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Translational Science

A Transcriptome-Wide Association Study Among 97,898 Women to Identify Candidate Susceptibility Genes for Epithelial Ovarian Cancer Risk

Yingchang Lu, Alicia Beeghly-Fadiel, Lang Wu, Xingyi Guo, Bingshan Li, Joellen M. Schildkraut, Hae Kyung Im, Yian A. Chen, Jennifer B. Permuth, Brett M. Reid, Jamie K. Teer, Kirsten B. Moysich, Irene L. Andrulis, Hoda Anton-Culver, Banu K. Arun, Elisa V. Bandera, Rosa B. Barkardottir, Daniel R. Barnes, Javier Benitez, Line Bjorge, James Brenton, Ralf Butzow, Trinidad Caldes, Maria A. Caligo, Ian Campbell, Jenny Chang-Claude, Kathleen B.M. Claes, Fergus J. Couch, Daniel W. Cramer, Mary B. Daly, Anna deFazio, Joe Dennis, Orland Diez, Susan M. Domchek, Thilo Dörk, Douglas F. Easton, Diana M. Eccles, Peter A. Fasching, Renée T. Fortner, George Fountzilas, Eitan Friedman, Patricia A. Ganz, Judy Garber, Graham G. Giles, Andrew K. Godwin, David E. Goldgar, Marc T. Goodman, Mark H. Greene, Jacek Gronwald, Ute Hamann, Florian Heitz, Michelle A.T. Hildebrandt, Claus K. Høgdall, Antoinette Hollestelle, Peter J. Hulick, David G. Huntsman, Evgeny N. Imyanitov, Claudine Isaacs, Anna Jakubowska, Paul James, Beth Y. Karlan, Linda E. Kelemen, Lambertus A. Kiemeney, Susanne K. Kjaer, Ava Kwong, Nhu D. Le, Goska Leslie, Fabienne Lesueur, Douglas A. Levine, Amalia Mattiello, Taymaa May, Lesley McGuffog, Iain A. McNeish, Melissa A. Merritt, Francesmary Modugno, Marco Montagna, Susan L. Neuhausen, Heli Nevanlinna, Finn C. Nielsen, Liene Nikitina-Zake, Robert L. Nussbaum, Kenneth Offit, Edith Olah, Olufunmilayo I. Olopade, Sara H. Olson, Håkan Olsson, Ana Osorio, Sue K. Park, Michael T. Parsons, Petra H.M. Peeters, Tanja Pejovic, Paolo Peterlongo, Catherine M. Phelan, Miquel Angel Pujana, Susan J. Ramus, Gad Rennert, Harvey Risch, Gustavo C. Rodriguez, Cristina Rodríguez-Antona, Isabelle Romieu, Matti A. Rookus, Mary Anne Rossing, Iwona K. Rzepecka, Dale P. Sandler, Rita K. Schmutzler, Veronica W. Setiawan, Priyanka Sharma, Weiva Sieh, Jacques Simard, Christian F. Singer, Honglin Song, Melissa C. Southey, Amanda B. Spurdle, Rebecca Sutphen, Anthony J. Swerdlow, Manuel R. Teixeira, Soo H. Teo, Mads Thomassen, Marc Tischkowitz, Amanda E. Toland, Antonia Trichopoulou, Nadine Tung, Shelley S. Tworoger, Elizabeth J. van Rensburg, Adriaan Vanderstichele, Ana Vega, Digna Velez Edwards, Penelope M. Webb, Jeffrey N. Weitzel, Nicolas Wentzensen, Emily White, Alicja Wolk, Anna H. Wu, Drakoulis Yannoukakos, Kristin K. Zorn, Simon A. Gayther, Antonis C. Antoniou, Andrew Berchuck, Ellen L. Goode, Georgia Chenevix-Trench, Thomas A. Sellers, Paul D.P. Pharoah, Wei Zheng and Jirong Long
Yingchang Lu
Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, Tennessee.
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Alicia Beeghly-Fadiel
Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, Tennessee.
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Lang Wu
Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, Tennessee.
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Xingyi Guo
Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, Tennessee.
