospital, University of Helsinki, Helsinki, Finland |

²⁸

Department of Oncology, Örebro University Hospital, Örebro, Sweden |

²⁹

N.N. Alexandrov Research Institute of Oncology and Medical Radiology, Minsk, Belarus |

³⁰

Gynaecology Research Unit, Hannover Medical School, Hannover, Germany |

³¹

Department of Radiation Oncology, Hannover Medical School, Hannover, Germany |

³²

Copenhagen General Population Study, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark |

³³

Department of Clinical Biochemistry, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark |

³⁴

Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark |

³⁵

Human Cancer Genetics Programme, Spanish National Cancer Research Centre (CNIO), Madrid, Spain |

³⁶

Division of Cancer Prevention and Genetics, European Institute of Oncology (IEO) IRCCS, Milan, Italy

Istituti di Ricovero e Cura a Carattere Scientifico

European Institute of Oncology

³⁷

Department of Oncology, Lund University and Skåne University Hospital, Lund, Sweden |

³⁸

Dr. Margarete Fischer–Bosch Institute of Clinical Pharmacology, Stuttgart, Germany |

³⁹

iFIT Cluster of Excellence, University of Tübingen, Tübingen, Germany |

⁴⁰

German Cancer Consortium (DKTK), DKFZ, Heidelberg, Germany |

⁴¹

Division of Preventive Oncology, DKFZ and National Center for Tumor Diseases (NCT), Heidelberg, Germany |

⁴²

Bioscience Department, Faculty of Medicine, Universidad de la Sabana, Chia, Colombia |

⁴³

Division of Molecular Pathology, The Netherlands Cancer Institute—Antoni van Leeuwenhoek Hospital, Amsterdam, the Netherlands |

⁴⁴

Department of Women’s Health, University of Tübingen, Tübingen, Germany |

⁴⁵

Institute for Prevention and Occupational Medicine of the German Social Accident Insurance (IPA), Ruhr University Bochum, Bochum, Germany |

⁴⁶

Molecular Epidemiology Group (C080), DKFZ, Heidelberg, Germany |

⁴⁷

Molecular Biology of Breast Cancer, University Women’s Clinic Heidelberg, University of Heidelberg, Heidelberg, Germany |

⁴⁸

Department of Medicine, Huntsman Cancer Institute, Salt Lake City, USA |

⁴⁹

Manchester Centre for Genomic Medicine, St Mary’s Hospital, Manchester NIHR Biomedical Research Centre, Manchester University Hospitals NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, UK

Manchester University NHS Foundation Trust

Manchester Academic Health Science Centre

⁵⁰

Medical Oncology Department, Hospital Clínico San Carlos, Instituto de Investigación Sanitaria San Carlos (IdISSC), Centro de Investigación Biomédica en Red de Cáncer (CIBERONC), Madrid, Spain

Centro de Investigación Biomédica en Red de Cáncer

Health Research Institute of the Hospital Clínico San Carlos

⁵¹

Section of Molecular Genetics, Department of Laboratory Medicine, University Hospital of Pisa, Pisa, Italy |

⁵²

Department of Biology, University of Pisa, Pisa, Italy |

⁵³

Oncology and Genetics Unit, Instituto de Investigacion Sanitaria Galicia Sur (IISGS), Xerencia de Xestion Integrada de Vigo–SERGAS, Vigo, Spain |

⁵⁴

Cancer Epidemiology Group, University Cancer Center Hamburg (UCCH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany

University Medical Center Hamburg-Eppendorf

University Cancer Center Hamburg

⁵⁵

Leuven Multidisciplinary Breast Center, Department of Oncology, Leuven Cancer Institute, University Hospitals Leuven, Leuven, Belgium |

⁵⁶

Departments of Pediatrics and Medicine, Columbia University, New York, USA |

⁵⁷

Centre for Medical Genetics, Ghent University, Ghent, Belgium |

⁵⁸

Westmead Institute for Medical Research, University of Sydney, Sydney, Australia |

