Cross-ancestry genome-wide meta-analysis of 61,047 cases and 947,237 controls identifies new susceptibility loci contributing to lung cancer

To identify new susceptibility loci to lung cancer among diverse populations, we performed cross-ancestry genome-wide association studies in European, East Asian and African populations and discovered five loci that have not been previously reported. We replicated 26 signals and identified 10 new le...

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Veröffentlicht in:	Nature genetics Jg. 54; H. 8; S. 1167 - 1177
Hauptverfasser:	Byun, Jinyoung, Han, Younghun, Li, Yafang, Xia, Jun, Long, Erping, Choi, Jiyeon, Xiao, Xiangjun, Zhu, Meng, Zhou, Wen, Sun, Ryan, Bossé, Yohan, Song, Zhuoyi, Schwartz, Ann, Lusk, Christine, Rafnar, Thorunn, Stefansson, Kari, Zhang, Tongwu, Zhao, Wei, Pettit, Rowland W., Liu, Yanhong, Li, Xihao, Zhou, Hufeng, Walsh, Kyle M., Gorlov, Ivan, Gorlova, Olga, Zhu, Dakai, Rosenberg, Susan M., Pinney, Susan, Bailey-Wilson, Joan E., Mandal, Diptasri, de Andrade, Mariza, Gaba, Colette, Willey, James C., You, Ming, Anderson, Marshall, Wiencke, John K., Albanes, Demetrius, Lam, Stephan, Tardon, Adonina, Chen, Chu, Goodman, Gary, Bojeson, Stig, Brenner, Hermann, Landi, Maria Teresa, Chanock, Stephen J., Johansson, Mattias, Muley, Thomas, Risch, Angela, Wichmann, H.-Erich, Bickeböller, Heike, Christiani, David C., Rennert, Gad, Arnold, Susanne, Field, John K., Shete, Sanjay, Le Marchand, Loic, Melander, Olle, Brunnstrom, Hans, Liu, Geoffrey, Andrew, Angeline S., Kiemeney, Lambertus A., Shen, Hongbing, Zienolddiny, Shanbeh, Grankvist, Kjell, Johansson, Mikael, Caporaso, Neil, Cox, Angela, Hong, Yun-Chul, Yuan, Jian-Min, Lazarus, Philip, Schabath, Matthew B., Aldrich, Melinda C., Patel, Alpa, Lan, Qing, Rothman, Nathaniel, Taylor, Fiona, Kachuri, Linda, Witte, John S., Sakoda, Lori C., Spitz, Margaret, Brennan, Paul, Lin, Xihong, McKay, James, Hung, Rayjean J., Amos, Christopher I.
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	New York Nature Publishing Group US 01.08.2022 Nature Publishing Group
Schlagworte:	38/39 38/62 45/43 631/208/205/2138 631/67/1612 Agriculture Animal Genetics and Genomics Basic Medicine Biomedical and Life Sciences Biomedicine Cancer Research Damage Datasets Deoxyribonucleic acid DNA DNA damage DNA-Binding Proteins - genetics Fibroblasts Gene Function Gene mapping Genes Genetic Predisposition to Disease Genome-wide association studies Genome-Wide Association Study Genomes Human Genetics Humans Interferon regulatory factor 4 Lung cancer Lung Neoplasms - genetics Medical and Health Sciences Medical Genetics and Genomics (including Gene Therapy) Medicin och hälsovetenskap Medicinsk genetik och genomik (Här ingår: Genterapi) Medicinska och farmaceutiska grundvetenskaper Meta-analysis Pleiotropy Polymorphism, Single Nucleotide - genetics Population Populations Quality control Quantitative trait loci Quantitative Trait Loci - genetics RNA-Binding Proteins - genetics Validation studies
ISSN:	1061-4036, 1546-1718, 1546-1718
Online-Zugang:	Volltext
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Abstract	To identify new susceptibility loci to lung cancer among diverse populations, we performed cross-ancestry genome-wide association studies in European, East Asian and African populations and discovered five loci that have not been previously reported. We replicated 26 signals and identified 10 new lead associations from previously reported loci. Rare-variant associations tended to be specific to populations, but even common-variant associations influencing smoking behavior, such as those with CHRNA5 and CYP2A6 , showed population specificity. Fine-mapping and expression quantitative trait locus colocalization nominated several candidate variants and susceptibility genes such as IRF4 and FUBP1 . DNA damage assays of prioritized genes in lung fibroblasts indicated that a subset of these genes, including the pleiotropic gene IRF4 , potentially exert effects by promoting endogenous DNA damage. A cross-ancestry genome-wide association meta-analysis of lung cancer including 61,047 cases and 947,237 controls identifies five new cross-ancestry susceptibility loci and highlights ancestry-specific effects of common and rare variants on lung cancer risk.