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Bingshan Li
Department of Molecular Physiology and Biophysics, Vanderbilt University Medical Center, Nashville, Tennessee.
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Joellen M. Schildkraut
Department of Public Health Sciences, University of Virginia, Charlottesville, Virginia.
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Hae Kyung Im
Section of Genetic Medicine, Department of Medicine, University of Chicago, Chicago, Illinois.
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Yian A. Chen
Department of Biostatistics, Moffitt Cancer Center, Tampa, Florida.
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Jennifer B. Permuth
Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, Florida.
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Brett M. Reid
Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, Florida.
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Jamie K. Teer
Department of Biostatistics, Moffitt Cancer Center, Tampa, Florida.
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  • ORCID record for Jamie K. Teer
Kirsten B. Moysich
Division of Cancer Prevention and Control, Roswell Park Cancer Institute, Buffalo, New York.
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Irene L. Andrulis
Fred A. Litwin Center for Cancer Genetics, Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Toronto, Ontario, Canada.Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada.
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Hoda Anton-Culver
Department of Epidemiology, Genetic Epidemiology Research Institute, University of California Irvine, Irvine, California.
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Banu K. Arun
Department of Breast Medical Oncology, University of Texas MD Anderson Cancer Center, Houston, Texas.
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Elisa V. Bandera
Cancer Prevention and Control Program, Rutgers Cancer Institute of New Jersey, New Brunswick, New Jersey.
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Rosa B. Barkardottir
Department of Pathology, Landspitali University Hospital, Reykjavik, Iceland.BMC (Biomedical Centre), Faculty of Medicine, University of Iceland, Reykjavik, Iceland.
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Daniel R. Barnes
Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom.
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Javier Benitez
Human Cancer Genetics Program, Spanish National Cancer Research Centre, Madrid, Spain.Centro de Investigación en Red de Enfermedades Raras (CIBERER), Valencia, Spain.
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Line Bjorge
Department of Gynecology and Obstetrics, Haukeland University Horpital, Bergen, Norway.Centre for Cancer Biomarkers, Department of Clinical Science, University of Bergen, Bergen, Norway.
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James Brenton
Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge, United Kingdom.
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Ralf Butzow
Department of Pathology, University of Helsinki and Helsinki University Hospital, Helsinki, Finland.
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Trinidad Caldes
Medical Oncology Department, Hospital Clínico San Carlos, Instituto de Investigación Sanitaria San Carlos (IdISSC), Centro Investigación Biomédica en Red de Cáncer (CIBERONC), Madrid, Spain.
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Maria A. Caligo
Section of Genetic Oncology, Department of Laboratory Medicine, University and University Hospital of Pisa, Pisa, Italy.
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Ian Campbell
Peter MacCallum Cancer Center, Melbourne, Victoria, Australia.Sir Peter MacCallum Department of Oncology, The University of Melbourne, Melbourne, Victoria, Australia.Department of Pathology, The University of Melbourne, Melbourne, Victoria, Australia.
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Jenny Chang-Claude
Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.Research Group Genetic Cancer Epidemiology, University Cancer Center Hamburg (UCCH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
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Kathleen B.M. Claes
Centre for Medical Genetics, Ghent University, Gent, Belgium.
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Fergus J. Couch
Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, Minnesota.
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Daniel W. Cramer
Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital, Boston, Massachusetts.Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
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Mary B. Daly
Department of Clinical Genetics, Fox Chase Cancer Center, Philadelphia, Pennsylvania.
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Anna deFazio
Centre for Cancer Research, The Westmead Institute for Medical Research, The University of Sydney, Sydney, New South Wales, Australia.Department of Gynaecological Oncology, Westmead Hospital, Sydney, New South Wales, Australia.
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Joe Dennis
Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom.
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Orland Diez
Oncogenetics Group, Clinical and Molecular Genetics Area, Vall d'Hebron Institute of Oncology (VHIO), University Hospital, Vall d'Hebron, Barcelona, Spain.
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Susan M. Domchek
Department of Medicine, Abramson Cancer Center, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania.
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Thilo Dörk
Gynaecology Research Unit, Hannover Medical School, Hannover, Germany.
