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Nat Genet. 2017 May;49(5):680-691. doi: 10.1038/ng.3826. Epub 2017 Mar 27.

Identification of 12 new susceptibility loci for different histotypes of epithelial ovarian cancer.

Phelan CM1,2, Kuchenbaecker KB3,4, Tyrer JP5, Kar SP5, Lawrenson K6, Winham SJ7, Dennis J5, Pirie A5, Riggan MJ8, Chornokur G1, Earp MA9, Lyra PC Jr1, Lee JM10, Coetzee S10, Beesley J11, McGuffog L12, Soucy P13, Dicks E5, Lee A12, Barrowdale D12, Lecarpentier J12, Leslie G12, Aalfs CM14, Aben KKH15,16, Adams M17, Adlard J18, Andrulis IL19,20, Anton-Culver H21,22, Antonenkova N23; AOCS study group, Aravantinos G24, Arnold N25, Arun BK26, Arver B27, Azzollini J28, Balmaña J29, Banerjee SN30, Barjhoux L31, Barkardottir RB32,33, Bean Y34,35, Beckmann MW36, Beeghly-Fadiel A37,38,39,40, Benitez J41,42, Bermisheva M43, Bernardini MQ44, Birrer MJ45, Bjorge L46,47, Black A48, Blankstein K49, Blok MJ50, Bodelon C48, Bogdanova N51, Bojesen A52, Bonanni B53, Borg Å54, Bradbury AR55, Brenton JD56, Brewer C57, Brinton L48, Broberg P58, Brooks-Wilson A59, Bruinsma F60, Brunet J61, Buecher B62, Butzow R63, Buys SS64, Caldes T65, Caligo MA66, Campbell I67,68, Cannioto R69, Carney ME70, Cescon T49, Chan SB71, Chang-Claude J72,73, Chanock S48, Chen XQ11, Chiew YE74,75, Chiquette J76, Chung WK77, Claes KBM78, Conner T64, Cook LS79, Cook J80, Cramer DW81, Cunningham JM82, D'Aloisio AA83, Daly MB84, Damiola F31, Damirovna SD85, Dansonka-Mieszkowska A86, Dao F87, Davidson R88, DeFazio A74,75, Delnatte C89, Doheny KF17, Diez O90,91, Ding YC92, Doherty JA93, Domchek SM55, Dorfling CM94, Dörk T95, Dossus L96, Duran M97, Dürst M98, Dworniczak B99, Eccles D100, Edwards T37,38,39,40, Eeles R101, Eilber U72, Ejlertsen B102, Ekici AB103, Ellis S12, Elvira M85; EMBRACE Study, Eng KH104, Engel C105, Evans DG106, Fasching PA36,107, Ferguson S44, Ferrer SF108, Flanagan JM109, Fogarty ZC7, Fortner RT72, Fostira F110, Foulkes WD111, Fountzilas G112, Fridley BL113, Friebel TM114, Friedman E115,116, Frost D12, Ganz PA117, Garber J118, García MJ41,42, Garcia-Barberan V65, Gehrig A119; GEMO Study Collaborators, Gentry-Maharaj A120, Gerdes AM121, Giles GG60,122,123, Glasspool R124, Glendon G125, Godwin AK126, Goldgar DE127, Goranova T56, Gore M128, Greene MH129, Gronwald J130, Gruber S131, Hahnen E132, Haiman CA133, Håkansson N134, Hamann U135, Hansen TVO136, Harrington PA5, Harris HR134, Hauke J132; HEBON Study, Hein A36, Henderson A137, Hildebrandt MAT138, Hillemanns P139, Hodgson S140, Høgdall CK141, Høgdall E142,143, Hogervorst FBL144, Holland H11, Hooning MJ145, Hosking K5, Huang RY146, Hulick PJ147, Hung J74,75, Hunter DJ148, Huntsman DG149,150, Huzarski T130, Imyanitov EN151, Isaacs C152, Iversen ES153, Izatt L154, Izquierdo A61, Jakubowska A130, James P155,156, Janavicius R157,158, Jernetz M159, Jensen A142, Jensen UB160, John EM161, Johnatty S11, Jones ME162, Kannisto P159, Karlan BY6, Karnezis A149,150, Kast K163; KConFab Investigators, Kennedy CJ74,75, Khusnutdinova E43, Kiemeney LA15, Kiiski JI164, Kim SW165, Kjaer SK141,142, Köbel M166, Kopperud RK46,47, Kruse TA167, Kupryjanczyk J86, Kwong A168,169,170, Laitman Y115,116, Lambrechts D171,172, Larrañaga N173,174, Larson MC7, Lazaro C175, Le ND176, Le Marchand L177, Lee JW178, Lele SB179, Leminen A164, Leroux D180, Lester J6, Lesueur F181,182, Levine DA87, Liang D183, Liebrich C184, Lilyquist J185, Lipworth L37,38,40, Lissowska J186, Lu KH187, Lubinński J130, Luccarini C5, Lundvall L188, Mai PL129, Mendoza-Fandiño G1, Manoukian S28, Massuger LFAG15, May T44, Mazoyer S189, McAlpine JN190, McGuire V191, McLaughlin JR192, McNeish I193, Meijers-Heijboer H194, Meindl A195, Menon U120, Mensenkamp AR196, Merritt MA197, Milne RL60,122, Mitchell G155,156, Modugno F198,199,200, Moes-Sosnowska J86, Moffitt M35,201, Montagna M202, Moysich KB69, Mulligan AM20,203, Musinsky