Genome-wide association study of lung adenocarcinoma in East Asia and comparison with a European population

Jianxin Shi (), Kouya Shiraishi, Jiyeon Choi, Keitaro Matsuo, Tzu-Yu Chen, Juncheng Dai, Rayjean J. Hung, Kexin Chen, Xiao-Ou Shu, Young Tae Kim, Maria Teresa Landi, Dongxin Lin, Wei Zheng, Zhihua Yin, Baosen Zhou, Bao Song, Jiucun Wang, Wei Jie Seow, Lei Song, I-Shou Chang, Wei Hu, Li-Hsin Chien, Qiuyin Cai, Yun-Chul Hong, Hee Nam Kim, Yi-Long Wu, Maria Pik Wong, Brian Douglas Richardson, Karen M. Funderburk, Shilan Li, Tongwu Zhang, Charles Breeze, Zhaoming Wang, Batel Blechter, Bryan A. Bassig, Jin Hee Kim, Demetrius Albanes, Jason Y. Y. Wong, Min-Ho Shin, Lap Ping Chung, Yang Yang, She-Juan An, Hong Zheng, Yasushi Yatabe, Xu-Chao Zhang, Young-Chul Kim, Neil E. Caporaso, Jiang Chang, James Chung Man Ho, Michiaki Kubo, Yataro Daigo, Minsun Song, Yukihide Momozawa, Yoichiro Kamatani, Masashi Kobayashi, Kenichi Okubo, Takayuki Honda, Dean H. Hosgood, Hideo Kunitoh, Harsh Patel, Shun-ichi Watanabe, Yohei Miyagi, Haruhiko Nakayama, Shingo Matsumoto, Hidehito Horinouchi, Masahiro Tsuboi, Ryuji Hamamoto, Koichi Goto, Yuichiro Ohe, Atsushi Takahashi, Akiteru Goto, Yoshihiro Minamiya, Megumi Hara, Yuichiro Nishida, Kenji Takeuchi, Kenji Wakai, Koichi Matsuda, Yoshinori Murakami, Kimihiro Shimizu, Hiroyuki Suzuki, Motonobu Saito, Yoichi Ohtaki, Kazumi Tanaka, Tangchun Wu, Fusheng Wei, Hongji Dai, Mitchell J. Machiela, Jian Su, Yeul Hong Kim, In-Jae Oh, Victor Ho Fun Lee, Gee-Chen Chang, Ying-Huang Tsai, Kuan-Yu Chen, Ming-Shyan Huang, Wu-Chou Su, Yuh-Min Chen, Adeline Seow, Jae Yong Park, Sun-Seog Kweon, Kun-Chieh Chen, Yu-Tang Gao, Biyun Qian, Chen Wu, Daru Lu, Jianjun Liu, Ann G. Schwartz, Richard Houlston, Margaret R. Spitz, Ivan P. Gorlov, Xifeng Wu, Ping Yang, Stephen Lam, Adonina Tardon, Chu Chen, Stig E. Bojesen, Mattias Johansson, Angela Risch, Heike Bickeböller, Bu-Tian Ji, H-Erich Wichmann, David C. Christiani, Gadi Rennert, Susanne Arnold, Paul Brennan, James McKay, John K. Field, Sanjay S. Shete, Loic Marchand, Geoffrey Liu, Angeline Andrew, Lambertus A. Kiemeney, Shan Zienolddiny-Narui, Kjell Grankvist, Mikael Johansson, Angela Cox, Fiona Taylor, Jian-Min Yuan, Philip Lazarus, Matthew B. Schabath, Melinda C. Aldrich, Hyo-Sung Jeon, Shih Sheng Jiang, Jae Sook Sung, Chung-Hsing Chen, Chin-Fu Hsiao, Yoo Jin Jung, Huan Guo, Zhibin Hu, Laurie Burdett, Meredith Yeager, Amy Hutchinson, Belynda Hicks, Jia Liu, Bin Zhu, Sonja I. Berndt, Wei Wu, Junwen Wang, Yuqing Li, Jin Eun Choi, Kyong Hwa Park, Sook Whan Sung, Li Liu, Chang Hyun Kang, Wen-Chang Wang, Jun Xu, Peng Guan, Wen Tan, Chong-Jen Yu, Gong Yang, Alan Dart Loon Sihoe, Ying Chen, Yi Young Choi, Jun Suk Kim, Ho-Il Yoon, In Kyu Park, Ping Xu, Qincheng He, Chih-Liang Wang, Hsiao-Han Hung, Roel C. H. Vermeulen, Iona Cheng, Junjie Wu, Wei-Yen Lim, Fang-Yu Tsai, John K. C. Chan, Jihua Li, Hongyan Chen, Hsien-Chih Lin, Li Jin, Jie Liu, Norie Sawada, Taiki Yamaji, Kathleen Wyatt, Shengchao A. Li, Hongxia Ma, Meng Zhu, Zhehai Wang, Sensen Cheng, Xuelian Li, Yangwu Ren, Ann Chao, Motoki Iwasaki, Junjie Zhu, Gening Jiang, Ke Fei, Guoping Wu, Chih-Yi Chen, Chien-Jen Chen, Pan-Chyr Yang, Jinming Yu, Victoria L. Stevens, Joseph F. Fraumeni, Nilanjan Chatterjee, Olga Y. Gorlova, Chao Agnes Hsiung, Christopher I. Amos, Hongbing Shen, Stephen J. Chanock, Nathaniel Rothman, Takashi Kohno and Qing Lan ()
