Characterizing prostate cancer risk through multi-ancestry genome-wide discovery of 187 novel risk variants

doi:10.1038/s41588-023-01534-4

. 2023 Dec;55(12):2065-2074.

doi: 10.1038/s41588-023-01534-4. Epub 2023 Nov 9.

Characterizing prostate cancer risk through multi-ancestry genome-wide discovery of 187 novel risk variants

Anqi Wang¹, Jiayi Shen¹, Alex A Rodriguez², Edward J Saunders³, Fei Chen¹, Rohini Janivara⁴, Burcu F Darst^{1

5}, Xin Sheng¹, Yili Xu¹, Alisha J Chou¹, Sara Benlloch⁶, Tokhir Dadaev³, Mark N Brook³, Anna Plym^{7

8}, Ali Sahimi⁹, Thomas J Hoffman^{10

11}, Atushi Takahashi^{12

13}, Koichi Matsuda¹⁴, Yukihide Momozawa¹⁵, Masashi Fujita¹⁶, Triin Laisk¹⁷, Jéssica Figuerêdo¹⁷, Kenneth Muir^{18

19}, Shuji Ito^{20

21}, Xiaoxi Liu²²; Biobank Japan Project; Yuji Uchio²⁰, Michiaki Kubo²¹, Yoichiro Kamatani^{22

23}, Artitaya Lophatananon¹⁸, Peggy Wan⁹, Caroline Andrews²⁴, Adriana Lori²⁵, Parichoy P Choudhury²⁶, Johanna Schleutker^{27

28}, Teuvo L J Tammela²⁹, Csilla Sipeky²⁷, Anssi Auvinen³⁰, Graham G Giles^{31

32

33}, Melissa C Southey³³, Robert J MacInnis^{31

32}, Cezary Cybulski³⁴, Dominika Wokolorczyk³⁴, Jan Lubinski³⁴, Christopher T Rentsch^{35

36

37}, Kelly Cho^{38

39}, Benjamin H Mcmahon⁴⁰, David E Neal^{41

42

43}, Jenny L Donovan⁴⁴, Freddie C Hamdy^{45

46}, Richard M Martin^{44

47

48}, Borge G Nordestgaard^{49

50}, Sune F Nielsen^{49

50}, Maren Weischer⁵⁰, Stig E Bojesen^{49

50}, Andreas Røder^{51

52}, Hein V Stroomberg⁵¹, Jyotsna Batra^{53

54}, Suzanne Chambers⁵⁵, Lisa Horvath^{56

57}, Judith A Clements⁵⁴, Wayne Tilly⁵⁸, Gail P Risbridger^{59

60}, Henrik Gronberg⁷, Markus Aly^{7

61

62}, Robert Szulkin^{7

63}, Martin Eklund⁷, Tobias Nordstrom^{7

64}, Nora Pashayan^{65

66}, Alison M Dunning⁶⁶, Maya Ghoussaini⁶⁷, Ruth C Travis⁶⁸, Tim J Key⁶⁸, Elio Riboli⁶⁹, Jong Y Park⁷⁰, Thomas A Sellers⁷⁰, Hui-Yi Lin⁷¹, Demetrius Albanes⁷², Stephanie Weinstein⁷², Michael B Cook⁷², Lorelei A Mucci⁷³, Edward Giovannucci⁷³, Sara Lindstrom⁷⁴, Peter Kraft⁷⁵, David J Hunter⁷⁶, Kathryn L Penney⁷⁷, Constance Turman⁷⁵, Catherine M Tangen⁷⁸, Phyllis J Goodman⁷⁸, Ian M Thompson Jr⁷⁹, Robert J Hamilton^{80

81}, Neil E Fleshner⁸⁰, Antonio Finelli⁸², Marie-Élise Parent⁸³, Janet L Stanford⁵, Elaine A Ostrander⁸⁴, Stella Koutros⁷², Laura E Beane Freeman⁷², Meir Stampfer⁷⁷, Alicja Wolk^{85

86}, Niclas Håkansson⁸⁵, Gerald L Andriole⁸⁷, Robert N Hoover⁷², Mitchell J Machiela⁷², Karina Dalsgaard Sørensen^{88

89}, Michael Borre^{89

90}, William J Blot^{91

92}, Wei Zheng⁹¹, Edward D Yeboah⁹³, James E Mensah^{93

94}, Yong-Jie Lu⁹⁵, Hong-Wei Zhang⁹⁶, Ninghan Feng⁹⁷, Xueying Mao⁹⁵, Yudong Wu⁹⁸, Shan-Chao Zhao⁹⁹, Zan Sun¹⁰⁰, Stephen N Thibodeau¹⁰¹, Shannon K McDonnell¹⁰², Daniel J Schaid¹⁰², Catharine M L West¹⁰³, Gill Barnett¹⁰⁴, Christiane Maier¹⁰⁵, Thomas Schnoeller¹⁰⁶, Manuel Luedeke¹⁰⁵, Adam S Kibel¹⁰⁷, Bettina F Drake¹⁰⁸, Olivier Cussenot^{109

110}, Geraldine Cancel-Tassin^{109

110}, Florence Menegaux¹¹¹, Thérèse Truong¹¹¹, Yves Akoli Koudou¹¹², Esther M John¹¹³, Eli Marie Grindedal¹¹⁴, Lovise Maehle¹¹⁴, Kay-Tee Khaw¹¹⁵, Sue A Ingles¹¹⁶, Mariana C Stern¹¹⁶, Ana Vega^{117

118

119}, Antonio Gómez-Caamaño¹²⁰, Laura Fachal^{117

118

119

121}, Barry S Rosenstein^{122

123}, Sarah L Kerns¹²⁴, Harry Ostrer¹²⁵, Manuel R Teixeira^{126

127

128}, Paula Paulo¹²⁷, Andreia Brandão¹²⁷, Stephen Watya¹²⁹, Alexander Lubwama¹²⁹, Jeannette T Bensen^{130

131}, Ebonee N Butler¹³⁰, James L Mohler^{131

132}, Jack A Taylor^{133

134}, Manolis Kogevinas^{135

136

137

138}, Trinidad Dierssen-Sotos^{138

139}, Gemma Castaño-Vinyals^{135

136

137

138}, Lisa Cannon-Albright^{140

141}, Craig C Teerlink^{140

141}, Chad D Huff¹⁴², Patrick Pilie¹⁴³, Yao Yu¹⁴², Ryan J Bohlender¹⁴², Jian Gu¹⁴², Sara S Strom¹⁴⁴, Luc Multigner¹⁴⁵, Pascal Blanchet¹⁴⁶, Laurent Brureau¹⁴⁶, Radka Kaneva¹⁴⁷, Chavdar Slavov¹⁴⁸, Vanio Mitev¹⁴⁷, Robin J Leach¹⁴⁹, Hermann Brenner^{150

151

152}, Xuechen Chen¹⁵⁰, Bernd Holleczek¹⁵³, Ben Schöttker¹⁵⁰, Eric A Klein^{154

155}, Ann W Hsing¹¹³, Rick A Kittles¹⁵⁶, Adam B Murphy¹⁵⁷, Christopher J Logothetis¹⁴³, Jeri Kim¹⁴³, Susan L Neuhausen¹⁵⁸, Linda Steele¹⁵⁸, Yuan Chun Ding¹⁵⁸, William B Isaacs¹⁵⁹, Barbara Nemesure¹⁶⁰, Anselm J M Hennis^{160

161}, John Carpten¹⁶², Hardev Pandha¹⁶³, Agnieszka Michael¹⁶³, Kim De Ruyck¹⁶⁴, Gert De Meerleer¹⁶⁵, Piet Ost¹⁶⁵, Jianfeng Xu¹⁶⁶, Azad Razack¹⁶⁷, Jasmine Lim¹⁶⁷, Soo-Hwang Teo¹⁶⁸, Lisa F Newcomb^{5

