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Research Article

Interplay between BRCA1 and RHAMM Regulates Epithelial Apicobasal Polarization and May Influence Risk of Breast Cancer

  • Christopher A. Maxwell mail,

    cmaxwell@cfri.ubc.ca (CAM); mapujana@ico.scs.es (MAP)

    Affiliation: Translational Research Laboratory, Catalan Institute of Oncology, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet, Catalonia, Spain

    Current address: Department of Pediatrics, Child and Family Research Institute, Vancouver, British Columbia, Canada

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  • Javier Benítez,

    Affiliations: Human Cancer Genetics Programme, Spanish National Cancer Research Centre, Madrid, Spain, Biomedical Research Centre Network for Rare Diseases, Spain

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  • Laia Gómez-Baldó,

    Affiliations: Translational Research Laboratory, Catalan Institute of Oncology, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet, Catalonia, Spain, Biomedical Research Centre Network for Epidemiology and Public Health, Spain

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  • Ana Osorio,

    Affiliations: Human Cancer Genetics Programme, Spanish National Cancer Research Centre, Madrid, Spain, Biomedical Research Centre Network for Rare Diseases, Spain

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  • Núria Bonifaci,

    Affiliations: Translational Research Laboratory, Catalan Institute of Oncology, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet, Catalonia, Spain, Biomedical Research Centre Network for Epidemiology and Public Health, Spain, Biomarkers and Susceptibility Unit, Catalan Institute of Oncology, IDIBELL, L'Hospitalet, Catalonia, Spain

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  • Ricardo Fernández-Ramires,

    Affiliations: Human Cancer Genetics Programme, Spanish National Cancer Research Centre, Madrid, Spain, Biomedical Research Centre Network for Rare Diseases, Spain

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  • Sylvain V. Costes,

    Affiliation: Life Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, United States of America

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  • Elisabet Guinó,

    Affiliations: Biomedical Research Centre Network for Epidemiology and Public Health, Spain, Biomarkers and Susceptibility Unit, Catalan Institute of Oncology, IDIBELL, L'Hospitalet, Catalonia, Spain

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  • Helen Chen,

    Affiliation: Child and Family Research Institute, Vancouver, British Columbia, Canada

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  • Gareth J. R. Evans,

    Affiliation: Child and Family Research Institute, Vancouver, British Columbia, Canada

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  • Pooja Mohan,

    Affiliation: Child and Family Research Institute, Vancouver, British Columbia, Canada

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  • Isabel Català,

    Affiliation: Department of Pathology, University Hospital of Bellvitge, IDIBELL, L'Hospitalet, Catalonia, Spain

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  • Anna Petit,

    Affiliation: Department of Pathology, University Hospital of Bellvitge, IDIBELL, L'Hospitalet, Catalonia, Spain

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  • Helena Aguilar,

    Affiliation: Translational Research Laboratory, Catalan Institute of Oncology, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet, Catalonia, Spain

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  • Alberto Villanueva,

    Affiliation: Translational Research Laboratory, Catalan Institute of Oncology, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet, Catalonia, Spain

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  • Alvaro Aytes,

    Affiliation: Translational Research Laboratory, Catalan Institute of Oncology, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet, Catalonia, Spain

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  • Jordi Serra-Musach,

    Affiliations: Translational Research Laboratory, Catalan Institute of Oncology, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet, Catalonia, Spain, Biomarkers and Susceptibility Unit, Catalan Institute of Oncology, IDIBELL, L'Hospitalet, Catalonia, Spain

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  • Gad Rennert,

    Affiliation: CHS National Cancer Control Center, Department of Community Medicine and Epidemiology, Carmel Medical Center and B. Rappaport Faculty of Medicine, Technion, Haifa, Israel

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  • Flavio Lejbkowicz,

    Affiliation: CHS National Cancer Control Center, Department of Community Medicine and Epidemiology, Carmel Medical Center and B. Rappaport Faculty of Medicine, Technion, Haifa, Israel

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  • Paolo Peterlongo,

    Affiliation: Unit of Molecular Bases of Genetic Risk and Genetic Testing, Department of Preventive and Predictive Medicine, Fondazione IRCCS Istituto Nazionale Tumori, and IFOM Fondazione Istituto FIRC di Oncologia Molecolare, Milan, Italy

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  • Siranoush Manoukian,

    Affiliation: Unit of Medical Genetics, Department of Preventive and Predictive Medicine, Fondazione IRCCS Istituto Nazionale Tumori, Milan, Italy

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  • Bernard Peissel,

    Affiliation: Unit of Medical Genetics, Department of Preventive and Predictive Medicine, Fondazione IRCCS Istituto Nazionale Tumori, Milan, Italy

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  • Carla B. Ripamonti,

    Affiliations: Unit of Molecular Bases of Genetic Risk and Genetic Testing, Department of Preventive and Predictive Medicine, Fondazione IRCCS Istituto Nazionale Tumori, and IFOM Fondazione Istituto FIRC di Oncologia Molecolare, Milan, Italy, Unit of Medical Genetics, Department of Preventive and Predictive Medicine, Fondazione IRCCS Istituto Nazionale Tumori, Milan, Italy