Additional contact information
Jianxin Shi: National Cancer Institute
Kouya Shiraishi: National Cancer Research Institute
Jiyeon Choi: National Cancer Institute
Keitaro Matsuo: Aichi Cancer Center Research Institute
Tzu-Yu Chen: National Health Research Institutes
Juncheng Dai: Nanjing Medical University
Rayjean J. Hung: Lunenfeld-Tanenbaum Research Institute, Sinai Health
Kexin Chen: Tianjin Medical University Cancer Institute and Hospital, Tianjin Medical University
Xiao-Ou Shu: Vanderbilt University Medical Center and Vanderbilt-Ingram Cancer Center
Young Tae Kim: Seoul National University College of Medicine
Maria Teresa Landi: National Cancer Institute
Dongxin Lin: Chinese Academy of Medical Sciences and Peking Union Medical College
Wei Zheng: Vanderbilt University Medical Center and Vanderbilt-Ingram Cancer Center
Zhihua Yin: China Medical University
Baosen Zhou: The First Hospital of China Medical University
Bao Song: Shandong Academy of Medical Sciences
Jiucun Wang: Fudan University
Wei Jie Seow: National Cancer Institute
Lei Song: National Cancer Institute
I-Shou Chang: National Health Research Institutes
Wei Hu: National Cancer Institute
Li-Hsin Chien: National Health Research Institutes
Qiuyin Cai: Vanderbilt University Medical Center and Vanderbilt-Ingram Cancer Center
Yun-Chul Hong: Seoul National University College of Medicine
Hee Nam Kim: Chonnam National University Medical School
Yi-Long Wu: Guangdong Academy of Medical Sciences
Maria Pik Wong: Queen Mary Hospital
Brian Douglas Richardson: National Cancer Institute
Karen M. Funderburk: National Cancer Institute
Shilan Li: National Cancer Institute
Tongwu Zhang: National Cancer Institute
Charles Breeze: National Cancer Institute
Zhaoming Wang: St. Jude Children’s Research Hospital
Batel Blechter: National Cancer Institute
Bryan A. Bassig: National Cancer Institute
Jin Hee Kim: Seoul National University
Demetrius Albanes: National Cancer Institute
Jason Y. Y. Wong: National Cancer Institute
Min-Ho Shin: Chonnam National University Medical School
Lap Ping Chung: Queen Mary Hospital
Yang Yang: Shanghai Pulmonary Hospital
She-Juan An: Guangdong Academy of Medical Sciences
Hong Zheng: Tianjin Medical University Cancer Institute and Hospital, Tianjin Medical University
Yasushi Yatabe: National Cancer Center Hospital
Xu-Chao Zhang: Guangdong Academy of Medical Sciences
Young-Chul Kim: Chonnam National University Hwasun Hospital
Neil E. Caporaso: National Cancer Institute
Jiang Chang: Chinese Academy of Medical Sciences and Peking Union Medical College
James Chung Man Ho: The University of Hong Kong, Queen Mary Hospital
Michiaki Kubo: RIKEN Center for Integrative Medical Sciences
Yataro Daigo: The University of Tokyo
Minsun Song: Sookmyung Women’s University
Yukihide Momozawa: RIKEN Center for Integrative Medical Sciences
Yoichiro Kamatani: RIKEN Center for Integrative Medical Sciences
Masashi Kobayashi: Tokyo Medical and Dental University
Kenichi Okubo: Tokyo Medical and Dental University
Takayuki Honda: Tokyo Medical and Dental University
Dean H. Hosgood: Albert Einstein College of Medicine
Hideo Kunitoh: Japanese Red Cross Medical Center