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Douglas F. Easton
Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom.Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, United Kingdom.
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Diana M. Eccles
Cancer Sciences Academic Unit, Faculty of Medicine, University of Southampton, Southampton, United Kingdom.
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Peter A. Fasching
Department of Gynaecology and Obstetrics, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg, Comprehensive Cancer Center Erlangen-EMN, Erlangen, Germany.David Geffen School of Medicine, Department of Medicine Division of Hematology and Oncology, University of California at Los Angeles, Los Angeles, California.
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Renée T. Fortner
Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
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George Fountzilas
Department of Medical Oncology, “Papageorgiou” Hospital, Aristotle University of Thessaloniki School of Medicine, Thessaloniki, Greece.
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Eitan Friedman
The Susanne Levy Gertner Oncogenetics Unit, Chaim Sheba Medical Center, Ramat Gan, Israel.Sackler Faculty of Medicine, Tel Aviv University, Ramat Aviv, Israel.
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Patricia A. Ganz
Schools of Medicine and Public Health, Division of Cancer Prevention & Control Research, Jonsson Comprehensive Cancer Centre, UCLA, Los Angeles, California.
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Judy Garber
Cancer Risk and Prevention Clinic, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Graham G. Giles
Cancer Epidemiology & Intelligence Division, Cancer Council Victoria, Melbourne, Victoria, Australia.Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia.Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, Victoria, Australia.
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Andrew K. Godwin
Department of Pathology and Laboratory Medicine, Kansas University Medical Center, Kansas City, Kansas.
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David E. Goldgar
Department of Dermatology, Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, Utah.
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Marc T. Goodman
Cancer Prevention and Control, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California.Community and Population Health Research Institute, Department of Biomedical Sciences, Cedars-Sinai Medical Center, Los Angeles, California.
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Mark H. Greene
Clinical Genetics Branch, DCEG, National Cancer Institute, Bethesda, Maryland.
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Jacek Gronwald
Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland.
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Ute Hamann
Molecular Genetics of Breast Cancer, German Cancer Research Center (DKFZ), Heidelberg, Germany.
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Florian Heitz
Department of Gynecology and Gynecologic Oncology, Dr. Horst Schmidt Kliniken Wiesbaden, Wiesbaden, Germany.Department of Gynecology and Gynecologic Oncology, Kliniken Essen-Mitte/Evang. Huyssens-Stiftung/Knappschaft GmbH, Essen, Germany.
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Michelle A.T. Hildebrandt
Department of Epidemiology, University of Texas MD Anderson Cancer Center, Houston, Texas.
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Claus K. Høgdall
Department of Gynecology, The Juliane Marie Centre, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark.
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Antoinette Hollestelle
Department of Medical Oncology, Family Cancer Clinic, Erasmus MC Cancer Institute, Rotterdam, The Netherlands.
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Peter J. Hulick
Center for Medical Genetics, NorthShore University HealthSystem, Evanston, Illinois.The University of Chicago Pritzker School of Medicine, Chicago, Illinois.
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David G. Huntsman
British Columbia's Ovarian Cancer Research (OVCARE) Program, Vancouver General Hospital, BC Cancer Agency and University of British Columbia, Vancouver, British Columbia, Canada.Department of Molecular Oncology, BC Cancer Agency Research Centre, Vancouver, British Columbia, Canada.Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, British Columbia, Canada.
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Evgeny N. Imyanitov
N.N. Petrov Institute of Oncology, St. Petersburg, Russia.
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Claudine Isaacs
Lombardi Comprehensive Cancer Center, Georgetown University, Washington, District of Columbia.
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Anna Jakubowska
Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland.
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Paul James
Sir Peter MacCallum Department of Oncology, The University of Melbourne, Melbourne, Victoria, Australia.Parkville Familial Cancer Centre, Peter MacCallum Cancer Center, Melbourne, Victoria, Australia.
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Beth Y. Karlan
Women's Cancer Program at the Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California.
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Linda E. Kelemen
Department of Public Health Sciences, Medical University of South Carolina, Charleston, South Carolina.
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Lambertus A. Kiemeney
Radboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, The Netherlands.
