A genome-wide association study integrated with single-cell and bulk profiles uncovers susceptibility genes for nasopharyngeal carcinoma involved in tumorigenesis via regulation of T cells
Abstract Background Nasopharyngeal carcinoma is an aggressive malignancy originating from the nasopharyngeal mucosa and associated with genetic factors. Many nasopharyngeal carcinoma susceptibility loci have been identified by genome-wide association studies (GWASs), but their underlying functional...
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| author | Tong-Min Wang Wen-Li Zhang Jin-Ru Xie Yong-Qiao He Minzhong Tang Wen-Qiong Xue Da-Wei Yang Chang-Mi Deng Hua Diao Zhi-Ming Mai Ruo-Wen Xiao Ying Liao Dan-Hua Li Yan-Xia Wu Cheng-Tao Jiang Jiang-Bo Zhang Xue-Yin Chen Yan Du Cao-Li Tang Wen-Hui Jia Ting Zhou Xi-Zhao Li Pei-Fen Zhang Xiao-Hui Zheng Shao-Dan Zhang Ye-Zhu Hu Yonglin Cai Yuming Zheng Zhe Zhang Guangfu Jin Wen Chen Hai-Qiang Mai Ying Sun Zhibin Hu Jianjun Liu Xin-Yuan Guan Fan Bai Jinxin Bei Jun Ma Musheng Zeng Maria Li Lung Hans-Olov Adami Weimin Ye Tai-Hing Lam Hongbing Shen Wei-Hua Jia |
| author_facet | Tong-Min Wang Wen-Li Zhang Jin-Ru Xie Yong-Qiao He Minzhong Tang Wen-Qiong Xue Da-Wei Yang Chang-Mi Deng Hua Diao Zhi-Ming Mai Ruo-Wen Xiao Ying Liao Dan-Hua Li Yan-Xia Wu Cheng-Tao Jiang Jiang-Bo Zhang Xue-Yin Chen Yan Du Cao-Li Tang Wen-Hui Jia Ting Zhou Xi-Zhao Li Pei-Fen Zhang Xiao-Hui Zheng Shao-Dan Zhang Ye-Zhu Hu Yonglin Cai Yuming Zheng Zhe Zhang Guangfu Jin Wen Chen Hai-Qiang Mai Ying Sun Zhibin Hu Jianjun Liu Xin-Yuan Guan Fan Bai Jinxin Bei Jun Ma Musheng Zeng Maria Li Lung Hans-Olov Adami Weimin Ye Tai-Hing Lam Hongbing Shen Wei-Hua Jia |
| author_sort | Tong-Min Wang |
| collection | DOAJ |
| description | Abstract Background Nasopharyngeal carcinoma is an aggressive malignancy originating from the nasopharyngeal mucosa and associated with genetic factors. Many nasopharyngeal carcinoma susceptibility loci have been identified by genome-wide association studies (GWASs), but their underlying functional insights are largely unexplained. Results A meta-GWAS including 5073 nasopharyngeal carcinoma patients and 5860 controls from nasopharyngeal carcinoma endemic areas identifies a total of 863 significant SNPs, including SNPs at a novel locus 3p24.1 (rs56365817; nearby genes: CMC1/EOMES). By integrating the GWAS signals with single-cell and bulk profiles, we find nasopharyngeal carcinoma susceptibility robustly associated with T cells in different methods and datasets. In nasopharyngeal carcinoma-associated cell type, we identify 234 putative susceptibility genes (81.62% of them novel), mainly enriched in immune-related biological processes. Five putative causal genes are prioritized. We perform in-depth bioinformatic analysis and functional experiments for EOMES, finding that the nasopharyngeal carcinoma-risk alleles of four functional SNPs upregulate EOMES expression by promoting the activity of regulatory elements in T cells, and EOMES participates in nasopharyngeal carcinoma tumorigenesis via regulation of CD8+ T cell exhaustion in the tumor microenvironment. Conclusions This study uncovers novel nasopharyngeal carcinoma susceptibility genes and their functional cell types, which improves the understanding of nasopharyngeal carcinoma genetic etiology. |
| format | Article |
| id | doaj-art-88bb1d76c00c4a5e91dc441ee747f699 |
| institution | Kabale University |
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| language | English |
| publishDate | 2025-07-01 |
| publisher | BMC |
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| series | Genome Biology |
