A transcriptome-wide association study of 229,000 women identifies new candidate susceptibility genes for breast cancer

Lang Wu¹, Wei Shi², Jirong Long¹, Xingyi Guo¹, Kyriaki Michailidou^{3

4}, Jonathan Beesley², Manjeet K Bolla³, Xiao-Ou Shu¹, Yingchang Lu¹, Qiuyin Cai¹, Fares Al-Ejeh², Esdy Rozali², Qin Wang³, Joe Dennis³, Bingshan Li⁵, Chenjie Zeng¹, Helian Feng^{6

7}, Alexander Gusev^{8

9

10}, Richard T Barfield⁶, Irene L Andrulis^{11

12}, Hoda Anton-Culver¹³, Volker Arndt¹⁴, Kristan J Aronson¹⁵, Paul L Auer^{16

17}, Myrto Barrdahl¹⁸, Caroline Baynes¹⁹, Matthias W Beckmann²⁰, Javier Benitez^{21

22}, Marina Bermisheva^{23

24}, Carl Blomqvist^{25

26}, Natalia V Bogdanova^{24

27

28}, Stig E Bojesen^{29

30

31}, Hiltrud Brauch^{32

33

34}, Hermann Brenner^{14

34

35}, Louise Brinton³⁶, Per Broberg³⁷, Sara Y Brucker³⁸, Barbara Burwinkel^{39

40}, Trinidad Caldés⁴¹, Federico Canzian⁴², Brian D Carter⁴³, J Esteban Castelao⁴⁴, Jenny Chang-Claude^{18

45}, Xiaoqing Chen², Ting-Yuan David Cheng⁴⁶, Hans Christiansen²⁷, Christine L Clarke⁴⁷; NBCS Collaborators; Margriet Collée⁴⁸, Sten Cornelissen⁴⁹, Fergus J Couch⁵⁰, David Cox^{51

52}, Angela Cox⁵³, Simon S Cross⁵⁴, Julie M Cunningham⁵⁰, Kamila Czene⁵⁵, Mary B Daly⁵⁶, Peter Devilee^{57

58}, Kimberly F Doheny⁵⁹, Thilo Dörk²⁴, Isabel Dos-Santos-Silva⁶⁰, Martine Dumont⁶¹, Miriam Dwek⁶², Diana M Eccles⁶³, Ursula Eilber¹⁸, A Heather Eliassen^{7

64}, Christoph Engel⁶⁵, Mikael Eriksson⁵⁵, Laura Fachal¹⁹, Peter A Fasching^{20

66}, Jonine Figueroa^{36

67}, Dieter Flesch-Janys^{68

69}, Olivia Fletcher⁷⁰, Henrik Flyger⁷¹, Lin Fritschi⁷², Marike Gabrielson⁵⁵, Manuela Gago-Dominguez^{73

74}, Susan M Gapstur⁴³, Montserrat García-Closas³⁶, Mia M Gaudet⁴³, Maya Ghoussaini¹⁹, Graham G Giles^{75

76}, Mark S Goldberg^{77

78}, David E Goldgar⁷⁹, Anna González-Neira²¹, Pascal Guénel⁸⁰, Eric Hahnen^{81

82

83}, Christopher A Haiman⁸⁴, Niclas Håkansson⁸⁵, Per Hall^{55

86}, Emily Hallberg⁸⁷, Ute Hamann⁸⁸, Patricia Harrington¹⁹, Alexander Hein²⁰, Belynda Hicks⁸⁹, Peter Hillemanns²⁴, Antoinette Hollestelle⁹⁰, Robert N Hoover³⁶, John L Hopper⁷⁶, Guanmengqian Huang⁸⁸, Keith Humphreys⁵⁵, David J Hunter^{7

91}, Anna Jakubowska^{92

93}, Wolfgang Janni⁹⁴, Esther M John^{95

96

97}, Nichola Johnson⁷⁰, Kristine Jones⁸⁹, Michael E Jones⁹⁸, Audrey Jung¹⁸, Rudolf Kaaks¹⁸, Michael J Kerin⁹⁹, Elza Khusnutdinova^{97

100}, Veli-Matti Kosma^{101

102

103}, Vessela N Kristensen^{104

105

106}, Diether Lambrechts^{107

108}, Loic Le Marchand¹⁰⁹, Jingmei Li¹¹⁰, Sara Lindström^{111

112}, Jolanta Lissowska¹¹³, Wing-Yee Lo^{32

33}, Sibylle Loibl¹¹⁴, Jan Lubinski⁹⁰, Craig Luccarini¹⁹, Michael P Lux²⁰, Robert J MacInnis^{75

76}, Tom Maishman¹¹⁵, Ivana Maleva Kostovska^{24

116}, Arto Mannermaa^{101

102

103}, JoAnn E Manson^{7

117}, Sara Margolin¹¹⁸, Dimitrios Mavroudis¹¹⁹, Hanne Meijers-Heijboer¹²⁰, Alfons Meindl¹²¹, Usha Menon¹²², Jeffery Meyer⁵⁰, Anna Marie Mulligan^{123