Harsh Patel: National Cancer Institute
Shun-ichi Watanabe: National Cancer Center Hospital
Yohei Miyagi: Kanagawa Cancer Center Research Institute
Haruhiko Nakayama: Kanagawa Cancer Center
Shingo Matsumoto: National Cancer Center Hospital East
Hidehito Horinouchi: National Cancer Center Hospital
Masahiro Tsuboi: National Cancer Center Hospital East
Ryuji Hamamoto: National Cancer Center Research Institute
Koichi Goto: National Cancer Center Hospital East
Yuichiro Ohe: National Cancer Center Hospital
Atsushi Takahashi: RIKEN Center for Integrative Medical Sciences
Akiteru Goto: Graduate School of Medicine, Akita University
Yoshihiro Minamiya: Graduate School of Medicine, Akita University
Megumi Hara: Saga University
Yuichiro Nishida: Saga University
Kenji Takeuchi: Nagoya University Graduate School of Medicine
Kenji Wakai: Nagoya University Graduate School of Medicine
Koichi Matsuda: The University of Tokyo
Yoshinori Murakami: The University of Tokyo
Kimihiro Shimizu: Shinshu University School of Medicine Asahi
Hiroyuki Suzuki: Fukushima Medical University School of Medicine
Motonobu Saito: Fukushima Medical University School of Medicine
Yoichi Ohtaki: Gunma University Hospital
Kazumi Tanaka: Gunma University Hospital
Tangchun Wu: Huazhong University of Science and Technology
Fusheng Wei: China National Environmental Monitoring Center
Hongji Dai: Tianjin Medical University Cancer Institute and Hospital, Tianjin Medical University
Mitchell J. Machiela: National Cancer Institute
Jian Su: Guangdong Academy of Medical Sciences
Yeul Hong Kim: Korea University Anam Hospital
In-Jae Oh: Chonnam National University Hwasun Hospital
Victor Ho Fun Lee: The University of Hong Kong, Queen Mary Hospital
Gee-Chen Chang: Chung Shan Medical University
Ying-Huang Tsai: Chang Gung University
Kuan-Yu Chen: National Taiwan University Hospital and College of Medicine
Ming-Shyan Huang: E-Da Cancer Hospital, I-Shou University and Kaohsiung Medical University
Wu-Chou Su: National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University
Yuh-Min Chen: Taipei Veterans General Hospital, and school of Medicine, National Yang Ming Chiao Tung University
Adeline Seow: Saw Swee Hock School of Public Health, National University of Singapore
Jae Yong Park: Kyungpook National University Medical Center
Sun-Seog Kweon: Chonnam National University Medical School
Kun-Chieh Chen: Chung Shan Medical University Hospital
Yu-Tang Gao: Shanghai Cancer Institute
Biyun Qian: Tianjin Medical University Cancer Institute and Hospital, Tianjin Medical University
Chen Wu: Chinese Academy of Medical Sciences and Peking Union Medical College
Daru Lu: Fudan University
Jianjun Liu: Technology and Research
Ann G. Schwartz: Karmanos Cancer Institute
Richard Houlston: Institute of Cancer Research
Margaret R. Spitz: Institute for Clinical and Translational Research
Ivan P. Gorlov: Institute for Clinical and Translational Research
Xifeng Wu: Zhejiang University
Ping Yang: Mayo Clinic
Stephen Lam: British Columbia Cancer Agency
Adonina Tardon: University of Oviedo and CIBERESP
Chu Chen: Fred Hutchinson Cancer Center
Stig E. Bojesen: University of Copenhagen
Mattias Johansson: International Agency for Research on Cancer (IARC/WHO)
Angela Risch: German Cancer Research Center (DKFZ)