169}, Daniel W Lin^{5

169}, Jay H Fowke¹⁷⁰, Christine M Neslund-Dudas¹⁷¹, Benjamin A Rybicki¹⁷¹, Marija Gamulin¹⁷², Davor Lessel¹⁷³, Tomislav Kulis¹⁷⁴, Nawaid Usmani^{175

176}, Aswin Abraham^{175

176}, Sandeep Singhal¹⁷⁵, Matthew Parliament^{175

176}, Frank Claessens¹⁷⁷, Steven Joniau¹⁷⁸, Thomas Van den Broeck^{177

178}, Manuela Gago-Dominguez^{179

180}, Jose Esteban Castelao¹⁸¹, Maria Elena Martinez¹⁸², Samantha Larkin¹⁸³, Paul A Townsend¹⁸⁴, Claire Aukim-Hastie¹⁸⁵, William S Bush¹⁸⁶, Melinda C Aldrich¹⁸⁷, Dana C Crawford¹⁸⁶, Shiv Srivastava¹⁸⁸, Jennifer Cullen^{186

189}, Gyorgy Petrovics¹⁸⁹, Graham Casey¹⁹⁰, Ying Wang²⁵, Yao Tettey^{94

191}, Joseph Lachance⁴, Wei Tang¹⁹², Richard B Biritwum⁹⁴, Andrew A Adjei¹⁹³, Evelyn Tay⁹⁴, Ann Truelove¹⁹⁴, Shelley Niwa¹⁹⁴, Kosj Yamoah^{70

195}, Koveela Govindasami³, Anand P Chokkalingam¹⁹⁶, Jacob M Keaton^{91

197}, Jacklyn N Hellwege^{91

198}, Peter E Clark¹⁹⁹, Mohamed Jalloh²⁰⁰, Serigne M Gueye²⁰⁰, Lamine Niang²⁰⁰, Olufemi Ogunbiyi²⁰¹, Olayiwola Shittu²⁰², Olukemi Amodu²⁰³, Akindele O Adebiyi²⁰⁴, Oseremen I Aisuodionoe-Shadrach²⁰⁵, Hafees O Ajibola²⁰⁵, Mustapha A Jamda²⁰⁵, Olabode P Oluwole²⁰⁵, Maxwell Nwegbu²⁰⁵, Ben Adusei²⁰⁶, Sunny Mante²⁰⁶, Afua Darkwa-Abrahams⁹⁴, Halimatou Diop²⁰⁷, Susan M Gundell¹, Monique J Roobol²⁰⁸, Guido Jenster²⁰⁸, Ron H N van Schaik²⁰⁹, Jennifer J Hu²¹⁰, Maureen Sanderson²¹¹, Linda Kachuri²¹², Rohit Varma²¹³, Roberta McKean-Cowdin⁹, Mina Torres²¹³, Michael H Preuss²¹⁴, Ruth J F Loos²¹⁴, Matthew Zawistowski^{215

216}, Sebastian Zöllner^{215

216

217}, Zeyun Lu⁹, Stephen K Van Den Eeden²¹⁸, Douglas F Easton¹²¹, Stefan Ambs¹⁹², Todd L Edwards⁹¹, Reedik Mägi¹⁷, Timothy R Rebbeck²⁴, Lars Fritsche²¹⁹, Stephen J Chanock⁷², Sonja I Berndt⁷², Fredrik Wiklund⁷, Hidewaki Nakagawa¹⁶, John S Witte^{212

220}, J Michael Gaziano^{38

39}, Amy C Justice³⁵, Nick Mancuso¹, Chikashi Terao^{22

221

222}, Rosalind A Eeles^{3

223}, Zsofia Kote-Jarai³, Ravi K Madduri², David V Conti^#¹, Christopher A Haiman^#²²⁴

