Imputation and subset-based association analysis across different cancer types identifies multiple independent risk loci in the TERT-CLPTM1L region on chromosome 5p15.33

doi:10.1093/hmg/ddu363

Multicenter Study

. 2014 Dec 15;23(24):6616-33.

doi: 10.1093/hmg/ddu363. Epub 2014 Jul 15.

Imputation and subset-based association analysis across different cancer types identifies multiple independent risk loci in the TERT-CLPTM1L region on chromosome 5p15.33

Zhaoming Wang¹, Bin Zhu², Mingfeng Zhang², Hemang Parikh², Jinping Jia², Charles C Chung¹, Joshua N Sampson², Jason W Hoskins², Amy Hutchinson¹, Laurie Burdette¹, Abdisamad Ibrahim², Christopher Hautman¹, Preethi S Raj², Christian C Abnet², Andrew A Adjei³, Anders Ahlbom⁴, Demetrius Albanes², Naomi E Allen⁵, Christine B Ambrosone⁶, Melinda Aldrich⁷, Pilar Amiano⁸, Christopher Amos⁹, Ulrika Andersson¹⁰, Gerald Andriole Jr¹¹, Irene L Andrulis¹², Cecilia Arici¹³, Alan A Arslan¹⁴, Melissa A Austin¹⁵, Dalsu Baris², Donald A Barkauskas¹⁶, Bryan A Bassig¹⁷, Laura E Beane Freeman², Christine D Berg¹⁸, Sonja I Berndt², Pier Alberto Bertazzi¹⁹, Richard B Biritwum³, Amanda Black², William Blot²⁰, Heiner Boeing²¹, Paolo Boffetta²², Kelly Bolton²³, Marie-Christine Boutron-Ruault²⁴, Paige M Bracci²⁵, Paul Brennan²⁶, Louise A Brinton², Michelle Brotzman²⁷, H Bas Bueno-de-Mesquita²⁸, Julie E Buring²⁹, Mary Ann Butler³⁰, Qiuyin Cai⁷, Geraldine Cancel-Tassin³¹, Federico Canzian³², Guangwen Cao³³, Neil E Caporaso², Alfredo Carrato³⁴, Tania Carreon³⁰, Angela Carta¹², Gee-Chen Chang³⁵, I-Shou Chang³⁶, Jenny Chang-Claude³², Xu Che³⁷, Chien-Jen Chen³⁸, Chih-Yi Chen³⁹, Chung-Hsing Chen³⁶, Constance Chen⁴⁰, Kuan-Yu Chen⁴¹, Yuh-Min Chen⁴², Anand P Chokkalingam⁴³, Lisa W Chu⁴⁴, Francoise Clavel-Chapelon⁴⁵, Graham A Colditz⁴⁶, Joanne S Colt², David Conti¹⁶, Michael B Cook², Victoria K Cortessis¹⁶, E David Crawford⁴⁷, Olivier Cussenot⁴⁸, Faith G Davis⁴⁹, Immaculata De Vivo⁵⁰, Xiang Deng¹, Ti Ding⁵¹, Colin P Dinney⁵², Anna Luisa Di Stefano⁵³, W Ryan Diver⁵⁴, Eric J Duell⁵⁵, Joanne W Elena⁵⁶, Jin-Hu Fan⁵⁷, Heather Spencer Feigelson⁵⁸, Maria Feychting⁴, Jonine D Figueroa², Adrienne M Flanagan⁵⁹, Joseph F Fraumeni Jr², Neal D Freedman², Brooke L Fridley⁶⁰, Charles S Fuchs⁶¹, Manuela Gago-Dominguez⁶², Steven Gallinger⁶³, Yu-Tang Gao⁶⁴, Susan M Gapstur⁵⁴, Montserrat Garcia-Closas⁶⁵, Reina Garcia-Closas⁶⁶, Julie M Gastier-Foster⁶⁷, J Michael Gaziano⁶⁸, Daniela S Gerhard⁶⁹, Carol A Giffen⁷⁰, Graham G Giles⁷¹, Elizabeth M Gillanders⁷², Edward L Giovannucci⁷³, Michael Goggins⁷⁴, Nalan Gokgoz⁷⁵, Alisa M Goldstein², Carlos Gonzalez⁷⁶, Richard Gorlick⁷⁷, Mark H Greene², Myron Gross⁷⁸, H Barton Grossman⁵², Robert Grubb 3rd⁷⁹, Jian Gu⁸⁰, Peng Guan⁸¹, Christopher A Haiman⁸², Goran Hallmans⁸³, Susan E Hankinson⁸⁴, Curtis C Harris⁸⁵, Patricia Hartge², Claudia Hattinger⁸⁶, Richard B Hayes⁸⁷, Qincheng He⁸¹, Lee Helman⁸⁸, Brian E Henderson⁸², Roger Henriksson¹⁰, Judith Hoffman-Bolton⁸⁹, Chancellor Hohensee⁹⁰, Elizabeth A Holly²⁵, Yun-Chul Hong⁹¹, Robert N Hoover², H Dean Hosgood 3rd⁹², Chin-Fu Hsiao⁹³, Ann W Hsing⁹⁴, Chao Agnes Hsiung⁹⁵, Nan Hu², Wei Hu², Zhibin Hu⁹⁶, Ming-Shyan Huang⁴¹, David J Hunter⁹⁷, Peter D Inskip², Hidemi Ito⁹⁸, Eric J Jacobs⁵⁴, Kevin B Jacobs⁹⁹, Mazda Jenab²⁶, Bu-Tian Ji², Christoffer Johansen¹⁰⁰, Mattias Johansson¹⁰¹, Alison Johnson¹⁰², Rudolf Kaaks³², Ashish M Kamat⁵², Aruna Kamineni¹⁰³, Margaret Karagas⁹, Chand Khanna⁸⁸, Kay-Tee Khaw¹⁰⁴, Christopher Kim², In-Sam Kim¹⁰⁵, Jin Hee Kim¹⁰⁶, Yeul Hong Kim¹⁰⁷, Young-Chul Kim¹⁰⁸, Young Tae Kim¹⁰⁹, Chang Hyun Kang¹⁰⁹, Yoo Jin Jung¹⁰⁹, Cari M Kitahara², Alison P Klein¹¹⁰, Robert Klein¹¹¹, Manolis Kogevinas¹¹², Woon-Puay Koh¹¹³, Takashi Kohno¹¹⁴, Laurence N Kolonel¹¹⁵, Charles Kooperberg⁹⁰, Christian P Kratz², Vittorio Krogh¹¹⁶, Hideo Kunitoh¹¹⁷, Robert C Kurtz¹¹¹, Nilgun Kurucu¹¹⁸, Qing Lan², Mark Lathrop¹¹⁹, Ching C Lau¹²⁰, Fernando Lecanda¹²¹, Kyoung-Mu Lee¹²², Maxwell P Lee⁸⁸, Loic Le Marchand¹¹⁵, Seth P Lerner¹²³, Donghui Li¹²⁴, Linda M Liao², Wei-Yen Lim¹²⁵, Dongxin Lin¹²⁶, Jie Lin⁸⁰, Sara Lindstrom⁴⁰, Martha S Linet², Jolanta Lissowska¹²⁷, Jianjun Liu¹²⁸, Börje Ljungberg¹²⁹, Josep Lloreta¹³⁰, Daru Lu¹³¹, Jing Ma¹³², Nuria Malats¹³³, Satu Mannisto¹³⁴, Neyssa Marina¹³⁵, Giuseppe Mastrangelo¹³⁶, Keitaro Matsuo¹³⁷, Katherine A McGlynn², Roberta McKean-Cowdin⁸⁰, Lorna H McNeill¹³⁸, Robert R McWilliams¹³⁹, Beatrice S Melin¹⁰, Paul S Meltzer⁸⁸, James E Mensah³, Xiaoping Miao¹⁴⁰, Dominique S Michaud¹⁴¹, Alison M Mondul², Lee E Moore², Kenneth Muir¹⁴², Shelley Niwa²⁷, Sara H Olson¹⁴³, Nick Orr¹⁴⁴, Salvatore Panico¹⁴⁵, Jae Yong Park¹⁴⁶, Alpa V Patel⁵⁴, Ana Patino-Garcia¹²¹, Sofia Pavanello¹³⁶, Petra H M Peeters¹⁴⁷, Beata Peplonska¹⁴⁸, Ulrike Peters⁹⁰, Gloria M Petersen¹³⁹, Piero Picci⁸⁶, Malcolm C Pike¹⁴⁹, Stefano Porru¹³, Jennifer Prescott⁵⁰, Xia Pu⁸⁰, Mark P Purdue², You-Lin Qiao¹⁵⁰, Preetha Rajaraman², Elio Riboli¹⁵¹, Harvey A Risch¹⁵², Rebecca J Rodabough⁹⁰, Nathaniel Rothman², Avima M Ruder³⁰, Jeong-Seon Ryu¹⁵³, Marc Sanson⁵³, Alan Schned⁹, Fredrick R Schumacher⁸², Ann G Schwartz¹⁵⁴, Kendra L Schwartz¹⁵⁵, Molly Schwenn¹⁵⁶, Katia Scotlandi⁸⁶, Adeline Seow¹²⁵, Consol Serra¹⁵⁷, Massimo Serra⁸⁶, Howard D Sesso²⁹, Gianluca Severi⁷¹, Hongbing Shen⁹⁶, Min Shen², Sanjay Shete¹⁵⁸, Kouya Shiraishi¹¹⁴, Xiao-Ou Shu⁷, Afshan Siddiq¹⁵⁹, Luis Sierrasesumaga¹²¹, Sabina Sierri¹⁶⁰, Alan Dart Loon Sihoe¹⁶¹, Debra T Silverman², Matthias Simon¹⁶², Melissa C Southey¹⁶³, Logan Spector¹⁶⁴, Margaret Spitz¹⁶⁵, Meir Stampfer¹³², Par Stattin¹²⁹, Mariana C Stern⁸², Victoria L Stevens⁵⁴, Rachael Z Stolzenberg-Solomon², Daniel O Stram⁸², Sara S Strom¹⁶⁶, Wu-Chou Su¹⁶⁷, Malin Sund¹⁶⁸, Sook Whan Sung¹⁶⁹, Anthony Swerdlow¹⁷⁰, Wen Tan¹²⁶, Hideo Tanaka⁹⁸, Wei Tang², Ze-Zhang Tang⁵¹, Adonina Tardon¹⁷¹, Evelyn Tay³, Philip R Taylor², Yao Tettey³, David M Thomas¹⁷², Roberto Tirabosco¹⁷³, Anne Tjonneland¹⁷⁴, Geoffrey S Tobias², Jorge R Toro², Ruth C Travis⁵, Dimitrios Trichopoulos¹⁷⁵, Rebecca Troisi², Ann Truelove²⁷, Ying-Huang Tsai¹⁷⁶, Margaret A Tucker², Rosario Tumino¹⁷⁷, David Van Den Berg⁸², Stephen K Van Den Eeden¹⁷⁸, Roel Vermeulen¹⁷⁹, Paolo Vineis¹⁸⁰, Kala Visvanathan⁸⁹, Ulla Vogel¹⁸¹, Chaoyu Wang², Chengfeng Wang³⁷, Junwen Wang¹⁸², Sophia S Wang¹⁸³, Elisabete Weiderpass¹⁸⁴, Stephanie J Weinstein², Nicolas Wentzensen², William Wheeler⁷⁰, Emily White⁹⁰, John K Wiencke¹⁸⁵, Alicja Wolk¹⁸⁶, Brian M Wolpin⁶¹, Maria Pik Wong¹⁸⁷, Margaret Wrensch¹⁸⁵, Chen Wu¹²⁶, Tangchun Wu¹³⁶, Xifeng Wu⁸⁰, Yi-Long Wu¹⁸⁸, Jay S Wunder¹¹, Yong-Bing Xiang⁶⁴, Jun Xu¹⁸⁹, Hannah P Yang², Pan-Chyr Yang⁴¹, Yasushi Yatabe¹⁹⁰, Yuanqing Ye⁸⁰, Edward D Yeboah³, Zhihua Yin⁸¹, Chen Ying¹²⁵, Chong-Jen Yu¹⁶⁷, Kai Yu², Jian-Min Yuan¹⁹¹, Krista A Zanetti⁵⁶, Anne Zeleniuch-Jacquotte¹⁹², Wei Zheng⁷, Baosen Zhou⁸¹, Lisa Mirabello², Sharon A Savage², Peter Kraft¹⁹³, Stephen J Chanock¹, Meredith Yeager¹, Maria Terese Landi², Jianxin Shi², Nilanjan Chatterjee², Laufey T Amundadottir¹⁹⁴