124}, Susan L Neuhausen¹²⁵, Heli Nevanlinna¹²⁶, Patrick Neven¹²⁷, Sune F Nielsen^{29

30}, Børge G Nordestgaard^{29

30

31}, Olufunmilayo I Olopade¹²⁸, Janet E Olson⁸⁷, Håkan Olsson³⁷, Paolo Peterlongo¹²⁹, Julian Peto⁶⁰, Dijana Plaseska-Karanfilska¹¹⁶, Ross Prentice¹⁶, Nadege Presneau⁶², Katri Pylkäs^{130

131}, Brigitte Rack⁹⁴, Paolo Radice¹³², Nazneen Rahman¹³³, Gad Rennert¹³⁴, Hedy S Rennert¹³⁴, Valerie Rhenius¹⁹, Atocha Romero^{41

135}, Jane Romm⁵⁹, Anja Rudolph¹⁸, Emmanouil Saloustros¹³⁶, Dale P Sandler¹³⁷, Elinor J Sawyer¹³⁸, Marjanka K Schmidt^{49

139}, Rita K Schmutzler^{81

82

83}, Andreas Schneeweiss^{39

140}, Rodney J Scott^{141

142}, Christopher G Scott⁸⁷, Sheila Seal¹³³, Mitul Shah¹⁹, Martha J Shrubsole¹, Ann Smeets¹²⁷, Melissa C Southey¹⁴³, John J Spinelli^{144

145}, Jennifer Stone^{146

147}, Harald Surowy^{39

40}, Anthony J Swerdlow^{98

148}, Rulla M Tamimi^{6

7

64}, William Tapper⁶³, Jack A Taylor^{137

149}, Mary Beth Terry¹⁵⁰, Daniel C Tessier¹⁵¹, Abigail Thomas⁸⁷, Kathrin Thöne⁴⁵, Rob A E M Tollenaar¹⁵², Diana Torres^{88

153}, Thérèse Truong⁸⁰, Michael Untch¹⁵⁴, Celine Vachon⁸⁷, David Van Den Berg⁸⁴, Daniel Vincent¹⁵¹, Quinten Waisfisz¹³¹, Clarice R Weinberg¹⁵⁵, Camilla Wendt¹¹⁸, Alice S Whittemore^{96

97}, Hans Wildiers¹²⁷, Walter C Willett^{7

64

156}, Robert Winqvist^{130

131}, Alicja Wolk⁸⁵, Lucy Xia⁸⁴, Xiaohong R Yang³⁶, Argyrios Ziogas¹³, Elad Ziv¹⁵⁷; kConFab/AOCS Investigators; Alison M Dunning¹⁹, Paul D P Pharoah^{3