J204, Nathanson KL55, Nedergaard L205, Ness RB206, Neuhausen SL92, Nevanlinna H164, Niederacher D207, Nussbaum RL208,209, Odunsi K179, Olah E210, Olopade OI211, Olsson H58,212, Olswold C185, O'Malley DM213, Ong KR214, Onland-Moret NC215; OPAL study group, Orr N216, Orsulic S6, Osorio A41, Palli D217, Papi L218, Park-Simon TW139, Paul J219, Pearce CL133,220, Pedersen IS221, Peeters PHM215, Peissel B28, Peixoto A222, Pejovic T35,201, Pelttari LM164, Permuth JB1, Peterlongo P223, Pezzani L28, Pfeiler G224, Phillips KA122,156,225, Piedmonte M226, Pike MC133,227, Piskorz AM56, Poblete SR179, Pocza T210, Poole EM228, Poppe B78, Porteous ME229, Prieur F230, Prokofyeva D85, Pugh E17, Pujana MA231, Pujol P232, Radice P233, Rantala J234, Rappaport-Fuerhauser C224, Rennert G235,236, Rhiem K132, Rice P49, Richardson A237, Robson M238, Rodriguez GC239, Rodríguez-Antona C42,240, Romm J17, Rookus MA241, Rossing MA242, Rothstein JH191, Rudolph A72, Runnebaum IB98, Salvesen HB46,47, Sandler DP243, Schoemaker MJ162, Senter L244, Setiawan VW133, Severi G245,246,247,248, Sharma P249, Shelford T17, Siddiqui N250, Side LE251, Sieh W191, Singer CF224, Sobol H252, Song H5, Southey MC253, Spurdle AB11, Stadler Z238, Steinemann D254, Stoppa-Lyonnet D62, Sucheston-Campbell LE255, Sukiennicki G130, Sutphen R256, Sutter C257, Swerdlow AJ162,258, Szabo CI259, Szafron L86, Tan YY224, Taylor JA243, Tea MK224, Teixeira MR222,260, Teo SH261,262, Terry KL81,263, Thompson PJ264, Thomsen LCV46,47, Thull DL265, Tihomirova L266, Tinker AV267, Tischkowitz M111,268, Tognazzo S202, Toland AE269, Tone A44, Trabert B48, Travis RC270, Trichopoulou A271,272, Tung N273, Tworoger SS228,263, van Altena AM274, Van Den Berg D133, van der Hout AH275, van der Luijt RB276, Van Heetvelde M78, Van Nieuwenhuysen E277, van Rensburg EJ94, Vanderstichele A277, Varon-Mateeva R278, Vega A279,280, Edwards DV38,40,281, Vergote I277, Vierkant RA7, Vijai J204, Vratimos A110, Walker L282, Walsh C6, Wand D283, Wang-Gohrke S284, Wappenschmidt B132, Webb PM285, Weinberg CR286, Weitzel JN287, Wentzensen N48, Whittemore AS191,288, Wijnen JT289, Wilkens LR177, Wolk A134, Woo M149,150, Wu X138, Wu AH133, Yang H48, Yannoukakos D110, Ziogas A22, Zorn KK265, Narod SA290, Easton DF4,5, Amos CI291, Schildkraut JM292, Ramus SJ293,294, Ottini L295, Goodman MT264,296, Park SK297,298,299, Kelemen LE300, Risch HA301, Thomassen M167, Offit K204, Simard J13, Schmutzler RK132, Hazelett D302, Monteiro AN1, Couch FJ82, Berchuck A8, Chenevix-Trench G11, Goode EL9, Sellers TA1, Gayther SA10, Antoniou AC4,5, Pharoah PDP4,5.

Author information

1
Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, Florida, USA.
2
Department of Gynecologic Oncology, Moffitt Cancer Center, Tampa, Florida, USA.
3
Wellcome Trust Sanger Institute, Wellcome Genome Campus, Hinxton, UK.
4
Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Strangeways Research Laboratory, Cambridge, UK.
5
Department of Oncology, Centre for Cancer Genetic Epidemiology, University of Cambridge, Strangeways Research Laboratory, Cambridge, UK.
6
Women's Cancer Program at the Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California, USA.
7
Division of Biomedical Statistics and Informatics, Department of Health Science Research, Mayo Clinic, Rochester, Minnesota, USA.
8
Department of Obstetrics and Gynecology, Duke University Medical Center, Durham, North Carolina, USA.
9
Department of Health Science Research, Division of Epidemiology, Mayo Clinic, Rochester, Minnesota, USA.
10
Center for Bioinformatics and Functional Genomics, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California, USA.
11
Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
12
Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
13
Genomics Center, Centre Hospitalier Universitaire de Québec Research Center and Laval University, Quebec City, Quebec, Canada.
