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Comprehensive functional annotation of susceptibility variants identifies genetic heterogeneity between lung adenocarcinoma and squamous cell carcinoma |
Na Qin1, Yuancheng Li1, Cheng Wang1,2,3, Meng Zhu1,4, Juncheng Dai1,2,4,5, Tongtong Hong1, Demetrius Albanes6, Stephen Lam7, Adonina Tardon8, Chu Chen9, Gary Goodman10, Stig E. Bojesen11, Maria Teresa Landi12, Mattias Johansson13, Angela Risch14, H-Erich Wichmann15, Heike Bickeboller16, Gadi Rennert17, Susanne Arnold18, Paul Brennan13, John K. Field19, Sanjay Shete20, Loic Le Marchand21, Olle Melander22, Hans Brunnstrom22, Geoffrey Liu23, Rayjean J. Hung24, Angeline Andrew25, Lambertus A. Kiemeney26, Shan Zienolddiny27, Kjell Grankvist28, Mikael Johansson29, Neil Caporaso30, Penella Woll31, Philip Lazarus32, Matthew B. Schabath33, Melinda C. Aldrich34, Victoria L. Stevens35, Guangfu Jin1,2,4,5, David C. Christiani5,36, Zhibin Hu1,2,5, Christopher I. Amos37, Hongxia Ma1,2,4,5( ), Hongbing Shen1,2,4,5() |
1. Department of Epidemiology, Center for Global Health, School of Public Health, Nanjing Medical University, Nanjing 211166, China
2. State Key Laboratory of Reproductive Medicine, Center for Global Health, Nanjing Medical University, Nanjing 211166, China
3. Department of Bioinformatics, School of Biomedical Engineering and Informatics, Nanjing Medical University, Nanjing 211166, China
4. Jiangsu Key Lab of Cancer Biomarkers, Prevention and Treatment, Collaborative Innovation Center for Cancer Medicine, Nanjing Medical University, Nanjing 211166, China
5. China International Cooperation Center for Environment and Human Health, School of Public Health, Nanjing Medical University, Nanjing 211166, China
6. Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD 20892-9304, USA
7. Department of Integrative Oncology, British Columbia Cancer Agency, Vancouver, BC V5Z 1L3, Canada
8. Faculty of Medicine, University of Oviedo and CIBERESP, Oviedo 33006, Spain
9. Program in Epidemiology, Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA 98109-1024, USA
10. Public Health Sciences Division, Swedish Cancer Institute, Seattle, WA 98026, USA
11. Department of Clinical Biochemistry, Copenhagen University Hospital, Copenhagen DK-1017, Denmark
12. National Cancer Institute, Bethesda, MD 20892-9304, USA
13. Genetic Epidemiology Group, International Agency for Research on Cancer, Lyon 69372, France
14. Cancer Center Cluster Salzburg at PLUS, Department of Molecular Biology, University of Salzburg, Heidelberg 5020, Austria
15. Institute of Medical Informatics, Biometry and Epidemiology, Chair of Epidemiology, Ludwig Maximilians University, Munich, Bavaria 80539, Germany
16. Department of Genetic Epidemiology, University Medical Center Goettingen, Goettingen 37075, Germany
17. Technion Faculty of Medicine, Carmel Medical Center, Haifa 3448516, Israel
18. Markey Cancer Center, University of Kentucky, Lexington, KY 40506-0054, USA
19. Department of Molecular and Clinical Cancer Medicine, Roy Castle Lung Cancer Research Programme, The University of Liverpool Institute of Translational Medicine, Liverpool L69 7ZX, UK
20. Department of Epidemiology, The University of Texas, MD Anderson Cancer Center, Houston, TX 77079, USA
21. Department of Epidemiology, University of Hawaii Cancer Center, Honolulu, HI 96813, USA
22. Department of Clinical Sciences, Lund University, BMC F12, 221 84, Sweden
23. Epidemiology Division, Princess Margaret Cancer Center, Toronto, ON M4Y 2H8, Canada
24. Epidemiology Division, Lunenfeld-Tanenbuaum Research Institute, Sinai Health System, Toronto, ON M5G 1X5, Canada
25. Department of Neurology, Dartmouth-Hitchcock Medical Center, Lebanon, NH 03756, USA
26. Department of Health Evidence, Radboud University Medical Center, Nijmegen 9101 6500 HB, Germany
27. National Institute of Occupational Health (STAMI), Oslo Pb 5330, Norway
28. Department of Medical Biosciences, Umeå University, Umea 901 87, Sweden
29. Department of Radiation Sciences, Umeå University, Umea 901 87, Sweden
30. Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD 20850, USA
31. Academic Unit of Clinical Oncology, University of Sheffield, Sheffield S10 2TN, UK
32. College of Pharmacy, Washington State University, Spokane, WA 99210, USA
33. Department of Cancer Epidemiology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL 12902, USA
34. Department of Thoracic Surgery, Division of Epidemiology, Vanderbilt University Medical Center, Nashville, TN 37232, USA
35. Department of Epidemiology Research Program, American Cancer Society, Atlanta, GA 30303, USA
36. Department of Environmental Health, Harvard School of Public Health, Department of Medicine, Harvard Medical School/Massachusetts General Hospital, Boston, MA 02115, USA
37. Baylor College of Medicine, Institute for Clinical and Translational Research, Houston, TX 21202, USA |
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Abstract Although genome-wide association studies have identified more than eighty genetic variants associated with non-small cell lung cancer (NSCLC) risk, biological mechanisms of these variants remain largely unknown. By integrating a large-scale genotype data of 15 581 lung adenocarcinoma (AD) cases, 8350 squamous cell carcinoma (SqCC) cases, and 27 355 controls, as well as multiple transcriptome and epigenomic databases, we conducted histology-specific meta-analyses and functional annotations of both reported and novel susceptibility variants. We identified 3064 credible risk variants for NSCLC, which were overrepresented in enhancer-like and promoter-like histone modification peaks as well as DNase I hypersensitive sites. Transcription factor enrichment analysis revealed that USF1 was AD-specific while CREB1 was SqCC-specific. Functional annotation and gene-based analysis implicated 894 target genes, including 274 specifics for AD and 123 for SqCC, which were overrepresented in somatic driver genes (ER=1.95, P=0.005). Pathway enrichment analysis and Gene-Set Enrichment Analysis revealed that AD genes were primarily involved in immune-related pathways, while SqCC genes were homologous recombination deficiency related. Our results illustrate the molecular basis of both well-studied and new susceptibility loci of NSCLC, providing not only novel insights into the genetic heterogeneity between AD and SqCC but also a set of plausible gene targets for post-GWAS functional experiments.
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| Keywords
lung cancer
genome-wide association study
function annotation
immune
homologous recombination repair deficiency
genetic heterogeneity
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Corresponding Author(s):
Hongxia Ma,Hongbing Shen
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Just Accepted Date: 24 July 2020
Online First Date: 09 September 2020
Issue Date: 23 April 2021
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