19}, Jacques Simard⁶¹, Roger L Milne^{75

76}, Stacey L Edwards², Peter Kraft^{6

7}, Douglas F Easton^{3

19}, Georgia Chenevix-Trench¹⁵⁸, Wei Zheng¹⁵⁹

Affiliations

¹ Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, TN, USA.
² Cancer Division, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
³ Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
⁴ Department of Electron Microscopy/Molecular Pathology, The Cyprus Institute of Neurology and Genetics, Nicosia, Cyprus.
⁵ Department of Molecular Physiology & Biophysics, Vanderbilt Genetics Institute, Vanderbilt University, Nashville, TN, USA.
⁶ Program in Genetic Epidemiology and Statistical Genetics, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
⁷ Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
⁸ Department of Medical Oncology, Dana Farber Cancer Institute, Boston, MA, USA.
⁹ Department of Medicine, Harvard Medical School, Boston, MA, USA.
¹⁰ Division of Genetics, Brigham and Women's Hospital, Boston, MA, USA.
¹¹ Fred A. Litwin Center for Cancer Genetics, Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Toronto, Ontario, Canada.
¹² Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada.
¹³ Department of Epidemiology, University of California Irvine, Irvine, CA, USA.
¹⁴ Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹⁵ Department of Public Health Sciences, and Cancer Research Institute, Queen's University, Kingston, Ontario, Canada.
¹⁶ Cancer Prevention Program, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
¹⁷ Zilber School of Public Health, University of Wisconsin-Milwaukee, Milwaukee, WI, USA.
¹⁸ Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹⁹ Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.
²⁰ Department of Gynaecology and Obstetrics, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg, Comprehensive Cancer Center Erlangen-EMN, Erlangen, Germany.
²¹ Human Cancer Genetics Program, Spanish National Cancer Research Centre, Madrid, Spain.
²² Centro de Investigación en Red de Enfermedades Raras (CIBERER), Valencia, Spain.
²³ Institute of Biochemistry and Genetics, Ufa Scientific Center of Russian Academy of Sciences, Ufa, Russia.
²⁴ Gynaecology Research Unit, Hannover Medical School, Hannover, Germany.
²⁵ Department of Oncology, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.
²⁶ Department of Oncology, University of Örebro, Örebro, Sweden.
²⁷ Department of Radiation Oncology, Hannover Medical School, Hannover, Germany.
²⁸ N.N. Alexandrov Research Institute of Oncology and Medical Radiology, Minsk, Belarus.
²⁹ Copenhagen General Population Study, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark.
³⁰ Department of Clinical Biochemistry, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark.
³¹ Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
³² Dr. Margarete Fischer-Bosch-Institute of Clinical Pharmacology, Stuttgart, Germany.
³³ University of Tübingen, Tübingen, Germany.
³⁴ German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.
³⁵ Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany.
³⁶ Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
³⁷ Department of Cancer Epidemiology, Clinical Sciences, Lund University, Lund, Sweden.
³⁸ Department of Gynecology and Obstetrics, University of Tübingen, Tübingen, Germany.
³⁹ Department of Obstetrics and Gynecology, University of Heidelberg, Heidelberg, Germany.
⁴⁰ Molecular Epidemiology Group, C080, German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁴¹ Medical Oncology Department, CIBERONC Hospital Clínico San Carlos, Madrid, Spain.
⁴² Genomic Epidemiology Group, German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁴³ Epidemiology Research Program, American Cancer Society, Atlanta, GA, USA.
⁴⁴ Oncology and Genetics Unit, Instituto de Investigacion Biomedica Galicia Sur (IISGS), Xerencia de Xestion Integrada de Vigo-SERGAS, Vigo, Spain.
⁴⁵ University Cancer Center Hamburg (UCCH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
⁴⁶ Department of Epidemiology, University of Florida, Gainesville, FL, USA.
⁴⁷ Westmead Institute for Medical Research, University of Sydney, Sydney, New South Wales, Australia.
⁴⁸ Department of Clinical Genetics, Erasmus University Medical Center, Rotterdam, The Netherlands.
⁴⁹ Division of Molecular Pathology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands.
⁵⁰ Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.
⁵¹ Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK.
⁵² INSERM U1052, Cancer Research Center of Lyon, Lyon, France.
⁵³ Sheffield Institute for Nucleic Acids, Department of Oncology and Metabolism, University of Sheffield, Sheffield, UK.
⁵⁴ Academic Unit of Pathology, Department of Neuroscience, University of Sheffield, Sheffield, UK.
⁵⁵ Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
⁵⁶ Department of Clinical Genetics, Fox Chase Cancer Center, Philadelphia, PA, USA.
⁵⁷ Department of Pathology, Leiden University Medical Center, Leiden, The Netherlands.
⁵⁸ Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands.
⁵⁹ Center for Inherited Disease Research (CIDR), Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
⁶⁰ Department of Non-Communicable Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, UK.
⁶¹ Genomics Center, Centre Hospitalier Universitaire de Québec - Université Laval Research Center, Québec City, QC, Canada.
⁶² Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, London, UK.
⁶³ Cancer Sciences Academic Unit, Faculty of Medicine, University of Southampton, Southampton, UK.
⁶⁴ Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
⁶⁵ Institute for Medical Informatics, Statistics and Epidemiology, University of Leipzig, Leipzig, Germany.
⁶⁶ David Geffen School of Medicine, Department of Medicine Division of Hematology and Oncology, University of California at Los Angeles, Los Angeles, CA, USA.
⁶⁷ Usher Institute of Population Health Sciences and Informatics, The University of Edinburgh Medical School, Edinburgh, UK.
⁶⁸ Institute for Medical Biometrics and Epidemiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
⁶⁹ Department of Cancer Epidemiology, Clinical Cancer Registry, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
⁷⁰ The Breast Cancer Now Toby Robins Research Centre, The Institute of Cancer Research, London, UK.
⁷¹ Department of Breast Surgery, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark.
⁷² School of Public Health, Curtin University, Perth, Western Australia, Australia.
⁷³ Genomic Medicine Group, Galician Foundation of Genomic Medicine, Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Complejo Hospitalario Universitario de Santiago, SERGAS, Santiago De Compostela, Spain.
⁷⁴ Moores Cancer Center, University of California San Diego, La Jolla, CA, USA.
⁷⁵ Cancer Epidemiology & Intelligence Division, Cancer Council Victoria, Melbourne, Victoria, Australia.
⁷⁶ Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia.
⁷⁷ Department of Medicine, McGill University, Montréal, Quebec, Canada.
⁷⁸ Division of Clinical Epidemiology, Royal Victoria Hospital, McGill University, Montréal, Quebec, Canada.
⁷⁹ Department of Dermatology, Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, UT, USA.
⁸⁰ Cancer & Environment Group, Center for Research in Epidemiology and Population Health (CESP), INSERM, University Paris-Sud, University Paris-Saclay, Villejuif, France.
⁸¹ Center for Hereditary Breast and Ovarian Cancer, University Hospital of Cologne, Cologne, Germany.
⁸² Center for Integrated Oncology (CIO), University Hospital of Cologne, Cologne, Germany.