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  • Bernardo Bonanni,

    Affiliation: Division of Cancer Prevention and Genetics, Istituto Europeo di Oncologia, Milan, Italy

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  • Alessandra Viel,

    Affiliation: Division of Experimental Oncology 1, Centro di Riferimento Oncologico, IRCCS, Aviano, Italy

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  • Anna Allavena,

    Affiliation: Department of Genetics, Biology and Biochemistry, University of Turin, Turin, Italy

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  • Loris Bernard,

    Affiliation: Department of Experimental Oncology, Istituto Europeo di Oncologia, and Consortium for Genomics Technology (Cogentech), Milan, Italy

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  • Paolo Radice,

    Affiliation: Unit of Molecular Bases of Genetic Risk and Genetic Testing, Department of Preventive and Predictive Medicine, Fondazione IRCCS Istituto Nazionale Tumori, and IFOM Fondazione Istituto FIRC di Oncologia Molecolare, Milan, Italy

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  • Eitan Friedman,

    Affiliations: The Susanne Levy Gertner Oncogenetics Unit, Institute of Human Genetics, Chaim Sheba Medical Center, Ramat Gan, Israel, Sackler Faculty of Medicine, Tel Aviv University, Ramat Aviv, Israel

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  • Bella Kaufman,

    Affiliation: The Susanne Levy Gertner Oncogenetics Unit, Institute of Human Genetics, Chaim Sheba Medical Center, Ramat Gan, Israel

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  • Yael Laitman,

    Affiliation: The Susanne Levy Gertner Oncogenetics Unit, Institute of Human Genetics, Chaim Sheba Medical Center, Ramat Gan, Israel

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  • Maya Dubrovsky,

    Affiliation: The Susanne Levy Gertner Oncogenetics Unit, Institute of Human Genetics, Chaim Sheba Medical Center, Ramat Gan, Israel

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  • Roni Milgrom,

    Affiliation: The Susanne Levy Gertner Oncogenetics Unit, Institute of Human Genetics, Chaim Sheba Medical Center, Ramat Gan, Israel

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  • Anna Jakubowska,

    Affiliation: International Hereditary Cancer Centre, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland

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  • Cezary Cybulski,

    Affiliation: International Hereditary Cancer Centre, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland

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  • Bohdan Gorski,

    Affiliation: International Hereditary Cancer Centre, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland

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  • Katarzyna Jaworska,

    Affiliation: International Hereditary Cancer Centre, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland

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  • Katarzyna Durda,

    Affiliation: International Hereditary Cancer Centre, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland

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  • Grzegorz Sukiennicki,

    Affiliation: International Hereditary Cancer Centre, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland

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  • Jan Lubiński,

    Affiliation: International Hereditary Cancer Centre, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland

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  • Yin Yao Shugart,

    Affiliation: Unit of Statistical Genetics, Division of Intramural Research Program, National Institute of Mental Health, National Institute of Health, Bethesda, Maryland, United States of America

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  • Susan M. Domchek,

    Affiliation: Abramson Cancer Center, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America

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  • Richard Letrero,

    Affiliation: Abramson Cancer Center, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America

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  • Barbara L. Weber,

    Affiliation: Abramson Cancer Center, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America

    Current address: Novartis Institutes for BioMedical Research, Cambridge, Massachusetts, United States of America

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  • Frans B. L. Hogervorst,

    Affiliation: Family Cancer Clinic, Department of Pathology, The Netherlands Cancer Institute, Amsterdam, the Netherlands

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  • Matti A. Rookus,

    Affiliation: Department of Epidemiology, The Netherlands Cancer Institute, Amsterdam, the Netherlands

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  • J. Margriet Collee,

    Affiliation: Department of Clinical Genetics, Rotterdam Family Cancer Clinic, Erasmus University Medical Center, Rotterdam, the Netherlands

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  • Peter Devilee,

    Affiliation: Department of Genetic Epidemiology, Leiden University Medical Center, Leiden, the Netherlands

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  • Marjolijn J. Ligtenberg,

    Affiliation: Department of Human Genetics, Radboud University Medical Center, Nijmegen, the Netherlands

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  • Rob B. van der Luijt,

    Affiliation: Department of Clinical Molecular Genetics, Utrecht University Medical Center, Utrecht, the Netherlands

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  • Cora M. Aalfs,

    Affiliation: Department of Clinical Genetics, Academic Medical Center, Amsterdam, the Netherlands

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  • Quinten Waisfisz,

    Affiliation: Department of Clinical Genetics, VU University Medical Center, Amsterdam, the Netherlands

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  • Juul Wijnen,

    Affiliation: Center for Human and Clinical Genetics, Leiden University Medical Center, Leiden, the Netherlands

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  • Cornelis E. P. van Roozendaal,

    Affiliation: Department of Clinical Genetics, University Medical Center, Maastricht, the Netherlands