14
Department of Clinical Genetics, Academic Medical Center, Amsterdam, the Netherlands.
15
Radboud University Medical Center, Radboud Institute for Health Sciences, Department for Health Evidence, Nijmegen, the Netherlands.
16
Netherlands Comprehensive Cancer Organisation, Utrecht, the Netherlands.
17
Center for Inherited Disease Research, Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.
18
Yorkshire Regional Genetics Service, Chapel Allerton Hospital, Leeds, UK.
19
Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital and Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada.
20
Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada.
21
Genetic Epidemiology Research Institute, UCI Center for Cancer Genetics Research and Prevention, School of Medicine, University of California-Irvine, Irvine, California, USA.
22
Department of Epidemiology, University of California-Irvine, Irvine, California, USA.
23
N.N. Alexandrov National Cancer Centre of Belarus, Minsk, Belarus.
24
'Agii Anargiri' Cancer Hospital, Athens, Greece.
25
Department of Gynaecology and Obstetrics, University Hospital of Schleswig-Holstein, Campus Kiel, Christian Albrechts University Kiel, Kiel, Germany.
26
Department of Breast Medical Oncology and Clinical Cancer Genetics Program, University of Texas MD Anderson Cancer Center, Houston, Texas, USA.
27
Department of Oncology and Pathology, Karolinska University Hospital and Karolinska Institutet, Stockholm, Sweden.
28
Unit of Medical Genetics, Department of Preventive and Predictive Medicine, Fondazione IRCCS (Istituto di Ricovero e Cura a Carattere Scientifico) Istituto Nazionale Tumori (INT), Milan, Italy.
29
Department of Medical Oncology, University Hospital, Vall d'Hebron, Barcelona, Spain.
30
Gynaecology Unit, Royal Marsden Hospital, London, UK.
31
Bâtiment Cheney D, Centre Léon Bérard, Lyon, France.
32
Laboratory of Cell Biology, Department of Pathology, Landspitali, Reykjavik, Iceland.
33
BMC (Biomedical Centre), Faculty of Medicine, University of Iceland, Reykjavik, Iceland.
34
Department of Gynecologic Oncology, Oregon Health &Science University, Portland, Oregon, USA.
35
Knight Cancer Institute, Oregon Health &Science University, Portland, Oregon, USA.
36
Department of Gynecology and Obstetrics, Universtiy Hospital Erlangen, Friedrich Alexander University Erlangen-Nuremberg, Comprehensive Cancer Center Erlangen-Nuremberg, Erlangen, Germany.
37
Division of Epidemiology, Department of Medicine, Vanderbilt School of Medicine, Nashville, Tennessee, USA.
38
Vanderbilt Epidemiology Center, Department of Medicine, Vanderbilt Medical School, Nashville, Tennessee, USA.
39
Institute for Medicine and Public Health, Vanderbilt School of Medicine, Nashville, Tennessee, USA.
40
Vanderbilt-Ingram Cancer Center, Vanderbilt School of Medicine, Nashville, Tennessee, USA.
41
Human Genetics Group, Spanish National Cancer Centre (CNIO), Madrid, Spain.
42
Biomedical Network on Rare Diseases (CIBERER), Madrid, Spain.
43
Institute of Biochemistry and Genetics, Ufa Science Center, Russian Academy of Sciences, Ufa, Russian Federation.
44
Division of Gynecologic Oncology, Princess Margaret Hospital, University Health Network, Toronto, Ontario, Canada.
45
Department of Medicine, Massachusetts General Hospital, Boston, Massachusetts, USA.
46
Department of Gynecology and Obstetrics, Haukeland University Hospital, Bergen, Norway.
47
Centre for Cancer Biomarkers, Department of Clinical Science, University of Bergen, Bergen, Norway.
48
Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Maryland, USA.
49
Clinical Cancer Genetics for the City of Hope, Clinical Cancer Genetics Community Research Network, Duarte, California, USA.
50
Department of Clinical Genetics, Maastricht University Medical Center, Maastricht, the Netherlands.
51
Radiation Oncology Research Unit, Hannover Medical School, Hannover, Germany.
52
Department of Clinical Genetics, Vejle Hospital, Vejle, Denmark.
53
Division of Cancer Prevention and Genetics, Istituto Europeo di Oncologia (IEO), Milan, Italy.
54
Department of Oncology, Clinical Sciences, Lund University and Skåne University Hospital, Lund, Sweden.
55
Department of Medicine, Abramson Cancer Center, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania, USA.
56
Cancer Research UK (CRUK) Cambridge Institute, University of Cambridge, Cambridge, UK.
57
Department of Clinical Genetics, Royal Devon and Exeter Hospital, Exeter, UK.
58
Department of Cancer Epidemiology, University Hospital, Lund, Lund University, Lund, Sweden.
59
Canada's Michael Smith Genome Sciences Centre, BC Cancer Agency, Vancouver, British Columbia, Canada.
60
Cancer Epidemiology Centre, Cancer Council Victoria, Melbourne, Victoria, Australia.
61
Genetic Counseling Unit, Hereditary Cancer Program, IDIBGI (Institut d'Investigació Biomèdica de Girona), Catalan Institute of Oncology, Girona, Spain.