⁸³ Center for Molecular Medicine Cologne (CMMC), University of Cologne, Cologne, Germany.
⁸⁴ Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
⁸⁵ Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
⁸⁶ Department of Oncology, Södersjukhuset, Stockholm, Sweden.
⁸⁷ Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA.
⁸⁸ Molecular Genetics of Breast Cancer, German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁸⁹ Cancer Genomics Research Laboratory, Leidos Biomedical Research, Frederick National Laboratory for Cancer Research, Frederick, MD, USA.
⁹⁰ Department of Medical Oncology, Family Cancer Clinic, Erasmus MC Cancer Institute, Rotterdam, The Netherlands.
⁹¹ Nuffield Department of Population Health, University of Oxford, Big Data Institute, Oxford, UK.
⁹² Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland.
⁹³ Independent Laboratory of Molecular Biology and Genetic Diagnostics, Pomeranian Medical University, Szczecin, Poland.
⁹⁴ Department of Gynecology and Obstetrics, University Hospital Ulm, Ulm, Germany.
⁹⁵ Department of Epidemiology, Cancer Prevention Institute of California, Fremont, CA, USA.
⁹⁶ Department of Health Research and Policy - Epidemiology, Stanford University School of Medicine, Stanford, CA, USA.
⁹⁷ Stanford Cancer Institute, Stanford University School of Medicine, Stanford, CA, USA.
⁹⁸ Division of Genetics and Epidemiology, The Institute of Cancer Research, London, UK.
⁹⁹ School of Medicine, National University of Ireland, Galway, Ireland.
¹⁰⁰ Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa, Russia.
¹⁰¹ Translational Cancer Research Area, University of Eastern Finland, Kuopio, Finland.
¹⁰² Institute of Clinical Medicine, Pathology and Forensic Medicine, University of Eastern Finland, Kuopio, Finland.
¹⁰³ Imaging Center, Department of Clinical Pathology, Kuopio University Hospital, Kuopio, Finland.
¹⁰⁴ Department of Cancer Genetics, Institute for Cancer Research, Oslo University Hospital Radiumhospitalet, Oslo, Norway.
¹⁰⁵ Institute of Clinical Medicine, Faculty of Medicine, University of Oslo, Oslo, Norway.
¹⁰⁶ Department of Clinical Molecular Biology, Oslo University Hospital, University of Oslo, Oslo, Norway.
¹⁰⁷ VIB KULeuven Center for Cancer Biology, VIB, Leuven, Belgium.
¹⁰⁸ Laboratory for Translational Genetics, Department of Human Genetics, KU Leuven, Leuven, Belgium.
¹⁰⁹ Epidemiology Program, University of Hawaii Cancer Center, Honolulu, HI, USA.
¹¹⁰ Human Genetics, Genome Institute of Singapore, Singapore, Singapore.
¹¹¹ Department of Epidemiology, University of Washington School of Public Health, Seattle, WA, USA.
¹¹² Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
¹¹³ Department of Cancer Epidemiology and Prevention, M. Sklodowska-Curie Institute - Oncology Center, Warsaw, Poland.
¹¹⁴ German Breast Group, GmbH, Neu Isenburg, Germany.
¹¹⁵ Southampton Clinical Trials Unit, University of Southampton, Southampton, UK.
¹¹⁶ Research Centre for Genetic Engineering and Biotechnology "Georgi D. Efremov", Macedonian Academy of Sciences and Arts, Skopje, Macedonia.
¹¹⁷ Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
¹¹⁸ Department of Oncology - Pathology, Karolinska Institutet, Stockholm, Sweden.
¹¹⁹ Department of Medical Oncology, University Hospital of Heraklion, Heraklion, Greece.
¹²⁰ Department of Clinical Genetics, VU University Medical Center, Amsterdam, The Netherlands.
¹²¹ Division of Gynaecology and Obstetrics, Technische Universität München, Munich, Germany.
¹²² Gynaecological Cancer Research Centre, Women's Cancer, Institute for Women's Health, University College London, London, UK.
¹²³ Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada.
¹²⁴ Laboratory Medicine Program, University Health Network, Toronto, Ontario, Canada.
¹²⁵ Department of Population Sciences, Beckman Research Institute of City of Hope, Duarte, CA, USA.
¹²⁶ Department of Obstetrics and Gynecology, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.
¹²⁷ Leuven Multidisciplinary Breast Center, Department of Oncology, Leuven Cancer Institute, University Hospitals Leuven, Leuven, Belgium.
¹²⁸ Center for Clinical Cancer Genetics and Global Health, The University of Chicago, Chicago, IL, USA.
¹²⁹ IFOM, The FIRC (Italian Foundation for Cancer Research) Institute of Molecular Oncology, Milan, Italy.
¹³⁰ Laboratory of Cancer Genetics and Tumor Biology, Cancer and Translational Medicine Research Unit, Biocenter Oulu, University of Oulu, Oulu, Finland.
¹³¹ Laboratory of Cancer Genetics and Tumor Biology, Northern Finland Laboratory Centre Oulu, Oulu, Finland.
¹³² Unit of Molecular Bases of Genetic Risk and Genetic Testing, Department of Research, Fondazione IRCCS (Istituto Di Ricovero e Cura a Carattere Scientifico) Istituto Nazionale dei Tumori (INT), Milan, Italy.
¹³³ Section of Cancer Genetics, The Institute of Cancer Research, London, UK.
¹³⁴ Department of Community Medicine and Epidemiology, Carmel Medical Center, Ruth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology and Clalit National Cancer Control Center, Haifa, Israel.
¹³⁵ Medical Oncology Department, Hospital Universitario Puerta de Hierro, Madrid, Spain.
¹³⁶ Hereditary Cancer Clinic, University Hospital of Heraklion, Heraklion, Greece.
¹³⁷ Epidemiology Branch, National Institute of Environmental Health Sciences, NIH, Research Triangle Park, NC, USA.
¹³⁸ Research Oncology, Guy's Hospital, King's College London, London, UK.
¹³⁹ Division of Psychosocial Research and Epidemiology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands.
¹⁴⁰ National Center for Tumor Diseases, University of Heidelberg, Heidelberg, Germany.
¹⁴¹ Division of Molecular Medicine, Pathology North, John Hunter Hospital, Newcastle, New South Wales, Australia.
¹⁴² Discipline of Medical Genetics, School of Biomedical Sciences and Pharmacy, Faculty of Health, University of Newcastle, Newcastle, New South Wales, Australia.
¹⁴³ Department of Pathology, The University of Melbourne, Melbourne, Victoria, Australia.
¹⁴⁴ Cancer Control Research, BC Cancer Agency, Vancouver, British Columbia, Canada.
¹⁴⁵ School of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada.
¹⁴⁶ The Curtin UWA Centre for Genetic Origins of Health and Disease, Curtin University and University of Western Australia, Perth, Western Australia, Australia.
¹⁴⁷ Department of Obstetrics and Gynaecology, University of Melbourne and the Royal Women's Hospital, Melbourne, Victoria, Australia.
¹⁴⁸ Division of Breast Cancer Research, The Institute of Cancer Research, London, UK.
¹⁴⁹ Epigenetic and Stem Cell Biology Laboratory, National Institute of Environmental Health Sciences, NIH, Research Triangle Park, NC, USA.
¹⁵⁰ Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY, USA.
¹⁵¹ McGill University and Génome Québec Innovation Centre, Montréal, Quebec, Canada.
¹⁵² Department of Surgery, Leiden University Medical Center, Leiden, The Netherlands.
¹⁵³ Institute of Human Genetics, Pontificia Universidad Javeriana, Bogota, Colombia.
¹⁵⁴ Department of Gynecology and Obstetrics, Helios Clinics Berlin-Buch, Berlin, Germany.
¹⁵⁵ Biostatistics and Computational Biology Branch, National Institute of Environmental Health Sciences, NIH, Research Triangle Park, NC, USA.
¹⁵⁶ Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
¹⁵⁷ Department of Medicine, Institute for Human Genetics, UCSF Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA.
¹⁵⁸ Cancer Division, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia. Georgia.Trench@qimrberghofer.edu.au.
¹⁵⁹ Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, TN, USA. wei.zheng@vanderbilt.edu.