AbstractList	To identify new susceptibility loci to lung cancer among diverse populations, we performed cross-ancestry genome-wide association studies in European, East Asian and African populations and discovered five loci that have not been previously reported. We replicated 26 signals and identified 10 new lead associations from previously reported loci. Rare-variant associations tended to be specific to populations, but even common-variant associations influencing smoking behavior, such as those with CHRNA5 and CYP2A6, showed population specificity. Fine-mapping and expression quantitative trait locus colocalization nominated several candidate variants and susceptibility genes such as IRF4 and FUBP1. DNA damage assays of prioritized genes in lung fibroblasts indicated that a subset of these genes, including the pleiotropic gene IRF4, potentially exert effects by promoting endogenous DNA damage. To identify new susceptibility loci to lung cancer among diverse populations, we performed cross-ancestry genome-wide association studies in European, East Asian and African populations and discovered five loci that have not been previously reported. We replicated 26 signals and identified 10 new lead associations from previously reported loci. Rare-variant associations tended to be specific to populations, but even common-variant associations influencing smoking behavior, such as those with CHRNA5 and CYP2A6 , showed population specificity. Fine-mapping and expression quantitative trait locus colocalization nominated several candidate variants and susceptibility genes such as IRF4 and FUBP1 . DNA damage assays of prioritized genes in lung fibroblasts indicated that a subset of these genes, including the pleiotropic gene IRF4 , potentially exert effects by promoting endogenous DNA damage. A cross-ancestry genome-wide association meta-analysis of lung cancer including 61,047 cases and 947,237 controls identifies five new cross-ancestry susceptibility loci and highlights ancestry-specific effects of common and rare variants on lung cancer risk. To identify new susceptibility loci to lung cancer among diverse populations, we performed cross-ancestry genome-wide association studies in European, East Asian, and African populations and discovered five loci that have not been previously reported. We replicated 26 signals and identified 10 new lead associations from previously reported loci. Rare-variant associations tended to be specific to populations, but even common-variant associations influencing smoking behavior, such as those with CHRNA5 and CYP2A6, showed population specificity. Fine-mapping and eQTL colocalization nominated several candidate variants and susceptibility genes such as IRF4 and FUBP1. DNA damage assays of prioritized genes in lung fibroblasts indicated that a subset of these genes, including the pleiotropic gene IRF4, potentially exert effects by promoting endogenous DNA damage. To identify new susceptibility loci to lung cancer among diverse populations, we performed cross-ancestry genome-wide association studies in European, East Asian and African populations and discovered five loci that have not been previously reported. We replicated 26 signals and identified 10 new lead associations from previously reported loci. Rare-variant associations tended to be specific to populations, but even common-variant associations influencing smoking behavior, such as those with CHRNA5 and CYP2A6, showed population specificity. Fine-mapping and expression quantitative trait locus colocalization nominated several candidate variants and susceptibility genes such as IRF4 and FUBP1. DNA damage assays of prioritized genes in lung fibroblasts indicated that a subset of these genes, including the pleiotropic gene IRF4, potentially exert effects by promoting endogenous DNA damage. © 2022, The Author(s), under exclusive licence to Springer Nature America, Inc. To identify new susceptibility loci to lung cancer