Affiliations

¹ Division of Cancer Epidemiology and Genetics, Cancer Genomics Research Laboratory, National Cancer Institute, Division of Cancer Epidemiology and Genetics, SAIC-Frederick, Inc., Frederick National Laboratory for Cancer Research, Frederick, MD, USA.
² Division of Cancer Epidemiology and Genetics.
³ Korle Bu Teaching Hospital, PO BOX 77, Accra, Ghana, University of Ghana Medical School, PO Box 4236, Accra, Ghana.
⁴ Unit of Epidemiology, Institute of Environmental Medicine.
⁵ Clinical Trial Service Unit and Epidemiological Studies Unit, University of Oxford, Oxford, UK.
⁶ Department of Cancer Prevention and Control, Roswell Park Cancer Institute, Buffalo, NY, USA.
⁷ Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, TN, USA.
⁸ Public Health Division of Gipuzkoa, Basque Regional Health Department, San Sebastian, Spain, CIBERESP, CIBER Epidemiologia y Salud Publica, Madrid, Spain.
⁹ Geisel School of Medicine at Dartmouth, Hanover, NH, USA.
¹⁰ Department of Radiation Sciences, Oncology.
¹¹ Division of Urologic Surgery, Washington University School of Medicine, St Louis, MO, USA.
¹² Litwin Centre for Cancer Genetics, Samuel Lunenfeld Research Institute, Mt Sinai Hospital, University of Toronto, Toronto, ON, Canada.
¹³ Department of Medical and Surgical Specialties, Radiological Sciences and Public Health, University of Brescia, Italy.
¹⁴ Department of Obstetrics and Gynecology and Department of Population Health, New York University School of Medicine, New York, NY, USA, New York University Cancer Institute, New York, NY, USA.
¹⁵ Department of Epidemiology, University of Washington, Seattle, WA, USA.
¹⁶ Department of Preventive Medicine, Biostatistics Division, Keck School of Medicine and.
¹⁷ Division of Cancer Epidemiology and Genetics, Division of Environmental Health Sciences, Yale School of Public Health, New Haven, Connecticut, USA.
¹⁸ Division of Cancer Prevention.
¹⁹ Department of Clinical Sciences and Community Health, University of Milan, Department of Preventive Medicine, Fondazione IRCCS Ca' Granda Policlinico Hospital, Milan, Italy.
²⁰ Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, TN, USA, International Epidemiology Institute, Rockville, MD, USA.
²¹ Department of Epidemiology, German Institute of Human Nutrition, Potsdam-Rehbruecke, Germany.
²² Institute for Translational Epidemiology, Hematology and Medical Oncology, Mount Sinai Hospital School of Medicine, New York, NY, USA.
²³ Division of Cancer Epidemiology and Genetics, Department of Oncology, University of Cambridge, Cambridge CB2 2RE, UK.
²⁴ Institut National de la Sante et de la Recherche Medicale (INSERM) and Institut Gustave Roussy, Villejuif, France.
²⁵ Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, CA, USA.
²⁶ International Agency for Research on Cancer (IARC-WHO), Lyon, France.
²⁷ Westat, Rockville, MD, USA.
²⁸ National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands, Department of Gastroenterology and Hepatology, University Medical Centre Utrecht, Utrecht, The Netherlands.
²⁹ Division of Preventive Medicine, Brigham and Women's Hospital, Boston, MA, USA.
³⁰ Centers for Disease Control and Prevention, National Institute for Occupational Safety and Health, Cincinnati, OH, USA.
³¹ CeRePP, Paris, France, UPMC Univ Paris 06, GRC n°5, ONCOTYPE-URO, Paris, France.
³² Genomic Epidemiology Group, German Cancer Research Center (DKFZ), Heidelberg, Germany.
³³ Department of Epidemiology, Second Military Medical University, Shanghai, China.
³⁴ Medical Oncology Department, Hospital Ramón y Cajal, Madrid, Spain.
³⁵ Faculty of Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan, Division of Chest Medicine, Department of Internal Medicine, Taichung Veterans General Hospital, Taichung, Taiwan.
³⁶ National Institute of Cancer Research.
³⁷ Department of Abdominal Surgery and.
³⁸ Genomics Research Center, Academia Sinica, Taipei, Taiwan, Graduate Institute of Epidemiology, College of Public Health, National Taiwan University, Taipei, Taiwan.
³⁹ Cancer Center, China Medical University Hospital, Taipei, Taiwan.
⁴⁰ Program in Molecular and Genetic Epidemiology.
⁴¹ Department of Internal Medicine, National Taiwan University Hospital and National Taiwan University College of Medicine, Taipei, Taiwan.
⁴² Department of Epidemiology and Public Health, Yong Loo Lin School of Medicine and Chest Department, Taipei Veterans General Hospital, Taipei, Taiwan, College of Medical Science and Technology, Taipei Medical University, Taiwan.
⁴³ School of Public Health, University of California, Berkeley, CA, USA.
⁴⁴ Cancer Prevention Institute of California, Fremont, CA, USA.
⁴⁵ Inserm, Centre for Research in Epidemiology and Population Health (CESP), Villejuif, France.
⁴⁶ Washington University School of Medicine, St Louis, MO, USA.
⁴⁷ Urologic Oncology, University of Colorado, Aurora, CO, USA.
⁴⁸ CeRePP, Paris, France, AP-HP, Department of Urology, Tenon Hospital, GHU-Est, Paris, France, UPMC Univ Paris 06, GRC n°5, ONCOTYPE-URO, Paris, France.
⁴⁹ Department of Public Health Sciences, School of Public Health, University of Alberta, Edmonton, AB, Canada T6G 2R3.
⁵⁰ Program in Molecular and Genetic Epidemiology, Department of Medicine, Channing Division of Network Medicine and Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.
⁵¹ Shanxi Cancer Hospital, Taiyuan, Shanxi, People's Republic of China.
⁵² Department of Urology.
⁵³ Service de Neurologie Mazarin, GH Pitie-Salpetriere, APHP, and UMR 975 INSERM-UPMC, CRICM, Paris, France.
⁵⁴ Epidemiology Research Program, American Cancer Society, Atlanta, GA, USA.
⁵⁵ Unit of Nutrition, Environment and Cancer, Cancer Epidemiology Research Program, Bellvitge Biomedical Research Institute, Catalan Institute of Oncology (ICO-IDIBELL), Barcelona, Spain.
⁵⁶ Epidemiology and Genomics Research Program, Division of Cancer Control and Population Sciences, Bethesda, MD, USA.
⁵⁷ Shanghai Cancer Institute, Shanghai, People's Republic of China.
⁵⁸ Institute for Health Research, Kaiser Permanente, Denver, CO, USA.
⁵⁹ UCL Cancer Institute, Huntley Street, London WC1E 6BT, UK, Royal National Orthopaedic Hospital NHS Trust, Stanmore, Middlesex HA7 4LP, UK.
⁶⁰ Department of Biostatistics, University of Kansas Medical Center, Kansas City, KS, USA.
⁶¹ Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA, Channing Laboratory, Department of Medicine.
⁶² Genomic Medicine Group, Galician Foundation of Genomic Medicine, Complejo Hospitalario Universitario de Santiago, Servicio Galego de Saude (SERGAS), Instituto de Investigación Sanitaria de Santiago (IDIS), Santiago de Compostela, Spain.
⁶³ Samuel Lunenfeld Research Institute and.
⁶⁴ Department of Epidemiology, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiaotaong University School of Medicine, Shanghai, China.
⁶⁵ Division of Cancer Epidemiology and Genetics, Division of Genetics and Epidemiology, Institute of Cancer Research, Sutton, UK.
⁶⁶ Unidad de Investigación, Hospital Universitario de Canarias, La Laguna, Spain.
⁶⁷ Nationwide Children's Hospital, and The Ohio State University Department of Pathology and Pediatrics, Columbus, OH, USA.
