title: Breast cancer risk variants at 6q25 display different phenotype associations and regulate ESR1, RMND1 and CCDC170.
abstract: We analyzed 3,872 common genetic variants across the ESR1 locus (encoding estrogen receptor α) in 118,816 subjects from three international consortia. We found evidence for at least five independent causal variants, each associated with different phenotype sets, including estrogen receptor (ER(+) or ER(-)) and human ERBB2 (HER2(+) or HER2(-)) tumor subtypes, mammographic density and tumor grade. The best candidate causal variants for ER(-) tumors lie in four separate enhancer elements, and their risk alleles reduce expression of ESR1, RMND1 and CCDC170, whereas the risk alleles of the strongest candidates for the remaining independent causal variant disrupt a silencer element and putatively increase ESR1 and RMND1 expression.
authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.
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authors.lastname: Dunning
authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
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authors.lastname: Michailidou
authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
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authors.lastname: Kuchenbaecker
authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
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authors.lastname: Thompson
authors.affiliation: Cancer Division, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
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authors.initials: JD
authors.lastname: French
authors.affiliation: Cancer Division, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
authors.forename: Jonathan
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authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.
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authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.
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authors.lastname: Kar
authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
authors.forename: Karen A
authors.initials: KA
authors.lastname: Pooley
authors.affiliation: Breast Cancer Research, Breakthrough Breast Cancer Research Centre, London, UK.|Academic Biochemistry, Royal Marsden Hospital, London, UK.
authors.forename: Elena
authors.initials: E
authors.lastname: Lopez-Knowles
authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.
authors.forename: Ed
authors.initials: E
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authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
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authors.affiliation: Department of Genetics, Stanford University School of Medicine, Stanford, California, USA.
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authors.initials: NA
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authors.affiliation: Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.
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authors.affiliation: Cancer Division, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
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authors.initials: KM
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authors.affiliation: Cancer Division, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
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authors.affiliation: Cancer Division, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
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authors.affiliation: Cancer Division, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
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authors.affiliation: Cancer Division, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
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authors.affiliation: Academic Biochemistry, Royal Marsden Hospital, London, UK.
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authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
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authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
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authors.affiliation: Department of Gynecology and Obstetrics, University Hospital Erlangen, Friedrich Alexander University Erlangen-Nuremberg, Comprehensive Cancer Center Erlangen-Nuremberg Metropolitan Region, Erlangen, Germany.
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authors.initials: MW
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authors.affiliation: Department of Gynecology and Obstetrics, University Hospital Erlangen, Friedrich Alexander University Erlangen-Nuremberg, Comprehensive Cancer Center Erlangen-Nuremberg Metropolitan Region, Erlangen, Germany.|Department of Medicine, Division of Hematology and Oncology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California, USA.
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authors.affiliation: Department of Non-Communicable Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, UK.
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authors.initials: I
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authors.affiliation: National Center for Tumor Diseases, University of Heidelberg, Heidelberg, Germany.|Department of Obstetrics and Gynecology, University of Heidelberg, Heidelberg, Germany.
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authors.initials: F
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authors.affiliation: Environmental Epidemiology of Cancer, Center for Research in Epidemiology and Population Health, INSERM, Villejuif, France.|University Paris-Sud, Villejuif, France.
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authors.initials: T
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authors.initials: SE
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authors.affiliation: Department of Breast Surgery, Herlev Hospital, Copenhagen University Hospital, Herlev, Denmark.
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authors.affiliation: Department of Gynaecology and Obstetrics, Technical University of Munich, Munich, Germany.
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authors.affiliation: Division of Molecular Gyneco-Oncology, Department of Gynaecology and Obstetrics, University Hospital of Cologne, Cologne, Germany.|Centre of Familial Breast and Ovarian Cancer, University Hospital of Cologne, Cologne, Germany.|Center for Integrated Oncology, University Hospital, Cologne, Germany.
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authors.initials: RK
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authors.affiliation: German Cancer Consortium, German Cancer Research Center, Heidelberg, Germany.|Dr. Margarete Fischer-Bosch Institute of Clinical Pharmacology, Stuttgart, Germany.|University of Tübingen, Tübingen, Germany.