62
Service de Génétique Oncologique, Institut Curie, Paris, France.
63
Department of Pathology, University of Helsinki and Helsinki University Hospital, Helsinki, Finland.
64
Department of Medicine, Huntsman Cancer Institute, Salt Lake City, Utah, USA.
65
Molecular Oncology Laboratory, Hospital Clínico San Carlos, IdISSC (Instituto de Investigación Sanitaria del Hospital Clínico San Carlos), Madrid, Spain.
66
Section of Genetic Oncology, Department of Laboratory Medicine, University and University Hospital of Pisa, Pisa, Italy.
67
Cancer Genetics Laboratory, Research Division, Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
68
Department of Pathology, University of Melbourne, Parkville, Victoria, Australia.
69
Cancer Pathology and Prevention, Division of Cancer Prevention and Population Sciences, Roswell Park Cancer Institute, Buffalo, New York, USA.
70
Department of Obstetrics and Gynecology, John A. Burns School of Medicine, University of Hawaii, Honolulu, Hawaii, USA.
71
Cancer Risk Program, University of California, San Francisco, San Francisco, California, USA.
72
Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
73
University Cancer Center Hamburg (UCCH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
74
Centre for Cancer Research, Westmead Institute for Medical Research, University of Sydney, Sydney, New South Wales, Australia.
75
Department of Gynaecological Oncology, Westmead Hospital, Sydney, New South Wales, Australia.
76
Unité de Recherche en Santé des Populations, Centre des Maladies du Sein Deschênes-Fabia, Centre de Recherche FRSQ du Centre Hospitalier Affilié Universitaire de Québec, Quebec City, Quebec, Canada.
77
Departments of Pediatrics and Medicine, Columbia University, New York, New York, USA.
78
Center for Medical Genetics, Ghent University, Ghent, Belgium.
79
Division of Epidemiology, Biostatistics and Preventative Medicine, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico, USA.
80
Sheffield Clinical Genetics Service, Sheffield Children's Hospital, Sheffield, UK.
81
Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA.
82
Division of Experimental Pathology, Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, Minnesota, USA.
83
Social &Scientific Systems, Inc., Durham, North Carolina, USA.
84
Department of Clinical Genetics, Fox Chase Cancer Center, Philadelphia, Pennsylvania, USA.
85
Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa, Russian Federation.
86
Department of Pathology and Laboratory Diagnostics, Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland.
87
Gynecology Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York, USA.
88
Department of Clinical Genetics, South Glasgow University Hospitals, Glasgow, UK.
89
Unité d'Oncogénétique, ICO-Centre René Gauducheau, Nantes, France.
90
Oncogenetics Group, Vall d'Hebron Institute of Oncology, Barcelona, Spain.
91
Clinical and Molecular Genetics Area, Vall d'Hebron University Hospital. Barcelona, Spain.
92
Department of Population Sciences, Beckman Research Institute of City of Hope, Duarte, California, USA.
93
Department of Epidemiology, Geisel School of Medicine at Dartmouth, Hanover, New Hampshire, USA.
94
Cancer Genetics Laboratory, Department of Genetics, University of Pretoria, Pretoria, South Africa.
95
Gynaecology Research Unit, Hannover Medical School, Hannover, Germany.
96
Nutrition and Metabolism Section, International Agency for Research on Cancer (IARC-WHO), Lyon, France.
97
Institute of Biology and Molecular Genetics, Universidad de Valladolid (IBGM-UVA), Valladolid, Spain.
98
Department of Gynecology, Jena University Hospital-Friedrich Schiller University, Jena, Germany.
99
Institute of Human Genetics, Münster, Germany.
100
University of Southampton Faculty of Medicine, Southampton University Hospitals NHS Trust, Southampton, UK.
101
Oncogenetics Team, Institute of Cancer Research and Royal Marsden NHS Foundation Trust, Sutton, UK.
102
Department of Oncology, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
103
Institute of Human Genetics, Friedrich Alexander University Erlangen-Nuremberg, Erlangen, Germany.
104
Department of Biostatistics and Bioinformatics, Roswell Park Institute, Buffalo, New York, USA.
105
Institute for Medical Informatics, Statistics and Epidemiology, University of Leipzig, Leipzig, Germany.
106
Genomic Medicine, Manchester Academic Health Sciences Centre, University of Manchester, Central Manchester University Hospitals NHS Foundation Trust, Manchester, UK.
107
Division of Hematology and Oncology, Department of Medicine, UCLA David Geffen School of Medicine, Los Angeles, California, USA.
108
Laboratoire de Génétique Chromosomique, Hôtel Dieu Centre Hospitalier, Chambéry, France.
109
Department of Surgery and Cancer, Imperial College London, London, UK.
110
Molecular Diagnostics Laboratory, INRASTES, National Centre for Scientific Research 'Demokritos', Aghia Paraskevi Attikis, Athens, Greece.
111
Program in Cancer Genetics, Departments of Human Genetics and Oncology, McGill University, Montreal, Quebec, Canada.
112
Department of Medical Oncology, Papageorgiou, Hospital, Aristotle University of Thessaloniki School of Medicine, Thessaloniki, Greece.