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  • ORCID record for Lambertus A. Kiemeney
Susanne K. Kjaer
Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark.Department of Gynaecology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark.
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Ava Kwong
Hong Kong Hereditary Breast Cancer Family Registry, Happy Valley, Hong Kong.Department of Surgery, The University of Hong Kong, Pok Fu Lam, Hong Kong.Department of Surgery, Hong Kong Sanatorium and Hospital, Happy Valley, Hong Kong.
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Nhu D. Le
Cancer Control Research, BC Cancer Agency, Vancouver, British Columbia, Canada.
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Goska Leslie
Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom.
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  • ORCID record for Goska Leslie
Fabienne Lesueur
Genetic Epidemiology of Cancer team, Inserm U900, Paris, France.Institut Curie, Paris, France.PSL University, Paris, France.Mines ParisTech, Fontainebleau, France.
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  • ORCID record for Fabienne Lesueur
Douglas A. Levine
Gynecology Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.Gynecologic Oncology, Laura and Isaac Pearlmutter Cancer Center, NYU Langone Medical Center, New York, New York.
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Amalia Mattiello
Dipertimento Di Medicina Clinica E Chirurgia, Federico II University, Naples, Italy.
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Taymaa May
Division of Gynecologic Oncology, University Health Network, Princess Margaret Hospital, Toronto, Ontario, Canada.
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Lesley McGuffog
Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom.
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Iain A. McNeish
Institute of Cancer Sciences, University of Glasgow, Wolfson Wohl Cancer Research Centre, Glasgow, United Kingdom.
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  • ORCID record for Iain A. McNeish
Melissa A. Merritt
Cancer Epidemiology Program, University of Hawaii Cancer Center, Honolulu, Hawaii.Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom.
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Francesmary Modugno
Ovarian Cancer Center of Excellence, Womens Cancer Research Program, Magee-Womens Research Institute and University of Pittsburgh Cancer Institute, Pittsburgh, Pennsylvania.Department of Epidemiology, University of Pittsburgh Graduate School of Public Health, Pittsburgh, Pennsylvania.Division of Gynecologic Oncology, Department of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.
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Marco Montagna
Immunology and Molecular Oncology Unit, Veneto Institute of Oncology IOV - IRCCS, Padua, Italy.
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Susan L. Neuhausen
Department of Population Sciences, Beckman Research Institute of City of Hope, Duarte, California.
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Heli Nevanlinna
Department of Obstetrics and Gynecology, University of Helsinki and Helsinki University Hospital, Helsinki, Finland.
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  • ORCID record for Heli Nevanlinna
Finn C. Nielsen
Center for Genomic Medicine, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
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Liene Nikitina-Zake
Latvian Biomedical Research and Study Centre, Riga, Latvia.
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Robert L. Nussbaum
Cancer Genetics and Prevention Program, University of California San Francisco, San Francisco, California.
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  • ORCID record for Robert L. Nussbaum
Kenneth Offit
Clinical Genetics Research Lab, Department of Cancer Biology and Genetics, Memorial Sloan-Kettering Cancer Center, New York, New York.Clinical Genetics Service, Department of Medicine, Memorial Sloan-Kettering Cancer Center, New York, New York.
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Edith Olah
Department of Molecular Genetics, National Institute of Oncology, Budapest, Hungary.
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Olufunmilayo I. Olopade
Center for Clinical Cancer Genetics, The University of Chicago, Chicago, Illinois.
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Sara H. Olson
Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, New York.
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Håkan Olsson
Department of Cancer Epidemiology, Clinical Sciences, Lund University, Lund, Sweden.
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Ana Osorio
Human Cancer Genetics Program, Spanish National Cancer Research Centre, Madrid, Spain.Biomedical Network on Rare Diseases (CIBERER), Madrid, Spain.
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Sue K. Park
Department of Preventive Medicine, Seoul National University College of Medicine, Seoul, Korea.Department of Biomedical Sciences, Seoul National University Graduate School, Seoul, Korea.Cancer Research Institute, Seoul National University, Seoul, Korea.
