Integrative multiomics enhancer activity profiling identifies therapeutic vulnerabilities in cholangiocarcinoma of different etiologies
ObjectivesCholangiocarcinoma (CCA) is a heterogeneous malignancy with high mortality and dismal prognosis, and an urgent clinical need for new therapies. Knowledge of the CCA epigenome is largely limited to aberrant DNA methylation. Dysregulation of enhancer activities has been identified to affect...
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| Published in | Gut Vol. 73; no. 6; pp. 966 - 984 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
BMJ Publishing Group Ltd and British Society of Gastroenterology
01.06.2024
BMJ Publishing Group LTD |
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| Abstract | ObjectivesCholangiocarcinoma (CCA) is a heterogeneous malignancy with high mortality and dismal prognosis, and an urgent clinical need for new therapies. Knowledge of the CCA epigenome is largely limited to aberrant DNA methylation. Dysregulation of enhancer activities has been identified to affect carcinogenesis and leveraged for new therapies but is uninvestigated in CCA. Our aim is to identify potential therapeutic targets in different subtypes of CCA through enhancer profiling.DesignIntegrative multiomics enhancer activity profiling of diverse CCA was performed. A panel of diverse CCA cell lines, patient-derived and cell line-derived xenografts were used to study identified enriched pathways and vulnerabilities. NanoString, multiplex immunohistochemistry staining and single-cell spatial transcriptomics were used to explore the immunogenicity of diverse CCA.ResultsWe identified three distinct groups, associated with different etiologies and unique pathways. Drug inhibitors of identified pathways reduced tumour growth in in vitro and in vivo models. The first group (ESTRO), with mostly fluke-positive CCAs, displayed activation in estrogen signalling and were sensitive to MTOR inhibitors. Another group (OXPHO), with mostly BAP1 and IDH-mutant CCAs, displayed activated oxidative phosphorylation pathways, and were sensitive to oxidative phosphorylation inhibitors. Immune-related pathways were activated in the final group (IMMUN), made up of an immunogenic CCA subtype and CCA with aristolochic acid (AA) mutational signatures. Intratumour differences in AA mutation load were correlated to intratumour variation of different immune cell populations.ConclusionOur study elucidates the mechanisms underlying enhancer dysregulation and deepens understanding of different tumourigenesis processes in distinct CCA subtypes, with potential significant therapeutics and clinical benefits. |
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| AbstractList | ObjectivesCholangiocarcinoma (CCA) is a heterogeneous malignancy with high mortality and dismal prognosis, and an urgent clinical need for new therapies. Knowledge of the CCA epigenome is largely limited to aberrant DNA methylation. Dysregulation of enhancer activities has been identified to affect carcinogenesis and leveraged for new therapies but is uninvestigated in CCA. Our aim is to identify potential therapeutic targets in different subtypes of CCA through enhancer profiling.DesignIntegrative multiomics enhancer activity profiling of diverse CCA was performed. A panel of diverse CCA cell lines, patient-derived and cell line-derived xenografts were used to study identified enriched pathways and vulnerabilities. NanoString, multiplex immunohistochemistry staining and single-cell spatial transcriptomics were used to explore the immunogenicity of diverse CCA.ResultsWe identified three distinct groups, associated with different etiologies and unique pathways. Drug inhibitors of identified pathways reduced tumour growth in in vitro and in vivo models. The first group (ESTRO), with mostly fluke-positive CCAs, displayed activation in estrogen signalling and were sensitive to MTOR inhibitors. Another group (OXPHO), with mostly BAP1 and IDH-mutant CCAs, displayed activated oxidative phosphorylation pathways, and were sensitive to oxidative phosphorylation inhibitors. Immune-related pathways were activated in the final group (IMMUN), made up of an immunogenic CCA subtype and CCA with aristolochic acid (AA) mutational signatures. Intratumour differences in AA mutation load were correlated to intratumour variation of