113
Biostatistics and Informatics Shared Resource, University of Kansas Medical Center, Kansas City, Kansas, USA.
114
Harvard T.H. Chan School of Public Health and Dana-Farber Cancer Institute, Boston, Massachusetts, USA.
115
Susanne Levy Gertner Oncogenetics Unit, Institute of Human Genetics, Chaim Sheba Medical Center, Ramat Gan, Israel.
116
Sackler Faculty of Medicine, Tel Aviv University, Ramat Aviv, Israel.
117
Division of Cancer Prevention and Control Research, Jonsson Comprehensive Cancer Center, UCLA Schools of Medicine and Public Health, Los Angeles, California, USA.
118
Cancer Risk and Prevention Clinic, Dana-Farber Cancer Institute, Boston, Massachusetts, USA.
119
Centre of Familial Breast and Ovarian Cancer, Department of Medical Genetics, Institute of Human Genetics, University Würzburg, Würzburg, Germany.
120
Women's Cancer, Institute for Women's Health, University College London, London, UK.
121
Department of Clinical Genetics, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
122
Centre for Epidemiology and Biostatistics, School of Population and Global Health, University of Melbourne, Melbourne, Victoria, Australia.
123
Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, Victoria, Australia.
124
Beatson West of Scotland Cancer Centre, Glasgow, UK.
125
Ontario Cancer Genetics Network: Samuel Lunenfeld Research Institute, Mount Sinai Hospital, Toronto, Ontario, Canada.
126
Department of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, Kansas, USA.
127
Department of Dermatology, University of Utah School of Medicine, Salt Lake City, Utah, USA.
128
Department of Medicine, Royal Marsden Hospital, London, UK.
129
Clinical Genetics Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, US National Institutes of Health, Bethesda, Maryland, USA.
130
Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland.
131
Keck School of Medicine and Norris Comprehensive Cancer Center, University of Southern California, Los Angeles, California, USA.
132
Center for Familial Breast and Ovarian Cancer, Center for Integrated Oncology (CIO) and Center for Molecular Medicine Cologne (CMMC), University Hospital Cologne, Cologne, Germany.
133
Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Los Angeles, California, USA.
134
Division of Nutritional Epidemiology, Department of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
135
Molecular Genetics of Breast Cancer, Deutsches Krebsforschungszentrum (DKFZ), Heidelberg, Germany.
136
Center for Genomic Medicine, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
137
Institute of Genetic Medicine, Centre for Life, Newcastle-upon-Tyne Hospitals NHS Trust, Newcastle-upon-Tyne, UK.
138
Department of Epidemiology, University of Texas MD Anderson Cancer Center, Houston, Texas, USA.
139
Clinics of Obstetrics and Gynaecology, Hannover Medical School, Hannover, Germany.
140
Medical Genetics Unit, St George's University of London, London, UK.
141
Department of Gynecology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark.
142
Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark.
143
Molecular Unit, Department of Pathology, Herlev Hospital, University of Copenhagen, Copenhagen, Denmark.
144
Family Cancer Clinic, Netherlands Cancer Institute, Amsterdam, the Netherlands.
145
Department of Medical Oncology, Family Cancer Clinic, Erasmus University Medical Center, Rotterdam, the Netherlands.
146
Center for Immunotherapy, Roswell Park Cancer Institute, Buffalo, New York, USA.
147
Center for Medical Genetics, NorthShore University HealthSystem, University of Chicago Pritzker School of Medicine, Evanston, Illinois, USA.
148
Program in Genetic Epidemiology and Statistical Genetics, Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.
149
Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, British Columbia, Canada.
150
British Columbia Cancer Agency, Vancouver, British Columbia, Canada.
151
N.N. Petrov Institute of Oncology, St. Petersburg, Russian Federation.
152
Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC, USA.
153
Department of Statistical Science, Duke University, Durham, North Carolina, USA.
154
Clinical Genetics, Guy's and St Thomas' NHS Foundation Trust, London, UK.
155
Familial Cancer Centre, Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
156
Sir Peter MacCallum Department of Oncology, University of Melbourne, Parkville, Victoria, Australia.
157
Department of Molecular and Regenerative Medicine, Hematology, Oncology and Transfusion Medicine Center, Vilnius University Hospital Santariskiu Clinics, Vilnius, Lithuania.
158
State Research Institute Centre for Innovative Medicine, Vilnius, Lithuania.
159
Department of Obstetrics and Gynecology, Lund University Hospital, Lund, Sweden.
160
Department of Clinical Genetics, Aarhus University Hospital, Aarhus, Denmark.
161
Department of Epidemiology, Cancer Prevention Institute of California, Fremont, California, USA.
162
Division of Genetics and Epidemiology, Institute of Cancer Research, London, UK.
163
Department of Gynaecology and Obstetrics, University Hospital Carl Gustav Carus, Technical University Dresden, Dresden, Germany.
164
Department of Obstetrics and Gynecology, University of Helsinki and Helsinki University Central Hospital, Helsinki, Finland.
165
Department of Surgery, Breast Care Center, Daerim St. Mary's Hospital, Seoul, Republic of Korea.