⁶⁸ Division of Preventive Medicine, Department of Medicine and Division of Aging, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA, Massachusetts Veteran's Epidemiology, Research and Information Center, Geriatric Research Education and Clinical Center, Veterans Affairs Boston Healthcare System, Boston, MA, USA.
⁶⁹ Office of Cancer Genomics, Department of Health and Human Services, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
⁷⁰ Information Management Services Inc., Calverton, MD, USA.
⁷¹ Cancer Epidemiology Centre, The Cancer Council Victoria & Centre for Molecular, Environmental, Genetic, and Analytic Epidemiology, The University of Melbourne, Victoria, Australia.
⁷² Division of Cancer Control and Population Sciences and.
⁷³ Program in Molecular and Genetic Epidemiology, Department of Nutrition and.
⁷⁴ Department of Oncology, Department of Pathology and Department of Medicine, The Sol Goldman Pancreatic Research Center, The Johns Hopkins University School of Medicine, Baltimore, MD, USA.
⁷⁵ Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, ON, Canada.
⁷⁶ Unit of Nutrition, Environment and Cancer, Cancer Epidemiology Research Programme, Catalan Institute of Oncology (ICO), Barcelona, Spain.
⁷⁷ Albert Einstein College of Medicine, The Children's Hospital at Montefiore, Bronx, NY, USA.
⁷⁸ Department of Laboratory Medicine and Pathology, School of Medicine, University of Minnesota, Minneapolis, MN, USA.
⁷⁹ Department of Urology, Washington University School of Medicine, St Louis, MO, USA.
⁸⁰ Department of Epidemiology.
⁸¹ Department of Epidemiology, School of Public Health, China Medical University, Shenyang, China.
⁸² Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
⁸³ Department of Public Health and Clinical Medicine/Nutritional Research.
⁸⁴ Channing Laboratory, Department of Medicine.
⁸⁵ Laboratory of Human Carcinogenesis, Center for Cancer Research, National Cancer Institute, Bethesda, MD, USA.
⁸⁶ Laboratory of Experimental Oncology, Orthopaedic Rizzoli Institute, Bologna, Italy.
⁸⁷ Division of Cancer Epidemiology and Genetics, Department of Population Health, New York University Langone Medical Center and Department of Environmental Medicine, New York University Langone Medical Center, New York University Cancer Institute, New York, NY, USA.
⁸⁸ Center for Cancer Research and.
⁸⁹ Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.
⁹⁰ Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
⁹¹ Institute of Environmental Medicine, Seoul National University Medical Research Center, Seoul, Republic of Korea, Department of Preventive Medicine and.
⁹² Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, NY, USA.
⁹³ Division of Biostatistics and Bioinformatics, Institute of Population Health Sciences and Taiwan Lung Cancer Tissue/Specimen Information Resource Center, National Health Research Institutes, Zhunan, Taiwan.
⁹⁴ Cancer Prevention Institute of California, Fremont, CA, USA, Stanford Cancer Institute, Stanford University, Stanford, CA, USA.
⁹⁵ Division of Biostatistics and Bioinformatics, Institute of Population Health Sciences and.
⁹⁶ Department of Epidemiology and Biostatistics, Cancer Center, Nanjing Medical University, Nanjing, China.
⁹⁷ Program in Molecular and Genetic Epidemiology, Department of Medicine, Channing Division of Network Medicine and Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA, Broad Institute of Harvard and MIT, Cambridge, MA, USA.
⁹⁸ Division of Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya, Japan.
⁹⁹ Cancer Genomics Research Laboratory, National Cancer Institute, Division of Cancer Epidemiology and Genetics, SAIC-Frederick, Inc., Frederick National Laboratory for Cancer Research, Frederick, MD, USA, Cancer Genomics Research Laboratory, National Cancer Institute, Division of Cancer Epidemiology and Genetics, SAIC-Frederick, Inc., Frederick National Laboratory for Cancer Research, Frederick, MD, USA, Bioinformed, LLC, Gaithersburg, MD, USA.
¹⁰⁰ Department of Oncology, Finsen Center, Rigshospitalet, Copenhagen, Denmark, Unit of Survivorship, Danish Cancer Society Research Center, Copenhagen, Denmark.
¹⁰¹ International Agency for Research on Cancer (IARC-WHO), Lyon, France, Department of Public Health and Clinical Medicine.
¹⁰² Vermont Cancer Registry, Burlington, VT, USA.
¹⁰³ Group Health Research Institute, Seattle, WA, USA.
¹⁰⁴ School of Clinical Medicine, University of Cambridge, UK.
¹⁰⁵ Department of Biochemistry and Department of Cell Biology, School of Medicine, Kyungpook National University, Daegu, Republic of Korea.
¹⁰⁶ Institute of Environmental Medicine, Seoul National University Medical Research Center, Seoul, Republic of Korea.
¹⁰⁷ Genomic Research Center for Lung and Breast/Ovarian Cancers, Korea University Anam Hospital, Seoul, Republic of Korea, Department of Internal Medicine and Division of Brain and Division of Oncology/Hematology, Department of Internal Medicine, Korea University College of Medicine, Seoul, Republic of Korea.
¹⁰⁸ Lung and Esophageal Cancer Clinic, Chonnam National University Hwasun Hospital, Hwasun-eup, Republic of Korea.
¹⁰⁹ Cancer Research Institute, Seoul National University College of Medicine, Seoul, Republic of Korea.
¹¹⁰ Department of Oncology, Department of Pathology and Department of Medicine, The Sol Goldman Pancreatic Research Center, The Johns Hopkins University School of Medicine, Baltimore, MD, USA, Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.
¹¹¹ Department of Medicine and.
¹¹² Centre for Research in Environmental Epidemiology (CREAL), Barcelona, Spain, IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain, CIBER Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain, National School of Public Health, Athens, Greece.
¹¹³ Duke-NUS Graduate Medical School, Singapore, Singapore, Saw Swee Hock School of Public Health, National University of Singapore, Singapore.
¹¹⁴ Division of Genome Biology, National Cancer Center Research Institute, Tokyo, Japan.
¹¹⁵ Epidemiology Program, University of Hawaii Cancer Center, Honolulu, HI, USA.
¹¹⁶ Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy.
¹¹⁷ Division of Genome Biology, National Cancer Center Research Institute, Tokyo, Japan, Department of Respiratory Medicine, Mitsui Memorial Hospital, Tokyo, Japan.
¹¹⁸ Department of Pediatric Oncology, A.Y. Ankara Oncology Training and Research Hospital, Yenimahalle- Ankara, Turkey.
¹¹⁹ Centre National de Genotypage, IG/CEA, Evry Cedex, France, Centre d'Étude du Polymorphism Humain (CEPH), Paris, France.
¹²⁰ Texas Children's Cancer and Hematology Centers.
¹²¹ Department of Pediatrics, University Clinic of Navarra, Universidad de Navarra, Pamplona, Spain.
¹²² Department of Preventive Medicine and Department of Environmental Health, Korea National Open University, Seoul, Republic of Korea.
¹²³ Scott Department of Urology and.
¹²⁴ Department of Gastrointestinal Medical Oncology.
¹²⁵ Saw Swee Hock School of Public Health, National University of Singapore, Singapore.
¹²⁶ State Key Laboratory of Molecular Oncology, Cancer Institute and Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China.
¹²⁷ Department of Cancer Epidemiology and Prevention, Maria Sklodowska-Curie Cancer Center and Institute of Oncology, Warsaw, Poland.
¹²⁸ Human Genetics Division, Genome Institute of Singapore, Singapore, School of Life Sciences, Anhui Medical University, Hefei, China.