Collaborators, Affiliations

Collaborators

Affiliations

¹ Center for Genetic Epidemiology, Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
² Argonne National Laboratory, Lemont, IL, USA.
³ The Institute of Cancer Research, London, UK.
⁴ School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USA.
⁵ Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
⁶ Department of Public Health and Primary Care, Centre for Cancer Genetic Epidemiology, University of Cambridge, Cambridge, UK.
⁷ Department of Medical Epidemiology and Biostatistics, Karolinska Institute, Stockholm, Sweden.
⁸ Urology Division, Department of Surgery, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
⁹ Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
¹⁰ Department of Epidemiology and Biostatistics, University of California, San Francisco, CA, USA.
¹¹ Institute for Human Genetics, University of California, San Francisco, CA, USA.
¹² Laboratory for Statistical Analysis, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
¹³ Department of Genomic Medicine, National Cerebral and Cardiovascular Center Research Institute, Suita, Japan.
¹⁴ Department of Computational Biology and Medical Sciences, Laboratory of Clinical Genome Sequencing, Graduate School of Frontier Sciences, The University of Tokyo, Tokyo, Japan.
¹⁵ Laboratory for Genotyping Development, RIKEN Center of Integrative Medical Sciences, Yokohama, Japan.
¹⁶ Laboratory for Cancer Genomics, RIKEN Center of Integrative Medical Sciences, Yokohama, Japan.
¹⁷ Estonian Genome Centre, Institute of Genomics, University of Tartu, Tartu, Estonia.
¹⁸ Division of Population Health, Health Services Research and Primary Care, School of Health Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK.
¹⁹ Warwick Medical School, University of Warwick, Coventry, UK.
²⁰ Department of Orthopaedics, Shimane University, Izumo, Japan.
²¹ RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
²² Laboratory for Statistical and Translational Genetics, Center for Integrative Medical Sciences, RIKEN, Yokohama, Japan.
²³ Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Tokyo, Japan.
²⁴ Harvard TH Chan School of Public Health and Division of Population Sciences, Dana Farber Cancer Institute, Boston, MA, USA.
²⁵ Department of Population Science, American Cancer Society, Kennesaw, GA, USA.
²⁶ Surveillance & Health Science Department, American Cancer Society, Kennesaw, GA, USA.
²⁷ Institute of Biomedicine, University of Turku, Turku, Finland.
²⁸ Department of Medical Genetics, Genomics, Laboratory Division, Turku University Hospital, Turku, Finland.
²⁹ Department of Urology, Tampere University Hospital, Tampere, Finland.
³⁰ Unit of Health Sciences, Faculty of Social Sciences, Tampere University, Tampere, Finland.
³¹ Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia.
³² Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia.
³³ Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, Victoria, Australia.
³⁴ International Hereditary Cancer Center, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland.
³⁵ Yale School of Medicine, New Haven, CT, USA.
³⁶ Faculty of Epidemiology and Population Health, London School of Hygiene & Tropical Medicine, London, UK.
³⁷ VA Connecticut Healthcare System, West Haven, CT, USA.
³⁸ Division of Aging, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
³⁹ VA Boston Healthcare System, Boston, MA, USA.
⁴⁰ Theoretical Biology Division, Los Alamos National Lab, Los Alamos, NM, USA.
⁴¹ Nuffield Department of Surgical Sciences, University of Oxford, John Radcliffe Hospital, Headington, UK.
⁴² University of Cambridge, Department of Oncology, Addenbrooke's Hospital, Cambridge, UK.
⁴³ Cancer Research UK, Cambridge Research Institute, Li Ka Shing Centre, Cambridge, UK.
⁴⁴ Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, UK.
⁴⁵ Nuffield Department of Surgical Sciences, University of Oxford, Oxford, UK.
⁴⁶ Faculty of Medical Science, University of Oxford, John Radcliffe Hospital, Oxford, UK.
⁴⁷ NIHR Bristol Biomedical Research Centre, University Hospitals Bristol and Weston NHS Foundation Trust and the University of Bristol, Bristol, UK.
⁴⁸ Medical Research Council (MRC) Integrative Epidemiology Unit, University of Bristol, Bristol, UK.
⁴⁹ Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
⁵⁰ Department of Clinical Biochemistry, Herlev and Gentofte Hospital, Copenhagen University Hospital, Copenhagen, Denmark.
⁵¹ Copenhagen Prostate Cancer Center, Department of Urology, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
⁵² Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark.
⁵³ Centre for Genomics and Personalised Health, Queensland University of Technology, Brisbane, Queensland, Australia.
⁵⁴ Translational Research Institute, Brisbane, Queensland, Australia.
⁵⁵ University of Technology, Sydney, New South Wales, Australia.
⁵⁶ Chris O'Brien Lifehouse, Camperdown, Sydney, New South Wales, Australia.
⁵⁷ Garvan Institute of Medical Research, Sydney, New South Wales, Australia.
⁵⁸ Dame Roma Mitchell Cancer Research Laboratories, University of Adelaide, Adelaide, South Australia, Australia.
⁵⁹ Department of Anatomy and Developmental Biology, Biomedicine Discovery Institute, Monash University, Melbourne, Victoria, Australia.
⁶⁰ Prostate Cancer Translational Research Program, Cancer Research Division, Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
⁶¹ Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden.
⁶² Department of Urology, Karolinska University Hospital, Stockholm, Sweden.
⁶³ SDS Life Sciences, Stockholm, Sweden.
⁶⁴ Department of Clinical Sciences at Danderyd Hospital, Karolinska Institutet, Stockholm, Sweden.
⁶⁵ Department of Applied Health Research, University College London, London, UK.
⁶⁶ Centre for Cancer Genetic Epidemiology, Department of Oncology, Strangeways Laboratory, University of Cambridge, Cambridge, UK.
⁶⁷ Open Targets, Wellcome Sanger Institute, Saffron Walden, UK.
⁶⁸ Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, UK.
⁶⁹ Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK.
⁷⁰ Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, USA.
⁷¹ School of Public Health, Louisiana State University Health Sciences Center, New Orleans, LA, USA.
⁷² Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, MD, USA.
⁷³ Department of Epidemiology, Harvard T. H. Chan School of Public Health, Boston, MA, USA.
⁷⁴ Department of Epidemiology, University of Washington, Seattle, WA, USA.
⁷⁵ Program in Genetic Epidemiology and Statistical Genetics, Department of Epidemiology, Harvard T. H. Chan School of Public Health, Boston, MA, USA.
⁷⁶ Nuffield Department of Population Health, University of Oxford, Oxford, UK.
⁷⁷ Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital/Harvard Medical School, Boston, MA, USA.
⁷⁸ SWOG Statistical Center, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
⁷⁹ CHRISTUS Santa Rosa Hospital-Medical Center, San Antonio, TX, USA.
⁸⁰ Department of Surgical Oncology, Princess Margaret Cancer Centre, Toronto, Ontario, Canada.
⁸¹ Department of Surgery (Urology), University of Toronto, Toronto, Ontario, Canada.
⁸² Division of Urology, Princess Margaret Cancer Centre, Toronto, Ontario, Canada.
⁸³ Epidemiology and Biostatistics Unit, Centre Armand-Frappier Santé Biotechnologie, Laval, Quebec, Canada.
⁸⁴ National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA.
⁸⁵ Division of Nutritional Epidemiology, Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
⁸⁶ Department of Surgical Sciences, Uppsala University, Uppsala, Sweden.
⁸⁷ Brady Urological Institute in National Capital Region, Johns Hopkins University, Baltimore, MD, USA.
⁸⁸ Department of Molecular Medicine, Aarhus University Hospital, Aarhus, Denmark.
⁸⁹ Department of Clinical Medicine, Aarhus University, Aarhus, Denmark.
⁹⁰ Department of Urology, Aarhus University Hospital, Aarhus, Denmark.
⁹¹ Division of Epidemiology, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA.
⁹² International Epidemiology Institute, Rockville, MD, USA.
⁹³ University of Ghana Medical School, Accra, Ghana.
⁹⁴ Korle Bu Teaching Hospital, Accra, Ghana.
⁹⁵ Centre for Molecular Oncology, Barts Cancer Institute, Queen Mary University of London, John Vane Science Centre, London, UK.
⁹⁶ Second Military Medical University, Shanghai, China.
⁹⁷ Wuxi Second Hospital, Nanjing Medical University, Wuxi, China.
⁹⁸ Department of Urology, First Affiliated Hospital, The Academy of Medical Sciences, Zhengzhou University, Zhengzhou, China.
⁹⁹ Department of Urology, Nanfang Hospital, Southern Medical University, Guangzhou, China.
¹⁰⁰ The People's Hospital of Liaoning Proviouce, The People's Hospital of China Medical University, Shenyang, China.
¹⁰¹ Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.
¹⁰² Department of Quantitative Health Sciences, Mayo Clinic, Rochester, MN, USA.
¹⁰³ Division of Cancer Sciences, University of Manchester, Manchester Academic Health Science Centre, Radiotherapy Related Research, The Christie Hospital NHS Foundation Trust, Manchester, UK.
¹⁰⁴ University of Cambridge Department of Oncology, Oncology Centre, Cambridge University Hospitals NHS Foundation Trust, Cambridge, UK.
¹⁰⁵ Humangenetik Tuebingen, Tuebingen, Germany.
¹⁰⁶ Department of Urology, University Hospital Ulm, Ulm, Germany.
¹⁰⁷ Division of Urologic Surgery, Brigham and Womens Hospital, Boston, MA, USA.
¹⁰⁸ Washington University School of Medicine, St. Louis, MO, USA.
¹⁰⁹ GRC 5 Predictive Onco-Urology, Sorbonne Université, Paris, France.
¹¹⁰ CeRePP, Paris, France.
¹¹¹ Exposome and Heredity, CESP (UMR 1018), Paris-Saclay Medical School, Paris-Saclay University, Inserm, Gustave Roussy, Villejuif, France.
¹¹² Cancer & Environment Group, Center for Research in Epidemiology and Population Health (CESP), INSERM, University Paris-Sud, University Paris-Saclay, Villejuif, France.
¹¹³ Department of Medicine and Stanford Cancer Institute, Stanford University School of Medicine, Stanford, CA, USA.
¹¹⁴ Department of Medical Genetics, Oslo University Hospital, Oslo, Norway.
¹¹⁵ Clinical Gerontology Unit, University of Cambridge, Cambridge, UK.
¹¹⁶ Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California/Norris Comprehensive Cancer Center, Los Angeles, CA, USA.