166
Department of Pathology, University of Calgary, Calgary, Alberta, Canada.
167
Department of Clinical Genetics, Odense University Hospital, Odense, Denmark.
168
Hong Kong Hereditary Breast Cancer Family Registry, Hong Kong.
169
Department of Surgery, University of Hong Kong, Hong Kong.
170
Cancer Genetics Center and Department of Surgery, Hong Kong Sanatorium and Hospital, Hong Kong.
171
Vesalius Research Center, VIB, Leuven, Belgium.
172
Laboratory for Translational Genetics, Department of Oncology, KU Leuven, Leuven, Belgium.
173
Public Health Division of Gipuzkoa, Regional Government of the Basque Country, Donostia-San Sebastian, Spain.
174
CIBER of Epidemiology and Public Health, Madrid, Spain.
175
Molecular Diagnostic Unit, Hereditary Cancer Program, IDIBELL-Catalan Institute of Oncology, Barcelona, Spain.
176
Cancer Control Research, BC Cancer Agency, Vancouver, British Columbia, Canada.
177
Cancer Epidemiology Program, University of Hawaii Cancer Center, Honolulu, Hawaii, USA.
178
Department of Surgery, Ulsan College of Medicine and Asan Medical Center, Seoul, Republic of Korea.
179
Department of Gynecological Oncology, Roswell Park Cancer Institute, Buffalo, New York, USA.
180
Département de Génétique, Centre Hospitalier Universitaire de Grenoble, Grenoble, France.
181
Institut Curie, PSL Research Unviersity and INSERM U900, Paris, France.
182
Mines Paris Tech, Fontainebleau, France.
183
College of Pharmacy and Health Sciences, Texas Southern University, Houston, Texas, USA.
184
Cancer Center Wolfsburg, Clinics of Gynaecology, Wolfsburg, Germany.
185
Department of Health Sciences Research, Division of Epidemiology, Mayo Clinic, Rochester, Minnesota, USA.
186
Department of Cancer Epidemiology and Prevention, Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland.
187
Department of Gynecologic Oncology, University of Texas MD Anderson Cancer Center, Houston, Texas, USA.
188
Juliane Marie Centre, Department of Gynecology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark.
189
INSERM U1052, CNRS UMR 5286, Université Lyon 1, Centre de Recherche en Cancérologie de Lyon, Centre Léon Bérard, Lyon, France.
190
Ovarian Cancer Research (OVCARE) Program-Gynecologic Tissue Bank, Vancouver General Hospital and BC Cancer Agency, Vancouver, British Columbia, Canada.
191
Department of Health Research and Policy-Epidemiology, Stanford University School of Medicine, Stanford, California, USA.
192
Public Health Ontario, Toronto, Ontario, Canada.
193
Institute of Cancer Sciences, University of Glasgow, Wolfson Wohl Cancer Research Centre, Beatson Institute for Cancer Research, Glasgow, UK.
194
Department of Clinical Genetics, VU University Medical Centre, Amsterdam, the Netherlands.
195
Department of Gynaecology and Obstetrics, Division of Tumor Genetics, Klinikum Rechts der Isar, Technical University of Munich, Munich, Germany.
196
Department of Human Genetics, Radboud University Medical Centre, Nijmegen, the Netherlands.
197
Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK.
198
Division of Gynecologic Oncology, Department of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.
199
Department of Epidemiology, University of Pittsburgh Graduate School of Public Health, Pittsburgh, Pennsylvania, USA.
200
Ovarian Cancer Center of Excellence, Womens Cancer Research Program, Magee-Womens Research Institute and University of Pittsburgh Cancer Institute, Pittsburgh, Pennsylvania, USA.
201
Department of Obstetrics and Gynecology, Oregon Health &Science University, Portland, Oregon, USA.
202
Immunology and Molecular Oncology Unit, Veneto Institute of Oncology IOV-IRCCS, Padua, Italy.
203
Department of Laboratory Medicine and Keenan Research Centre of the Li Ka Shing Knowledge Institute, St Michael's Hospital, Toronto, Ontario, Canada.
204
Clinical Genetics Research Laboratory, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, New York, USA.
205
Department of Pathology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark.
206
University of Texas School of Public Health, Houston, Texas, USA.
207
Department of Gynaecology and Obstetrics, University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Düsseldorf, Germany.
208
Invitae Corporation, San Francisco, California, USA.
209
Department of Medicine, University of California, San Francisco, San Francisco, California, USA.
210
Department of Molecular Genetics, National Institute of Oncology, Budapest, Hungary.
211
Center for Clinical Cancer Genetics and Global Health, University of Chicago Medical Center, Chicago, Illinois, USA.
212
Department of Oncology, Lund University Hospital, Lund, Sweden.
213
Department of Obstetrics and Gynecology, Ohio State University and the James Cancer Center, Columbus, Ohio, USA.
214
West Midlands Regional Genetics Service, Birmingham Women's Hospital Healthcare NHS Trust, Edgbaston, Birmingham, UK.
215
Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, the Netherlands.
216
Breast Cancer Now Toby Robins Research Centre, Institute of Cancer Research, London, UK.