¹²⁹ Department of Surgical and Perioperative Sciences, Urology and Andrology and.
¹³⁰ CIBER Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain.
¹³¹ Ministry of Education Key Laboratory of Contemporary Anthropology, School of Life Sciences, Fudan University, Shanghai, China, State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai, China.
¹³² Department of Medicine, Channing Division of Network Medicine and Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.
¹³³ Centro Nacional de Investigaciones Oncologicas, Melchor Fernández Almagro, 3, Madrid E-28029, Spain.
¹³⁴ National Institute for Health and Welfare, Helsinki, Finland.
¹³⁵ Lucile Packard Children's Hospital, Stanford University, Palo Alto, CA, USA.
¹³⁶ Department of Cardiac, Thoracic and Vascular Sciences, University of Padova, Padua, Italy.
¹³⁷ Division of Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya, Japan, Department of Preventive Medicine, Kyushu University Faculty of Medical Scicence, Fukuoka, Japan.
¹³⁸ Department of Health Disparities Research, Division of OVP, Cancer Prevention and Population Sciences, and Center for Community-Engaged Translational Research, Duncan Family Institute and.
¹³⁹ Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA.
¹⁴⁰ Key Laboratory for Environment and Health, School of Public Health, Tongji Medical College, Huazhong University of Sciences and Technology, Wuhan, China.
¹⁴¹ Department of Epidemiology, Division of Biology and Medicine, Brown University, Providence, RI, USA.
¹⁴² Health Sciences Research Institute, University of Warwick, Coventry, UK.
¹⁴³ Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, NY, USA.
¹⁴⁴ Complex Traits Genetics Team and.
¹⁴⁵ Dipartimento di Medicina Clinica e Chirurgia, Federico II University, Naples, Italy.
¹⁴⁶ Department of Biochemistry and Department of Cell Biology, School of Medicine, Kyungpook National University, Daegu, Republic of Korea, Lung Cancer Center, Kyungpook National University Medical Center, Daegu, Republic of Korea.
¹⁴⁷ Julius Center for Health Sciences and Primary Care, University Medical Center, Utrecht, Utrecht, The Netherlands, Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK.
¹⁴⁸ Nofer Institute of Occupational Medicine, Lodz, Poland.
¹⁴⁹ Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA, Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, NY, USA.
¹⁵⁰ Department of Epidemiology, Cancer Institute (Hospital), Chinese Academy of Medical Sciences, Beijing, People's Republic of China.
¹⁵¹ Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK.
¹⁵² Yale School of Public Health, New Haven, CT, USA.
¹⁵³ Department of Internal Medicine, Inha University College of Medicine, Incheon, Korea.
¹⁵⁴ Karmanos Cancer Institute and Department of Oncology and.
¹⁵⁵ Karmanos Cancer Institute and Department of Family Medicine and Public Health Sciences, Wayne State University School of Medicine, Detroit, MI, USA.
¹⁵⁶ Maine Cancer Registry, Augusta, ME, USA.
¹⁵⁷ Centre for Research in Occupational Health, Universitat Pompeu Fabra, Barcelona, Spain, CIBER of Epidemiology and Public Health (CIBERESP).
¹⁵⁸ Department of Biostatistics, MD Anderson Cancer Center, Houston, TX, USA.
¹⁵⁹ Department of Genomics of Common Disease, School of Public Health, Imperial College London, London, UK.
¹⁶⁰ Nutritional Epidemiology Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.
¹⁶¹ Department of Surgery, Division of Cardiothoracic Surgery, Queen Mary Hospital, Hong Kong, China.
¹⁶² Department of Neurosurgery, University of Bonn Medical Center, Bonn, Germany.
¹⁶³ Department of Pathology, The University of Melbourne, Melbourne, VIC, Australia.
¹⁶⁴ University of Minnesota, Minneapolis, MN, USA.
¹⁶⁵ Dan L. Duncan Center, Baylor College of Medicine, Houston, TX, USA.
¹⁶⁶ Department of Epidemiology, Division of Cancer Prevention and Population Sciences, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.
¹⁶⁷ Department of Internal Medicine, National Cheng Kung University Hospital and College of Medicine, Tainan, Taiwan.
¹⁶⁸ Department of Surgical and Perioperative Sciences/Surgery, Umeå University, Umeå, Sweden.
¹⁶⁹ Department of Thoracic and Cardiovascular Surgery, Seoul St Mary's Hospital, Seoul, South Korea.
¹⁷⁰ Division of Genetics and Epidemiology, Institute of Cancer Research, Sutton, UK, Division of Breast Cancer Research, Institute of Cancer Research, London, UK.
¹⁷¹ Instituto Universitario de Oncología, Universidad de Oviedo, Oviedo, Spain.
¹⁷² Sir Peter MacCallum Department of Oncology, University of Melbourne, St Andrew's Place, East Melbourne, VIC, Australia.
¹⁷³ Royal National Orthopaedic Hospital NHS Trust, Stanmore, Middlesex HA7 4LP, UK.
¹⁷⁴ Danish Cancer Society Research Center, Copenhagen, Denmark.
¹⁷⁵ Department of Epidemiology, Harvard School of Public Health, Boston, MA, USA.
¹⁷⁶ Department of Pulmonary Medicine, Chang Gung Memorial Hospital, Chiayi, Taiwan.
¹⁷⁷ Cancer Registry Associazione Iblea Ricerca Epidemiologica, Onlus and Asp Ragusa, Ragusa Italy.
¹⁷⁸ Kaiser Permanente Northern California, Oakland, CA, USA.
¹⁷⁹ Division of Environmental Epidemiology, Institute for Risk Assessment Sciences (IRAS), Utrecht University, Utrecht, The Netherlands.
¹⁸⁰ Imperial College, London, UK, Human Genetics Foundation (HuGeF), Torino Italy.
¹⁸¹ National Research Centre for the Working Environment, Copenhagen, Denmark, National Food Institute, Technical University of Denmark, Soborg, Denmark.
¹⁸² Division of Cancer Epidemiology and Genetics, Cancer Genomics Research Laboratory, National Cancer Institute, Division of Cancer Epidemiology and Genetics, SAIC-Frederick, Inc., Frederick National Laboratory for Cancer Research, Frederick, MD, USA, Department of Biochemistry and Centre for Genomic Sciences, LKS Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China.
¹⁸³ Division of Cancer Etiology, Department of Population Sciences, City of Hope and the Beckman Research Institute, Duarte, CA, USA.
¹⁸⁴ Department of Community Medicine, Faculty of Health Sciences, University of Tromsø, The Arctic University of Norway, Tromsø, Norway, Department of Research, Cancer Registry of Norway, Oslo, Norway, Department of Medical Epidemiology and Biostatistics and Samfundet Folkhälsan, Helsinki, Finland.
¹⁸⁵ University of California San Francisco, San Francisco, CA, USA.
¹⁸⁶ Unit of Nutritional Epidemiology, Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
¹⁸⁷ Department of Pathology and.
¹⁸⁸ Guangdong Lung Cancer Institute, Medical Research Center and Cancer Center of Guangdong General Hospital, Guangdong Academy of Medical Sciences, Guangzhou, China.
¹⁸⁹ School of Public Health, Li Ka Shing (LKS) Faculty of Medicine, The University of Hong Kong, Hong Kong, China.
¹⁹⁰ Department of Pathology and Molecular Diagnostics, Aichi Cancer Center Hospital and.
¹⁹¹ University of Pittsburgh Cancer Institute, Pittsburgh, PA, USA and.
¹⁹² Department of Population Health, New York University School of Medicine, New York, NY, USA, New York University Cancer Institute, New York, NY, USA.
¹⁹³ Program in Molecular and Genetic Epidemiology, Department of Epidemiology, Harvard School of Public Health, Boston, MA, USA.
¹⁹⁴ Division of Cancer Epidemiology and Genetics, [email protected].