Heike Bickeböller: University Medical Center Goettingen
Bu-Tian Ji: National Cancer Institute
H-Erich Wichmann: Ludwig Maximilians University
David C. Christiani: Harvard TH Chan School of Public Health
Gadi Rennert: Carmel Medical Center
Susanne Arnold: Markey Cancer Center
Paul Brennan: International Agency for Research on Cancer (IARC/WHO)
James McKay: International Agency for Research on Cancer (IARC/WHO)
John K. Field: Liverpool University
Sanjay S. Shete: The University of Texas MD Anderson Cancer Center
Loic Marchand: University of Hawaii Cancer Center
Geoffrey Liu: Princess Margaret Cancer Center
Angeline Andrew: Norris Cotton Cancer Center
Lambertus A. Kiemeney: Radboud University Medical Center
Shan Zienolddiny-Narui: National Institute of Occupational Health
Kjell Grankvist: Umeå University
Mikael Johansson: Umeå University
Angela Cox: University of Sheffield
Fiona Taylor: University of Sheffield
Jian-Min Yuan: University of Pittsburgh
Philip Lazarus: Washington State University College of Pharmacy
Matthew B. Schabath: H. Lee Moffitt Cancer Center and Research Institute
Melinda C. Aldrich: Vanderbilt University Medical Center
Hyo-Sung Jeon: Kyungpook National University Medical Center
Shih Sheng Jiang: National Health Research Institutes
Jae Sook Sung: Korea University Anam Hospital
Chung-Hsing Chen: National Health Research Institutes
Chin-Fu Hsiao: National Health Research Institutes
Yoo Jin Jung: Seoul National University College of Medicine
Huan Guo: Huazhong University of Science and Technology
Zhibin Hu: Nanjing Medical University
Laurie Burdett: National Cancer Institute
Meredith Yeager: National Cancer Institute
Amy Hutchinson: National Cancer Institute
Belynda Hicks: National Cancer Institute
Jia Liu: National Cancer Institute
Bin Zhu: National Cancer Institute
Sonja I. Berndt: National Cancer Institute
Wei Wu: China Medical University
Junwen Wang: The University of Hong Kong
Yuqing Li: Genome Institute of Singapore
Jin Eun Choi: Kyungpook National University Medical Center
Kyong Hwa Park: Korea University Anam Hospital
Sook Whan Sung: Seoul National University Bundang Hospital
Li Liu: Huazhong University of Science and Technology
Chang Hyun Kang: Seoul National University College of Medicine
Wen-Chang Wang: Taipei Medical University
Jun Xu: The University of Hong Kong
Peng Guan: China Medical University
Wen Tan: Chinese Academy of Medical Sciences and Peking Union Medical College
Chong-Jen Yu: National Taiwan University Hospital Hsin-Chu Branch
Gong Yang: Vanderbilt University Medical Center and Vanderbilt-Ingram Cancer Center
Alan Dart Loon Sihoe: Gleneagles Hong Kong Hospital
Ying Chen: Saw Swee Hock School of Public Health, National University of Singapore
Yi Young Choi: Kyungpook National University Medical Center
Jun Suk Kim: Korea University Guro Hospital
Ho-Il Yoon: Seoul National University Bundang Hospital
In Kyu Park: Seoul National University College of Medicine
Ping Xu: Wuhan Iron and Steel (Group) Corporation Staff-Worker Hospital
Qincheng He: China Medical University
Chih-Liang Wang: Chang Gung Memorial Hospital
Hsiao-Han Hung: National Health Research Institutes
Roel C. H. Vermeulen: Utrecht University
Iona Cheng: University of California, San Francisco
Junjie Wu: Fudan University