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authors.forename: Sara
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authors.affiliation: Cancer Center, Kuopio University Hospital, Kuopio, Finland.|Institute of Clinical Medicine, Pathology and Forensic Medicine, University of Eastern Finland, Kuopio, Finland.|Imaging Center, Department of Clinical Pathology, Kuopio University Hospital, Kuopio, Finland.
authors.forename: Veli-Matti
authors.initials: VM
authors.lastname: Kosma
authors.affiliation: Cancer Center, Kuopio University Hospital, Kuopio, Finland.|Institute of Clinical Medicine, Pathology and Forensic Medicine, University of Eastern Finland, Kuopio, Finland.|Imaging Center, Department of Clinical Pathology, Kuopio University Hospital, Kuopio, Finland.
authors.forename: Arto
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authors.affiliation: Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
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authors.initials: CC
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authors.affiliation: Vesalius Research Center, Leuven, Belgium.|Laboratory for Translational Genetics, Department of Oncology, University of Leuven, Leuven, Belgium.
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authors.initials: D
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authors.affiliation: Multidisciplinary Breast Center, Department of General Medical Oncology, University Hospitals Leuven, Leuven, Belgium.
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authors.initials: H
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authors.affiliation: Division of Cancer Epidemiology, German Cancer Research Center, Heidelberg, Germany.|University Cancer Center Hamburg (UCCH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
authors.forename: Jenny
authors.initials: J
authors.lastname: Chang-Claude
authors.affiliation: Division of Cancer Epidemiology, German Cancer Research Center, Heidelberg, Germany.
authors.forename: Anja
authors.initials: A
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authors.affiliation: IFOM, Fondazione Istituto FIRC di Oncologia Molecolare, Milan, Italy.
authors.forename: Paolo
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authors.affiliation: Unit of Molecular Basis of Genetic Risk and Genetic Testing, Department of Preventive and Predictive Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.
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authors.affiliation: Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota, USA.
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authors.initials: JE
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authors.affiliation: Centre for Epidemiology and Biostatistics, School of Population and Global Health, University of Melbourne, Melbourne, Victoria, Australia.|Cancer Epidemiology Centre, Cancer Council Victoria, Melbourne, Victoria, Australia.
authors.forename: Graham G
authors.initials: GG
authors.lastname: Giles
authors.affiliation: Centre for Epidemiology and Biostatistics, School of Population and Global Health, University of Melbourne, Melbourne, Victoria, Australia.|Cancer Epidemiology Centre, Cancer Council Victoria, Melbourne, Victoria, Australia.
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authors.initials: RL
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authors.affiliation: Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
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authors.initials: CA
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authors.affiliation: Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
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authors.initials: BE
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authors.affiliation: Department of Medicine, McGill University, Montreal, Quebec, Canada.|Division of Clinical Epidemiology, Royal Victoria Hospital, McGill University, Montreal, Quebec, Canada.
authors.forename: Mark S
authors.initials: MS
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authors.affiliation: Cancer Research Initiatives Foundation, Sime Darby Medical Centre, Subang Jaya, Malaysia.|Breast Cancer Research Unit, University Malaya Cancer Research Institute, University Malaya Medical Centre, Kuala Lumpur, Malaysia.
authors.forename: Soo H
authors.initials: SH
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authors.affiliation: Breast Cancer Research Unit, University Malaya Cancer Research Institute, University Malaya Medical Centre, Kuala Lumpur, Malaysia.
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authors.affiliation: Department of Genetics, Institute for Cancer Research, Oslo University Hospital, Radiumhospitalet, Oslo, Norway.
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authors.initials: S
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authors.affiliation: Department of Genetics, Institute for Cancer Research, Oslo University Hospital, Radiumhospitalet, Oslo, Norway.|Institute of Clinical Medicine, University of Oslo, Oslo, Norway.
authors.forename: Anne-Lise
authors.initials: AL
authors.lastname: Borresen-Dale
authors.affiliation: Department of Genetics, Institute for Cancer Research, Oslo University Hospital, Radiumhospitalet, Oslo, Norway.|Institute of Clinical Medicine, University of Oslo, Oslo, Norway.|Department of Clinical Molecular Biology, Oslo University Hospital, University of Oslo, Oslo, Norway.
authors.forename: Vessela
authors.initials: V
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authors.initials: J
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authors.affiliation: Division of Epidemiology, Department of Medicine, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, Tennessee, USA.
authors.forename: Wei
authors.initials: W
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authors.affiliation: Laboratory of Cancer Genetics and Tumor Biology, Department of Clinical Chemistry and Biocenter Oulu, University of Oulu, NordLab Oulu University Hospital, Oulu, Finland.|Laboratory of Cancer Genetics and Tumor Biology, Northern Finland Laboratory Centre NordLab, Oulu, Finland.