¹¹⁷ Fundación Pública Galega Medicina Xenómica, Santiago de Compostela, Spain.
¹¹⁸ Instituto de Investigación Sanitaria de Santiago de Compostela, Santiago de Compostela, Spain.
¹¹⁹ Centro de Investigación en Red de Enfermedades Raras, Madrid, Spain.
¹²⁰ Department of Radiation Oncology, Complexo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain.
¹²¹ Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Strangeways Research Laboratory, Cambridge, UK.
¹²² Department of Radiation Oncology, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
¹²³ Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
¹²⁴ Department of Radiation Oncology, Medical College of Wisconsin, Milwaukee, WI, USA.
¹²⁵ Department of Pathology, Albert Einstein College of Medicine, Bronx, NY, USA.
¹²⁶ Department of Laboratory Genetics, Portuguese Oncology Institute of Porto (IPO Porto)/Porto Comprehensive Cancer Center, Porto, Portugal.
¹²⁷ Cancer Genetics Group, IPO Porto Research Center (CI-IPOP)/RISE@CI-IPOP (Health Research Network), Portuguese Oncology Institute of Porto (IPO Porto)/Porto Comprehensive Cancer Center, Porto, Portugal.
¹²⁸ School of Medicine and Biomedical Sciences (ICBAS), University of Porto, Porto, Portugal.
¹²⁹ Uro Care, Kampala, Uganda.
¹³⁰ Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.
¹³¹ Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.
¹³² Department of Urology, Roswell Park Comprehensive Cancer Center, Buffalo, NY, USA.
¹³³ Epidemiology Branch, National Institute of Environmental Health Sciences, Research Triangle Park, NC, USA.
¹³⁴ Laboratory of Molecular Carcinogenesis, National Institute of Environmental Health Sciences, Research Triangle Park, NC, USA.
¹³⁵ ISGlobal, Barcelona, Spain.
¹³⁶ Hospital del Mar Medical Research Institute, Barcelona, Spain.
¹³⁷ Universitat Pompeu Fabra, Barcelona, Spain.
¹³⁸ CIBER Epidemiología y Salud Pública, Madrid, Spain.
¹³⁹ University of Cantabria-IDIVAL, Santander, Spain.
¹⁴⁰ Division of Epidemiology, Department of Internal Medicine, University of Utah School of Medicine, Salt Lake City, UT, USA.
¹⁴¹ George E. Wahlen Department of Veterans Affairs Medical Center, Salt Lake City, UT, USA.
¹⁴² Department of Epidemiology, University of Texas MD Anderson Cancer Center, Houston, TX, USA.
¹⁴³ Department of Genitourinary Medical Oncology, University of Texas MD Anderson Cancer Center, Houston, TX, USA.
¹⁴⁴ The University of Texas MD Anderson Cancer Center, Houston, TX, USA.
¹⁴⁵ Univ Rennes, Inserm, EHESP, Institut de recherche en santé, environnement et travail, Rennes, France.
¹⁴⁶ CHU de Pointe-à-Pitre, Univ Antilles, Univ Rennes, Inserm, EHESP, Institut de recherche en santé, environnement et travail, Pointe-à-Pitre, France.
¹⁴⁷ Molecular Medicine Center, Department of Medical Chemistry and Biochemistry, Medical University of Sofia, Sofia, Bulgaria.
¹⁴⁸ Department of Urology and Alexandrovska University Hospital, Medical University of Sofia, Sofia, Bulgaria.
¹⁴⁹ Department of Cell Systems and Anatomy and Mays Cancer Center, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA.
¹⁵⁰ Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹⁵¹ German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹⁵² Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany.
¹⁵³ Saarland Cancer Registry, Saarbrücken, Germany.
¹⁵⁴ Cleveland Clinic Lerner Research Institute, Cleveland, OH, USA.
¹⁵⁵ Glickman Urological & Kidney Institute, Cleveland Clinic, Cleveland, OH, USA.
¹⁵⁶ City of Hope Comprehensive Cancer Center, Duarte, CA, USA.
¹⁵⁷ Department of Urology, Northwestern University, Chicago, IL, USA.
¹⁵⁸ Department of Population Sciences, Beckman Research Institute of the City of Hope, Duarte, CA, USA.
¹⁵⁹ James Buchanan Brady Urological Institute, Johns Hopkins Hospital and Medical Institution, Baltimore, MD, USA.
¹⁶⁰ Department of Family, Population and Preventive Medicine, Stony Brook University, Stony Brook, NY, USA.
¹⁶¹ Chronic Disease Research Centre and Faculty of Medical Sciences, University of the West Indies, Bridgetown, Barbados.
¹⁶² Department of Translational Genomics, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
¹⁶³ The University of Surrey, Guildford, UK.
¹⁶⁴ Ghent University, Faculty of Medicine and Health Sciences, Basic Medical Sciences, Ghent, Belgium.
¹⁶⁵ Department of Radiotherapy, Ghent University Hospital, Ghent, Belgium.
¹⁶⁶ Program for Personalized Cancer Care and Department of Surgery, NorthShore University HealthSystem, Evanston, IL, USA.
¹⁶⁷ Department of Surgery, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia.
¹⁶⁸ Cancer Research Malaysia, Outpatient Centre, Subang Jaya Medical Centre, Subang Jaya, Malaysia.
¹⁶⁹ Department of Urology, University of Washington, Seattle, WA, USA.
¹⁷⁰ Department of Preventive Medicine, Division of Epidemiology, The University of Tennessee Health Science Center, Memphis, TN, USA.
¹⁷¹ Department of Public Health Sciences, Henry Ford Hospital, Detroit, MI, USA.
¹⁷² Division of Medical Oncology, Urogenital Unit, Department of Oncology, University Hospital Centre Zagreb, Zagreb, Croatia.
¹⁷³ Institute of Human Genetics, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
¹⁷⁴ Department of Urology, University Hospital Center Zagreb, University of Zagreb School of Medicine, Zagreb, Croatia.
¹⁷⁵ Department of Oncology, Cross Cancer Institute, University of Alberta, Edmonton, Alberta, Canada.
¹⁷⁶ Division of Radiation Oncology, Cross Cancer Institute, Edmonton, Alberta, Canada.
¹⁷⁷ Department of Cellular and Molecular Medicine, Molecular Endocrinology Laboratory, Leuven, Belgium.
¹⁷⁸ Department of Urology, University Hospitals Leuven, Leuven, Belgium.
¹⁷⁹ Genomic Medicine Group, Galician Foundation of Genomic Medicine, Instituto de Investigacion Sanitaria de Santiago de Compostela (IDIS), Complejo Hospitalario Universitario de Santiago, Servicio Galego de Saúde, SERGAS, Santiago de Compostela, Spain.
¹⁸⁰ Moores Cancer Center, University of California San Diego, La Jolla, CA, USA.
¹⁸¹ Genetic Oncology Unit, CHUVI Hospital, Complexo Hospitalario Universitario de Vigo, Instituto de Investigación Biomédica Galicia Sur, Vigo, Spain.
¹⁸² Moores Cancer Center, Department of Family Medicine and Public Health, University of California San Diego, La Jolla, CA, USA.
¹⁸³ Scientific Education Support, Thames Ditton, Surrey, Formerly Cancer Sciences, University of Southampton, Southampton, UK.
¹⁸⁴ School of Biosciences and Medicine, Faculty of Health and Medical Sciences, University of Surrey, Surrey, UK.
¹⁸⁵ Scientific Education Support, Thames Ditton, UK.
¹⁸⁶ Department of Population and Quantitative Health Sciences, Cleveland Institute for Computational Biology, Case Western Reserve University, Cleveland, OH, USA.
¹⁸⁷ Division of Genetic Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA.
¹⁸⁸ Department of Biochemistry and Molecular & Cellular Biology, Georgetown University Medical Center, Washington DC, USA.
¹⁸⁹ Department of Surgery, Center for Prostate Disease Research, Uniformed Services University of the Health Sciences, Bethesda, MD, USA.
¹⁹⁰ Department of Public Health Science, Center for Public Health Genomics, University of Virginia, Charlottesville, VA, USA.
¹⁹¹ Department of Pathology, University of Ghana, Accra, Ghana.
¹⁹² Laboratory of Human Carcinogenesis, Center for Cancer Research, National Cancer Institute, Bethesda, MD, USA.
¹⁹³ Department of Pathology, University of Ghana Medical School, Accra, Ghana.
¹⁹⁴ Westat, Rockville, MD, USA.
¹⁹⁵ Department of Radiation Oncology, Moffitt Cancer Center, Tampa, FL, USA.
¹⁹⁶ School of Public Health, University of California, Berkeley, Berkeley, CA, USA.
¹⁹⁷ Center for Precision Health Research, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA.
¹⁹⁸ Division of Genetic Medicine, Department of Medicine, Vanderbilt Genetics Institute, Nashville, TN, USA.
¹⁹⁹ Atrium Health/Levine Cancer Institute, Charlotte, NC, USA.
²⁰⁰ Hôpital Général Idrissa Pouye, Dakar, Senegal.
²⁰¹ Department of Pathology, College of Medicine, University of Ibadan, Ibadan, Nigeria.
²⁰² Department of Surgery, College of Medicine, University of Ibadan and Univerity College Hospital, Ibadan, Nigeria.
²⁰³ Institute of Child Health, College of Medicine, University of Ibadan and University College Hospital, Ibadan, Nigeria.
²⁰⁴ Clinical Epidemiology Unit, Department of Community Medicine, College of Medicine, University of Ibadan, Ibadan, Nigeria.
²⁰⁵ College of Health Sciences, University of Abuja, University of Abuja Teaching Hospital and Cancer Science Center, Abuja, Nigeria.
²⁰⁶ 37 Military Hospital, Accra, Ghana.
²⁰⁷ Laboratoires Bacteriologie et Virologie, Hôpital Aristide Le Dantec, Dakar, Senegal.
²⁰⁸ Department of Urology, Erasmus University Medical Center, Rotterdam, the Netherlands.
²⁰⁹ Department of Clinical Chemistry, Erasmus University Medical Center, Rotterdam, the Netherlands.
²¹⁰ The University of Miami School of Medicine, Sylvester Comprehensive Cancer Center, Miami, FL, USA.
²¹¹ Department of Family and Community Medicine, Meharry Medical College, Nashville, TN, USA.
²¹² Department of Epidemiology and Population Health, Stanford Cancer Institute, Stanford University School of Medicine, Stanford, CA, USA.
²¹³ Southern California Eye Institute, CHA Hollywood Presbyterian Medical Center, Los Angeles, CA, USA.
²¹⁴ The Charles Bronfman Institute for Personalized Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
²¹⁵ Department of Biostatistics, University of Michigan School of Public Health, Ann Arbor, MI, USA.
²¹⁶ Center for Statistical Genetics, University of Michigan School of Public Health, Ann Arbor, MI, USA.
²¹⁷ Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA.
²¹⁸ Division of Research, Kaiser Permanente, Oakland, CA, USA.
²¹⁹ Department of Biostatistics and Center for Statistical Genetics, University of Michigan, Ann Arbor, MI, USA.
²²⁰ Department of Biomedical Data Science, Stanford University, Stanford, CA, USA.
²²¹ Clinical Research Center, Shizuoka General Hospital, Shizuoka, Japan.
²²² The Department of Applied Genetics, School of Pharmaceutical Sciences, University of Shizuoka, Shizuoka, Japan.
²²³ Royal Marsden NHS Foundation Trust, London, UK.
²²⁴ Center for Genetic Epidemiology, Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA. [email protected].