Wei-Yen Lim: Saw Swee Hock School of Public Health, National University of Singapore
Fang-Yu Tsai: National Health Research Institutes
John K. C. Chan: Queen Elizabeth Hospital
Jihua Li: Qujing Center for Diseases Control and Prevention
Hongyan Chen: Fudan University
Hsien-Chih Lin: National Health Research Institutes
Li Jin: Fudan University
Jie Liu: Shandong Academy of Medical Sciences
Norie Sawada: National Cancer Center
Taiki Yamaji: National Cancer Center
Kathleen Wyatt: National Cancer Institute
Shengchao A. Li: National Cancer Institute
Hongxia Ma: Nanjing Medical University
Meng Zhu: Nanjing Medical University
Zhehai Wang: Shandong Academy of Medical Sciences
Sensen Cheng: Shandong Academy of Medical Sciences
Xuelian Li: China Medical University
Yangwu Ren: China Medical University
Ann Chao: National Cancer Institute
Motoki Iwasaki: National Cancer Center
Junjie Zhu: Shanghai Pulmonary Hospital
Gening Jiang: Shanghai Pulmonary Hospital
Ke Fei: Shanghai Pulmonary Hospital
Guoping Wu: China National Environmental Monitoring Center
Chih-Yi Chen: Chung Shan Medical University
Chien-Jen Chen: Academia Sinica
Pan-Chyr Yang: National Taiwan University Hospital
Jinming Yu: Shandong Academy of Medical Sciences
Victoria L. Stevens: American Cancer Society
Joseph F. Fraumeni: National Cancer Institute
Nilanjan Chatterjee: National Cancer Institute
Olga Y. Gorlova: Institute for Clinical and Translational Research
Chao Agnes Hsiung: National Health Research Institutes
Christopher I. Amos: Institute for Clinical and Translational Research
Hongbing Shen: Nanjing Medical University
Stephen J. Chanock: National Cancer Institute
Nathaniel Rothman: National Cancer Institute
Takashi Kohno: National Cancer Research Institute
Qing Lan: National Cancer Institute

Nature Communications, 2023, vol. 14, issue 1, 1-17

Abstract: Abstract Lung adenocarcinoma is the most common type of lung cancer. Known risk variants explain only a small fraction of lung adenocarcinoma heritability. Here, we conducted a two-stage genome-wide association study of lung adenocarcinoma of East Asian ancestry (21,658 cases and 150,676 controls; 54.5% never-smokers) and identified 12 novel susceptibility variants, bringing the total number to 28 at 25 independent loci. Transcriptome-wide association analyses together with colocalization studies using a Taiwanese lung expression quantitative trait loci dataset (n = 115) identified novel candidate genes, including FADS1 at 11q12 and ELF5 at 11p13. In a multi-ancestry meta-analysis of East Asian and European studies, four loci were identified at 2p11, 4q32, 16q23, and 18q12. At the same time, most of our findings in East Asian populations showed no evidence of association in European populations. In our studies drawn from East Asian populations, a polygenic risk score based on the 25 loci had a stronger association in never-smokers vs. individuals with a history of smoking (Pinteraction = 0.0058). These findings provide new insights into the etiology of lung adenocarcinoma in individuals from East Asian populations, which could be important in developing translational applications.

Date: 2023
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DOI: 10.1038/s41467-023-38196-z

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