different immune cell populations.ConclusionOur study elucidates the mechanisms underlying enhancer dysregulation and deepens understanding of different tumourigenesis processes in distinct CCA subtypes, with potential significant therapeutics and clinical benefits. Cholangiocarcinoma (CCA) is a heterogeneous malignancy with high mortality and dismal prognosis, and an urgent clinical need for new therapies. Knowledge of the CCA epigenome is largely limited to aberrant DNA methylation. Dysregulation of enhancer activities has been identified to affect carcinogenesis and leveraged for new therapies but is uninvestigated in CCA. Our aim is to identify potential therapeutic targets in different subtypes of CCA through enhancer profiling. Integrative multiomics enhancer activity profiling of diverse CCA was performed. A panel of diverse CCA cell lines, patient-derived and cell line-derived xenografts were used to study identified enriched pathways and vulnerabilities. NanoString, multiplex immunohistochemistry staining and single-cell spatial transcriptomics were used to explore the immunogenicity of diverse CCA. We identified three distinct groups, associated with different etiologies and unique pathways. Drug inhibitors of identified pathways reduced tumour growth in and models. The first group (ESTRO), with mostly fluke-positive CCAs, displayed activation in estrogen signalling and were sensitive to MTOR inhibitors. Another group (OXPHO), with mostly and -mutant CCAs, displayed activated oxidative phosphorylation pathways, and were sensitive to oxidative phosphorylation inhibitors. Immune-related pathways were activated in the final group (IMMUN), made up of an immunogenic CCA subtype and CCA with aristolochic acid (AA) mutational signatures. Intratumour differences in AA mutation load were correlated to intratumour variation of different immune cell populations. Our study elucidates the mechanisms underlying enhancer dysregulation and deepens understanding of different tumourigenesis processes in distinct CCA subtypes, with potential significant therapeutics and clinical benefits. Cholangiocarcinoma (CCA) is a heterogeneous malignancy with high mortality and dismal prognosis, and an urgent clinical need for new therapies. Knowledge of the CCA epigenome is largely limited to aberrant DNA methylation. Dysregulation of enhancer activities has been identified to affect carcinogenesis and leveraged for new therapies but is uninvestigated in CCA. Our aim is to identify potential therapeutic targets in different subtypes of CCA through enhancer profiling.OBJECTIVESCholangiocarcinoma (CCA) is a heterogeneous malignancy with high mortality and dismal prognosis, and an urgent clinical need for new therapies. Knowledge of the CCA epigenome is largely limited to aberrant DNA methylation. Dysregulation of enhancer activities has been identified to affect carcinogenesis and leveraged for new therapies but is uninvestigated in CCA. Our aim is to identify potential therapeutic targets in different subtypes of CCA through enhancer profiling.Integrative multiomics enhancer activity profiling of diverse CCA was performed. A panel of diverse CCA cell lines, patient-derived and cell line-derived xenografts were used to study identified enriched pathways and vulnerabilities. NanoString, multiplex immunohistochemistry staining and single-cell spatial transcriptomics were used to explore the immunogenicity of diverse CCA.DESIGNIntegrative multiomics enhancer activity profiling of diverse CCA was performed. A panel of diverse CCA cell lines, patient-derived and cell line-derived xenografts were used to study identified enriched pathways and vulnerabilities. NanoString, multiplex immunohistochemistry staining and single-cell spatial transcriptomics were used to explore the immunogenicity of diverse CCA.We identified three distinct groups, associated with different etiologies and unique pathways. Drug inhibitors of identified pathways reduced tumour growth in in vitro and in vivo models. The first group (ESTRO), with mostly fluke-positive CCAs, displayed activation in estrogen signalling and were sensitive to MTOR inhibitors. Another group (OXPHO), with mostly BAP1 and IDH-mutant CCAs, displayed activated oxidative phosphorylation pathways, and were sensitive to oxidative phosphorylation inhibitors. Immune-related pathways were