PMID: 25027329
PMCID: PMC4240198
DOI: 10.1093/hmg/ddu363

Multicenter Study

Imputation and subset-based association analysis across different cancer types identifies multiple independent risk loci in the TERT-CLPTM1L region on chromosome 5p15.33

Zhaoming Wang et al. Hum Mol Genet. 2014.

. 2014 Dec 15;23(24):6616-33.

doi: 10.1093/hmg/ddu363. Epub 2014 Jul 15.

Authors

Affiliations

¹ Division of Cancer Epidemiology and Genetics, Cancer Genomics Research Laboratory, National Cancer Institute, Division of Cancer Epidemiology and Genetics, SAIC-Frederick, Inc., Frederick National Laboratory for Cancer Research, Frederick, MD, USA.
² Division of Cancer Epidemiology and Genetics.
³ Korle Bu Teaching Hospital, PO BOX 77, Accra, Ghana, University of Ghana Medical School, PO Box 4236, Accra, Ghana.
⁴ Unit of Epidemiology, Institute of Environmental Medicine.
⁵ Clinical Trial Service Unit and Epidemiological Studies Unit, University of Oxford, Oxford, UK.
⁶ Department of Cancer Prevention and Control, Roswell Park Cancer Institute, Buffalo, NY, USA.
⁷ Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, TN, USA.
⁸ Public Health Division of Gipuzkoa, Basque Regional Health Department, San Sebastian, Spain, CIBERESP, CIBER Epidemiologia y Salud Publica, Madrid, Spain.
⁹ Geisel School of Medicine at Dartmouth, Hanover, NH, USA.
¹⁰ Department of Radiation Sciences, Oncology.
¹¹ Division of Urologic Surgery, Washington University School of Medicine, St Louis, MO, USA.
¹² Litwin Centre for Cancer Genetics, Samuel Lunenfeld Research Institute, Mt Sinai Hospital, University of Toronto, Toronto, ON, Canada.
¹³ Department of Medical and Surgical Specialties, Radiological Sciences and Public Health, University of Brescia, Italy.
¹⁴ Department of Obstetrics and Gynecology and Department of Population Health, New York University School of Medicine, New York, NY, USA, New York University Cancer Institute, New York, NY, USA.
¹⁵ Department of Epidemiology, University of Washington, Seattle, WA, USA.
¹⁶ Department of Preventive Medicine, Biostatistics Division, Keck School of Medicine and.
¹⁷ Division of Cancer Epidemiology and Genetics, Division of Environmental Health Sciences, Yale School of Public Health, New Haven, Connecticut, USA.
¹⁸ Division of Cancer Prevention.
¹⁹ Department of Clinical Sciences and Community Health, University of Milan, Department of Preventive Medicine, Fondazione IRCCS Ca' Granda Policlinico Hospital, Milan, Italy.
²⁰ Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, TN, USA, International Epidemiology Institute, Rockville, MD, USA.
²¹ Department of Epidemiology, German Institute of Human Nutrition, Potsdam-Rehbruecke, Germany.
²² Institute for Translational Epidemiology, Hematology and Medical Oncology, Mount Sinai Hospital School of Medicine, New York, NY, USA.
²³ Division of Cancer Epidemiology and Genetics, Department of Oncology, University of Cambridge, Cambridge CB2 2RE, UK.
²⁴ Institut National de la Sante et de la Recherche Medicale (INSERM) and Institut Gustave Roussy, Villejuif, France.
²⁵ Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, CA, USA.
²⁶ International Agency for Research on Cancer (IARC-WHO), Lyon, France.
²⁷ Westat, Rockville, MD, USA.
²⁸ National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands, Department of Gastroenterology and Hepatology, University Medical Centre Utrecht, Utrecht, The Netherlands.
²⁹ Division of Preventive Medicine, Brigham and Women's Hospital, Boston, MA, USA.
³⁰ Centers for Disease Control and Prevention, National Institute for Occupational Safety and Health, Cincinnati, OH, USA.
³¹ CeRePP, Paris, France, UPMC Univ Paris 06, GRC n°5, ONCOTYPE-URO, Paris, France.
³² Genomic Epidemiology Group, German Cancer Research Center (DKFZ), Heidelberg, Germany.
³³ Department of Epidemiology, Second Military Medical University, Shanghai, China.
³⁴ Medical Oncology Department, Hospital Ramón y Cajal, Madrid, Spain.
³⁵ Faculty of Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan, Division of Chest Medicine, Department of Internal Medicine, Taichung Veterans General Hospital, Taichung, Taiwan.
³⁶ National Institute of Cancer Research.
³⁷ Department of Abdominal Surgery and.
³⁸ Genomics Research Center, Academia Sinica, Taipei, Taiwan, Graduate Institute of Epidemiology, College of Public Health, National Taiwan University, Taipei, Taiwan.
³⁹ Cancer Center, China Medical University Hospital, Taipei, Taiwan.
⁴⁰ Program in Molecular and Genetic Epidemiology.
⁴¹ Department of Internal Medicine, National Taiwan University Hospital and National Taiwan University College of Medicine, Taipei, Taiwan.
⁴² Department of Epidemiology and Public Health, Yong Loo Lin School of Medicine and Chest Department, Taipei Veterans General Hospital, Taipei, Taiwan, College of Medical Science and Technology, Taipei Medical University, Taiwan.
⁴³ School of Public Health, University of California, Berkeley, CA, USA.
⁴⁴ Cancer Prevention Institute of California, Fremont, CA, USA.
⁴⁵ Inserm, Centre for Research in Epidemiology and Population Health (CESP), Villejuif, France.
⁴⁶ Washington University School of Medicine, St Louis, MO, USA.
⁴⁷ Urologic Oncology, University of Colorado, Aurora, CO, USA.
⁴⁸ CeRePP, Paris, France, AP-HP, Department of Urology, Tenon Hospital, GHU-Est, Paris, France, UPMC Univ Paris 06, GRC n°5, ONCOTYPE-URO, Paris, France.
⁴⁹ Department of Public Health Sciences, School of Public Health, University of Alberta, Edmonton, AB, Canada T6G 2R3.
⁵⁰ Program in Molecular and Genetic Epidemiology, Department of Medicine, Channing Division of Network Medicine and Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.
⁵¹ Shanxi Cancer Hospital, Taiyuan, Shanxi, People's Republic of China.
⁵² Department of Urology.
⁵³ Service de Neurologie Mazarin, GH Pitie-Salpetriere, APHP, and UMR 975 INSERM-UPMC, CRICM, Paris, France.
⁵⁴ Epidemiology Research Program, American Cancer Society, Atlanta, GA, USA.
⁵⁵ Unit of Nutrition, Environment and Cancer, Cancer Epidemiology Research Program, Bellvitge Biomedical Research Institute, Catalan Institute of Oncology (ICO-IDIBELL), Barcelona, Spain.
⁵⁶ Epidemiology and Genomics Research Program, Division of Cancer Control and Population Sciences, Bethesda, MD, USA.
⁵⁷ Shanghai Cancer Institute, Shanghai, People's Republic of China.
⁵⁸ Institute for Health Research, Kaiser Permanente, Denver, CO, USA.
⁵⁹ UCL Cancer Institute, Huntley Street, London WC1E 6BT, UK, Royal National Orthopaedic Hospital NHS Trust, Stanmore, Middlesex HA7 4LP, UK.
⁶⁰ Department of Biostatistics, University of Kansas Medical Center, Kansas City, KS, USA.
⁶¹ Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA, Channing Laboratory, Department of Medicine.
⁶² Genomic Medicine Group, Galician Foundation of Genomic Medicine, Complejo Hospitalario Universitario de Santiago, Servicio Galego de Saude (SERGAS), Instituto de Investigación Sanitaria de Santiago (IDIS), Santiago de Compostela, Spain.
⁶³ Samuel Lunenfeld Research Institute and.
⁶⁴ Department of Epidemiology, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiaotaong University School of Medicine, Shanghai, China.
⁶⁵ Division of Cancer Epidemiology and Genetics, Division of Genetics and Epidemiology, Institute of Cancer Research, Sutton, UK.
⁶⁶ Unidad de Investigación, Hospital Universitario de Canarias, La Laguna, Spain.