PMID: 29915430
PMCID: PMC6314198
DOI: 10.1038/s41588-018-0132-x

A transcriptome-wide association study of 229,000 women identifies new candidate susceptibility genes for breast cancer

Lang Wu et al. Nat Genet. 2018 Jul.

. 2018 Jul;50(7):968-978.

doi: 10.1038/s41588-018-0132-x. Epub 2018 Jun 18.

Authors

Affiliations

¹ Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, TN, USA.
² Cancer Division, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
³ Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
⁴ Department of Electron Microscopy/Molecular Pathology, The Cyprus Institute of Neurology and Genetics, Nicosia, Cyprus.
⁵ Department of Molecular Physiology & Biophysics, Vanderbilt Genetics Institute, Vanderbilt University, Nashville, TN, USA.
⁶ Program in Genetic Epidemiology and Statistical Genetics, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
⁷ Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
⁸ Department of Medical Oncology, Dana Farber Cancer Institute, Boston, MA, USA.
⁹ Department of Medicine, Harvard Medical School, Boston, MA, USA.
¹⁰ Division of Genetics, Brigham and Women's Hospital, Boston, MA, USA.
¹¹ Fred A. Litwin Center for Cancer Genetics, Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Toronto, Ontario, Canada.
¹² Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada.
¹³ Department of Epidemiology, University of California Irvine, Irvine, CA, USA.
¹⁴ Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹⁵ Department of Public Health Sciences, and Cancer Research Institute, Queen's University, Kingston, Ontario, Canada.
¹⁶ Cancer Prevention Program, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
¹⁷ Zilber School of Public Health, University of Wisconsin-Milwaukee, Milwaukee, WI, USA.
¹⁸ Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹⁹ Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.
²⁰ Department of Gynaecology and Obstetrics, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg, Comprehensive Cancer Center Erlangen-EMN, Erlangen, Germany.
²¹ Human Cancer Genetics Program, Spanish National Cancer Research Centre, Madrid, Spain.
²² Centro de Investigación en Red de Enfermedades Raras (CIBERER), Valencia, Spain.
²³ Institute of Biochemistry and Genetics, Ufa Scientific Center of Russian Academy of Sciences, Ufa, Russia.
²⁴ Gynaecology Research Unit, Hannover Medical School, Hannover, Germany.
²⁵ Department of Oncology, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.
²⁶ Department of Oncology, University of Örebro, Örebro, Sweden.
²⁷ Department of Radiation Oncology, Hannover Medical School, Hannover, Germany.
²⁸ N.N. Alexandrov Research Institute of Oncology and Medical Radiology, Minsk, Belarus.
²⁹ Copenhagen General Population Study, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark.
³⁰ Department of Clinical Biochemistry, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark.
³¹ Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
³² Dr. Margarete Fischer-Bosch-Institute of Clinical Pharmacology, Stuttgart, Germany.
³³ University of Tübingen, Tübingen, Germany.
³⁴ German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.
³⁵ Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany.
³⁶ Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
³⁷ Department of Cancer Epidemiology, Clinical Sciences, Lund University, Lund, Sweden.
³⁸ Department of Gynecology and Obstetrics, University of Tübingen, Tübingen, Germany.
³⁹ Department of Obstetrics and Gynecology, University of Heidelberg, Heidelberg, Germany.
⁴⁰ Molecular Epidemiology Group, C080, German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁴¹ Medical Oncology Department, CIBERONC Hospital Clínico San Carlos, Madrid, Spain.
⁴² Genomic Epidemiology Group, German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁴³ Epidemiology Research Program, American Cancer Society, Atlanta, GA, USA.
⁴⁴ Oncology and Genetics Unit, Instituto de Investigacion Biomedica Galicia Sur (IISGS), Xerencia de Xestion Integrada de Vigo-SERGAS, Vigo, Spain.
⁴⁵ University Cancer Center Hamburg (UCCH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
⁴⁶ Department of Epidemiology, University of Florida, Gainesville, FL, USA.
⁴⁷ Westmead Institute for Medical Research, University of Sydney, Sydney, New South Wales, Australia.
⁴⁸ Department of Clinical Genetics, Erasmus University Medical Center, Rotterdam, The Netherlands.
⁴⁹ Division of Molecular Pathology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands.
⁵⁰ Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.
⁵¹ Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK.
⁵² INSERM U1052, Cancer Research Center of Lyon, Lyon, France.
⁵³ Sheffield Institute for Nucleic Acids, Department of Oncology and Metabolism, University of Sheffield, Sheffield, UK.
⁵⁴ Academic Unit of Pathology, Department of Neuroscience, University of Sheffield, Sheffield, UK.
⁵⁵ Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
⁵⁶ Department of Clinical Genetics, Fox Chase Cancer Center, Philadelphia, PA, USA.
⁵⁷ Department of Pathology, Leiden University Medical Center, Leiden, The Netherlands.