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Michael T. Parsons
Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
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Petra H.M. Peeters
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IFOM, the FIRC (Italian Foundation for Cancer Research) Institute of Molecular Oncology, Milan, Italy.
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Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, Florida.
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Catalan Institute of Oncology, ProCURE, Oncobell, Bellvitge Biomedical Research Institute (IDIBELL). Barcelona, Spain.
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School of Women's and Children's Health, University of NSW Sydney, Sydney, New South Wales, Australia.The Kinghorn Cancer Centre, Garvan Institute of Medical Research, Sydney, New South Wales, Australia.
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Clalit National Cancer Control Center, Carmel Medical Center and Technion Faculty of Medicine, Haifa, Israel.
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School of Public Health, Yale University, New Haven, Connecticut.
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Division of Gynecologic Oncology, NorthShore University HealthSystem, University of Chicago, Evanston, Illinois.
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Cristina Rodríguez-Antona
Hereditary Endocrine Cancer group, Spanish National Cancer Research Center (CNIO), Madrid, Spain.
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Isabelle Romieu
Nutrition and Metabolism Section, International Agency for Research on Cancer (IARC-WHO), Lyon, France.
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Matti A. Rookus
Department of Epidemiology, The Netherlands Cancer Institute, Amsterdam, The Netherlands.
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Mary Anne Rossing
Program in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington.Department of Epidemiology, University of Washington, Seattle, Washington.
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Iwona K. Rzepecka
Department of Pathology and Laboratory Diagnostics, Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland.
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Dale P. Sandler
Epidemiology Branch, National Institute of Environmental Health Sciences, NIH, Research Triangle Park, Maryland.
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Rita K. Schmutzler
Center for Hereditary Breast and Ovarian Cancer, University Hospital of Cologne, Cologne, Germany.Center for Molecular Medicine Cologne (CMMC), University of Cologne, Cologne, Germany.
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Veronica W. Setiawan
Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California.
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Priyanka Sharma
Department of Medicine, University of Kansas Medical Center, Kansas City, Kansas.
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Weiva Sieh
Department of Genetics and Genomic Sciences, Department of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, New York, New York.
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Jacques Simard
Genomics Center, Centre Hospitalier Universitaire de Québec Research Center, Laval University, Québec City, Québec, Canada.
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Christian F. Singer
Dept of OB/GYN and Comprehensive Cancer Center, Medical University of Vienna, Vienna, Austria.
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Honglin Song
Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, United Kingdom.
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Melissa C. Southey
Department of Pathology, The University of Melbourne, Melbourne, Victoria, Australia.
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Amanda B. Spurdle
Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
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Rebecca Sutphen
Epidemiology Center, College of Medicine, University of South Florida, Tampa, Florida.
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Anthony J. Swerdlow
Division of Genetics and Epidemiology, The Institute of Cancer Research, London, United Kingdom.Division of Breast Cancer Research, The Institute of Cancer Research, London, United Kingdom.
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Manuel R. Teixeira
Department of Genetics, Portuguese Oncology Institute, Porto, Portugal.Biomedical Sciences Institute (ICBAS), University of Porto, Porto, Portugal.
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Soo H. Teo
Cancer Research Malaysia, Subang Jaya, Selangor, Malaysia.Breast Cancer Research Unit, Cancer Research Institute, University Malaya Medical Centre, Kuala Lumpur, Malaysia.
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Mads Thomassen
Department of Clinical Genetics, Odense University Hospital, Odence C, Denmark.
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Marc Tischkowitz
Program in Cancer Genetics, Departments of Human Genetics and Oncology, McGill University, Montréal, Québec, Canada.Department of Medical Genetics, Cambridge University, Cambridge, United Kingdom.
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Amanda E. Toland
Department of Cancer Biology and Genetics, Comprehensive Cancer Center, The Ohio State University, Columbus, Ohio.
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Antonia Trichopoulou
Hellenic Health Foundation, Athens, Greece.WHO Collaborating Center for Nutrition and Health, Unit of Nutritional Epidemiology and Nutrition in Public Health, Department of Hygiene, Epidemiology and Medical Statistics, University of Athens Medical School, Athens, Greece.