authors.forename: Katri
authors.initials: K
authors.lastname: Pylkäs
authors.affiliation: Laboratory of Cancer Genetics and Tumor Biology, Department of Clinical Chemistry and Biocenter Oulu, University of Oulu, NordLab Oulu University Hospital, Oulu, Finland.|Laboratory of Cancer Genetics and Tumor Biology, Northern Finland Laboratory Centre NordLab, Oulu, Finland.
authors.forename: Robert
authors.initials: R
authors.lastname: Winqvist
authors.affiliation: Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Toronto, Ontario, Canada.|Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada.
authors.forename: Irene L
authors.initials: IL
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authors.affiliation: Prosserman Centre for Health Research, Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Toronto, Ontario, Canada.|Division of Epidemiology, Dalla Lana School of Public Health, University of Toronto, Toronto, Ontario, Canada.
authors.forename: Julia A
authors.initials: JA
authors.lastname: Knight
authors.affiliation: Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands.|Department of Human Genetics, Leiden University Medical Center, Leiden, the Netherlands.
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authors.initials: P
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authors.affiliation: Department of Medical Oncology, Erasmus University Medical Center, Rotterdam, the Netherlands.
authors.forename: Caroline
authors.initials: C
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authors.affiliation: Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, Maryland, USA.
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authors.initials: J
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authors.affiliation: Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, Maryland, USA.
authors.forename: Mark E
authors.initials: ME
authors.lastname: Sherman
authors.affiliation: Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
authors.forename: Kamila
authors.initials: K
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authors.affiliation: Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
authors.forename: Hatef
authors.initials: H
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authors.affiliation: Department of Medical Oncology, Erasmus University Medical Center, Rotterdam, the Netherlands.
authors.forename: Antoinette
authors.initials: A
authors.lastname: Hollestelle
authors.affiliation: Department of Clinical Genetics, Erasmus University Medical Center, Rotterdam, the Netherlands.
authors.forename: Ans M W
authors.initials: AM
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authors.affiliation: Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
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authors.initials: K
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authors.affiliation: Department of Epidemiology, Shanghai Cancer Institute, Shanghai, China.
authors.forename: Yu-Tang
authors.initials: YT
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authors.affiliation: Division of Epidemiology, Department of Medicine, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, Tennessee, USA.
authors.forename: Xiao-Ou
authors.initials: XO
authors.lastname: Shu
authors.affiliation: Sheffield Cancer Research, Department of Oncology, University of Sheffield, Sheffield, UK.
authors.forename: Angela
authors.initials: A
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authors.affiliation: Academic Unit of Pathology, Department of Neuroscience, University of Sheffield, Sheffield, UK.
authors.forename: Simon S
authors.initials: SS
authors.lastname: Cross
authors.affiliation: Division of Epidemiology, Department of Medicine, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, Tennessee, USA.|International Epidemiology Institute, Rockville, Maryland, USA.
authors.forename: William
authors.initials: W
authors.lastname: Blot
authors.affiliation: Division of Epidemiology, Department of Medicine, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, Tennessee, USA.
authors.forename: Qiuyin
authors.initials: Q
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authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.
authors.forename: Maya
authors.initials: M
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authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.
authors.forename: Barbara J
authors.initials: BJ
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authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.
authors.forename: Mitul
authors.initials: M
authors.lastname: Shah
authors.affiliation: Department of Preventive Medicine, Seoul National University College of Medicine, Seoul, Korea.|Department of Biomedical Sciences, Seoul National University College of Medicine, Seoul, Korea.
authors.forename: Ji-Yeob
authors.initials: JY
authors.lastname: Choi
authors.affiliation: Department of Preventive Medicine, Seoul National University College of Medicine, Seoul, Korea.|Department of Biomedical Sciences, Seoul National University College of Medicine, Seoul, Korea.|Cancer Research Institute, Seoul National University College of Medicine, Seoul, Korea.
authors.forename: Daehee
authors.initials: D
authors.lastname: Kang
authors.affiliation: Department of Haematology-Oncology, National University Health System, Singapore.|Cancer Science Institute of Singapore, National University of Singapore, Singapore.
authors.forename: Soo Chin
authors.initials: SC
authors.lastname: Lee
authors.affiliation: Saw Swee Hock School of Public Health, National University of Singapore, Singapore.|Department of Surgery, National University Health System, Singapore.