⁶⁷ Nationwide Children's Hospital, and The Ohio State University Department of Pathology and Pediatrics, Columbus, OH, USA.
⁶⁸ Division of Preventive Medicine, Department of Medicine and Division of Aging, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA, Massachusetts Veteran's Epidemiology, Research and Information Center, Geriatric Research Education and Clinical Center, Veterans Affairs Boston Healthcare System, Boston, MA, USA.
⁶⁹ Office of Cancer Genomics, Department of Health and Human Services, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
⁷⁰ Information Management Services Inc., Calverton, MD, USA.
⁷¹ Cancer Epidemiology Centre, The Cancer Council Victoria & Centre for Molecular, Environmental, Genetic, and Analytic Epidemiology, The University of Melbourne, Victoria, Australia.
⁷² Division of Cancer Control and Population Sciences and.
⁷³ Program in Molecular and Genetic Epidemiology, Department of Nutrition and.
⁷⁴ Department of Oncology, Department of Pathology and Department of Medicine, The Sol Goldman Pancreatic Research Center, The Johns Hopkins University School of Medicine, Baltimore, MD, USA.
⁷⁵ Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, ON, Canada.
⁷⁶ Unit of Nutrition, Environment and Cancer, Cancer Epidemiology Research Programme, Catalan Institute of Oncology (ICO), Barcelona, Spain.
⁷⁷ Albert Einstein College of Medicine, The Children's Hospital at Montefiore, Bronx, NY, USA.
⁷⁸ Department of Laboratory Medicine and Pathology, School of Medicine, University of Minnesota, Minneapolis, MN, USA.
⁷⁹ Department of Urology, Washington University School of Medicine, St Louis, MO, USA.
⁸⁰ Department of Epidemiology.
⁸¹ Department of Epidemiology, School of Public Health, China Medical University, Shenyang, China.
⁸² Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
⁸³ Department of Public Health and Clinical Medicine/Nutritional Research.
⁸⁴ Channing Laboratory, Department of Medicine.
⁸⁵ Laboratory of Human Carcinogenesis, Center for Cancer Research, National Cancer Institute, Bethesda, MD, USA.
⁸⁶ Laboratory of Experimental Oncology, Orthopaedic Rizzoli Institute, Bologna, Italy.
⁸⁷ Division of Cancer Epidemiology and Genetics, Department of Population Health, New York University Langone Medical Center and Department of Environmental Medicine, New York University Langone Medical Center, New York University Cancer Institute, New York, NY, USA.
⁸⁸ Center for Cancer Research and.
⁸⁹ Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.
⁹⁰ Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
⁹¹ Institute of Environmental Medicine, Seoul National University Medical Research Center, Seoul, Republic of Korea, Department of Preventive Medicine and.
⁹² Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, NY, USA.
⁹³ Division of Biostatistics and Bioinformatics, Institute of Population Health Sciences and Taiwan Lung Cancer Tissue/Specimen Information Resource Center, National Health Research Institutes, Zhunan, Taiwan.
⁹⁴ Cancer Prevention Institute of California, Fremont, CA, USA, Stanford Cancer Institute, Stanford University, Stanford, CA, USA.
⁹⁵ Division of Biostatistics and Bioinformatics, Institute of Population Health Sciences and.
⁹⁶ Department of Epidemiology and Biostatistics, Cancer Center, Nanjing Medical University, Nanjing, China.
⁹⁷ Program in Molecular and Genetic Epidemiology, Department of Medicine, Channing Division of Network Medicine and Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA, Broad Institute of Harvard and MIT, Cambridge, MA, USA.
⁹⁸ Division of Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya, Japan.
⁹⁹ Cancer Genomics Research Laboratory, National Cancer Institute, Division of Cancer Epidemiology and Genetics, SAIC-Frederick, Inc., Frederick National Laboratory for Cancer Research, Frederick, MD, USA, Cancer Genomics Research Laboratory, National Cancer Institute, Division of Cancer Epidemiology and Genetics, SAIC-Frederick, Inc., Frederick National Laboratory for Cancer Research, Frederick, MD, USA, Bioinformed, LLC, Gaithersburg, MD, USA.
¹⁰⁰ Department of Oncology, Finsen Center, Rigshospitalet, Copenhagen, Denmark, Unit of Survivorship, Danish Cancer Society Research Center, Copenhagen, Denmark.
¹⁰¹ International Agency for Research on Cancer (IARC-WHO), Lyon, France, Department of Public Health and Clinical Medicine.
¹⁰² Vermont Cancer Registry, Burlington, VT, USA.
¹⁰³ Group Health Research Institute, Seattle, WA, USA.
¹⁰⁴ School of Clinical Medicine, University of Cambridge, UK.
¹⁰⁵ Department of Biochemistry and Department of Cell Biology, School of Medicine, Kyungpook National University, Daegu, Republic of Korea.
¹⁰⁶ Institute of Environmental Medicine, Seoul National University Medical Research Center, Seoul, Republic of Korea.
¹⁰⁷ Genomic Research Center for Lung and Breast/Ovarian Cancers, Korea University Anam Hospital, Seoul, Republic of Korea, Department of Internal Medicine and Division of Brain and Division of Oncology/Hematology, Department of Internal Medicine, Korea University College of Medicine, Seoul, Republic of Korea.
¹⁰⁸ Lung and Esophageal Cancer Clinic, Chonnam National University Hwasun Hospital, Hwasun-eup, Republic of Korea.
¹⁰⁹ Cancer Research Institute, Seoul National University College of Medicine, Seoul, Republic of Korea.
¹¹⁰ Department of Oncology, Department of Pathology and Department of Medicine, The Sol Goldman Pancreatic Research Center, The Johns Hopkins University School of Medicine, Baltimore, MD, USA, Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.
¹¹¹ Department of Medicine and.
¹¹² Centre for Research in Environmental Epidemiology (CREAL), Barcelona, Spain, IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain, CIBER Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain, National School of Public Health, Athens, Greece.
¹¹³ Duke-NUS Graduate Medical School, Singapore, Singapore, Saw Swee Hock School of Public Health, National University of Singapore, Singapore.
¹¹⁴ Division of Genome Biology, National Cancer Center Research Institute, Tokyo, Japan.
¹¹⁵ Epidemiology Program, University of Hawaii Cancer Center, Honolulu, HI, USA.
¹¹⁶ Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy.
¹¹⁷ Division of Genome Biology, National Cancer Center Research Institute, Tokyo, Japan, Department of Respiratory Medicine, Mitsui Memorial Hospital, Tokyo, Japan.
¹¹⁸ Department of Pediatric Oncology, A.Y. Ankara Oncology Training and Research Hospital, Yenimahalle- Ankara, Turkey.
¹¹⁹ Centre National de Genotypage, IG/CEA, Evry Cedex, France, Centre d'Étude du Polymorphism Humain (CEPH), Paris, France.
¹²⁰ Texas Children's Cancer and Hematology Centers.
¹²¹ Department of Pediatrics, University Clinic of Navarra, Universidad de Navarra, Pamplona, Spain.
¹²² Department of Preventive Medicine and Department of Environmental Health, Korea National Open University, Seoul, Republic of Korea.
¹²³ Scott Department of Urology and.
¹²⁴ Department of Gastrointestinal Medical Oncology.
¹²⁵ Saw Swee Hock School of Public Health, National University of Singapore, Singapore.
¹²⁶ State Key Laboratory of Molecular Oncology, Cancer Institute and Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China.
¹²⁷ Department of Cancer Epidemiology and Prevention, Maria Sklodowska-Curie Cancer Center and Institute of Oncology, Warsaw, Poland.