⁵⁸ Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands.
⁵⁹ Center for Inherited Disease Research (CIDR), Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
⁶⁰ Department of Non-Communicable Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, UK.
⁶¹ Genomics Center, Centre Hospitalier Universitaire de Québec - Université Laval Research Center, Québec City, QC, Canada.
⁶² Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, London, UK.
⁶³ Cancer Sciences Academic Unit, Faculty of Medicine, University of Southampton, Southampton, UK.
⁶⁴ Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
⁶⁵ Institute for Medical Informatics, Statistics and Epidemiology, University of Leipzig, Leipzig, Germany.
⁶⁶ David Geffen School of Medicine, Department of Medicine Division of Hematology and Oncology, University of California at Los Angeles, Los Angeles, CA, USA.
⁶⁷ Usher Institute of Population Health Sciences and Informatics, The University of Edinburgh Medical School, Edinburgh, UK.
⁶⁸ Institute for Medical Biometrics and Epidemiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
⁶⁹ Department of Cancer Epidemiology, Clinical Cancer Registry, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
⁷⁰ The Breast Cancer Now Toby Robins Research Centre, The Institute of Cancer Research, London, UK.
⁷¹ Department of Breast Surgery, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark.
⁷² School of Public Health, Curtin University, Perth, Western Australia, Australia.
⁷³ Genomic Medicine Group, Galician Foundation of Genomic Medicine, Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Complejo Hospitalario Universitario de Santiago, SERGAS, Santiago De Compostela, Spain.
⁷⁴ Moores Cancer Center, University of California San Diego, La Jolla, CA, USA.
⁷⁵ Cancer Epidemiology & Intelligence Division, Cancer Council Victoria, Melbourne, Victoria, Australia.
⁷⁶ Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia.
⁷⁷ Department of Medicine, McGill University, Montréal, Quebec, Canada.
⁷⁸ Division of Clinical Epidemiology, Royal Victoria Hospital, McGill University, Montréal, Quebec, Canada.
⁷⁹ Department of Dermatology, Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, UT, USA.
⁸⁰ Cancer & Environment Group, Center for Research in Epidemiology and Population Health (CESP), INSERM, University Paris-Sud, University Paris-Saclay, Villejuif, France.
⁸¹ Center for Hereditary Breast and Ovarian Cancer, University Hospital of Cologne, Cologne, Germany.
⁸² Center for Integrated Oncology (CIO), University Hospital of Cologne, Cologne, Germany.
⁸³ Center for Molecular Medicine Cologne (CMMC), University of Cologne, Cologne, Germany.
⁸⁴ Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
⁸⁵ Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
⁸⁶ Department of Oncology, Södersjukhuset, Stockholm, Sweden.
⁸⁷ Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA.
⁸⁸ Molecular Genetics of Breast Cancer, German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁸⁹ Cancer Genomics Research Laboratory, Leidos Biomedical Research, Frederick National Laboratory for Cancer Research, Frederick, MD, USA.
⁹⁰ Department of Medical Oncology, Family Cancer Clinic, Erasmus MC Cancer Institute, Rotterdam, The Netherlands.
⁹¹ Nuffield Department of Population Health, University of Oxford, Big Data Institute, Oxford, UK.
⁹² Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland.
⁹³ Independent Laboratory of Molecular Biology and Genetic Diagnostics, Pomeranian Medical University, Szczecin, Poland.
⁹⁴ Department of Gynecology and Obstetrics, University Hospital Ulm, Ulm, Germany.
⁹⁵ Department of Epidemiology, Cancer Prevention Institute of California, Fremont, CA, USA.
⁹⁶ Department of Health Research and Policy - Epidemiology, Stanford University School of Medicine, Stanford, CA, USA.
⁹⁷ Stanford Cancer Institute, Stanford University School of Medicine, Stanford, CA, USA.
⁹⁸ Division of Genetics and Epidemiology, The Institute of Cancer Research, London, UK.
⁹⁹ School of Medicine, National University of Ireland, Galway, Ireland.
¹⁰⁰ Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa, Russia.
¹⁰¹ Translational Cancer Research Area, University of Eastern Finland, Kuopio, Finland.
¹⁰² Institute of Clinical Medicine, Pathology and Forensic Medicine, University of Eastern Finland, Kuopio, Finland.
¹⁰³ Imaging Center, Department of Clinical Pathology, Kuopio University Hospital, Kuopio, Finland.
¹⁰⁴ Department of Cancer Genetics, Institute for Cancer Research, Oslo University Hospital Radiumhospitalet, Oslo, Norway.
¹⁰⁵ Institute of Clinical Medicine, Faculty of Medicine, University of Oslo, Oslo, Norway.
¹⁰⁶ Department of Clinical Molecular Biology, Oslo University Hospital, University of Oslo, Oslo, Norway.
¹⁰⁷ VIB KULeuven Center for Cancer Biology, VIB, Leuven, Belgium.
¹⁰⁸ Laboratory for Translational Genetics, Department of Human Genetics, KU Leuven, Leuven, Belgium.
¹⁰⁹ Epidemiology Program, University of Hawaii Cancer Center, Honolulu, HI, USA.
¹¹⁰ Human Genetics, Genome Institute of Singapore, Singapore, Singapore.