⁵⁹

Department of laboratory medicine and pathology, Mayo Clinic, Rochester, USA |

⁶⁰

Sheffield Institute for Nucleic Acids (SInFoNiA), Department of Oncology and Metabolism, University of Sheffield, Sheffield, UK |

⁶¹

Academic Unit of Pathology, Department of Neuroscience, University of Sheffield, Sheffield, UK |

⁶²

Department of medical epidemiology and biostatistics, Karolinska Institutet, Stockholm, Sweden |

⁶³

Department of Clinical Genetics, Fox Chase Cancer Center, Philadelphia, USA |

⁶⁴

Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands |

⁶⁵

Oncogenetics Group, Vall d’Hebron Institute of Oncology (VHIO), Barcelona, Spain |

⁶⁶

Department of Medicine, Abramson Cancer Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, USA |

⁶⁷

Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, London, UK |

⁶⁸

Cancer Sciences Academic Unit, Faculty of Medicine, University of Southampton, Southampton, UK |

⁶⁹

Institute of Human Genetics, University Hospital Erlangen, Friedrich–Alexander University Erlangen–Nuremberg, Comprehensive Cancer Center ER-EMN, Erlangen, Germany |

⁷⁰

Division of Evolution and Genomic Medicine, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, UK

University of Manchester

Manchester Academic Health Science Centre

⁷¹

David Geffen School of Medicine, Department of Medicine, Division of Hematology and Oncology, University of California, Los Angeles, Los Angeles, USA |

⁷²

Usher Institute of Population Health Sciences and Informatics, University of Edinburgh Medical School, Edinburgh, UK |

⁷³

Department of Cancer Epidemiology and Genetics, Masaryk Memorial Cancer Institute, Brno, Czech Republic |

⁷⁴

Molecular Diagnostics Laboratory, INRaSTES, National Centre for Scientific Research ‘Demokritos’, Athens, Greece |

⁷⁵

The Susanne Levy Gertner Oncogenetics Unit, Chaim Sheba Medical Center, Ramat Gan, Israel |

⁷⁶

Genomic Medicine Group, Galician Foundation of Genomic Medicine, IDIS, Complejo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain |

⁷⁷

Moores Cancer Center, University of California, San Diego, La Jolla, USA |

⁷⁸

Behavioral and Epidemiology Research Group, American Cancer Society, Atlanta, USA |

⁷⁹

Cancer Risk and Prevention Clinic, Dana-Farber Cancer Institute, Boston, USA |

⁸⁰

Center for Bioinformatics and Functional Genomics and the Cedars-Sinai Genomics Core, Cedars-Sinai Medical Center, Los Angeles, USA |

⁸¹

Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, Australia |

⁸²

Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Melbourne, Australia |

⁸³

Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Melbourne, Australia

Monash University

Monash Health

⁸⁴

Department of Pathology and Laboratory Medicine, Kansas University Medical Center, Kansas City, USA |

⁸⁵

Department of medicine, McGill University, Montréal, Canada |

⁸⁶

Division of Clinical Epidemiology, Royal Victoria Hospital, McGill University, Montréal, Canada |

⁸⁷

Breast Cancer Research Unit, Cancer Research Institute, University Malaya Medical Centre, Kuala Lumpur, Malaysia |

⁸⁸

Department of Dermatology, Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, USA |

⁸⁹

Clinical Genetics Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, USA |

⁹⁰

Cancer and Environment Group, Center for Research in Epidemiology and Population Health (CESP), INSERM, University Paris-Sud, University of Paris-Saclay, Paris, France

Université Paris-Saclay

French Institute of Health and Medical Research

⁹¹

Department of Gynaecology and Obstetrics, University Hospital Erlangen, Friedrich–Alexander University Erlangen–Nuremberg, Comprehensive Cancer Center ER-EMN, Erlangen, Germany |

⁹²

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

⁹³

Department of preventive medicine, Keck School of Medicine, University of Southern California, Los Angeles, USA |

⁹⁴

Waukesha Memorial Hospital Pro Health Care, Waukesha, USA |

⁹⁵

Department of Oncology, Södersjukhuset, Stockholm, Sweden |

⁹⁶

Molecular Genetics of Breast Cancer, DKFZ, Heidelberg, Germany |

⁹⁷

Division of Informatics, Imaging and Data Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, UK