217
Molecular and Nutritional Epidemiology Unit, Cancer Research and Prevention Institute-ISPO, Florence, Italy.
218
Unit of Medical Genetics, Department of Biomedical, Experimental and Clinical Sciences, University of Florence, Florence, Italy.
219
Cancer Research UK Clinical Trials Unit, Institute of Cancer Sciences, University of Glasgow, Glasgow, UK.
220
Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, Michigan, USA.
221
Section of Molecular Diagnostics, Clinical Biochemistry, Aalborg University Hospital, Aalborg, Denmark.
222
Department of Genetics, Portuguese Oncology Institute, Porto, Portugal.
223
IFOM, FIRC (Italian Foundation for Cancer Research) Institute of Molecular Oncology, Milan, Italy.
224
Department of Obstetrics and Gynecology, Medical University of Vienna and Comprehensive Cancer Center, Vienna, Austria.
225
Division of Cancer Medicine, Peter MacCallum Cancer Centre, East Melbourne, Victoria, Australia.
226
NRG Oncology, Statistics and Data Management Center, Roswell Park Cancer Institute, Buffalo, New York, USA.
227
Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, New York, USA.
228
Channing Division of Network Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA.
229
South East of Scotland Regional Genetics Service, Western General Hospital, Edinburgh, UK.
230
Service de Génétique Clinique Chromosomique et Moléculaire, Centre Hospitalier Universitaire de St Etienne, St Etienne, France.
231
Translational Research Laboratory, IDIBELL (Bellvitge Biomedical Research Institute), Catalan Institute of Oncology, Barcelona, Spain.
232
Unité d'Oncogénétique, Centre Hospitalier Universitaire Arnaud de Villeneuve, Montpellier, France.
233
Unit of Molecular Bases of Genetic Risk and Genetic Testing, Department of Preventive and Predictive Medicine, Fondazione IRCCS (Istituto di Ricovero e Cura a Carattere Scientifico) Istituto Nazionale Tumori (INT), Milan, Italy.
234
Department of Clinical Genetics, Karolinska University Hospital, Stockholm, Sweden.
235
Clalit National Israeli Cancer Control Center, Haifa, Israel.
236
Department of Community Medicine and Epidemiology, Carmel Medical Center and B. Rappaport Faculty of Medicine, Haifa, Israel.
237
Department of Pathology, Brigham and Women's Hospital, Dana-Farber Cancer Institute, Boston, Massachusetts, USA.
238
Clinical Genetics Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, New York, USA.
239
Division of Gynecologic Oncology, NorthShore University HealthSystem, University of Chicago, Evanston, Illinois, USA.
240
Hereditary Endocrine Cancer Group, Spanish National Cancer Research Center (CNIO), Madrid, Spain.
241
Department of Epidemiology, Netherlands Cancer Institute, Amsterdam, the Netherlands.
242
Program in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington, USA.
243
Epidemiology Branch, Division of Intramural Research, National Institute of Environmental Health Sciences, US National Institutes of Health, Research Triangle Park, North Carolina, USA.
244
Clinical Cancer Genetics Program, Division of Human Genetics, Department of Internal Medicine, Comprehensive Cancer Center, Ohio State University, Columbus, Ohio, USA.
245
Facultés de Médecin, Université Paris-Sud, Villejuif, France.
246
Institut Gustave Roussy, Villejuif, France.
247
Human Genetics Foundation (HuGeF), Turin, Italy.
248
Facultés de Médecin, Université Paris-Saclay, Paris, France.
249
Department of Hematology and Oncology, University of Kansas Medical Center, Kansas City, Kansas, USA.
250
Department of Gynaecological Oncology, Glasgow Royal Infirmary, Glasgow, UK.
251
North East Thames Regional Genetics Service, Great Ormond Street Hospital for Children NHS Trust, London, UK.
252
Département Oncologie Génétique, Institut Paoli-Calmettes, Marseille, France.
253
Genetic Epidemiology Laboratory, Department of Pathology, University of Melbourne, Parkville, Victoria, Australia.
254
Institute of Human Genetics, Hannover Medical School, Hannover, Germany.
255
Department of Cancer Prevention and Control, Roswell Park Cancer Institute, Buffalo, New York, USA.
256
Epidemiology Center, College of Medicine, University of South Florida, Tampa, Florida, USA.
257
Institute of Human Genetics, Department of Human Genetics, University Hospital Heidelberg, Heidelberg, Germany.
258
Division of Breast Cancer Research, Institute of Cancer Research, London, UK.
259
National Human Genome Research Institute, US National Institutes of Health, Bethesda, Maryland, USA.
260
Biomedical Sciences Institute (ICBAS), University of Porto, Porto, Portugal.
261
Cancer Research Initiatives Foundation, Sime Darby Medical Centre, Subang Jaya, Malaysia.
262
University Malaya Cancer Research Institute, Faculty of Medicine, University Malaya Medical Centre, University Malaya, Kuala Lumpur, Malaysia.
263
Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.
264
Cancer Prevention and Control, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California, USA.
265
Magee-Womens Hospital of UPMC, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.
266
Latvian Biomedical Research and Study Centre, Riga, Latvia.