¹¹¹ Department of Epidemiology, University of Washington School of Public Health, Seattle, WA, USA.
¹¹² Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
¹¹³ Department of Cancer Epidemiology and Prevention, M. Sklodowska-Curie Institute - Oncology Center, Warsaw, Poland.
¹¹⁴ German Breast Group, GmbH, Neu Isenburg, Germany.
¹¹⁵ Southampton Clinical Trials Unit, University of Southampton, Southampton, UK.
¹¹⁶ Research Centre for Genetic Engineering and Biotechnology "Georgi D. Efremov", Macedonian Academy of Sciences and Arts, Skopje, Macedonia.
¹¹⁷ Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
¹¹⁸ Department of Oncology - Pathology, Karolinska Institutet, Stockholm, Sweden.
¹¹⁹ Department of Medical Oncology, University Hospital of Heraklion, Heraklion, Greece.
¹²⁰ Department of Clinical Genetics, VU University Medical Center, Amsterdam, The Netherlands.
¹²¹ Division of Gynaecology and Obstetrics, Technische Universität München, Munich, Germany.
¹²² Gynaecological Cancer Research Centre, Women's Cancer, Institute for Women's Health, University College London, London, UK.
¹²³ Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada.
¹²⁴ Laboratory Medicine Program, University Health Network, Toronto, Ontario, Canada.
¹²⁵ Department of Population Sciences, Beckman Research Institute of City of Hope, Duarte, CA, USA.
¹²⁶ Department of Obstetrics and Gynecology, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.
¹²⁷ Leuven Multidisciplinary Breast Center, Department of Oncology, Leuven Cancer Institute, University Hospitals Leuven, Leuven, Belgium.
¹²⁸ Center for Clinical Cancer Genetics and Global Health, The University of Chicago, Chicago, IL, USA.
¹²⁹ IFOM, The FIRC (Italian Foundation for Cancer Research) Institute of Molecular Oncology, Milan, Italy.
¹³⁰ Laboratory of Cancer Genetics and Tumor Biology, Cancer and Translational Medicine Research Unit, Biocenter Oulu, University of Oulu, Oulu, Finland.
¹³¹ Laboratory of Cancer Genetics and Tumor Biology, Northern Finland Laboratory Centre Oulu, Oulu, Finland.
¹³² Unit of Molecular Bases of Genetic Risk and Genetic Testing, Department of Research, Fondazione IRCCS (Istituto Di Ricovero e Cura a Carattere Scientifico) Istituto Nazionale dei Tumori (INT), Milan, Italy.
¹³³ Section of Cancer Genetics, The Institute of Cancer Research, London, UK.
¹³⁴ Department of Community Medicine and Epidemiology, Carmel Medical Center, Ruth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology and Clalit National Cancer Control Center, Haifa, Israel.
¹³⁵ Medical Oncology Department, Hospital Universitario Puerta de Hierro, Madrid, Spain.
¹³⁶ Hereditary Cancer Clinic, University Hospital of Heraklion, Heraklion, Greece.
¹³⁷ Epidemiology Branch, National Institute of Environmental Health Sciences, NIH, Research Triangle Park, NC, USA.
¹³⁸ Research Oncology, Guy's Hospital, King's College London, London, UK.
¹³⁹ Division of Psychosocial Research and Epidemiology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands.
¹⁴⁰ National Center for Tumor Diseases, University of Heidelberg, Heidelberg, Germany.
¹⁴¹ Division of Molecular Medicine, Pathology North, John Hunter Hospital, Newcastle, New South Wales, Australia.
¹⁴² Discipline of Medical Genetics, School of Biomedical Sciences and Pharmacy, Faculty of Health, University of Newcastle, Newcastle, New South Wales, Australia.
¹⁴³ Department of Pathology, The University of Melbourne, Melbourne, Victoria, Australia.
¹⁴⁴ Cancer Control Research, BC Cancer Agency, Vancouver, British Columbia, Canada.
¹⁴⁵ School of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada.
¹⁴⁶ The Curtin UWA Centre for Genetic Origins of Health and Disease, Curtin University and University of Western Australia, Perth, Western Australia, Australia.
¹⁴⁷ Department of Obstetrics and Gynaecology, University of Melbourne and the Royal Women's Hospital, Melbourne, Victoria, Australia.
¹⁴⁸ Division of Breast Cancer Research, The Institute of Cancer Research, London, UK.
¹⁴⁹ Epigenetic and Stem Cell Biology Laboratory, National Institute of Environmental Health Sciences, NIH, Research Triangle Park, NC, USA.
¹⁵⁰ Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY, USA.
¹⁵¹ McGill University and Génome Québec Innovation Centre, Montréal, Quebec, Canada.
¹⁵² Department of Surgery, Leiden University Medical Center, Leiden, The Netherlands.
¹⁵³ Institute of Human Genetics, Pontificia Universidad Javeriana, Bogota, Colombia.
¹⁵⁴ Department of Gynecology and Obstetrics, Helios Clinics Berlin-Buch, Berlin, Germany.
¹⁵⁵ Biostatistics and Computational Biology Branch, National Institute of Environmental Health Sciences, NIH, Research Triangle Park, NC, USA.
¹⁵⁶ Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
¹⁵⁷ Department of Medicine, Institute for Human Genetics, UCSF Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA.
¹⁵⁸ Cancer Division, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia. Georgia.Trench@qimrberghofer.edu.au.
¹⁵⁹ Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, TN, USA. wei.zheng@vanderbilt.edu.