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  • HEBON,

    Affiliation: Hereditary Breast and Ovarian Cancer Group, the Netherlands

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  • EMBRACE,

    Affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom

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  • Douglas F. Easton,

    Affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom

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  • Susan Peock,

    Affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom

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  • Margaret Cook,

    Affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom

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  • Clare Oliver,

    Affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom

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  • Debra Frost,

    Affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom

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  • Patricia Harrington,

    Affiliation: Department of Oncology, University of Cambridge, Cambridge, United Kingdom

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  • D. Gareth Evans,

    Affiliation: Genetic Medicine, Manchester Academic Health Sciences Centre, Central Manchester University Hospitals NHS Foundation Trust, Manchester, United Kingdom

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  • Fiona Lalloo,

    Affiliation: Genetic Medicine, Manchester Academic Health Sciences Centre, Central Manchester University Hospitals NHS Foundation Trust, Manchester, United Kingdom

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  • Rosalind Eeles,

    Affiliation: The Oncogenetics Team, The Institute of Cancer Research and Royal Marsden NHS Foundation Trust, Surrey, United Kingdom

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  • Louise Izatt,

    Affiliation: Clinical Genetics, Guy's and St. Thomas' NHS Foundation Trust, London, United Kingdom

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  • Carol Chu,

    Affiliation: Yorkshire Regional Genetics Service, St. James's Hospital, Leeds, United Kingdom

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  • Diana Eccles,

    Affiliation: Wessex Clinical Genetics Service, Princess Anne Hospital, Southampton, United Kingdom

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  • Fiona Douglas,

    Affiliation: Institute of Human Genetics, Centre for Life, Newcastle Upon Tyne Hospitals NHS Trust, Newcastle upon Tyne, United Kingdom

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  • Carole Brewer,

    Affiliation: Department of Clinical Genetics, Royal Devon & Exeter Hospital, Exeter, United Kingdom

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  • Heli Nevanlinna,

    Affiliation: Department of Obstetrics and Gynecology, Helsinki University Central Hospital, Helsinki, Finland

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  • Tuomas Heikkinen,

    Affiliation: Department of Obstetrics and Gynecology, Helsinki University Central Hospital, Helsinki, Finland

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  • Fergus J. Couch,

    Affiliation: Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, Minnesota, United States of America

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  • Noralane M. Lindor,

    Affiliation: Department of Medical Genetics, Mayo Clinic, Rochester, Minnesota, United States of America

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  • Xianshu Wang,

    Affiliation: Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, Minnesota, United States of America

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  • Andrew K. Godwin,

    Affiliation: Department of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, Kansas, United States of America

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  • Maria A. Caligo,

    Affiliation: Section of Genetic Oncology, Department of Oncology, University of Pisa, and Department of Laboratory Medicine, University Hospital of Pisa, Pisa, Italy

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  • Grazia Lombardi,

    Affiliation: Section of Genetic Oncology, Department of Oncology, University of Pisa, and Department of Laboratory Medicine, University Hospital of Pisa, Pisa, Italy

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  • Niklas Loman,

    Affiliation: Department of Oncology, Lund University Hospital, Lund, Sweden

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  • Per Karlsson,

    Affiliation: Department of Oncology, Sahlgrenska University Hospital, Gothenburg, Sweden

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  • Hans Ehrencrona,

    Affiliation: Department of Genetics and Pathology, Rudbeck Laboratory, Uppsala University, Uppsala, Sweden

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  • Anna von Wachenfeldt,

    Affiliation: Department of Oncology, Karolinska University Hospital, Stockholm, Sweden

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  • SWE-BRCA,

    Affiliation: Swedish Breast Cancer Study, Sweden

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  • Rosa Bjork Barkardottir,

    Affiliation: Department of Pathology, Landspitali-University Hospital, Reykjavik, Iceland

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  • Ute Hamann,

    Affiliation: Molecular Genetics of Breast Cancer, Deutsches Krebsforschungszentrum, Heidelberg, Germany

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  • Muhammad U. Rashid,

    Affiliation: Molecular Genetics of Breast Cancer, Deutsches Krebsforschungszentrum, Heidelberg, Germany, and Department of Basic Sciences, Shaukat Khanum Memorial Cancer Hospital and Research Centre, Lahore, Pakistan

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  • Adriana Lasa,

    Affiliation: Genetic Service, Hospital de la Santa Creu i Sant Pau, Barcelona, Catalonia, Spain

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  • Trinidad Caldés,

    Affiliation: Molecular Oncology Laboratory, Hospital Clínico San Carlos, Madrid, Spain

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  • Raquel Andrés,

    Affiliation: Medical Oncology Division, Hospital Clínico de Zaragoza, Zaragoza, Spain

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  • Michael Schmitt,

    Affiliation: Department of Internal Medicine III, University of Rostock, Rostock, Germany

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  • Volker Assmann,

    Affiliation: Center for Experimental Medicine, Institute of Tumor Biology, University Hospital Hamburg–Eppendorf, Hamburg, Germany

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  • Kristen Stevens,

    Affiliation: Department of Epidemiology, University of Michigan, Ann Arbor, Michigan, United States of America

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  • Kenneth Offit,

    Affiliation: Clinical Genetics Service, Department of Medicine, Memorial Sloan-Kettering Cancer Center, New York, New York, United States of America