^# Contributed equally.

PMID: 37945903
PMCID: PMC10841479
DOI: 10.1038/s41588-023-01534-4

Characterizing prostate cancer risk through multi-ancestry genome-wide discovery of 187 novel risk variants

Anqi Wang et al. Nat Genet. 2023 Dec.

. 2023 Dec;55(12):2065-2074.

doi: 10.1038/s41588-023-01534-4. Epub 2023 Nov 9.

Authors

Collaborators

Affiliations

¹ Center for Genetic Epidemiology, Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
² Argonne National Laboratory, Lemont, IL, USA.
³ The Institute of Cancer Research, London, UK.
⁴ School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USA.
⁵ Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
⁶ Department of Public Health and Primary Care, Centre for Cancer Genetic Epidemiology, University of Cambridge, Cambridge, UK.
⁷ Department of Medical Epidemiology and Biostatistics, Karolinska Institute, Stockholm, Sweden.
⁸ Urology Division, Department of Surgery, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
⁹ Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
¹⁰ Department of Epidemiology and Biostatistics, University of California, San Francisco, CA, USA.
¹¹ Institute for Human Genetics, University of California, San Francisco, CA, USA.
¹² Laboratory for Statistical Analysis, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
¹³ Department of Genomic Medicine, National Cerebral and Cardiovascular Center Research Institute, Suita, Japan.
¹⁴ Department of Computational Biology and Medical Sciences, Laboratory of Clinical Genome Sequencing, Graduate School of Frontier Sciences, The University of Tokyo, Tokyo, Japan.
¹⁵ Laboratory for Genotyping Development, RIKEN Center of Integrative Medical Sciences, Yokohama, Japan.
¹⁶ Laboratory for Cancer Genomics, RIKEN Center of Integrative Medical Sciences, Yokohama, Japan.
¹⁷ Estonian Genome Centre, Institute of Genomics, University of Tartu, Tartu, Estonia.
¹⁸ Division of Population Health, Health Services Research and Primary Care, School of Health Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK.
¹⁹ Warwick Medical School, University of Warwick, Coventry, UK.
²⁰ Department of Orthopaedics, Shimane University, Izumo, Japan.
²¹ RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
²² Laboratory for Statistical and Translational Genetics, Center for Integrative Medical Sciences, RIKEN, Yokohama, Japan.
²³ Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Tokyo, Japan.
²⁴ Harvard TH Chan School of Public Health and Division of Population Sciences, Dana Farber Cancer Institute, Boston, MA, USA.
²⁵ Department of Population Science, American Cancer Society, Kennesaw, GA, USA.
²⁶ Surveillance & Health Science Department, American Cancer Society, Kennesaw, GA, USA.
²⁷ Institute of Biomedicine, University of Turku, Turku, Finland.
²⁸ Department of Medical Genetics, Genomics, Laboratory Division, Turku University Hospital, Turku, Finland.
²⁹ Department of Urology, Tampere University Hospital, Tampere, Finland.
³⁰ Unit of Health Sciences, Faculty of Social Sciences, Tampere University, Tampere, Finland.
³¹ Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia.
³² Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia.
³³ Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, Victoria, Australia.
³⁴ International Hereditary Cancer Center, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland.
³⁵ Yale School of Medicine, New Haven, CT, USA.
³⁶ Faculty of Epidemiology and Population Health, London School of Hygiene & Tropical Medicine, London, UK.
³⁷ VA Connecticut Healthcare System, West Haven, CT, USA.
³⁸ Division of Aging, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
³⁹ VA Boston Healthcare System, Boston, MA, USA.
⁴⁰ Theoretical Biology Division, Los Alamos National Lab, Los Alamos, NM, USA.
⁴¹ Nuffield Department of Surgical Sciences, University of Oxford, John Radcliffe Hospital, Headington, UK.
⁴² University of Cambridge, Department of Oncology, Addenbrooke's Hospital, Cambridge, UK.
⁴³ Cancer Research UK, Cambridge Research Institute, Li Ka Shing Centre, Cambridge, UK.
⁴⁴ Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, UK.
⁴⁵ Nuffield Department of Surgical Sciences, University of Oxford, Oxford, UK.
⁴⁶ Faculty of Medical Science, University of Oxford, John Radcliffe Hospital, Oxford, UK.
⁴⁷ NIHR Bristol Biomedical Research Centre, University Hospitals Bristol and Weston NHS Foundation Trust and the University of Bristol, Bristol, UK.
⁴⁸ Medical Research Council (MRC) Integrative Epidemiology Unit, University of Bristol, Bristol, UK.
⁴⁹ Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
⁵⁰ Department of Clinical Biochemistry, Herlev and Gentofte Hospital, Copenhagen University Hospital, Copenhagen, Denmark.
⁵¹ Copenhagen Prostate Cancer Center, Department of Urology, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
⁵² Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark.
⁵³ Centre for Genomics and Personalised Health, Queensland University of Technology, Brisbane, Queensland, Australia.
⁵⁴ Translational Research Institute, Brisbane, Queensland, Australia.
⁵⁵ University of Technology, Sydney, New South Wales, Australia.
⁵⁶ Chris O'Brien Lifehouse, Camperdown, Sydney, New South Wales, Australia.
⁵⁷ Garvan Institute of Medical Research, Sydney, New South Wales, Australia.
⁵⁸ Dame Roma Mitchell Cancer Research Laboratories, University of Adelaide, Adelaide, South Australia, Australia.
⁵⁹ Department of Anatomy and Developmental Biology, Biomedicine Discovery Institute, Monash University, Melbourne, Victoria, Australia.
⁶⁰ Prostate Cancer Translational Research Program, Cancer Research Division, Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
⁶¹ Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden.
⁶² Department of Urology, Karolinska University Hospital, Stockholm, Sweden.
⁶³ SDS Life Sciences, Stockholm, Sweden.
⁶⁴ Department of Clinical Sciences at Danderyd Hospital, Karolinska Institutet, Stockholm, Sweden.
⁶⁵ Department of Applied Health Research, University College London, London, UK.
⁶⁶ Centre for Cancer Genetic Epidemiology, Department of Oncology, Strangeways Laboratory, University of Cambridge, Cambridge, UK.
⁶⁷ Open Targets, Wellcome Sanger Institute, Saffron Walden, UK.
⁶⁸ Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, UK.
⁶⁹ Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK.
⁷⁰ Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, USA.
⁷¹ School of Public Health, Louisiana State University Health Sciences Center, New Orleans, LA, USA.
⁷² Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, MD, USA.
⁷³ Department of Epidemiology, Harvard T. H. Chan School of Public Health, Boston, MA, USA.
⁷⁴ Department of Epidemiology, University of Washington, Seattle, WA, USA.
⁷⁵ Program in Genetic Epidemiology and Statistical Genetics, Department of Epidemiology, Harvard T. H. Chan School of Public Health, Boston, MA, USA.