activated in the final group (IMMUN), made up of an immunogenic CCA subtype and CCA with aristolochic acid (AA) mutational signatures. Intratumour differences in AA mutation load were correlated to intratumour variation of different immune cell populations.RESULTSWe identified three distinct groups, associated with different etiologies and unique pathways. Drug inhibitors of identified pathways reduced tumour growth in in vitro and in vivo models. The first group (ESTRO), with mostly fluke-positive CCAs, displayed activation in estrogen signalling and were sensitive to MTOR inhibitors. Another group (OXPHO), with mostly BAP1 and IDH-mutant CCAs, displayed activated oxidative phosphorylation pathways, and were sensitive to oxidative phosphorylation inhibitors. Immune-related pathways were activated in the final group (IMMUN), made up of an immunogenic CCA subtype and CCA with aristolochic acid (AA) mutational signatures. Intratumour differences in AA mutation load were correlated to intratumour variation of different immune cell populations.Our study elucidates the mechanisms underlying enhancer dysregulation and deepens understanding of different tumourigenesis processes in distinct CCA subtypes, with potential significant therapeutics and clinical benefits.CONCLUSIONOur study elucidates the mechanisms underlying enhancer dysregulation and deepens understanding of different tumourigenesis processes in distinct CCA subtypes, with potential significant therapeutics and clinical benefits. |
| Author | Zeng, Xian Zhang, Yaojun Tai, David Wai Meng Guan, Peiyong Heng, Hong Lee Teh, Bin Tean Lim, Abner Herbert Lee, Jing Yi Popescu, Irinel Chan, Jason Yongsheng Loilome, Watcharin Kongpetch, Sarinya Boot, Arnoud Yong, Chern Han Chu, Pek Lim Lau, Mai Chan Ng, Cedric Chuan Young Pairojkul, Chawalit Tan, Jing Kwek, Xiu Yi Yu, Ming-Chin Jusakul, Apinya Liu, Wei Yao, Xiaosai Yeong, Joe Hsieh, Sen-Yung Wang, Peili Koh, Joanna Hong, Jing Han Ng, Sheng Rong Sun, Yichen Dima, Simona Klanrit, Poramate Tan, Patrick Lim, Jeffrey Chun Tatt Xiao, Rong Chen, Jianfeng Li, Zhimei Wee, Felicia Yu Ting Lai, Jiaming |
| Author_xml | – sequence: 1 givenname: Jing Han orcidid: 0000-0002-2173-9192 surname: Hong fullname: Hong, Jing Han organization: Cancer and Stem Cell Biology Programme, Duke-NUS Medical School, Singapore – sequence: 2 givenname: Chern Han surname: Yong fullname: Yong, Chern Han organization: Department of Computer Science, National University of Singapore, Singapore – sequence: 3 givenname: Hong Lee surname: Heng fullname: Heng, Hong Lee organization: Laboratory of Cancer Epigenome, National Cancer Centre Singapore, Singapore – sequence: 4 givenname: Jason Yongsheng surname: Chan fullname: Chan, Jason Yongsheng organization: Oncology Academic Clinical Program, Duke-NUS Medical School, Singapore – sequence: 5 givenname: Mai Chan surname: Lau fullname: Lau, Mai Chan organization: Bioinformatics Institute (BII), Agency for Science Technology and Research (ASTAR), Singapore – sequence: 6 givenname: Jianfeng surname: Chen fullname: Chen, Jianfeng organization: State Key Laboratory of Oncology in South China, Collaborative Innovation Center of Cancer Medicine, Sun Yat-sen University Cancer Center, Guangzhou, China – sequence: 7 givenname: Jing Yi surname: Lee fullname: Lee, Jing Yi organization: Cancer Discovery Hub, National Cancer Centre Singapore, Singapore – sequence: 8 givenname: Abner Herbert surname: Lim fullname: Lim, Abner Herbert organization: Cancer Discovery Hub, National Cancer Centre Singapore, Singapore – sequence: 9 givenname: Zhimei surname: Li fullname: Li, Zhimei organization: Cancer Discovery Hub, National Cancer Centre Singapore, Singapore – sequence: 10 givenname: Peiyong surname: Guan fullname: Guan, Peiyong organization: Genome Institute of Singapore, Agency for Science Technology and Research (ASTAR), Singapore – sequence: 11 givenname: Pek Lim surname: Chu fullname: Chu, Pek Lim organization: Cancer and Stem Cell Biology Programme, Duke-NUS Medical School, Singapore – sequence: 12 givenname: Arnoud surname: Boot fullname: Boot, Arnoud organization: Centre for Computational Biology, Duke-NUS Medical School, Singapore – sequence: 13 givenname: Sheng Rong orcidid: 0000-0003-1655-2443 surname: Ng fullname: Ng, Sheng Rong organization: Institute of Molecular and Cell Biology, Agency for Science