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  • João Curado,

    Affiliation: Bioinformatics and Genomics Group, Centre for Genomic Regulation (CRG), Biomedical Research Park of Barcelona (PRBB), Barcelona, Catalonia, Spain

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  • Hagen Tilgner,

    Affiliation: Bioinformatics and Genomics Group, Centre for Genomic Regulation (CRG), Biomedical Research Park of Barcelona (PRBB), Barcelona, Catalonia, Spain

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  • Roderic Guigó,

    Affiliation: Bioinformatics and Genomics Group, Centre for Genomic Regulation (CRG), Biomedical Research Park of Barcelona (PRBB), Barcelona, Catalonia, Spain

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  • Gemma Aiza,

    Affiliation: Translational Research Laboratory, Catalan Institute of Oncology, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet, Catalonia, Spain

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  • Joan Brunet,

    Affiliation: Genetic Counseling and Hereditary Cancer Programme, Catalan Institute of Oncology, IDIBELL and Girona Biomedical Research Institute (IdIBGi), Catalonia, Spain

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  • Joan Castellsagué,

    Affiliation: Genetic Counseling and Hereditary Cancer Programme, Catalan Institute of Oncology, IDIBELL and Girona Biomedical Research Institute (IdIBGi), Catalonia, Spain

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  • Griselda Martrat,

    Affiliation: Translational Research Laboratory, Catalan Institute of Oncology, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet, Catalonia, Spain

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  • Ander Urruticoechea,

    Affiliation: Translational Research Laboratory, Catalan Institute of Oncology, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet, Catalonia, Spain

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  • Ignacio Blanco,

    Affiliation: Genetic Counseling and Hereditary Cancer Programme, Catalan Institute of Oncology, IDIBELL and Girona Biomedical Research Institute (IdIBGi), Catalonia, Spain

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  • Laima Tihomirova,

    Affiliation: Latvian Biomedical Research and Study Center, Riga, Latvia

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  • David E. Goldgar,

    Affiliation: Department of Dermatology, University of Utah School of Medicine, Salt Lake City, Utah, United States of America

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  • Saundra Buys,

    Affiliation: Department of Internal Medicine, Huntsman Cancer Institute, Salt Lake City, Utah, United States of America

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  • Esther M. John,

    Affiliation: Cancer Prevention Institute of California, Fremont, California, United States of America

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  • Alexander Miron,

    Affiliation: Department of Cancer Biology, Dana-Farber Cancer Institute, and Department of Surgery, Harvard Medical School, Boston, Massachusetts, United States of America

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  • Melissa Southey,

    Affiliation: Centre for Molecular, Environmental, Genetic and Analytic (MEGA) Epidemiology, Melbourne School of Population Health, The University of Melbourne, Victoria, Australia

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  • Mary B. Daly,

    Affiliation: Division of Population Science, Fox Chase Cancer Center, Philadelphia, Pennsylvania, United States of America

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  • BCFR,

    Affiliation: Breast Cancer Family Registry, United States of America

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  • Rita K. Schmutzler,

    Affiliation: Center for Familial Breast and Ovarian Cancer and Center of Integrated Oncology, University of Cologne, Cologne, Germany

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  • Barbara Wappenschmidt,

    Affiliation: Center for Familial Breast and Ovarian Cancer and Center of Integrated Oncology, University of Cologne, Cologne, Germany

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  • Alfons Meindl,

    Affiliation: Department of Obstetrics and Gynaecology, Klinikum rechts der Isar, Technical University, Munich, Germany

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  • Norbert Arnold,

    Affiliation: Division of Oncology, Department of Gynaecology and Obstetrics, University Hospital Schleswig-Holstein, Kiel, Germany

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  • Helmut Deissler,

    Affiliation: Department of Obstetrics and Gynecology, Ulm University, Ulm, Germany

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  • Raymonda Varon-Mateeva,

    Affiliation: Institut für Humangenetik, Charité-Universitätsmedizin Berlin, Berlin, Germany

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  • Christian Sutter,

    Affiliation: Institute of Human Genetics, University of Heidelberg, Heidelberg, Germany

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  • Dieter Niederacher,

    Affiliation: Division of Molecular Genetics, Department of Gynaecology and Obstetrics, Clinical Center University of Düsseldorf, Düsseldorf, Germany

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  • Evgeny Imyamitov,

    Affiliation: N. N. Petrov Institute of Oncology, Saint-Petersburg, Russian Federation

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  • Olga M. Sinilnikova,

    Affiliations: Unité Mixte de Génétique Constitutionnelle des Cancers Fréquents, Centre Hospitalier Universitaire de Lyon, Centre Léon Bérard, Lyon, France, Equipe labellisée LIGUE 2008, UMR5201 CNRS, Centre Léon Bérard, Université de Lyon, Lyon, France

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  • Dominique Stoppa-Lyonne,

    Affiliation: INSERM U509, Service de Génétique Oncologique, Institut Curie, Université Paris-Descartes, Paris, France

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  • Sylvie Mazoyer,

    Affiliation: Equipe labellisée LIGUE 2008, UMR5201 CNRS, Centre Léon Bérard, Université de Lyon, Lyon, France