| spelling | doaj-art-88bb1d76c00c4a5e91dc441ee747f6992025-08-20T04:03:02ZengBMCGenome Biology1474-760X2025-07-0126112810.1186/s13059-025-03657-9A genome-wide association study integrated with single-cell and bulk profiles uncovers susceptibility genes for nasopharyngeal carcinoma involved in tumorigenesis via regulation of T cellsTong-Min Wang0Wen-Li Zhang1Jin-Ru Xie2Yong-Qiao He3Minzhong Tang4Wen-Qiong Xue5Da-Wei Yang6Chang-Mi Deng7Hua Diao8Zhi-Ming Mai9Ruo-Wen Xiao10Ying Liao11Dan-Hua Li12Yan-Xia Wu13Cheng-Tao Jiang14Jiang-Bo Zhang15Xue-Yin Chen16Yan Du17Cao-Li Tang18Wen-Hui Jia19Ting Zhou20Xi-Zhao Li21Pei-Fen Zhang22Xiao-Hui Zheng23Shao-Dan Zhang24Ye-Zhu Hu25Yonglin Cai26Yuming Zheng27Zhe Zhang28Guangfu Jin29Wen Chen30Hai-Qiang Mai31Ying Sun32Zhibin Hu33Jianjun Liu34Xin-Yuan Guan35Fan Bai36Jinxin Bei37Jun Ma38Musheng Zeng39Maria Li Lung40Hans-Olov Adami41Weimin Ye42Tai-Hing Lam43Hongbing Shen44Wei-Hua Jia45State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterWuzhou Red Cross HospitalState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterSchool of Public Health, Sun Yat-Sen UniversityState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterSchool of Public Health, Sun Yat-Sen UniversitySchool of Public Health, The University of Hong KongState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterSchool of Public Health, Sun Yat-Sen UniversitySchool of Public Health, Sun Yat-Sen UniversityState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterWuzhou Red Cross HospitalWuzhou Red Cross HospitalDepartment of Otolaryngology-Head and Neck Surgery, First Affiliated Hospital of Guangxi Medical UniversityDepartment of Epidemiology, International Joint Research Center On Environment and Human Health, Center for Global Health, Jiangsu Key Lab of Cancer Biomarkers, Prevention and Treatment, Collaborative Innovation Center for Cancer Medicine, Nanjing Medical UniversitySchool of Public Health, Sun Yat-Sen UniversityDepartment of Nasopharyngeal Carcinoma, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterDepartment of Radiation Oncology, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterDepartment of Epidemiology, International Joint Research Center On Environment and Human Health, Center for Global Health, Jiangsu Key Lab of Cancer Biomarkers, Prevention and Treatment, Collaborative Innovation Center for Cancer Medicine, Nanjing Medical UniversityHuman Genetics, Agency for Science, Technology and Research (A*STAR), Genome Institute of SingaporeState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterBiomedical Pioneering Innovation Center (BIOPIC), Beijing Advanced Innovation Center for Genomics (ICG), School of Life Sciences, Peking UniversityState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterDepartment of Radiation Oncology, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterDepartment of Clinical Oncology, School of Clinical Medicine, University of Hong Kong Clinical Effectiveness Group, Institute of Health and Society, University of OsloDepartment of Medical Epidemiology and Biostatistics, Karolinska InstitutetSchool of Public Health, The University of Hong KongDepartment of Epidemiology, International Joint Research Center On Environment and Human Health, Center for Global Health, Jiangsu Key Lab of Cancer Biomarkers, Prevention and Treatment, Collaborative Innovation Center for Cancer Medicine, Nanjing Medical UniversityState Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-Sen University Cancer CenterAbstract Background Nasopharyngeal carcinoma is an aggressive malignancy originating from the nasopharyngeal