¹²⁸ Human Genetics Division, Genome Institute of Singapore, Singapore, School of Life Sciences, Anhui Medical University, Hefei, China.
¹²⁹ Department of Surgical and Perioperative Sciences, Urology and Andrology and.
¹³⁰ CIBER Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain.
¹³¹ Ministry of Education Key Laboratory of Contemporary Anthropology, School of Life Sciences, Fudan University, Shanghai, China, State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai, China.
¹³² Department of Medicine, Channing Division of Network Medicine and Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.
¹³³ Centro Nacional de Investigaciones Oncologicas, Melchor Fernández Almagro, 3, Madrid E-28029, Spain.
¹³⁴ National Institute for Health and Welfare, Helsinki, Finland.
¹³⁵ Lucile Packard Children's Hospital, Stanford University, Palo Alto, CA, USA.
¹³⁶ Department of Cardiac, Thoracic and Vascular Sciences, University of Padova, Padua, Italy.
¹³⁷ Division of Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya, Japan, Department of Preventive Medicine, Kyushu University Faculty of Medical Scicence, Fukuoka, Japan.
¹³⁸ Department of Health Disparities Research, Division of OVP, Cancer Prevention and Population Sciences, and Center for Community-Engaged Translational Research, Duncan Family Institute and.
¹³⁹ Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA.
¹⁴⁰ Key Laboratory for Environment and Health, School of Public Health, Tongji Medical College, Huazhong University of Sciences and Technology, Wuhan, China.
¹⁴¹ Department of Epidemiology, Division of Biology and Medicine, Brown University, Providence, RI, USA.
¹⁴² Health Sciences Research Institute, University of Warwick, Coventry, UK.
¹⁴³ Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, NY, USA.
¹⁴⁴ Complex Traits Genetics Team and.
¹⁴⁵ Dipartimento di Medicina Clinica e Chirurgia, Federico II University, Naples, Italy.
¹⁴⁶ Department of Biochemistry and Department of Cell Biology, School of Medicine, Kyungpook National University, Daegu, Republic of Korea, Lung Cancer Center, Kyungpook National University Medical Center, Daegu, Republic of Korea.
¹⁴⁷ Julius Center for Health Sciences and Primary Care, University Medical Center, Utrecht, Utrecht, The Netherlands, Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK.
¹⁴⁸ Nofer Institute of Occupational Medicine, Lodz, Poland.
¹⁴⁹ Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA, Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, NY, USA.
¹⁵⁰ Department of Epidemiology, Cancer Institute (Hospital), Chinese Academy of Medical Sciences, Beijing, People's Republic of China.
¹⁵¹ Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK.
¹⁵² Yale School of Public Health, New Haven, CT, USA.
¹⁵³ Department of Internal Medicine, Inha University College of Medicine, Incheon, Korea.
¹⁵⁴ Karmanos Cancer Institute and Department of Oncology and.
¹⁵⁵ Karmanos Cancer Institute and Department of Family Medicine and Public Health Sciences, Wayne State University School of Medicine, Detroit, MI, USA.
¹⁵⁶ Maine Cancer Registry, Augusta, ME, USA.
¹⁵⁷ Centre for Research in Occupational Health, Universitat Pompeu Fabra, Barcelona, Spain, CIBER of Epidemiology and Public Health (CIBERESP).
¹⁵⁸ Department of Biostatistics, MD Anderson Cancer Center, Houston, TX, USA.
¹⁵⁹ Department of Genomics of Common Disease, School of Public Health, Imperial College London, London, UK.
¹⁶⁰ Nutritional Epidemiology Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.
¹⁶¹ Department of Surgery, Division of Cardiothoracic Surgery, Queen Mary Hospital, Hong Kong, China.
¹⁶² Department of Neurosurgery, University of Bonn Medical Center, Bonn, Germany.
¹⁶³ Department of Pathology, The University of Melbourne, Melbourne, VIC, Australia.
¹⁶⁴ University of Minnesota, Minneapolis, MN, USA.
¹⁶⁵ Dan L. Duncan Center, Baylor College of Medicine, Houston, TX, USA.
¹⁶⁶ Department of Epidemiology, Division of Cancer Prevention and Population Sciences, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.
¹⁶⁷ Department of Internal Medicine, National Cheng Kung University Hospital and College of Medicine, Tainan, Taiwan.
¹⁶⁸ Department of Surgical and Perioperative Sciences/Surgery, Umeå University, Umeå, Sweden.
¹⁶⁹ Department of Thoracic and Cardiovascular Surgery, Seoul St Mary's Hospital, Seoul, South Korea.
¹⁷⁰ Division of Genetics and Epidemiology, Institute of Cancer Research, Sutton, UK, Division of Breast Cancer Research, Institute of Cancer Research, London, UK.
¹⁷¹ Instituto Universitario de Oncología, Universidad de Oviedo, Oviedo, Spain.
¹⁷² Sir Peter MacCallum Department of Oncology, University of Melbourne, St Andrew's Place, East Melbourne, VIC, Australia.
¹⁷³ Royal National Orthopaedic Hospital NHS Trust, Stanmore, Middlesex HA7 4LP, UK.
¹⁷⁴ Danish Cancer Society Research Center, Copenhagen, Denmark.
¹⁷⁵ Department of Epidemiology, Harvard School of Public Health, Boston, MA, USA.
¹⁷⁶ Department of Pulmonary Medicine, Chang Gung Memorial Hospital, Chiayi, Taiwan.
¹⁷⁷ Cancer Registry Associazione Iblea Ricerca Epidemiologica, Onlus and Asp Ragusa, Ragusa Italy.
¹⁷⁸ Kaiser Permanente Northern California, Oakland, CA, USA.
¹⁷⁹ Division of Environmental Epidemiology, Institute for Risk Assessment Sciences (IRAS), Utrecht University, Utrecht, The Netherlands.
¹⁸⁰ Imperial College, London, UK, Human Genetics Foundation (HuGeF), Torino Italy.
¹⁸¹ National Research Centre for the Working Environment, Copenhagen, Denmark, National Food Institute, Technical University of Denmark, Soborg, Denmark.
¹⁸² Division of Cancer Epidemiology and Genetics, Cancer Genomics Research Laboratory, National Cancer Institute, Division of Cancer Epidemiology and Genetics, SAIC-Frederick, Inc., Frederick National Laboratory for Cancer Research, Frederick, MD, USA, Department of Biochemistry and Centre for Genomic Sciences, LKS Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China.
¹⁸³ Division of Cancer Etiology, Department of Population Sciences, City of Hope and the Beckman Research Institute, Duarte, CA, USA.
¹⁸⁴ Department of Community Medicine, Faculty of Health Sciences, University of Tromsø, The Arctic University of Norway, Tromsø, Norway, Department of Research, Cancer Registry of Norway, Oslo, Norway, Department of Medical Epidemiology and Biostatistics and Samfundet Folkhälsan, Helsinki, Finland.
¹⁸⁵ University of California San Francisco, San Francisco, CA, USA.
¹⁸⁶ Unit of Nutritional Epidemiology, Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
¹⁸⁷ Department of Pathology and.
¹⁸⁸ Guangdong Lung Cancer Institute, Medical Research Center and Cancer Center of Guangdong General Hospital, Guangdong Academy of Medical Sciences, Guangzhou, China.
¹⁸⁹ School of Public Health, Li Ka Shing (LKS) Faculty of Medicine, The University of Hong Kong, Hong Kong, China.
¹⁹⁰ Department of Pathology and Molecular Diagnostics, Aichi Cancer Center Hospital and.
¹⁹¹ University of Pittsburgh Cancer Institute, Pittsburgh, PA, USA and.
¹⁹² Department of Population Health, New York University School of Medicine, New York, NY, USA, New York University Cancer Institute, New York, NY, USA.
¹⁹³ Program in Molecular and Genetic Epidemiology, Department of Epidemiology, Harvard School of Public Health, Boston, MA, USA.
¹⁹⁴ Division of Cancer Epidemiology and Genetics, [email protected].