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  • Carole Verny-Pierre,

    Affiliation: Equipe labellisée LIGUE 2008, UMR5201 CNRS, Centre Léon Bérard, Université de Lyon, Lyon, France

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  • Laurent Castera,

    Affiliation: INSERM U509, Service de Génétique Oncologique, Institut Curie, Université Paris-Descartes, Paris, France

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  • Antoine de Pauw,

    Affiliation: INSERM U509, Service de Génétique Oncologique, Institut Curie, Université Paris-Descartes, Paris, France

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  • Yves-Jean Bignon,

    Affiliation: Département d'Oncogénétique, Centre Jean Perrin, Université de Clermont-Ferrand, Clermont-Ferrand, France

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  • Nancy Uhrhammer,

    Affiliation: Département d'Oncogénétique, Centre Jean Perrin, Université de Clermont-Ferrand, Clermont-Ferrand, France

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  • Jean-Philippe Peyrat,

    Affiliation: Laboratoire d'Oncologie Moléculaire Humaine, Centre Oscar Lambret, Lille, France

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  • Philippe Vennin,

    Affiliation: Consultation d'Oncogénétique, Centre Oscar Lambret, Lille, France

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  • Sandra Fert Ferrer,

    Affiliation: Laboratoire de Génétique Chromosomique, Hôtel Dieu Centre Hospitalier, Chambéry, France

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  • Marie-Agnès Collonge-Rame,

    Affiliation: Service de Génétique-Histologie-Biologie du Développement et de la Reproduction, Centre Hospitalier Universitaire de Besançon, Besançon, France

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  • Isabelle Mortemousque,

    Affiliation: Service de Génétique, Centre Hospitalier Universitaire Bretonneau, Tours, France

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  • GEMO Study Collaborators,

    Affiliation: GEMO Study (Genetics Network “Groupe Génétique et Cancer”), Fédération Nationale des Centres de Lutte Contre le Cancer, France

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  • Amanda B. Spurdle,

    Affiliation: Queensland Institute of Medical Research, Brisbane, Australia

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  • Jonathan Beesley,

    Affiliation: Queensland Institute of Medical Research, Brisbane, Australia

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  • Xiaoqing Chen,

    Affiliation: Queensland Institute of Medical Research, Brisbane, Australia

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  • Sue Healey,

    Affiliation: Queensland Institute of Medical Research, Brisbane, Australia

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  • kConFab,

    Affiliation: The Kathleen Cuningham Foundation Consortium for Research into Familial Breast Cancer, Peter MacCallum Cancer Institute, East Melbourne, Australia

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  • Mary Helen Barcellos-Hoff,

    Affiliation: Life Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, United States of America

    Current address: Department of Radiation Oncology, New York University Langone School of Medicine, New York, New York, United States of America

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  • Marc Vidal,

    Affiliation: Center for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana-Farber Cancer Institute, and Department of Genetics, Harvard Medical School, Boston, Massachusetts, United States of America

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  • Stephen B. Gruber,

    Affiliation: Department of Internal Medicine, Epidemiology, Human Genetics, University of Michigan, Ann Arbor, Michigan, United States of America

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  • Conxi Lázaro,

    Affiliation: Genetic Counseling and Hereditary Cancer Programme, Catalan Institute of Oncology, IDIBELL and Girona Biomedical Research Institute (IdIBGi), Catalonia, Spain

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  • Gabriel Capellá,

    Affiliation: Genetic Counseling and Hereditary Cancer Programme, Catalan Institute of Oncology, IDIBELL and Girona Biomedical Research Institute (IdIBGi), Catalonia, Spain

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  • Lesley McGuffog,

    Affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom

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  • Katherine L. Nathanson,

    Affiliation: Abramson Cancer Center, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America

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  • Antonis C. Antoniou,

    Affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom

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  • Georgia Chenevix-Trench,

    Affiliation: Queensland Institute of Medical Research, Brisbane, Australia

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  • Markus C. Fleisch,

    Affiliation: Department of Obstetrics and Gynaecologie, Heinrich-Heine-University, Duesseldorf, Germany

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  • Víctor Moreno,

    Affiliations: Biomedical Research Centre Network for Epidemiology and Public Health, Spain, Biomarkers and Susceptibility Unit, Catalan Institute of Oncology, IDIBELL, L'Hospitalet, Catalonia, Spain

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  • Miguel Angel Pujana mail

    cmaxwell@cfri.ubc.ca (CAM); mapujana@ico.scs.es (MAP)

    Affiliations: Translational Research Laboratory, Catalan Institute of Oncology, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet, Catalonia, Spain, Biomedical Research Centre Network for Epidemiology and Public Health, Spain, Biomarkers and Susceptibility Unit, Catalan Institute of Oncology, IDIBELL, L'Hospitalet, Catalonia, Spain

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  • Published: November 15, 2011
  • DOI: 10.1371/journal.pbio.1001199