University of Manchester

Manchester Academic Health Science Centre

⁹⁸

Nightingale Breast Screening Centre, Wythenshawe Hospital, Manchester University NHS Foundation Trust, Manchester, UK |

⁹⁹

Department of Medical Oncology, Family Cancer Clinic, Erasmus MC Cancer Institute, Rotterdam, The Netherlands |

¹⁰⁰

Family Cancer Clinic, The Netherlands Cancer Institute—Antoni van Leeuwenhoek Hospital, Amsterdam, the Netherlands |

¹⁰¹

Saarland cancer registry, Saarbrücken, Germany |

¹⁰²

Division of Cancer Sciences, University of Manchester, Manchester, UK |

¹⁰³

Center for Medical Genetics, NorthShore University HealthSystem, Evanston, USA |

¹⁰⁴

N.N. Petrov Institute of Oncology, St. Petersburg, Russia |

¹⁰⁵

Lombardi Comprehensive Cancer Center, Georgetown University, Washington, USA |

¹⁰⁶

Clinical Genetics, Guy’s and St. Thomas’ NHS Foundation Trust, London, UK |

¹⁰⁷

Research Centre for Genetic Engineering and Biotechnology ‘Georgi D. Efremov’, Macedonian Academy of Sciences and Arts, Skopje, Republic of Macedonia |

¹⁰⁸

Independent laboratory of Molecular Biology and Genetic Diagnostics, Pomeranian Medical University, Szczecin, Poland |

¹⁰⁹

Parkville Familial Cancer Centre, Peter MacCallum Cancer Center, Melbourne, Australia |

¹¹⁰

Hematology, Oncology and Transfusion Medicine Center, Department of Molecular and Regenerative Medicine, Vilnius University Hospital Santariskiu Clinics, Vilnius, Lithuania |

¹¹¹

State Research Institute Center for Innovative Medicine, Vilnius, Lithuania |

¹¹²

Department of Gynaecology and Obstetrics, University Hospital Ulm, Ulm, Germany |

¹¹³

Department of Medicine, Division of Oncology, Stanford Cancer Institute, School of Medicine, Stanford University, Stanford, USA |

¹¹⁴

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

¹¹⁵

Faculty of Medicine, University of Heidelberg, Heidelberg, Germany |

¹¹⁶

David Geffen School of Medicine, Department of Obstetrics and Gynecology, University of California, Los Angeles, Los Angeles, USA |

¹¹⁷

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

¹¹⁸

Department of Genetics and Fundamental Medicine, Bashkir State Medical University, Ufa, Russia |

¹¹⁹

Radiation Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, USA |

¹²⁰

Department of Internal Medicine, Evangelische Kliniken Bonn, Johanniter Krankenhaus, Bonn, Germany |

¹²¹

Department of Surgical Oncology, Family Cancer Clinic, Erasmus MC Cancer Institute, Rotterdam, the Netherlands |

¹²²

Department of Cancer Genetics, Institute for Cancer Research, Oslo University Hospital-Radiumhospitalet, Oslo, Norway |

¹²³

Institute of Clinical medicine, Faculty of Medicine, University of Oslo, Oslo, Norway |

¹²⁴

Department of Surgical Pathology, Zealand University Hospital, Slagelse, Denmark |

¹²⁵

VIB Center for Cancer Biology, VIB, Leuven, Belgium |

¹²⁶

Laboratory of Translational Genetics, Department of Human Genetics, University of Leuven, Leuven, Belgium |

¹²⁷

Institute of Environmental Medicine, Karolinska institutet, Stockholm, Sweden |

¹²⁸

Department of Surgical sciences, Uppsala University, Uppsala, Sweden |

¹²⁹

Université Paris Sorbonne Cité, INSERM UMR-S1147, Paris, France |

¹³⁰

Molecular Diagnostic Unit, Hereditary Cancer Program, Bellvitge Biomedical Research Institute (IDIBELL), Catalan Institute of Oncology (ICO), CIBERONC, Barcelona, Spain