mucosa and associated with genetic factors. Many nasopharyngeal carcinoma susceptibility loci have been identified by genome-wide association studies (GWASs), but their underlying functional insights are largely unexplained. Results A meta-GWAS including 5073 nasopharyngeal carcinoma patients and 5860 controls from nasopharyngeal carcinoma endemic areas identifies a total of 863 significant SNPs, including SNPs at a novel locus 3p24.1 (rs56365817; nearby genes: CMC1/EOMES). By integrating the GWAS signals with single-cell and bulk profiles, we find nasopharyngeal carcinoma susceptibility robustly associated with T cells in different methods and datasets. In nasopharyngeal carcinoma-associated cell type, we identify 234 putative susceptibility genes (81.62% of them novel), mainly enriched in immune-related biological processes. Five putative causal genes are prioritized. We perform in-depth bioinformatic analysis and functional experiments for EOMES, finding that the nasopharyngeal carcinoma-risk alleles of four functional SNPs upregulate EOMES expression by promoting the activity of regulatory elements in T cells, and EOMES participates in nasopharyngeal carcinoma tumorigenesis via regulation of CD8+ T cell exhaustion in the tumor microenvironment. Conclusions This study uncovers novel nasopharyngeal carcinoma susceptibility genes and their functional cell types, which improves the understanding of nasopharyngeal carcinoma genetic etiology.https://doi.org/10.1186/s13059-025-03657-9 |
| spellingShingle | Tong-Min Wang Wen-Li Zhang Jin-Ru Xie Yong-Qiao He Minzhong Tang Wen-Qiong Xue Da-Wei Yang Chang-Mi Deng Hua Diao Zhi-Ming Mai Ruo-Wen Xiao Ying Liao Dan-Hua Li Yan-Xia Wu Cheng-Tao Jiang Jiang-Bo Zhang Xue-Yin Chen Yan Du Cao-Li Tang Wen-Hui Jia Ting Zhou Xi-Zhao Li Pei-Fen Zhang Xiao-Hui Zheng Shao-Dan Zhang Ye-Zhu Hu Yonglin Cai Yuming Zheng Zhe Zhang Guangfu Jin Wen Chen Hai-Qiang Mai Ying Sun Zhibin Hu Jianjun Liu Xin-Yuan Guan Fan Bai Jinxin Bei Jun Ma Musheng Zeng Maria Li Lung Hans-Olov Adami Weimin Ye Tai-Hing Lam Hongbing Shen Wei-Hua Jia A genome-wide association study integrated with single-cell and bulk profiles uncovers susceptibility genes for nasopharyngeal carcinoma involved in tumorigenesis via regulation of T cells Genome Biology |
| title | A genome-wide association study integrated with single-cell and bulk profiles uncovers susceptibility genes for nasopharyngeal carcinoma involved in tumorigenesis via regulation of T cells |
| title_full | A genome-wide association study integrated with single-cell and bulk profiles uncovers susceptibility genes for nasopharyngeal carcinoma involved in tumorigenesis via regulation of T cells |
| title_fullStr | A genome-wide association study integrated with single-cell and bulk profiles uncovers susceptibility genes for nasopharyngeal carcinoma involved in tumorigenesis via regulation of T cells |
| title_full_unstemmed | A genome-wide association study integrated with single-cell and bulk profiles uncovers susceptibility genes for nasopharyngeal carcinoma involved in tumorigenesis via regulation of T cells |
| title_short | A genome-wide association study integrated with single-cell and bulk profiles uncovers susceptibility genes for nasopharyngeal carcinoma involved in tumorigenesis via regulation of T cells |
| title_sort | genome wide association study integrated with single cell and bulk profiles uncovers susceptibility genes for nasopharyngeal carcinoma involved in tumorigenesis via regulation of t cells |
| url | https://doi.org/10.1186/s13059-025-03657-9 |
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