About the Authors

Christopher A. Maxwell, Laia Gómez-Baldó, Núria Bonifaci, Helena Aguilar, Alberto Villanueva, Alvaro Aytes, Jordi Serra-Musach, Gemma Aiza, Griselda Martrat, Ander Urruticoechea, Miguel Angel Pujana
Translational Research Laboratory, Catalan Institute of Oncology, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet, Catalonia, Spain
Javier Benítez, Ana Osorio, Ricardo Fernández-Ramires
Human Cancer Genetics Programme, Spanish National Cancer Research Centre, Madrid, Spain
Javier Benítez, Ana Osorio, Ricardo Fernández-Ramires
Biomedical Research Centre Network for Rare Diseases, Spain
Laia Gómez-Baldó, Núria Bonifaci, Elisabet Guinó, Víctor Moreno, Miguel Angel Pujana
Biomedical Research Centre Network for Epidemiology and Public Health, Spain
Núria Bonifaci, Elisabet Guinó, Jordi Serra-Musach, Víctor Moreno, Miguel Angel Pujana
Biomarkers and Susceptibility Unit, Catalan Institute of Oncology, IDIBELL, L'Hospitalet, Catalonia, Spain
Sylvain V. Costes, Mary Helen Barcellos-Hoff
Life Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, United States of America
Helen Chen, Gareth J. R. Evans, Pooja Mohan
Child and Family Research Institute, Vancouver, British Columbia, Canada
Isabel Català, Anna Petit
Department of Pathology, University Hospital of Bellvitge, IDIBELL, L'Hospitalet, Catalonia, Spain
Gad Rennert, Flavio Lejbkowicz
CHS National Cancer Control Center, Department of Community Medicine and Epidemiology, Carmel Medical Center and B. Rappaport Faculty of Medicine, Technion, Haifa, Israel
Paolo Peterlongo, Carla B. Ripamonti, Paolo Radice
Unit of Molecular Bases of Genetic Risk and Genetic Testing, Department of Preventive and Predictive Medicine, Fondazione IRCCS Istituto Nazionale Tumori, and IFOM Fondazione Istituto FIRC di Oncologia Molecolare, Milan, Italy
Siranoush Manoukian, Bernard Peissel, Carla B. Ripamonti
Unit of Medical Genetics, Department of Preventive and Predictive Medicine, Fondazione IRCCS Istituto Nazionale Tumori, Milan, Italy
Bernardo Bonanni
Division of Cancer Prevention and Genetics, Istituto Europeo di Oncologia, Milan, Italy
Alessandra Viel
Division of Experimental Oncology 1, Centro di Riferimento Oncologico, IRCCS, Aviano, Italy
Anna Allavena
Department of Genetics, Biology and Biochemistry, University of Turin, Turin, Italy
Loris Bernard
Department of Experimental Oncology, Istituto Europeo di Oncologia, and Consortium for Genomics Technology (Cogentech), Milan, Italy
Eitan Friedman, Bella Kaufman, Yael Laitman, Maya Dubrovsky, Roni Milgrom
The Susanne Levy Gertner Oncogenetics Unit, Institute of Human Genetics, Chaim Sheba Medical Center, Ramat Gan, Israel
Eitan Friedman
Sackler Faculty of Medicine, Tel Aviv University, Ramat Aviv, Israel
Anna Jakubowska, Cezary Cybulski, Bohdan Gorski, Katarzyna Jaworska, Katarzyna Durda, Grzegorz Sukiennicki, Jan Lubiński
International Hereditary Cancer Centre, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland
Yin Yao Shugart
Unit of Statistical Genetics, Division of Intramural Research Program, National Institute of Mental Health, National Institute of Health, Bethesda, Maryland, United States of America
Susan M. Domchek, Richard Letrero, Barbara L. Weber, Katherine L. Nathanson
Abramson Cancer Center, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America
Frans B. L. Hogervorst
Family Cancer Clinic, Department of Pathology, The Netherlands Cancer Institute, Amsterdam, the Netherlands
Matti A. Rookus
Department of Epidemiology, The Netherlands Cancer Institute, Amsterdam, the Netherlands
J. Margriet Collee
Department of Clinical Genetics, Rotterdam Family Cancer Clinic, Erasmus University Medical Center, Rotterdam, the Netherlands
Peter Devilee
Department of Genetic Epidemiology, Leiden University Medical Center, Leiden, the Netherlands
Marjolijn J. Ligtenberg
Department of Human Genetics, Radboud University Medical Center, Nijmegen, the Netherlands
Rob B. van der Luijt
Department of Clinical Molecular Genetics, Utrecht University Medical Center, Utrecht, the Netherlands
Cora M. Aalfs
Department of Clinical Genetics, Academic Medical Center, Amsterdam, the Netherlands
Quinten Waisfisz
Department of Clinical Genetics, VU University Medical Center, Amsterdam, the Netherlands
Juul Wijnen
Center for Human and Clinical Genetics, Leiden University Medical Center, Leiden, the Netherlands
Cornelis E. P. van Roozendaal
Department of Clinical Genetics, University Medical Center, Maastricht, the Netherlands
HEBON
Hereditary Breast and Ovarian Cancer Group, the Netherlands
EMBRACE, Douglas F. Easton, Susan Peock, Margaret Cook, Clare Oliver, Debra Frost, Lesley McGuffog, Antonis C. Antoniou
Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom
Patricia Harrington
Department of Oncology, University of Cambridge, Cambridge, United Kingdom
D. Gareth Evans, Fiona Lalloo
Genetic Medicine, Manchester Academic Health Sciences Centre, Central Manchester University Hospitals NHS Foundation Trust, Manchester, United Kingdom
Rosalind Eeles
The Oncogenetics Team, The Institute of Cancer Research and Royal Marsden NHS Foundation Trust, Surrey, United Kingdom
Louise Izatt
Clinical Genetics, Guy's and St. Thomas' NHS Foundation Trust, London, United Kingdom
Carol Chu
Yorkshire Regional Genetics Service, St. James's Hospital, Leeds, United Kingdom
Diana Eccles
Wessex Clinical Genetics Service, Princess Anne Hospital, Southampton, United Kingdom
Fiona Douglas
Institute of Human Genetics, Centre for Life, Newcastle Upon Tyne Hospitals NHS Trust, Newcastle upon Tyne, United Kingdom
Carole Brewer
Department of Clinical Genetics, Royal Devon & Exeter Hospital, Exeter, United Kingdom
Heli Nevanlinna, Tuomas Heikkinen
Department of Obstetrics and Gynecology, Helsinki University Central Hospital, Helsinki, Finland
Fergus J. Couch, Xianshu Wang
Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, Minnesota, United States of America
Noralane M. Lindor
Department of Medical Genetics, Mayo Clinic, Rochester, Minnesota, United States of America
Andrew K. Godwin
Department of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, Kansas, United States of America
Maria A. Caligo, Grazia Lombardi