PMID: 29915430
PMCID: PMC6314198
DOI: 10.1038/s41588-018-0132-x

Abstract

The breast cancer risk variants identified in genome-wide association studies explain only a small fraction of the familial relative risk, and the genes responsible for these associations remain largely unknown. To identify novel risk loci and likely causal genes, we performed a transcriptome-wide association study evaluating associations of genetically predicted gene expression with breast cancer risk in 122,977 cases and 105,974 controls of European ancestry. We used data from the Genotype-Tissue Expression Project to establish genetic models to predict gene expression in breast tissue and evaluated model performance using data from The Cancer Genome Atlas. Of the 8,597 genes evaluated, significant associations were identified for 48 at a Bonferroni-corrected threshold of P < 5.82 × 10^-6, including 14 genes at loci not yet reported for breast cancer. We silenced 13 genes and showed an effect for 11 on cell proliferation and/or colony-forming efficiency. Our study provides new insights into breast cancer genetics and biology.

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Conflict of interest statement

Competing financial interests

The authors declare no competing financial interests.

Figures

**Figure 1.. Manhattan plot of association results from the breast cancer transcriptome-wide association study.**
Results are based on 122,977 cases and 105,974 controls. The red line represents P = 5.82 × 10⁻⁶. The blue line represents P = 1.00 × 10⁻³.

**Figure 2.. Heat maps of proliferation and colony formation efficiency in breast cells.**
**(a)** Proliferation efficiency. **(b)** colony formation efficiency. Error bars, SD (N=2). P-values were determined by one-way ANOVA followed by Dunnett’s multiple comparisons test: *P-value < 0.05. NTC: non-target control.

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A transcriptome-wide association study of 229,000 women identifies new candidate susceptibility genes for breast cancer

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A transcriptome-wide association study of 229,000 women identifies new candidate susceptibility genes for breast cancer

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Conflict of interest statement

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