⁷⁶ Nuffield Department of Population Health, University of Oxford, Oxford, UK.
⁷⁷ Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital/Harvard Medical School, Boston, MA, USA.
⁷⁸ SWOG Statistical Center, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
⁷⁹ CHRISTUS Santa Rosa Hospital-Medical Center, San Antonio, TX, USA.
⁸⁰ Department of Surgical Oncology, Princess Margaret Cancer Centre, Toronto, Ontario, Canada.
⁸¹ Department of Surgery (Urology), University of Toronto, Toronto, Ontario, Canada.
⁸² Division of Urology, Princess Margaret Cancer Centre, Toronto, Ontario, Canada.
⁸³ Epidemiology and Biostatistics Unit, Centre Armand-Frappier Santé Biotechnologie, Laval, Quebec, Canada.
⁸⁴ National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA.
⁸⁵ Division of Nutritional Epidemiology, Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
⁸⁶ Department of Surgical Sciences, Uppsala University, Uppsala, Sweden.
⁸⁷ Brady Urological Institute in National Capital Region, Johns Hopkins University, Baltimore, MD, USA.
⁸⁸ Department of Molecular Medicine, Aarhus University Hospital, Aarhus, Denmark.
⁸⁹ Department of Clinical Medicine, Aarhus University, Aarhus, Denmark.
⁹⁰ Department of Urology, Aarhus University Hospital, Aarhus, Denmark.
⁹¹ Division of Epidemiology, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA.
⁹² International Epidemiology Institute, Rockville, MD, USA.
⁹³ University of Ghana Medical School, Accra, Ghana.
⁹⁴ Korle Bu Teaching Hospital, Accra, Ghana.
⁹⁵ Centre for Molecular Oncology, Barts Cancer Institute, Queen Mary University of London, John Vane Science Centre, London, UK.
⁹⁶ Second Military Medical University, Shanghai, China.
⁹⁷ Wuxi Second Hospital, Nanjing Medical University, Wuxi, China.
⁹⁸ Department of Urology, First Affiliated Hospital, The Academy of Medical Sciences, Zhengzhou University, Zhengzhou, China.
⁹⁹ Department of Urology, Nanfang Hospital, Southern Medical University, Guangzhou, China.
¹⁰⁰ The People's Hospital of Liaoning Proviouce, The People's Hospital of China Medical University, Shenyang, China.
¹⁰¹ Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.
¹⁰² Department of Quantitative Health Sciences, Mayo Clinic, Rochester, MN, USA.
¹⁰³ Division of Cancer Sciences, University of Manchester, Manchester Academic Health Science Centre, Radiotherapy Related Research, The Christie Hospital NHS Foundation Trust, Manchester, UK.
¹⁰⁴ University of Cambridge Department of Oncology, Oncology Centre, Cambridge University Hospitals NHS Foundation Trust, Cambridge, UK.
¹⁰⁵ Humangenetik Tuebingen, Tuebingen, Germany.
¹⁰⁶ Department of Urology, University Hospital Ulm, Ulm, Germany.
¹⁰⁷ Division of Urologic Surgery, Brigham and Womens Hospital, Boston, MA, USA.
¹⁰⁸ Washington University School of Medicine, St. Louis, MO, USA.
¹⁰⁹ GRC 5 Predictive Onco-Urology, Sorbonne Université, Paris, France.
¹¹⁰ CeRePP, Paris, France.
¹¹¹ Exposome and Heredity, CESP (UMR 1018), Paris-Saclay Medical School, Paris-Saclay University, Inserm, Gustave Roussy, Villejuif, France.
¹¹² Cancer & Environment Group, Center for Research in Epidemiology and Population Health (CESP), INSERM, University Paris-Sud, University Paris-Saclay, Villejuif, France.
¹¹³ Department of Medicine and Stanford Cancer Institute, Stanford University School of Medicine, Stanford, CA, USA.
¹¹⁴ Department of Medical Genetics, Oslo University Hospital, Oslo, Norway.
¹¹⁵ Clinical Gerontology Unit, University of Cambridge, Cambridge, UK.
¹¹⁶ Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California/Norris Comprehensive Cancer Center, Los Angeles, CA, USA.
¹¹⁷ Fundación Pública Galega Medicina Xenómica, Santiago de Compostela, Spain.
¹¹⁸ Instituto de Investigación Sanitaria de Santiago de Compostela, Santiago de Compostela, Spain.
¹¹⁹ Centro de Investigación en Red de Enfermedades Raras, Madrid, Spain.
¹²⁰ Department of Radiation Oncology, Complexo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain.
¹²¹ Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Strangeways Research Laboratory, Cambridge, UK.
¹²² Department of Radiation Oncology, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
¹²³ Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
¹²⁴ Department of Radiation Oncology, Medical College of Wisconsin, Milwaukee, WI, USA.
¹²⁵ Department of Pathology, Albert Einstein College of Medicine, Bronx, NY, USA.
¹²⁶ Department of Laboratory Genetics, Portuguese Oncology Institute of Porto (IPO Porto)/Porto Comprehensive Cancer Center, Porto, Portugal.
¹²⁷ Cancer Genetics Group, IPO Porto Research Center (CI-IPOP)/RISE@CI-IPOP (Health Research Network), Portuguese Oncology Institute of Porto (IPO Porto)/Porto Comprehensive Cancer Center, Porto, Portugal.
¹²⁸ School of Medicine and Biomedical Sciences (ICBAS), University of Porto, Porto, Portugal.
¹²⁹ Uro Care, Kampala, Uganda.
¹³⁰ Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.
¹³¹ Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.
¹³² Department of Urology, Roswell Park Comprehensive Cancer Center, Buffalo, NY, USA.
¹³³ Epidemiology Branch, National Institute of Environmental Health Sciences, Research Triangle Park, NC, USA.
¹³⁴ Laboratory of Molecular Carcinogenesis, National Institute of Environmental Health Sciences, Research Triangle Park, NC, USA.
¹³⁵ ISGlobal, Barcelona, Spain.
¹³⁶ Hospital del Mar Medical Research Institute, Barcelona, Spain.
¹³⁷ Universitat Pompeu Fabra, Barcelona, Spain.
¹³⁸ CIBER Epidemiología y Salud Pública, Madrid, Spain.
¹³⁹ University of Cantabria-IDIVAL, Santander, Spain.
¹⁴⁰ Division of Epidemiology, Department of Internal Medicine, University of Utah School of Medicine, Salt Lake City, UT, USA.
¹⁴¹ George E. Wahlen Department of Veterans Affairs Medical Center, Salt Lake City, UT, USA.
¹⁴² Department of Epidemiology, University of Texas MD Anderson Cancer Center, Houston, TX, USA.
¹⁴³ Department of Genitourinary Medical Oncology, University of Texas MD Anderson Cancer Center, Houston, TX, USA.
¹⁴⁴ The University of Texas MD Anderson Cancer Center, Houston, TX, USA.
¹⁴⁵ Univ Rennes, Inserm, EHESP, Institut de recherche en santé, environnement et travail, Rennes, France.
¹⁴⁶ CHU de Pointe-à-Pitre, Univ Antilles, Univ Rennes, Inserm, EHESP, Institut de recherche en santé, environnement et travail, Pointe-à-Pitre, France.
¹⁴⁷ Molecular Medicine Center, Department of Medical Chemistry and Biochemistry, Medical University of Sofia, Sofia, Bulgaria.
¹⁴⁸ Department of Urology and Alexandrovska University Hospital, Medical University of Sofia, Sofia, Bulgaria.
¹⁴⁹ Department of Cell Systems and Anatomy and Mays Cancer Center, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA.
¹⁵⁰ Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹⁵¹ German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹⁵² Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany.
¹⁵³ Saarland Cancer Registry, Saarbrücken, Germany.
¹⁵⁴ Cleveland Clinic Lerner Research Institute, Cleveland, OH, USA.