Bellvitge Biomedical Research Institute

Centro de Investigación Biomédica en Red de Cáncer

Catalan Institute of Oncology

¹³¹

Ss. Cyril and Methodius University in Skopje, Medical Faculty, University Clinic of Radiotherapy and Oncology, Skopje, Republic of North Macedonia |

¹³²

Genetic Epidemiology of Cancer team, Inserm U900, Paris, France |

¹³³

Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden |

¹³⁴

Department of Clinical genetics, Karolinska University Hospital, Stockholm, Sweden |

¹³⁵

Department of Cancer Epidemiology and Prevention, M. Sklodowska-Curie Cancer Center, Oncology Institute, Warsaw, Poland |

¹³⁶

University of Tübingen, Tübingen, Germany |

¹³⁷

Translational Cancer Research Area, University of Eastern Finland, Kuopio, Finland |

¹³⁸

Institute of Clinical Medicine, Pathology and Forensic Medicine, University of Eastern Finland, Kuopio, Finland |

¹³⁹

Imaging Center, Department of Clinical Pathology, Kuopio University Hospital, Kuopio, Finland |

¹⁴⁰

Department of Clinical Science and Education, Södersjukhuset, Karolinska Institutet, Stockholm, Sweden |

¹⁴¹

Department of Family Medicine and Public Health, University of California, San Diego, La Jolla, USA |

¹⁴²

Immunology and Molecular Oncology Unit, Veneto Institute of Oncology (IOV)-IRCCS, Padua, Italy

Istituti di Ricovero e Cura a Carattere Scientifico

Veneto Institute of Oncology

¹⁴³

Department of Anatomical Pathology, The Alfred Hospital, Melbourne, Australia |

¹⁴⁴

Genetic Epidemiology of Cancer Team, INSERM U900, Institut Curie, PSL University, Mines ParisTech, Paris, France

Institut Curie

École Nationale Supérieure des Mines de Paris

Paris Sciences et Lettres

French Institute of Health and Medical Research

¹⁴⁵

Department of Gynecology and Obstetrics, Ludwig Maximilian University of Munich, Munich, Germany |

¹⁴⁶

MRC Clinical Trials Unit at UCL, Institute of Clinical Trials and Methodology, University College London, London, UK |

¹⁴⁷

NRG Oncology, Statistics and Data Management Center, Roswell Park Cancer Institute, Buffalo, USA |

¹⁴⁸

Laboratory Medicine Program, University Health Network, Toronto, Canada |

¹⁴⁹

Department of Laboratory Medicine and Pathobiology, University Of Toronto, Toronto, Canada |

¹⁵⁰

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

¹⁵¹

Center for Genomic Medicine, Rigshospitalet, Copenhagen University hospital, Copenhagen, Denmark |

¹⁵²

Latvian Biomedical Research and Study centre, Riga, Latvia |

¹⁵³

Department of Family Medicine and Public Health, School of Medicine, University of California, San Diego, La Jolla, USA |

¹⁵⁴

Clinical Genetics Research Laboratory, Department of Cancer Biology and Genetics, Memorial Sloan Kettering Cancer Center, New York, USA |

¹⁵⁵

Department of Molecular Genetics, National Institute of Oncology, Budapest, Hungary |

¹⁵⁶

Center for Clinical Cancer Genetics, The University of Chicago, Chicago, USA |

¹⁵⁷

Department of Clinical Pathology, University of Melbourne, Melbourne, Australia |

¹⁵⁸

Department of Cancer Epidemiology, Clinical Sciences, Lund University, Lund, Sweden |

¹⁵⁹

Clinical Genetics Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, USA |

¹⁶⁰

Centre for Cancer Research and Cell Biology, Queen’s University Belfast, Belfast, UK |

¹⁶¹

Unit of Medical Genetics, Department of Biomedical, Experimental and Clinical Sciences, University of Florence, Florence, Italy |

¹⁶²

Department of Genetics, Portuguese Oncology Institute, Porto, Portugal |

¹⁶³

Department of Oncology, Lombardi Comprehensive Cancer Center, Georgetown University, Washington, USA |