PMID: 25027329
PMCID: PMC4240198
DOI: 10.1093/hmg/ddu363

Abstract

Genome-wide association studies (GWAS) have mapped risk alleles for at least 10 distinct cancers to a small region of 63 000 bp on chromosome 5p15.33. This region harbors the TERT and CLPTM1L genes; the former encodes the catalytic subunit of telomerase reverse transcriptase and the latter may play a role in apoptosis. To investigate further the genetic architecture of common susceptibility alleles in this region, we conducted an agnostic subset-based meta-analysis (association analysis based on subsets) across six distinct cancers in 34 248 cases and 45 036 controls. Based on sequential conditional analysis, we identified as many as six independent risk loci marked by common single-nucleotide polymorphisms: five in the TERT gene (Region 1: rs7726159, P = 2.10 × 10(-39); Region 3: rs2853677, P = 3.30 × 10(-36) and PConditional = 2.36 × 10(-8); Region 4: rs2736098, P = 3.87 × 10(-12) and PConditional = 5.19 × 10(-6), Region 5: rs13172201, P = 0.041 and PConditional = 2.04 × 10(-6); and Region 6: rs10069690, P = 7.49 × 10(-15) and PConditional = 5.35 × 10(-7)) and one in the neighboring CLPTM1L gene (Region 2: rs451360; P = 1.90 × 10(-18) and PConditional = 7.06 × 10(-16)). Between three and five cancers mapped to each independent locus with both risk-enhancing and protective effects. Allele-specific effects on DNA methylation were seen for a subset of risk loci, indicating that methylation and subsequent effects on gene expression may contribute to the biology of risk variants on 5p15.33. Our results provide strong support for extensive pleiotropy across this region of 5p15.33, to an extent not previously observed in other cancer susceptibility loci.

Published by Oxford University Press 2014. This work is written by (a) US Government employee(s) and is in the public domain in the US.

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Figures

**Figure 1.**
Sequential conditional analyses and ASSET meta-analyses identified up to six independent signals for the *TERT*-*CLPTM1L* region on chromosome 5p15.33. SNPs marking each region are plotted in the upper panel with two P-values (solid diamonds correspond to an unconditional test and open diamonds correspond to a conditional test) on a negative log scale (left y-axis) against genomic coordinates (x-axis, hg19). Cancers from different GWAS scans (acronyms detailed in box in top panel) that are associated within each region in the subset meta-analysis are listed (red, positively associated; green, negatively associated) from the unconditional ASSET meta-analysis. Effect alleles are shown next to SNP identifiers. Recombination hotspots (curved lines, top panel) were inferred from three populations from the DCEG Imputation Reference Set version 1 (red, CEU; green, ASN; blue, YRI) as the likelihood ratio statistics (right y-axis). Also shown are the gene structures for *TERT*, *MIR4457* and *CLPTM1L* (middle panel), and LD heat map based on r² using the 1000 Genomes CEU population (lower panel). Results are shown for the ALL analysis except the region marked by rs10069690 (top panel) and labeled with a ‘*’ that was identified in the European ancestry-only analysis (EUR).

**Figure 2.**
(A–F) Forest plots for individual risk loci on chr5p15.33 for the unconditional ASSET meta-analysis. For each cancer/GWAS scan, OR and 95% CI were listed and plotted along each line as per the unconditional association analysis. A vertical line of OR = 1 indicates the null. Two summary lines list ORs for the positively or negatively associated subsets as estimated by the ASSET program. (A) rs7726159, (B) rs451360, (C) rs2853677, (D) rs2736098, (E) rs13172201 and (F) rs10069690 in the analysis of European-ancestry studies only. Forest plots for the conditional analyses are shown in Supplementary Material, Figure S1A–E.

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References

1. Rothman N., Garcia-Closas M., Chatterjee N., Malats N., Wu X., Figueroa J.D., Real F.X., Van Den Berg D., Matullo G., Baris D., et al. A multi-stage genome-wide association study of bladder cancer identifies multiple susceptibility loci. Nat. Genet. 2010;42:978–984. - PMC - PubMed
1. Haiman C.A., Chen G.K., Vachon C.M., Canzian F., Dunning A., Millikan R.C., Wang X., Ademuyiwa F., Ahmed S., Ambrosone C.B., et al. A common variant at the TERT-CLPTM1L locus is associated with estrogen receptor-negative breast cancer. Nat. Genet. 2011;43:1210–1214. - PMC - PubMed
1. Shete S., Hosking F.J., Robertson L.B., Dobbins S.E., Sanson M., Malmer B., Simon M., Marie Y., Boisselier B., Delattre J.Y., et al. Genome-wide association study identifies five susceptibility loci for glioma. Nat. Genet. 2009;41:899–904. - PMC - PubMed
1. Wang Y., Broderick P., Webb E., Wu X., Vijayakrishnan J., Matakidou A., Qureshi M., Dong Q., Gu X., Chen W.V., et al. Common 5p15.33 and 6p21.33 variants influence lung cancer risk. Nat. Genet. 2008;40:1407–1409. - PMC - PubMed
1. McKay J.D., Hung R.J., Gaborieau V., Boffetta P., Chabrier A., Byrnes G., Zaridze D., Mukeria A., Szeszenia-Dabrowska N., Lissowska J., et al. Lung cancer susceptibility locus at 5p15.33. Nat. Genet. 2008;40:1404–1406. - PMC - PubMed

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[1] Rothman N., Garcia-Closas M., Chatterjee N., Malats N., Wu X., Figueroa J.D., Real F.X., Van Den Berg D., Matullo G., Baris D., et al. A multi-stage genome-wide association study of bladder cancer identifies multiple susceptibility loci. Nat. Genet. 2010;42:978–984. - PMC - PubMed

[2] Rothman N., Garcia-Closas M., Chatterjee N., Malats N., Wu X., Figueroa J.D., Real F.X., Van Den Berg D., Matullo G., Baris D., et al. A multi-stage genome-wide association study of bladder cancer identifies multiple susceptibility loci. Nat. Genet. 2010;42:978–984. - PMC - PubMed

[3] Haiman C.A., Chen G.K., Vachon C.M., Canzian F., Dunning A., Millikan R.C., Wang X., Ademuyiwa F., Ahmed S., Ambrosone C.B., et al. A common variant at the TERT-CLPTM1L locus is associated with estrogen receptor-negative breast cancer. Nat. Genet. 2011;43:1210–1214. - PMC - PubMed

[4] Haiman C.A., Chen G.K., Vachon C.M., Canzian F., Dunning A., Millikan R.C., Wang X., Ademuyiwa F., Ahmed S., Ambrosone C.B., et al. A common variant at the TERT-CLPTM1L locus is associated with estrogen receptor-negative breast cancer. Nat. Genet. 2011;43:1210–1214. - PMC - PubMed

[5] Shete S., Hosking F.J., Robertson L.B., Dobbins S.E., Sanson M., Malmer B., Simon M., Marie Y., Boisselier B., Delattre J.Y., et al. Genome-wide association study identifies five susceptibility loci for glioma. Nat. Genet. 2009;41:899–904. - PMC - PubMed

[6] Shete S., Hosking F.J., Robertson L.B., Dobbins S.E., Sanson M., Malmer B., Simon M., Marie Y., Boisselier B., Delattre J.Y., et al. Genome-wide association study identifies five susceptibility loci for glioma. Nat. Genet. 2009;41:899–904. - PMC - PubMed

[7] Wang Y., Broderick P., Webb E., Wu X., Vijayakrishnan J., Matakidou A., Qureshi M., Dong Q., Gu X., Chen W.V., et al. Common 5p15.33 and 6p21.33 variants influence lung cancer risk. Nat. Genet. 2008;40:1407–1409. - PMC - PubMed

[8] Wang Y., Broderick P., Webb E., Wu X., Vijayakrishnan J., Matakidou A., Qureshi M., Dong Q., Gu X., Chen W.V., et al. Common 5p15.33 and 6p21.33 variants influence lung cancer risk. Nat. Genet. 2008;40:1407–1409. - PMC - PubMed

[9] McKay J.D., Hung R.J., Gaborieau V., Boffetta P., Chabrier A., Byrnes G., Zaridze D., Mukeria A., Szeszenia-Dabrowska N., Lissowska J., et al. Lung cancer susceptibility locus at 5p15.33. Nat. Genet. 2008;40:1404–1406. - PMC - PubMed

[10] McKay J.D., Hung R.J., Gaborieau V., Boffetta P., Chabrier A., Byrnes G., Zaridze D., Mukeria A., Szeszenia-Dabrowska N., Lissowska J., et al. Lung cancer susceptibility locus at 5p15.33. Nat. Genet. 2008;40:1404–1406. - PMC - PubMed

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Imputation and subset-based association analysis across different cancer types identifies multiple independent risk loci in the TERT-CLPTM1L region on chromosome 5p15.33

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Imputation and subset-based association analysis across different cancer types identifies multiple independent risk loci in the TERT-CLPTM1L region on chromosome 5p15.33

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