¹⁵⁵ Glickman Urological & Kidney Institute, Cleveland Clinic, Cleveland, OH, USA.
¹⁵⁶ City of Hope Comprehensive Cancer Center, Duarte, CA, USA.
¹⁵⁷ Department of Urology, Northwestern University, Chicago, IL, USA.
¹⁵⁸ Department of Population Sciences, Beckman Research Institute of the City of Hope, Duarte, CA, USA.
¹⁵⁹ James Buchanan Brady Urological Institute, Johns Hopkins Hospital and Medical Institution, Baltimore, MD, USA.
¹⁶⁰ Department of Family, Population and Preventive Medicine, Stony Brook University, Stony Brook, NY, USA.
¹⁶¹ Chronic Disease Research Centre and Faculty of Medical Sciences, University of the West Indies, Bridgetown, Barbados.
¹⁶² Department of Translational Genomics, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
¹⁶³ The University of Surrey, Guildford, UK.
¹⁶⁴ Ghent University, Faculty of Medicine and Health Sciences, Basic Medical Sciences, Ghent, Belgium.
¹⁶⁵ Department of Radiotherapy, Ghent University Hospital, Ghent, Belgium.
¹⁶⁶ Program for Personalized Cancer Care and Department of Surgery, NorthShore University HealthSystem, Evanston, IL, USA.
¹⁶⁷ Department of Surgery, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia.
¹⁶⁸ Cancer Research Malaysia, Outpatient Centre, Subang Jaya Medical Centre, Subang Jaya, Malaysia.
¹⁶⁹ Department of Urology, University of Washington, Seattle, WA, USA.
¹⁷⁰ Department of Preventive Medicine, Division of Epidemiology, The University of Tennessee Health Science Center, Memphis, TN, USA.
¹⁷¹ Department of Public Health Sciences, Henry Ford Hospital, Detroit, MI, USA.
¹⁷² Division of Medical Oncology, Urogenital Unit, Department of Oncology, University Hospital Centre Zagreb, Zagreb, Croatia.
¹⁷³ Institute of Human Genetics, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
¹⁷⁴ Department of Urology, University Hospital Center Zagreb, University of Zagreb School of Medicine, Zagreb, Croatia.
¹⁷⁵ Department of Oncology, Cross Cancer Institute, University of Alberta, Edmonton, Alberta, Canada.
¹⁷⁶ Division of Radiation Oncology, Cross Cancer Institute, Edmonton, Alberta, Canada.
¹⁷⁷ Department of Cellular and Molecular Medicine, Molecular Endocrinology Laboratory, Leuven, Belgium.
¹⁷⁸ Department of Urology, University Hospitals Leuven, Leuven, Belgium.
¹⁷⁹ Genomic Medicine Group, Galician Foundation of Genomic Medicine, Instituto de Investigacion Sanitaria de Santiago de Compostela (IDIS), Complejo Hospitalario Universitario de Santiago, Servicio Galego de Saúde, SERGAS, Santiago de Compostela, Spain.
¹⁸⁰ Moores Cancer Center, University of California San Diego, La Jolla, CA, USA.
¹⁸¹ Genetic Oncology Unit, CHUVI Hospital, Complexo Hospitalario Universitario de Vigo, Instituto de Investigación Biomédica Galicia Sur, Vigo, Spain.
¹⁸² Moores Cancer Center, Department of Family Medicine and Public Health, University of California San Diego, La Jolla, CA, USA.
¹⁸³ Scientific Education Support, Thames Ditton, Surrey, Formerly Cancer Sciences, University of Southampton, Southampton, UK.
¹⁸⁴ School of Biosciences and Medicine, Faculty of Health and Medical Sciences, University of Surrey, Surrey, UK.
¹⁸⁵ Scientific Education Support, Thames Ditton, UK.
¹⁸⁶ Department of Population and Quantitative Health Sciences, Cleveland Institute for Computational Biology, Case Western Reserve University, Cleveland, OH, USA.
¹⁸⁷ Division of Genetic Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA.
¹⁸⁸ Department of Biochemistry and Molecular & Cellular Biology, Georgetown University Medical Center, Washington DC, USA.
¹⁸⁹ Department of Surgery, Center for Prostate Disease Research, Uniformed Services University of the Health Sciences, Bethesda, MD, USA.
¹⁹⁰ Department of Public Health Science, Center for Public Health Genomics, University of Virginia, Charlottesville, VA, USA.
¹⁹¹ Department of Pathology, University of Ghana, Accra, Ghana.
¹⁹² Laboratory of Human Carcinogenesis, Center for Cancer Research, National Cancer Institute, Bethesda, MD, USA.
¹⁹³ Department of Pathology, University of Ghana Medical School, Accra, Ghana.
¹⁹⁴ Westat, Rockville, MD, USA.
¹⁹⁵ Department of Radiation Oncology, Moffitt Cancer Center, Tampa, FL, USA.
¹⁹⁶ School of Public Health, University of California, Berkeley, Berkeley, CA, USA.
¹⁹⁷ Center for Precision Health Research, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA.
¹⁹⁸ Division of Genetic Medicine, Department of Medicine, Vanderbilt Genetics Institute, Nashville, TN, USA.
¹⁹⁹ Atrium Health/Levine Cancer Institute, Charlotte, NC, USA.
²⁰⁰ Hôpital Général Idrissa Pouye, Dakar, Senegal.
²⁰¹ Department of Pathology, College of Medicine, University of Ibadan, Ibadan, Nigeria.
²⁰² Department of Surgery, College of Medicine, University of Ibadan and Univerity College Hospital, Ibadan, Nigeria.
²⁰³ Institute of Child Health, College of Medicine, University of Ibadan and University College Hospital, Ibadan, Nigeria.
²⁰⁴ Clinical Epidemiology Unit, Department of Community Medicine, College of Medicine, University of Ibadan, Ibadan, Nigeria.
²⁰⁵ College of Health Sciences, University of Abuja, University of Abuja Teaching Hospital and Cancer Science Center, Abuja, Nigeria.
²⁰⁶ 37 Military Hospital, Accra, Ghana.
²⁰⁷ Laboratoires Bacteriologie et Virologie, Hôpital Aristide Le Dantec, Dakar, Senegal.
²⁰⁸ Department of Urology, Erasmus University Medical Center, Rotterdam, the Netherlands.
²⁰⁹ Department of Clinical Chemistry, Erasmus University Medical Center, Rotterdam, the Netherlands.
²¹⁰ The University of Miami School of Medicine, Sylvester Comprehensive Cancer Center, Miami, FL, USA.
²¹¹ Department of Family and Community Medicine, Meharry Medical College, Nashville, TN, USA.
²¹² Department of Epidemiology and Population Health, Stanford Cancer Institute, Stanford University School of Medicine, Stanford, CA, USA.
²¹³ Southern California Eye Institute, CHA Hollywood Presbyterian Medical Center, Los Angeles, CA, USA.
²¹⁴ The Charles Bronfman Institute for Personalized Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
²¹⁵ Department of Biostatistics, University of Michigan School of Public Health, Ann Arbor, MI, USA.
²¹⁶ Center for Statistical Genetics, University of Michigan School of Public Health, Ann Arbor, MI, USA.
²¹⁷ Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA.
²¹⁸ Division of Research, Kaiser Permanente, Oakland, CA, USA.
²¹⁹ Department of Biostatistics and Center for Statistical Genetics, University of Michigan, Ann Arbor, MI, USA.
²²⁰ Department of Biomedical Data Science, Stanford University, Stanford, CA, USA.
²²¹ Clinical Research Center, Shizuoka General Hospital, Shizuoka, Japan.
²²² The Department of Applied Genetics, School of Pharmaceutical Sciences, University of Shizuoka, Shizuoka, Japan.
²²³ Royal Marsden NHS Foundation Trust, London, UK.
²²⁴ Center for Genetic Epidemiology, Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA. [email protected].