¹⁶⁴

Genome Diagnostics Program, IFOM, FIRC Institute of Molecular Oncology, Milan, Italy |

¹⁶⁵

Department of non-communicable disease epidemiology, London School of Hygiene and Tropical Medicine, London, UK |

¹⁶⁶

Peter Maccallum Cancer Center, Melbourne, Australia |

¹⁶⁷

Sir Peter Maccallum Department of Oncology, University of Melbourne, Melbourne, Australia |

¹⁶⁸

Unit of Molecular Bases of Genetic Risk and Genetic Testing, Department of Research, INT, Milan, Italy |

¹⁶⁹

Adult Cancer Program, Lowy Cancer Research Centre, University of NSW Sydney, Sydney, Australia |

¹⁷⁰

School of Women’s and Children’s Health, Faculty of Medicine, University of NSW Sydney, Sydney, Australia |

¹⁷¹

The Kinghorn Cancer Centre, Garvan Institute of Medical Research, Sydney, Australia |

¹⁷²

Clinical Genetics, Karolinska Institutet, Stockholm, Sweden |

¹⁷³

Department of Basic Sciences, Shaukat Khanum Memorial Cancer Hospital and Research Centre (SKMCH&RC), Lahore, Pakistan |

¹⁷⁴

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

¹⁷⁵

Medical Oncology Department, Hospital Universitario Puerta de Hierro, Madrid, Spain |

¹⁷⁶

Biomedical Sciences Institute (ICBAS), University of Porto, Porto, Portugal |

¹⁷⁷

Department of Epidemiology, the Netherlands Cancer Institute, Amsterdam, the Netherlands |

¹⁷⁸

Institute of Pathology, Staedtisches Klinikum Karlsruhe, Karlsruhe, Germany |

¹⁷⁹

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

¹⁸⁰

Prevent Breast Cancer Centre and Nightingale Breast Screening Centre, Manchester University NHS Foundation Trust, Manchester, UK |

¹⁸¹

Epidemiology Branch, National Institute of Environmental Health Sciences, NIH, Durham, USA |

¹⁸²

Research Oncology, Guy’s Hospital, King’s College London, London, UK |

¹⁸³

Cancer Genetics and Prevention Program, University of California, San Francisco, San Francisco, USA |

¹⁸⁴

NCT, University Hospital and DKFZ, Heidelberg, Germany |

¹⁸⁵

Clinical Cancer Genetics Program, Division of Human Genetics, Department of Internal Medicine, Comprehensive Cancer Center, The Ohio State University, Columbus, USA |

¹⁸⁶

Department of Internal Medicine, Division of Oncology, University of Kansas Medical Center, Westwood, Kansas City, USA |

¹⁸⁷

Department of Health Sciences Research, Mayo Clinic College of Medicine, Jacksonville, USA |

¹⁸⁸

Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, USA |

¹⁸⁹

Department of Obstetrics and Gynecology and Comprehensive Cancer Center, Medical University of Vienna, Vienna, Austria |

¹⁹⁰

Genomics Center, Centre Hospitalier Universitaire de Québec—Université Laval Research Center, Québec City, Canada

Université Laval

Centre Hospitalier Universitaire de Québec

¹⁹¹

Population Oncology, BC Cancer, Vancouver, Canada |

¹⁹²

School of Population and Public Health, University of British Columbia, Vancouver, CANADA |

¹⁹³

Curtin UWA Centre for Genetic Origins of Health and Disease, Curtin University and University of Western Australia, Perth, Australia |

¹⁹⁴

Department of Genetics, INSERM U830, Institut Curie, Paris Descartes Sorbonne-Paris Cité University, Paris, France

Paris Cité University

Institut Curie

French Institute of Health and Medical Research

¹⁹⁵

Division of Breast Cancer Research, The Institute of Cancer Research, London, UK |

¹⁹⁶

National Human Genome Research Institute, National Cancer Institute, Bethesda, USA

National Human Genome Research Institute

National Cancer Institute

¹⁹⁷

Channing Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, USA

Harvard University

Brigham and Women's Hospital

¹⁹⁸

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

¹⁹⁹

Faculty of Medicine, University of Southampton, Southampton, UK |

²⁰⁰

Epigenetic and Stem Cell Biology Laboratory, National Institute of Environmental Health Sciences, NIH, Durham, USA |