among diverse populations, we performed cross-ancestry genome-wide association studies in European, East Asian and African populations and discovered five loci that have not been previously reported. We replicated 26 signals and identified 10 new lead associations from previously reported loci. Rare-variant associations tended to be specific to populations, but even common-variant associations influencing smoking behavior, such as those with CHRNA5 and CYP2A6, showed population specificity. Fine-mapping and expression quantitative trait locus colocalization nominated several candidate variants and susceptibility genes such as IRF4 and FUBP1. DNA damage assays of prioritized genes in lung fibroblasts indicated that a subset of these genes, including the pleiotropic gene IRF4, potentially exert effects by promoting endogenous DNA damage.To identify new susceptibility loci to lung cancer among diverse populations, we performed cross-ancestry genome-wide association studies in European, East Asian and African populations and discovered five loci that have not been previously reported. We replicated 26 signals and identified 10 new lead associations from previously reported loci. Rare-variant associations tended to be specific to populations, but even common-variant associations influencing smoking behavior, such as those with CHRNA5 and CYP2A6, showed population specificity. Fine-mapping and expression quantitative trait locus colocalization nominated several candidate variants and susceptibility genes such as IRF4 and FUBP1. DNA damage assays of prioritized genes in lung fibroblasts indicated that a subset of these genes, including the pleiotropic gene IRF4, potentially exert effects by promoting endogenous DNA damage.
Author	Gorlova, Olga de Andrade, Mariza Taylor, Fiona Chen, Chu Liu, Yanhong You, Ming Johansson, Mikael Witte, John S. Brunnstrom, Hans Zienolddiny, Shanbeh Gaba, Colette Pettit, Rowland W. Lan, Qing Chanock, Stephen J. Andrew, Angeline S. Rafnar, Thorunn Shete, Sanjay Schabath, Matthew B. Albanes, Demetrius Byun, Jinyoung Rothman, Nathaniel Risch, Angela Melander, Olle Anderson, Marshall Yuan, Jian-Min Stefansson, Kari Xia, Jun Gorlov, Ivan Hong, Yun-Chul Li, Yafang Zhang, Tongwu Han, Younghun Zhu, Meng Lusk, Christine Liu, Geoffrey Tardon, Adonina Bojeson, Stig Field, John K. Grankvist, Kjell Willey, James C. Goodman, Gary Bossé, Yohan Kiemeney, Lambertus A. Kachuri, Linda Christiani, David C. Choi, Jiyeon Wiencke, John K. Rosenberg, Susan M. Lam, Stephan Shen, Hongbing Xiao, Xiangjun Muley, Thomas Li, Xihao Lazarus, Philip Caporaso, Neil Bailey-Wilson, Joan E. Zhao, Wei Rennert, Gad Spitz, Margaret Hung, Rayjean J. Zhou, Wen Arnold, Susanne Patel, Alpa Johansson, Mattias Cox, Angela Amos, Christopher I. Le Marchand, Loic Brenner, Hermann Landi, Maria Tere
AuthorAffiliation	26. Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark 22. Public Health Department, University of Oviedo, ISPA and CIBERESP, Asturias, Spain 37. Department of Epidemiology, Harvard T.H.Chan School of Public Health, Boston, MA 46. Radboud University Medical Center, Nijmegen, The Netherlands 21. Department of Integrative Oncology, BC Cancer, Vancouver, British Columbia, Canada 33. Department of Biosciences and Medical Biology, Allergy-Cancer-BioNano Research Centre, University of Salzburg, Austria 43. Faculty of Medicine, Lund University, Lund, Sweden 40. Roy Castle Lung Cancer Research Programme, Department of Molecular and Clinical Cancer Medicine, University of Liverpool, Liverpool, United Kingdom 59. Department of Epidemiology and Population Health, Stanford University, Stanford, CA 2. Section of Epidemiology and Population Sciences, Department of Medicine, Baylor College of Medicine, Houston, TX 36. Department of Genetic Epidemiology, University Medical Cen