Section of Genetic Oncology, Department of Oncology, University of Pisa, and Department of Laboratory Medicine, University Hospital of Pisa, Pisa, Italy
Niklas Loman
Department of Oncology, Lund University Hospital, Lund, Sweden
Per Karlsson
Department of Oncology, Sahlgrenska University Hospital, Gothenburg, Sweden
Hans Ehrencrona
Department of Genetics and Pathology, Rudbeck Laboratory, Uppsala University, Uppsala, Sweden
Anna von Wachenfeldt
Department of Oncology, Karolinska University Hospital, Stockholm, Sweden
SWE-BRCA
Swedish Breast Cancer Study, Sweden
Rosa Bjork Barkardottir
Department of Pathology, Landspitali-University Hospital, Reykjavik, Iceland
Ute Hamann
Molecular Genetics of Breast Cancer, Deutsches Krebsforschungszentrum, Heidelberg, Germany
Muhammad U. Rashid
Molecular Genetics of Breast Cancer, Deutsches Krebsforschungszentrum, Heidelberg, Germany, and Department of Basic Sciences, Shaukat Khanum Memorial Cancer Hospital and Research Centre, Lahore, Pakistan
Adriana Lasa
Genetic Service, Hospital de la Santa Creu i Sant Pau, Barcelona, Catalonia, Spain
Trinidad Caldés
Molecular Oncology Laboratory, Hospital Clínico San Carlos, Madrid, Spain
Raquel Andrés
Medical Oncology Division, Hospital Clínico de Zaragoza, Zaragoza, Spain
Michael Schmitt
Department of Internal Medicine III, University of Rostock, Rostock, Germany
Volker Assmann
Center for Experimental Medicine, Institute of Tumor Biology, University Hospital Hamburg–Eppendorf, Hamburg, Germany
Kristen Stevens
Department of Epidemiology, University of Michigan, Ann Arbor, Michigan, United States of America
Kenneth Offit
Clinical Genetics Service, Department of Medicine, Memorial Sloan-Kettering Cancer Center, New York, New York, United States of America
João Curado, Hagen Tilgner, Roderic Guigó
Bioinformatics and Genomics Group, Centre for Genomic Regulation (CRG), Biomedical Research Park of Barcelona (PRBB), Barcelona, Catalonia, Spain
Joan Brunet, Joan Castellsagué, Ignacio Blanco, Conxi Lázaro, Gabriel Capellá
Genetic Counseling and Hereditary Cancer Programme, Catalan Institute of Oncology, IDIBELL and Girona Biomedical Research Institute (IdIBGi), Catalonia, Spain
Laima Tihomirova
Latvian Biomedical Research and Study Center, Riga, Latvia
David E. Goldgar
Department of Dermatology, University of Utah School of Medicine, Salt Lake City, Utah, United States of America
Saundra Buys
Department of Internal Medicine, Huntsman Cancer Institute, Salt Lake City, Utah, United States of America
Esther M. John
Cancer Prevention Institute of California, Fremont, California, United States of America
Alexander Miron
Department of Cancer Biology, Dana-Farber Cancer Institute, and Department of Surgery, Harvard Medical School, Boston, Massachusetts, United States of America
Melissa Southey
Centre for Molecular, Environmental, Genetic and Analytic (MEGA) Epidemiology, Melbourne School of Population Health, The University of Melbourne, Victoria, Australia
Mary B. Daly
Division of Population Science, Fox Chase Cancer Center, Philadelphia, Pennsylvania, United States of America
BCFR
Breast Cancer Family Registry, United States of America
Rita K. Schmutzler, Barbara Wappenschmidt
Center for Familial Breast and Ovarian Cancer and Center of Integrated Oncology, University of Cologne, Cologne, Germany
Alfons Meindl
Department of Obstetrics and Gynaecology, Klinikum rechts der Isar, Technical University, Munich, Germany
Norbert Arnold
Division of Oncology, Department of Gynaecology and Obstetrics, University Hospital Schleswig-Holstein, Kiel, Germany
Helmut Deissler
Department of Obstetrics and Gynecology, Ulm University, Ulm, Germany
Raymonda Varon-Mateeva
Institut für Humangenetik, Charité-Universitätsmedizin Berlin, Berlin, Germany
Christian Sutter
Institute of Human Genetics, University of Heidelberg, Heidelberg, Germany
Dieter Niederacher
Division of Molecular Genetics, Department of Gynaecology and Obstetrics, Clinical Center University of Düsseldorf, Düsseldorf, Germany
Evgeny Imyamitov
N. N. Petrov Institute of Oncology, Saint-Petersburg, Russian Federation
Olga M. Sinilnikova
Unité Mixte de Génétique Constitutionnelle des Cancers Fréquents, Centre Hospitalier Universitaire de Lyon, Centre Léon Bérard, Lyon, France
Olga M. Sinilnikova, Sylvie Mazoyer, Carole Verny-Pierre
Equipe labellisée LIGUE 2008, UMR5201 CNRS, Centre Léon Bérard, Université de Lyon, Lyon, France
Dominique Stoppa-Lyonne, Laurent Castera, Antoine de Pauw
INSERM U509, Service de Génétique Oncologique, Institut Curie, Université Paris-Descartes, Paris, France
Yves-Jean Bignon, Nancy Uhrhammer
Département d'Oncogénétique, Centre Jean Perrin, Université de Clermont-Ferrand, Clermont-Ferrand, France
Jean-Philippe Peyrat
Laboratoire d'Oncologie Moléculaire Humaine, Centre Oscar Lambret, Lille, France
Philippe Vennin
Consultation d'Oncogénétique, Centre Oscar Lambret, Lille, France
Sandra Fert Ferrer
Laboratoire de Génétique Chromosomique, Hôtel Dieu Centre Hospitalier, Chambéry, France
Marie-Agnès Collonge-Rame
Service de Génétique-Histologie-Biologie du Développement et de la Reproduction, Centre Hospitalier Universitaire de Besançon, Besançon, France
Isabelle Mortemousque
Service de Génétique, Centre Hospitalier Universitaire Bretonneau, Tours, France
GEMO Study Collaborators
GEMO Study (Genetics Network “Groupe Génétique et Cancer”), Fédération Nationale des Centres de Lutte Contre le Cancer, France
Amanda B. Spurdle, Jonathan Beesley, Xiaoqing Chen, Sue Healey, Georgia Chenevix-Trench
Queensland Institute of Medical Research, Brisbane, Australia
kConFab
The Kathleen Cuningham Foundation Consortium for Research into Familial Breast Cancer, Peter MacCallum Cancer Institute, East Melbourne, Australia
Marc Vidal
Center for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana-Farber Cancer Institute, and Department of Genetics, Harvard Medical School, Boston, Massachusetts, United States of America
Stephen B. Gruber
Department of Internal Medicine, Epidemiology, Human Genetics, University of Michigan, Ann Arbor, Michigan, United States of America
Markus C. Fleisch
Department of Obstetrics and Gynaecologie, Heinrich-Heine-University, Duesseldorf, Germany