²⁰¹

Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, USA |

²⁰²

Department of Clinical Genetics, Odense University Hospital, Odense, Denmark |

²⁰³

Department of Medicine, Magee-Womens Hospital, School of Medicine, University of Pittsburgh , Pittsburgh, USA

Magee-Womens Hospital

University of Pittsburgh

²⁰⁴

Program in Cancer Genetics, Departments of Human Genetics and Oncology, McGill University, Montréal, Canada |

²⁰⁵

Department of Medical Genetics, National Institute for Health Research, Cambridge Biomedical Research Centre, University of Cambridge, Cambridge, UK

University of Cambridge

NIHR Cambridge Biomedical Research Centre

²⁰⁶

Department of Cancer Biology and Genetics, The Ohio State University, Columbus, USA |

²⁰⁷

Department of surgery, Leiden University Medical Center, Leiden, the Netherlands |

²⁰⁸

Institute of Cancer and Genomic Sciences, University of Birmingham, Birmingham, UK |

²⁰⁹

Wellcome Trust Centre for Human Genetics and Oxford NIHR Biomedical Research Centre, University of Oxford, Oxford, UK |

²¹⁰

Institute of Human Genetics, Pontificia Universidad Javeriana, Bogota, Colombia |

²¹¹

Department of Epidemiology, Gillings School of Global Public Health and UNC Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, USA |

²¹²

Department of Medical Oncology, Beth Israel Deaconess Medical Center, Boston, USA |

²¹³

Department of Gynecology and Obstetrics, Helios Clinics Berlin-Buch, Berlin, Germany |

²¹⁴

Department of Health Science Research, Division of Epidemiology, Mayo Clinic, Rochester, USA |

²¹⁵

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

²¹⁶

Department of Genetics, University of Pretoria, Pretoria, South Africa |

²¹⁷

Biostatistics and Computational Biology Branch, National Institute of Environmental Health Sciences, NIH, Durham, USA |

²¹⁸

Clinical Cancer Genomics, City of Hope, Duarte, USA |

²¹⁹

Laboratory of Cancer Genetics and Tumor Biology, Cancer and Translational Medicine Research Unit, Biocenter Oulu, University of Oulu, Oulu, Finland |

²²⁰

Laboratory of Cancer Genetics and Tumor Biology, Northern Finland Laboratory Centre Oulu, Oulu, Finland |

²²¹

Department of Molecular Genetics, University of Toronto, Toronto, Canada |

²²²

Department of Human genetics, Leiden University Medical Center, Leiden, The Netherlands |

²²³

Magee-Womens Hospital, University of Pittsburgh School of Medicine, Pittsburgh, USA

Magee-Womens Hospital

University of Pittsburgh

²²⁴

Biostatistics Unit, The Cyprus Institute of Neurology and Genetics, Nicosia, Cyprus |

²²⁵

Cyprus School of Molecular Medicine, Nicosia, Cyprus |

²²⁶

Division of Psychosocial Research and Epidemiology, The Netherlands Cancer Institute—Antoni van Leeuwenhoek Hospital, Amsterdam, the Netherlands |

²²⁷

Department of Oncology, School of Medicine, Johns Hopkins University, Baltimore, USA |