AuthorAffiliation_xml	– name: 17. Mayo Clinic, College of Medicine, Rochester, MN – name: 41. Department of Epidemiology, The University of Texas MD Anderson Cancer Center, Houston, TX – name: 9. Department of Oncology, Wayne State University School of Medicine, Detroit, MI – name: 38. Clalit National Cancer Control Center at Carmel Medical Center and Technion Faculty of Medicine, Haifa, Israel – name: 15. National Human Genome Research Institute, NIH, Baltimore, MD – name: 44. University Health Network- The Princess Margaret Cancer Centre, Toronto, CA – name: 25. Department of Clinical Biochemistry, Herlev Gentofte Hospital, Copenhagen University Hospital, Denmark – name: 21. Department of Integrative Oncology, BC Cancer, Vancouver, British Columbia, Canada – name: 39. University of Kentucky, Markey Cancer Center, Lexington, Kentucky – name: 4. Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX – name: 50. Department of Radiation Sciences, Oncology, Umeå University, Umeå, Sweden – name: 20. Department of Neurological Surgery, The University of California, San Francisco, San Francisco, CA – name: 6. Department of Epidemiology, Center for Global Health, School of Public Health, Nanjing Medical University, Nanjing, P.R. China – name: 5. Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, MD – name: 43. Faculty of Medicine, Lund University, Lund, Sweden – name: 51. Department of Oncology and Metabolism, University of Sheffield, Sheffield, UK – name: 59. Department of Epidemiology and Population Health, Stanford University, Stanford, CA – name: 54. Department of Pharmaceutical Sciences, College of Pharmacy, Washington State University, Spokane, Washington – name: 60. Division of Research, Kaiser Permanente Northern California, Oakland, CA – name: 40. Roy Castle Lung Cancer Research Programme, Department of Molecular and Clinical Cancer Medicine, University of Liverpool, Liverpool, United Kingdom – name: 53. UPMC Hillman Cancer Center and Department of Epidemiology, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, PA – name: 52. Department of Preventive Medicine, Seoul National University College of Medicine, Seoul, Republic of Korea – name: 62. Division of Epidemiology, Dalla Lana School of Public Health, University of Toronto, Canada – name: 1. Institute for Clinical and Translational Research, Baylor College of Medicine, Houston, TX – name: 27. Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany – name: 37. Department of Epidemiology, Harvard T.H.Chan School of Public Health, Boston, MA – name: 46. Radboud University Medical Center, Nijmegen, The Netherlands – name: 19. Center for Cancer Prevention, Houston Methodist Research Institute, Houston, TX – name: 12. Department of Biostatistics, Harvard TH Chan School of Public Health, Boston, MA – name: 45. Departments of Epidemiology and Community and Family Medicine, Dartmouth College, Hanover, NH – name: 26. Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark – name: 42. Epidemiology Program, University of Hawaii Cancer Center, Honolulu, HI – name: 36. Department of Genetic Epidemiology, University Medical Center, Georg-August-University Göttingen, Germany – name: 31. Division of Cancer Epigenomics, DKFZ – German Cancer Research Center, Heidelberg, Germany – name: 28. Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany – name: 35. Institute of Epidemiology, Helmholtz Center, München, Germany – name: 8. Institut universitaire de cardiologie et de pneumologie de Québec – Université Laval, Department of Molecular Medicine, Laval University, Quebec City, Canada – name: 18. The University of Toledo College of Medicine and Life Sciences, University of Toledo, Toledo, OH – name: 49. Department of Medical Biosciences, Umeå University, Umeå, Sweden – name: 3. Dan L Duncan Comprehensive Cancer Center, Baylor College of Medicine, Houston, TX – name: 24. Swedish Cancer Institute, Seattle, WA – name: 47. Department of Epidemiology and Biostatistics, Jiangsu Key Lab of Cancer Biomarkers, Prevention and Treatment, Collaborative Innovation Center for Cancer Personalized Medicine, School of Public