Corresponding Authors

Competing Interests

The authors have declared that no competing interests exist.

Author Contributions

The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: CAM J Benitez MAP. Performed the experiments: CAM LG-B AO RF-R SVC HC GJRE PM HA A Villanueva A Aytes GA J Castellsagué DN MCF MAP. Analyzed the data: NB EG IC AP JS-M GR FLejbkowicz RL WLB JCurado HT RG SBG CL LM KLN ACA VM MAP. Contributed reagents/materials/analysis tools: CAM JBenitez AO GR FLejbkowicz PP S Manoukian BP CBR BB A Viel AAllavena LB PR EF BK YL MD RM AJ CCybulski BG KJ KD GS JL YYS SMD RL BLW FBLH MAR JMC PD MJL RBvdL CMA QW JW CEPvR HEBON EMBRACE DFE SP MC CO DF PH DGE FLalloo RE LI CChu DE FD CB HN TH FJC NML XW AKG MAC GL NL PK HE AvW SWE-BRCA RBB UH MUR AL TC RA MS VA KS KO JBrunet GM AU IB LT DEG SB EMJ AM MS MBD BCFR RKS BW AM NA HD RV-M CS DN EI OMS DS-L SMazoyer CV-P LC AdP Y-JB NU J-PP PV SFF M-AC-R IM GEMO ABS JBeesley XC SH kConFab MHB-H MV CL GC LM KLN ACA GC-T MCF VM MAP. Wrote the paper: CAM MAP.