267
Ovarian Cancer Research (OVCARE) Program-Cheryl Brown Ovarian Cancer Outcomes Unit (CBOCOU), BC Cancer Agency, Vancouver, British Columbia, Canada.
268
Department of Medical Genetics, Addenbrooke's Treatment Centre, Addenbrooke's Hospital, Cambridge, UK.
269
Division of Human Cancer Genetics, Departments of Internal Medicine and Molecular Virology, Immunology and Medical Genetics, Comprehensive Cancer Center, Ohio State University, Columbus, Ohio, USA.
270
Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, UK.
271
Hellenic Health Foundation, Athens, Greece.
272
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.
273
Department of Medical Oncology, Beth Israel Deaconess Medical Center, Boston, Massachusetts, USA.
274
Division of Gynecologic Oncology, Department of Obstetrics and Gynaecology, Radboud University Medical Centre, Nijmegen, the Netherlands.
275
Department of Genetics, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands.
276
Department of Medical Genetics, University Medical Center Utrecht, Utrecht, the Netherlands.
277
Division of Gynecologic Oncology, Department of Obstetrics and Gynaecology and Leuven Cancer Institute, University Hospitals Leuven, Leuven, Belgium.
278
Institute of Medical and Human Genetics, Charité Universitätsmedizin, Campus Virchov Klinikum, Berlin, Germany.
279
Fundación Pública Galega de Medicina Xenómica, Servizo Galego de Saúde (SERGAS), Instituto de Investigación Sanitaria (IDIS), Santiago de Compostela, Spain.
280
Grupo de Medicina Xenómica, Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Universidade de Santiago de Compostela (USC), Santiago de Compostela, Spain.
281
Vanderbilt Genetics Institute and Department of Obstetrics and Gynecology, Vanderbilt University Medical Center, Nashville, Tennessee, USA.
282
Oxford Regional Genetics Service, Churchill Hospital, Oxford, UK.
283
Institute of Human Genetics, University Hospital, Leipzig, Germany.
284
Department of Obstetrics and Gynecology, University of Ulm, Ulm, Germany.
285
Population Health Department, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia.
286
Biostatistics and Computational Biology Branch, Division of Intramural Research, National Institute of Environmental Health Sciences, US National Institutes of Health, Research Triangle Park, North Carolina, USA.
287
Clinical Cancer Genetics, City of Hope, Duarte, California, USA.
288
Department of Data Management Science, Stanford University School of Medicine, Stanford, California, USA.
289
Departments of Human Genetics and Clinical Genetics, Leiden University Medical Center, Leiden, the Netherlands.
290
Women's College Research Institute, University of Toronto, Toronto, Ontario, Canada.
291
Center for Genomic Medicine, Department of Biomedical Data Science, Geisel School of Medicine at Dartmouth, Lebanon, New Hampshire, USA.
292
Department of Public Health Sciences, University of Virginia, Charlottesville, Virginia, USA.
293
School of Women's and Children's Health, Lowy Cancer Research Centre, University of New South Wales, Sydney, New South Wales, Australia.
294
Kinghorn Cancer Centre, Garvan Institute of Medical Research, Darlinghurst, New South Wales, Australia.
295
Department of Molecular Medicine, University La Sapienza, Rome, Italy.
296
Community and Population Health Research Institute, Department of Biomedical Sciences, Cedars-Sinai Medical Center, Los Angeles, California, USA.
297
Department of Preventive Medicine, College of Medicine, Seoul National University, Seoul, Republic of Korea.
298
Seoul National University Cancer Research Institute, Seoul, Republic of Korea.
299
Department of Biomedical Science, Graduate School, Seoul National University, Seoul, Republic of Korea.
300
Department of Public Health Sciences, College of Medicine, Medical University of South Carolina, Charleston, South Carolina, USA.
301
Department of Chronic Disease Epidemiology, Yale School of Public Health, New Haven, Connecticut, USA.
302
Department of Biomedical Sciences, Cedars-Sinai Medical Center, Los Angeles, California, USA.

Abstract

To identify common alleles associated with different histotypes of epithelial ovarian cancer (EOC), we pooled data from multiple genome-wide genotyping projects totaling 25,509 EOC cases and 40,941 controls. We identified nine new susceptibility loci for different EOC histotypes: six for serous EOC histotypes (3q28, 4q32.3, 8q21.11, 10q24.33, 18q11.2 and 22q12.1), two for mucinous EOC (3q22.3 and 9q31.1) and one for endometrioid EOC (5q12.3). We then performed meta-analysis on the results for high-grade serous ovarian cancer with the results from analysis of 31,448 BRCA1 and BRCA2 mutation carriers, including 3,887 mutation carriers with EOC. This identified three additional susceptibility loci at 2q13, 8q24.1 and 12q24.31. Integrated analyses of genes and regulatory biofeatures at each locus predicted candidate susceptibility genes, including OBFC1, a new candidate susceptibility gene for low-grade and borderline serous EOC.

PMID:
28346442
PMCID:
PMC5612337
DOI:
10.1038/ng.3826
[Indexed for MEDLINE]
Free PMC Article

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