^# Contributed equally.

PMID: 37945903
PMCID: PMC10841479
DOI: 10.1038/s41588-023-01534-4

Abstract

The transferability and clinical value of genetic risk scores (GRSs) across populations remain limited due to an imbalance in genetic studies across ancestrally diverse populations. Here we conducted a multi-ancestry genome-wide association study of 156,319 prostate cancer cases and 788,443 controls of European, African, Asian and Hispanic men, reflecting a 57% increase in the number of non-European cases over previous prostate cancer genome-wide association studies. We identified 187 novel risk variants for prostate cancer, increasing the total number of risk variants to 451. An externally replicated multi-ancestry GRS was associated with risk that ranged from 1.8 (per standard deviation) in African ancestry men to 2.2 in European ancestry men. The GRS was associated with a greater risk of aggressive versus non-aggressive disease in men of African ancestry (P = 0.03). Our study presents novel prostate cancer susceptibility loci and a GRS with effective risk stratification across ancestry groups.

PubMed Disclaimer

Conflict of interest statement

Competing interests

The authors declare no competing interests.

Figures

**Extended Data Fig. 1**
Venn diagram of prostate cancer risk variants common (MAF>1%) among European, African, Asian and Hispanic populations. The plot illustrates the distribution of 451 prostate cancer risk variants, highlighting the number of variants that are either unique to or shared among European, African, Asian, and Hispanic populations. Five variants with a minor allele frequency (MAF) of ≤1% across all populations are specifically included under the European population, where they have the highest MAF. Numbers in parentheses denote the total count of variants common to each respective population.

**Extended Data Fig. 2**
The associations of GRS₄₅₁ and total prostate cancer risk in GWAS discovery and replication sub-studies and meta-analysis by ancestry. Odds ratios and 95% confidence intervals for one SD increase in GRS₄₅₁ and total prostate cancer risk were calculated from logistic regression. The columns ‘case’ and ‘control’ show the case and control sample sizes, respectively. ‘META’ refers to the meta-analyzed results using the inverse-variance weighted method. The y-axis shows each individual sub-studies (details of each sub-studies are available in Supplemental Table 1 and 2) and their corresponding meta-analyzed results by ancestry and study phase (GWAS discovery or replication), as well as overall meta-analyzed results.

**Figure 1.**
Manhattan plot of results from the multi-ancestry prostate cancer meta-analysis. Multi-ancestry meta-analysis (156,319 cases and 788,443 controls) was performed using an inverse-variance-weighted fixed-effects model. Nominal statistical significance is shown as −log₁₀P (two-sided) of z statistics on the y axis. Purple and orange circles indicate previously known or novel risk variants, respectively, that were genome-wide significant in multi-ancestry or ancestry-specific meta-analyses. The plot is truncated at −log₁₀P=600.

**Figure 2.**
Comparison of the ancestry-specific results of the 451 risk variants for prostate cancer. (a) Venn diagram of genome-wide significant variants (P<5x10⁻⁸) among European, African, Asian, and Hispanic populations. (b) Venn diagram of nominally significant variants (P<0.05) among European, African, Asian, and Hispanic populations. (c) Comparison of ancestry-specific odds ratios (ORs) between European and African, Asian, and Hispanic populations, respectively. The number of variants is denoted in the lower right corner. Genome-wide significant variants among African, Asian, or Hispanic populations are highlighted in orange. Two-sided Pearson correlation tests were performed. The Pearson’s correlation coefficient between effect size and corresponding P-value are denoted in the upper left in each sub-panel. Only common variants across all populations (MAF>1%, n=370) were included in (a), (b), and (c).

**Figure 3.**
Percentage of cases in the lowest and highest genetic risk score (GRS) quintiles based on GRS₁₀₀, GRS₁₈₁, GRS₂₆₉, and GRS₄₅₁ in the multi-ancestry sample. GRS risk quintiles were categorized based on GRS distributions among controls. Quintile 1 (orange bar) refers to the lowest quintile (0–20%), and quintile 5 (yellow bar) refers to the highest quintile (80–100%).

**Figure 4.**
The associations of GRS and prostate cancer risk in GWAS discovery and replication samples. ORs and 95% Confidence Intervals (CIs) from logistic regression for one standard deviation (SD) increase in (a) GRS₁₀₀, GRS₁₈₁, GRS₂₆₉, and GRS₄₅₁ and total prostate cancer risk by ancestry in the GWAS discovery studies; (b) GRS₂₆₉ and GRS₄₅₁ and total prostate cancer risk in the replication studies: Michigan Genomics Initiative (MGI), Mass General Brigham Biobank (MGB), Estonian Biobank (EstBB ), and Men of African Descent and Carcinoma of the Prostate (MADCaP); (c) GRS₄₅₁ and total prostate cancer risk by age; (d) GRS₄₅₁ and GRS₄₀₀ and prostate cancer aggressiveness among prostate cancer cases in the GWAS discovery studies. ‘META’ refers to the meta-analyzed results for all populations using the inverse-variance weighted method. Incremental percentage change of ORs were calculated for each comparison. The columns ‘case’ and ‘control’ show the case and control sample sizes, and the columns ‘agg’ and ‘non-agg’ show the aggressive and non-aggressive cases sample sizes, respectively.

**Figure 5.**
Cumulative absolute risk by age. Solid lines are the cumulative absolute risk for individuals in the top 16% GRS for African ancestry and top 20% for European ancestry. These GRS categories represent the percent of individuals in each population with at least a 2-fold increase in risk in comparison to the median GRS (as indicated in the inset distributions for African and European ancestries, respectively). Dashed horizontal lines indicate the lifetime absolute risk achieved at age 85 for the average (50% GRS) in African (11.6%) and European (7.8%) ancestry populations. Solid dots indicate the ages at which lifetime absolute risk levels are achieved for men of African ancestry in the top 16% GRS (age = 66 years) and men of European ancestry in the top 20% GRS (age = 69 years).

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References

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[1] Bray F et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68, 394–424 (2018). - PubMed

[2] Bray F et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68, 394–424 (2018). - PubMed

[3] Conti DV et al. Trans-ancestry genome-wide association meta-analysis of prostate cancer identifies new susceptibility loci and informs genetic risk prediction. Nature Genetics 53, 65–75 (2021). - PMC - PubMed

[4] Conti DV et al. Trans-ancestry genome-wide association meta-analysis of prostate cancer identifies new susceptibility loci and informs genetic risk prediction. Nature Genetics 53, 65–75 (2021). - PMC - PubMed

[5] Schumacher FR et al. Association analyses of more than 140,000 men identify 63 new prostate cancer susceptibility loci. Nat Genet 50, 928–936 (2018). - PMC - PubMed

[6] Schumacher FR et al. Association analyses of more than 140,000 men identify 63 new prostate cancer susceptibility loci. Nat Genet 50, 928–936 (2018). - PMC - PubMed

[7] Dadaev T et al. Fine-mapping of prostate cancer susceptibility loci in a large meta-analysis identifies candidate causal variants. Nat Commun 9, 2256 (2018). - PMC - PubMed

[8] Dadaev T et al. Fine-mapping of prostate cancer susceptibility loci in a large meta-analysis identifies candidate causal variants. Nat Commun 9, 2256 (2018). - PMC - PubMed

[9] Conti DV et al. Two Novel Susceptibility Loci for Prostate Cancer in Men of African Ancestry. J Natl Cancer Inst 109(2017). - PMC - PubMed

[10] Conti DV et al. Two Novel Susceptibility Loci for Prostate Cancer in Men of African Ancestry. J Natl Cancer Inst 109(2017). - PMC - PubMed

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Characterizing prostate cancer risk through multi-ancestry genome-wide discovery of 187 novel risk variants

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Characterizing prostate cancer risk through multi-ancestry genome-wide discovery of 187 novel risk variants

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