Publication type: Journal Article

Publication date: 2020-05-18

Springer Nature

Nature Genetics

scimago Q1

wos Q1

SJR: 16.586

CiteScore: 45.1

Impact factor: 29.0

ISSN: 10614036, 15461718

DOI: 10.1038/s41588-020-0609-2

Copy DOI

PubMed ID: 32424353

Genetics

Abstract

Breast cancer susceptibility variants frequently show heterogeneity in associations by tumor subtype1–3. To identify novel loci, we performed a genome-wide association study including 133,384 breast cancer cases and 113,789 controls, plus 18,908 BRCA1 mutation carriers (9,414 with breast cancer) of European ancestry, using both standard and novel methodologies that account for underlying tumor heterogeneity by estrogen receptor, progesterone receptor and human epidermal growth factor receptor 2 status and tumor grade. We identified 32 novel susceptibility loci (P < 5.0 × 10−8), 15 of which showed evidence for associations with at least one tumor feature (false discovery rate < 0.05). Five loci showed associations (P < 0.05) in opposite directions between luminal and non-luminal subtypes. In silico analyses showed that these five loci contained cell-specific enhancers that differed between normal luminal and basal mammary cells. The genetic correlations between five intrinsic-like subtypes ranged from 0.35 to 0.80. The proportion of genome-wide chip heritability explained by all known susceptibility loci was 54.2% for luminal A-like disease and 37.6% for triple-negative disease. The odds ratios of polygenic risk scores, which included 330 variants, for the highest 1% of quantiles compared with middle quantiles were 5.63 and 3.02 for luminal A-like and triple-negative disease, respectively. These findings provide an improved understanding of genetic predisposition to breast cancer subtypes and will inform the development of subtype-specific polygenic risk scores. Genome-wide analysis identifies 32 loci associated with breast cancer susceptibility, accounting for estrogen receptor, progesterone receptor and human epidermal growth factor receptor 2 status and tumor grade.

Found

1 citation

Falco Antonio

79 publications, 640 citations, 62 reviews

h-index: 12

CEU Cardinal Herrera University

Research interests

Computational mathematics

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GOST Copy

Zhang H. et al. Genome-wide association study identifies 32 novel breast cancer susceptibility loci from overall and subtype-specific analyses // Nature Genetics. 2020. Vol. 52. No. 6. pp. 572-581.

GOST all authors (up to 50) Copy

Zhang H. et al. Genome-wide association study identifies 32 novel breast cancer susceptibility loci from overall and subtype-specific analyses // Nature Genetics. 2020. Vol. 52. No. 6. pp. 572-581.

RIS |

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BibTex (up to 50 authors) Copy

@article{2020_Zhang,

author = {Haoyu Zhang and Thomas U. Ahearn and Julie Lecarpentier and Daniel R. Barnes and Jonathan Beesley and Guanghao Qi and Xia Jiang and Tracy A Omara and Zhao Ni and Manjeet K. Bolla and ALISON DUNNING and Joe Dennis and Qin Wang and Zumuruda Abu Ful and Kristiina Aittomäki and I Andrulis and Hoda Anton-Culver and Volker Arndt and Kristan J Aronson and Banu K Arun and Paul L. Auer and Jacopo Azzollini and Daniel Barrowdale and Heiko Becher and Matthias W. Beckmann and Sabine Behrens and Javier Benitez and Marina Bermisheva and Katarzyna Bialkowska and Ana Blanco and Carl Blomqvist and Natalia V. Bogdanova and Stig Egil Bojesen and Bernardo Bonanni and Bondavalli Davide and Ake Borg and H. Brauch and Hermann Brenner and Ignacio Briceno and Annegien Broeks and Sara Y. Brucker and Thomas Brüning and Barbara Burwinkel and Saundra S. Buys and Helen Byers and Trinidad Caldes and Maria A Caligo and Mariarosaria Calvello and Daniele Campa and Jose E. Castelao and others},

title = {Genome-wide association study identifies 32 novel breast cancer susceptibility loci from overall and subtype-specific analyses},

journal = {Nature Genetics},

year = {2020},

volume = {52},

publisher = {Springer Nature},

month = {may},

url = {https://doi.org/10.1038/s41588-020-0609-2},

number = {6},

pages = {572--581},

doi = {10.1038/s41588-020-0609-2}

}

MLA

Cite this

MLA Copy

Zhang, Haoyu, et al. “Genome-wide association study identifies 32 novel breast cancer susceptibility loci from overall and subtype-specific analyses.” Nature Genetics, vol. 52, no. 6, May. 2020, pp. 572-581. https://doi.org/10.1038/s41588-020-0609-2.

Publisher

Springer Nature

Journal

Nature Genetics

scimago Q1

wos Q1

SJR

16.586

CiteScore

45.1

Impact factor

29.0

ISSN

10614036 (Print)

15461718 (Electronic)