authors.forename: Mikael
authors.initials: M
authors.lastname: Hartman
authors.affiliation: Molecular Genetics of Breast Cancer, German Cancer Research Center, Heidelberg, Germany.
authors.forename: Maria
authors.initials: M
authors.lastname: Kabisch
authors.affiliation: Molecular Genetics of Breast Cancer, German Cancer Research Center, Heidelberg, Germany.|Institute of Human Genetics, Pontificia Universidad Javerianar, Bogota, Colombia.
authors.forename: Diana
authors.initials: D
authors.lastname: Torres
authors.affiliation: Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland.
authors.forename: Anna
authors.initials: A
authors.lastname: Jakubowska
authors.affiliation: Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland.
authors.forename: Jan
authors.initials: J
authors.lastname: Lubinski
authors.affiliation: International Agency for Research on Cancer, Lyon, France.
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authors.initials: P
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authors.affiliation: National Cancer Institute, Bangkok, Thailand.
authors.forename: Suleeporn
authors.initials: S
authors.lastname: Sangrajrang
authors.affiliation: Roswell Park Cancer Institute, Buffalo, New York, USA.
authors.forename: Christine B
authors.initials: CB
authors.lastname: Ambrosone
authors.affiliation: Department of Molecular Virology, Immunology and Medical Genetics, Comprehensive Cancer Center, The Ohio State University, Columbus, Ohio, USA.
authors.forename: Amanda E
authors.initials: AE
authors.lastname: Toland
authors.affiliation: School of Public Health, China Medical University, Taichung, Taiwan.|Taiwan Biobank, Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan.
authors.forename: Chen-Yang
authors.initials: CY
authors.lastname: Shen
authors.affiliation: Taiwan Biobank, Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan.
authors.forename: Pei-Ei
authors.initials: PE
authors.lastname: Wu
authors.affiliation: Division of Cancer Studies, Breakthrough Breast Cancer Research Centre, Institute of Cancer Research, London, UK.
authors.forename: Nick
authors.initials: N
authors.lastname: Orr
authors.affiliation: Division of Genetics and Epidemiology, Institute of Cancer Research, London, UK.|Division of Breast Cancer Research, Institute of Cancer Research, London, UK.
authors.forename: Anthony
authors.initials: A
authors.lastname: Swerdlow
authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
authors.forename: Lesley
authors.initials: L
authors.lastname: McGuffog
authors.affiliation: Cancer Division, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
authors.forename: Sue
authors.initials: S
authors.lastname: Healey
authors.affiliation: Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
authors.forename: Andrew
authors.initials: A
authors.lastname: Lee
authors.affiliation: Centre for Epidemiology and Biostatistics, University of Melbourne, Melbourne, Victoria, Australia.
authors.forename: Miroslav
authors.initials: M
authors.lastname: Kapuscinski
authors.affiliation: Department of Epidemiology, Cancer Prevention Institute of California, Fremont, California, USA.
authors.forename: Esther M
authors.initials: EM
authors.lastname: John
authors.affiliation: Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, New York, USA.
authors.forename: Mary Beth
authors.initials: MB
authors.lastname: Terry
authors.affiliation: Department of Clinical Genetics, Fox Chase Cancer Center, Philadelphia, Pennsylvania, USA.
authors.forename: Mary B
authors.initials: MB
authors.lastname: Daly
authors.affiliation: Department of Dermatology, Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, Utah, USA.
authors.forename: David E
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mesh_terms: D001483:Base Sequence; D001943:Breast Neoplasms / Q000235:genetics* / Q000378:metabolism; D002352:Carrier Proteins / Q000235:genetics* / Q000378:metabolism; D018797:Cell Cycle Proteins / Q000235:genetics* / Q000378:metabolism; D002896:Chromosomes, Human, Pair 6 / Q000235:genetics*; D047628:Estrogen Receptor alpha / Q000235:genetics* / Q000378:metabolism; D005260:Female; D015870:Gene Expression; D015972:Gene Expression Regulation, Neoplastic; D056726:Genetic Association Studies; D020022:Genetic Predisposition to Disease; D006801:Humans; D010641:Phenotype; D020641:Polymorphism, Single Nucleotide; D011485:Protein Binding; D012307:Risk Factors
chemical_list: C000599973:CCDC170 protein, human; D002352:Carrier Proteins; D018797:Cell Cycle Proteins; C506487:ESR1 protein, human; D047628:Estrogen Receptor alpha; C578871:RMND1 protein, human