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Nadine Tung
Department of Medical Oncology, Beth Israel Deaconess Medical Center, Boston, Massachusetts.
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Shelley S. Tworoger
Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, Florida.Research Institute and Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
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Department of Genetics, University of Pretoria, Arcadia, South Africa.
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Adriaan Vanderstichele
Division of Gynecologic Oncology, Department of Obstetrics and Gynaecology and Leuven Cancer Institute, University Hospitals Leuven, Leuven, Belgium.
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Fundación Pública Galega Medicina Xenómica, Santiago De Compostela, Spain.
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Vanderbilt Epidemiology Center, Vanderbilt Genetics Institute, Department of Obstetrics and Gynecology, Vanderbilt University Medical Center, Nashville, Tennessee.
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Population Health Department, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
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Clinical Cancer Genetics, City of Hope, Duarte, California.
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Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Maryland.
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Fred Hutchinson Cancer Research Center, Seattle, Washington.Department of Epidemiology, University of Washington, Seattle, Washington.
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Department of Environmental Medicine, Division of Nutritional Epidemiology, Karolinska Institutet, Stockholm, Sweden.
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Molecular Diagnostics Laboratory, INRASTES, National Centre for Scientific Research ‘Demokritos’, Athens, Greece.
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Magee-Womens Hospital, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.
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Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California.Center for Cancer Prevention and Translational Genomics, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California.Department of Biomedical Sciences, Cedars-Sinai Medical Center, Los Angeles, California.
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Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom.
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Andrew Berchuck
Department of Obstetrics and Gynecology, Duke University Medical Center, Durham, North Carolina.
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Ellen L. Goode
Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota.
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Georgia Chenevix-Trench
Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
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Thomas A. Sellers
Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, Florida.
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Paul D.P. Pharoah
Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom.Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, United Kingdom.
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Wei Zheng
Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, Tennessee.
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Jirong Long
Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, Tennessee.
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  • For correspondence: jirong.long@vanderbilt.edu
DOI: 10.1158/0008-5472.CAN-18-0951 Published September 2018
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Abstract

Large-scale genome-wide association studies (GWAS) have identified approximately 35 loci associated with epithelial ovarian cancer (EOC) risk. The majority of GWAS-identified disease susceptibility variants are located in noncoding regions, and causal genes underlying these associations remain largely unknown. Here, we performed a transcriptome-wide association study to search for novel genetic loci and plausible causal genes at known GWAS loci. We used RNA sequencing data (68 normal ovarian tissue samples from 68 individuals and 6,124 cross-tissue samples from 369 individuals) and high-density genotyping data from European descendants of the Genotype-Tissue Expression (GTEx V6) project to build ovarian and cross-tissue models of genetically regulated expression using elastic net methods. We evaluated 17,121 genes for their cis-predicted gene expression in relation to EOC risk using summary statistics data from GWAS of 97,898 women, including 29,396 EOC cases. With a Bonferroni-corrected significance level of P < 2.2 × 10−6, we identified 35 genes, including FZD4 at 11q14.2 (Z = 5.08, P = 3.83 × 10−7, the cross-tissue model; 1 Mb away from any GWAS-identified EOC risk variant), a potential novel locus for EOC risk. All other 34 significantly associated genes were located within 1 Mb of known GWAS-identified loci, including 23 genes at 6 loci not previously linked to EOC risk. Upon conditioning on nearby known EOC GWAS-identified variants, the associations for 31 genes disappeared and three genes remained (P < 1.47 × 10−3). These data identify one novel locus (FZD4) and 34 genes at 13 known EOC risk loci associated with EOC risk, providing new insights into EOC carcinogenesis.

Significance: Transcriptomic analysis of a large cohort confirms earlier GWAS loci and reveals FZD4 as a novel locus associated with EOC risk. Cancer Res; 78(18); 5419–30. ©2018 AACR.

Footnotes

  • Note: Supplementary data for this article are available at Cancer Research Online (http://cancerres.aacrjournals.org/).

  • Received March 29, 2018.
  • Revision received May 17, 2018.
  • Accepted July 24, 2018.
  • Published first July 27, 2018.
  • ©2018 American Association for Cancer Research.