Health, Nanjing Medical University, Nanjing, P.R. China – name: 32. Translational Lung Research Center Heidelberg (TLRC-H), German Center for Lung Research (DZL), Heidelberg, Germany – name: 11. deCODE genetics/Amgen Sturlugata 8, 101, Reykjavik, Iceland – name: 55. Department of Cancer Epidemiology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL – name: 29. German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany – name: 33. Department of Biosciences and Medical Biology, Allergy-Cancer-BioNano Research Centre, University of Salzburg, Austria – name: 57. American Cancer Society, Inc., Atlanta, Georgia – name: 13. Duke Cancer Institute, Duke University Medical Center, Durham, NC – name: 58. Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, CA – name: 56. Department of Medicine, Division of Genetic Medicine, Vanderbilt University Medical Center, Nashville, TN – name: 34. Cancer Cluster Salzburg, Salzburg, Austria – name: 14. University of Cincinnati College of Medicine, Cincinnati, OH – name: 7. Department of Biostatistics, University of Texas, M.D. Anderson Cancer Center, Houston, TX – name: 23. Program in Epidemiology, Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA – name: 10. Karmanos Cancer Institute, Detroit, MI – name: 22. Public Health Department, University of Oviedo, ISPA and CIBERESP, Asturias, Spain – name: 30. Section of Genetics, International Agency for Research on Cancer, World Health Organization, Lyon, France – name: 61. Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, Canada – name: 48. National Institute of Occupational Health, Oslo, Norway – name: 2. Section of Epidemiology and Population Sciences, Department of Medicine, Baylor College of Medicine, Houston, TX – name: 16. Louisiana State University Health Sciences Center, New Orleans, LA
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Lee Moffitt Cancer Center and Research Institute – sequence: 72 givenname: Melinda C. orcidid: 0000-0003-3833-8448 surname: Aldrich fullname: Aldrich, Melinda C. organization: Department of Medicine, Division of Genetic Medicine, Vanderbilt University Medical Center – sequence: 73 givenname: Alpa surname: Patel fullname: Patel, Alpa organization: American Cancer Society – sequence: 74 givenname: Qing surname: Lan fullname: Lan, Qing organization: Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health – sequence: 75 givenname: Nathaniel surname: Rothman fullname: Rothman, Nathaniel organization: Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health – sequence: 76 givenname: Fiona surname: Taylor fullname: Taylor, Fiona organization: Department of Oncology and Metabolism, University of Sheffield – sequence: 77 givenname: Linda surname: Kachuri fullname: Kachuri, Linda organization: Department of Epidemiology and Biostatistics, University of California, San Francisco – sequence: 78 givenname: John S. surname: Witte fullname: Witte, John S. organization: Department of Epidemiology and Population Health, Stanford University – sequence: 79 givenname: Lori C. orcidid: 0000-0002-0900-5735 surname: Sakoda fullname: Sakoda, Lori C. organization: Division of Research, Kaiser Permanente Northern California – sequence: 80 givenname: Margaret surname: Spitz fullname: Spitz, Margaret organization: Section of Epidemiology and Population Sciences, Department of Medicine, Baylor College of Medicine – sequence: 81 givenname: Paul orcidid: 0000-0002-0518-8714 surname: Brennan fullname: Brennan, Paul organization: Section of Genetics, International Agency for Research on Cancer, World Health Organization – sequence: 82 givenname: Xihong orcidid: 0000-0001-7067-7752 surname: Lin fullname: Lin, Xihong organization: Department of Biostatistics, Harvard TH Chan School of Public Health – sequence: 83 givenname: James orcidid: 0000-0002-1787-3874 surname: McKay fullname: McKay, James organization: Section of Genetics, International Agency for Research on Cancer, World Health Organization – sequence: 84 givenname: Rayjean J. surname: Hung fullname: Hung, Rayjean J. organization: Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Division of Epidemiology, Dalla Lana School of Public Health, University of Toronto – sequence: 85 givenname: Christopher I. orcidid: 0000-0002-8540-7023 surname: Amos fullname: Amos, Christopher I. email: Chris.Amos@bcm.edu organization: Institute for Clinical and Translational Research, Baylor College of Medicine, Section of Epidemiology and Population Sciences, Department of Medicine, Baylor College of Medicine, Dan L Duncan Comprehensive Cancer Center, Baylor College of Medicine
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Copyright	The Author(s), under exclusive licence to Springer Nature America, Inc. 2022 2022. The Author(s), under exclusive licence to Springer Nature America, Inc. Copyright Nature Publishing Group Aug 2022
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Notes	ObjectType-Article-2 SourceType-Scholarly Journals-1 content type line 14 ObjectType-Feature-3 ObjectType-Evidence Based Healthcare-1 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 These authors have equal contributions. Author Contributions: J.B., Y.H., Y.L., and C.I.A. conceived and designed the study. Y.H. and X.X. acquired the data. Y.H., E.L., J.C., and X.X. performed the analysis. J.X. performed experimental validation. M.Z., W.Z., R.S., A.S., C.L., T.R., L.K., L.S. provided substantial support on validation study. J.B., Y.H., Y.L., J.X., E.L., J.C., and C.I.A. interpreted the results. J.B., J.X., E.L., and J.C. wrote the first draft of the manuscript. J.B., Y.H., J.X., E.L., J.C., and X.X. provided supplementary materials. J.B. and C.I.A. provided supervision and contributed to analyses. All authors reviewed and commented on the manuscript and approved the final version of the manuscript.
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PublicationDate	2022-08-01
PublicationDateYYYYMMDD	2022-08-01
PublicationDate_xml	– month: 08 year: 2022 text: 2022-08-01 day: 01
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PublicationTitle	Nature genetics
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PublicationYear	2022
Publisher	Nature Publishing Group US Nature Publishing Group
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Snippet	To identify new susceptibility loci to lung cancer among diverse populations, we performed cross-ancestry genome-wide association studies in European, East...
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SubjectTerms	38/39 38/62 45/43 631/208/205/2138 631/67/1612 Agriculture Animal Genetics and Genomics Basic Medicine Biomedical and Life Sciences Biomedicine Cancer Research Damage Datasets Deoxyribonucleic acid DNA DNA damage DNA-Binding Proteins - genetics Fibroblasts Gene Function Gene mapping Genes Genetic Predisposition to Disease Genome-wide association studies Genome-Wide Association Study Genomes Human Genetics Humans Interferon regulatory factor 4 Lung cancer Lung Neoplasms - genetics Medical and Health Sciences Medical Genetics and Genomics (including Gene Therapy) Medicin och hälsovetenskap Medicinsk genetik och genomik (Här ingår: Genterapi) Medicinska och farmaceutiska grundvetenskaper Meta-analysis Pleiotropy Polymorphism, Single Nucleotide - genetics Population Populations Quality control Quantitative trait loci Quantitative Trait Loci - genetics RNA-Binding Proteins - genetics Validation studies
Title	Cross-ancestry genome-wide meta-analysis of 61,047 cases and 947,237 controls identifies new susceptibility loci contributing to lung cancer
URI	https://link.springer.com/article/10.1038/s41588-022-01115-x https://www.ncbi.nlm.nih.gov/pubmed/35915169 https://www.proquest.com/docview/2700012209 https://www.proquest.com/docview/2697366986 https://pubmed.ncbi.nlm.nih.gov/PMC9373844 https://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-198568
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