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Cancer Research: 78 (18)
September 2018
Volume 78, Issue 18
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A Transcriptome-Wide Association Study Among 97,898 Women to Identify Candidate Susceptibility Genes for Epithelial Ovarian Cancer Risk
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A Transcriptome-Wide Association Study Among 97,898 Women to Identify Candidate Susceptibility Genes for Epithelial Ovarian Cancer Risk
Yingchang Lu, Alicia Beeghly-Fadiel, Lang Wu, Xingyi Guo, Bingshan Li, Joellen M. Schildkraut, Hae Kyung Im, Yian A. Chen, Jennifer B. Permuth, Brett M. Reid, Jamie K. Teer, Kirsten B. Moysich, Irene L. Andrulis, Hoda Anton-Culver, Banu K. Arun, Elisa V. Bandera, Rosa B. Barkardottir, Daniel R. Barnes, Javier Benitez, Line Bjorge, James Brenton, Ralf Butzow, Trinidad Caldes, Maria A. Caligo, Ian Campbell, Jenny Chang-Claude, Kathleen B.M. Claes, Fergus J. Couch, Daniel W. Cramer, Mary B. Daly, Anna deFazio, Joe Dennis, Orland Diez, Susan M. Domchek, Thilo Dörk, Douglas F. Easton, Diana M. Eccles, Peter A. Fasching, Renée T. Fortner, George Fountzilas, Eitan Friedman, Patricia A. Ganz, Judy Garber, Graham G. Giles, Andrew K. Godwin, David E. Goldgar, Marc T. Goodman, Mark H. Greene, Jacek Gronwald, Ute Hamann, Florian Heitz, Michelle A.T. Hildebrandt, Claus K. Høgdall, Antoinette Hollestelle, Peter J. Hulick, David G. Huntsman, Evgeny N. Imyanitov, Claudine Isaacs, Anna Jakubowska, Paul James, Beth Y. Karlan, Linda E. Kelemen, Lambertus A. Kiemeney, Susanne K. Kjaer, Ava Kwong, Nhu D. Le, Goska Leslie, Fabienne Lesueur, Douglas A. Levine, Amalia Mattiello, Taymaa May, Lesley McGuffog, Iain A. McNeish, Melissa A. Merritt, Francesmary Modugno, Marco Montagna, Susan L. Neuhausen, Heli Nevanlinna, Finn C. Nielsen, Liene Nikitina-Zake, Robert L. Nussbaum, Kenneth Offit, Edith Olah, Olufunmilayo I. Olopade, Sara H. Olson, Håkan Olsson, Ana Osorio, Sue K. Park, Michael T. Parsons, Petra H.M. Peeters, Tanja Pejovic, Paolo Peterlongo, Catherine M. Phelan, Miquel Angel Pujana, Susan J. Ramus, Gad Rennert, Harvey Risch, Gustavo C. Rodriguez, Cristina Rodríguez-Antona, Isabelle Romieu, Matti A. Rookus, Mary Anne Rossing, Iwona K. Rzepecka, Dale P. Sandler, Rita K. Schmutzler, Veronica W. Setiawan, Priyanka Sharma, Weiva Sieh, Jacques Simard, Christian F. Singer, Honglin Song, Melissa C. Southey, Amanda B. Spurdle, Rebecca Sutphen, Anthony J. Swerdlow, Manuel R. Teixeira, Soo H. Teo, Mads Thomassen, Marc Tischkowitz, Amanda E. Toland, Antonia Trichopoulou, Nadine Tung, Shelley S. Tworoger, Elizabeth J. van Rensburg, Adriaan Vanderstichele, Ana Vega, Digna Velez Edwards, Penelope M. Webb, Jeffrey N. Weitzel, Nicolas Wentzensen, Emily White, Alicja Wolk, Anna H. Wu, Drakoulis Yannoukakos, Kristin K. Zorn, Simon A. Gayther, Antonis C. Antoniou, Andrew Berchuck, Ellen L. Goode, Georgia Chenevix-Trench, Thomas A. Sellers, Paul D.P. Pharoah, Wei Zheng and Jirong Long
Cancer Res September 15 2018 (78) (18) 5419-5430; DOI: 10.1158/0008-5472.CAN-18-0951

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A Transcriptome-Wide Association Study Among 97,898 Women to Identify Candidate Susceptibility Genes for Epithelial Ovarian Cancer Risk
Yingchang Lu, Alicia Beeghly-Fadiel, Lang Wu, Xingyi Guo, Bingshan Li, Joellen M. Schildkraut, Hae Kyung Im, Yian A. Chen, Jennifer B. Permuth, Brett M. Reid, Jamie K. Teer, Kirsten B. Moysich, Irene L. Andrulis, Hoda Anton-Culver, Banu K. Arun, Elisa V. Bandera, Rosa B. Barkardottir, Daniel R. Barnes, Javier Benitez, Line Bjorge, James Brenton, Ralf Butzow, Trinidad Caldes, Maria A. Caligo, Ian Campbell, Jenny Chang-Claude, Kathleen B.M. Claes, Fergus J. Couch, Daniel W. Cramer, Mary B. Daly, Anna deFazio, Joe Dennis, Orland Diez, Susan M. Domchek, Thilo Dörk, Douglas F. Easton, Diana M. Eccles, Peter A. Fasching, Renée T. Fortner, George Fountzilas, Eitan Friedman, Patricia A. Ganz, Judy Garber, Graham G. Giles, Andrew K. Godwin, David E. Goldgar, Marc T. Goodman, Mark H. Greene, Jacek Gronwald, Ute Hamann, Florian Heitz, Michelle A.T. Hildebrandt, Claus K. Høgdall, Antoinette Hollestelle, Peter J. Hulick, David G. Huntsman, Evgeny N. Imyanitov, Claudine Isaacs, Anna Jakubowska, Paul James, Beth Y. Karlan, Linda E. Kelemen, Lambertus A. Kiemeney, Susanne K. Kjaer, Ava Kwong, Nhu D. Le, Goska Leslie, Fabienne Lesueur, Douglas A. Levine, Amalia Mattiello, Taymaa May, Lesley McGuffog, Iain A. McNeish, Melissa A. Merritt, Francesmary Modugno, Marco Montagna, Susan L. Neuhausen, Heli Nevanlinna, Finn C. Nielsen, Liene Nikitina-Zake, Robert L. Nussbaum, Kenneth Offit, Edith Olah, Olufunmilayo I. Olopade, Sara H. Olson, Håkan Olsson, Ana Osorio, Sue K. Park, Michael T. Parsons, Petra H.M. Peeters, Tanja Pejovic, Paolo Peterlongo, Catherine M. Phelan, Miquel Angel Pujana, Susan J. Ramus, Gad Rennert, Harvey Risch, Gustavo C. Rodriguez, Cristina Rodríguez-Antona, Isabelle Romieu, Matti A. Rookus, Mary Anne Rossing, Iwona K. Rzepecka, Dale P. Sandler, Rita K. Schmutzler, Veronica W. Setiawan, Priyanka Sharma, Weiva Sieh, Jacques Simard, Christian F. Singer, Honglin Song, Melissa C. Southey, Amanda B. Spurdle, Rebecca Sutphen, Anthony J. Swerdlow, Manuel R. Teixeira, Soo H. Teo, Mads Thomassen, Marc Tischkowitz, Amanda E. Toland, Antonia Trichopoulou, Nadine Tung, Shelley S. Tworoger, Elizabeth J. van Rensburg, Adriaan Vanderstichele, Ana Vega, Digna Velez Edwards, Penelope M. Webb, Jeffrey N. Weitzel, Nicolas Wentzensen, Emily White, Alicja Wolk, Anna H. Wu, Drakoulis Yannoukakos, Kristin K. Zorn, Simon A. Gayther, Antonis C. Antoniou, Andrew Berchuck, Ellen L. Goode, Georgia Chenevix-Trench, Thomas A. Sellers, Paul D.P. Pharoah, Wei Zheng and Jirong Long
Cancer Res September 15 2018 (78) (18) 5419-5430; DOI: 10.1158/0008-5472.CAN-18-0951
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