Technology and Research (ASTAR), Singapore – sequence: 14 givenname: Xiaosai surname: Yao fullname: Yao, Xiaosai organization: Institute of Molecular and Cell Biology, Agency for Science Technology and Research (ASTAR), Singapore – sequence: 15 givenname: Felicia Yu Ting surname: Wee fullname: Wee, Felicia Yu Ting organization: Institute of Molecular and Cell Biology, Integrative Biology for Theranostics Lab, Agency for Science Technology and Research (ASTAR), Singapore – sequence: 16 givenname: Jeffrey Chun Tatt surname: Lim fullname: Lim, Jeffrey Chun Tatt organization: Institute of Molecular and Cell Biology, Integrative Biology for Theranostics Lab, Agency for Science Technology and Research (ASTAR), Singapore – sequence: 17 givenname: Wei surname: Liu fullname: Liu, Wei organization: Laboratory of Cancer Epigenome, National Cancer Centre Singapore, Singapore – sequence: 18 givenname: Peili surname: Wang fullname: Wang, Peili organization: State Key Laboratory of Oncology in South China, Collaborative Innovation Center of Cancer Medicine, Sun Yat-sen University Cancer Center, Guangzhou, China – sequence: 19 givenname: Rong surname: Xiao fullname: Xiao, Rong organization: State Key Laboratory of Oncology in South China, Collaborative Innovation Center of Cancer Medicine, Sun Yat-sen University Cancer Center, Guangzhou, China – sequence: 20 givenname: Xian surname: Zeng fullname: Zeng, Xian organization: State Key Laboratory of Oncology in South China, Collaborative Innovation Center of Cancer Medicine, Sun Yat-sen University Cancer Center, Guangzhou, China – sequence: 21 givenname: Yichen surname: Sun fullname: Sun, Yichen organization: State Key Laboratory of Oncology in South China, Collaborative Innovation Center of Cancer Medicine, Sun Yat-sen University Cancer Center, Guangzhou, China – sequence: 22 givenname: Joanna surname: Koh fullname: Koh, Joanna organization: Institute of Molecular and Cell Biology, Agency for Science Technology and Research (ASTAR), Singapore – sequence: 23 givenname: Xiu Yi surname: Kwek fullname: Kwek, Xiu Yi organization: Laboratory of Cancer Epigenome, National Cancer Centre Singapore, Singapore – sequence: 24 givenname: Cedric Chuan Young surname: Ng fullname: Ng, Cedric Chuan Young organization: Cancer Discovery Hub, National Cancer Centre Singapore, Singapore – sequence: 25 givenname: Poramate surname: Klanrit fullname: Klanrit, Poramate organization: Department of Biochemistry, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand – sequence: 26 givenname: Yaojun surname: Zhang fullname: Zhang, Yaojun organization: Department of Liver Surgery, Sun Yat-Sen University Cancer Center, Guangzhou, Guangdong – sequence: 27 givenname: Jiaming surname: Lai fullname: Lai, Jiaming organization: Department of Pancreaticobiliary Surgery, Sun Yat-sen University, Guangzhou, China – sequence: 28 givenname: David Wai Meng surname: Tai fullname: Tai, David Wai Meng organization: Oncology Academic Clinical Program, Duke-NUS Medical School, Singapore – sequence: 29 givenname: Chawalit surname: Pairojkul fullname: Pairojkul, Chawalit organization: Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand – sequence: 30 givenname: Simona surname: Dima fullname: Dima, Simona organization: Center of Digestive Diseases and Liver Transplantation, Fundeni Clinical Institute, Bucuresti, Romania – sequence: 31 givenname: Irinel surname: Popescu fullname: Popescu, Irinel organization: Center of Digestive Diseases and Liver Transplantation, Fundeni Clinical Institute, Bucuresti, Romania – sequence: 32 givenname: Sen-Yung surname: Hsieh fullname: Hsieh, Sen-Yung organization: Department of Gastroenterology and Hepatology, Chang Gung Memorial Hospital and Chang Gung University, Taoyuan, Taiwan – sequence: 33 givenname: Ming-Chin surname: Yu fullname: Yu, Ming-Chin organization: Department of General Surgery, Chang Gung Memorial Hospital and Chang Gung University, Taoyuan, Taiwan – sequence: 34 givenname: Joe orcidid: 0000-0002-6674-7153 surname: Yeong fullname: Yeong, Joe organization: Pathology Academic Clinical Program, Duke-NUS Medical School, Singapore – sequence: 35 givenname: Sarinya surname: Kongpetch fullname: Kongpetch, Sarinya organization: Department of Pharmacology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand – sequence: 36 givenname: Apinya surname: Jusakul fullname: Jusakul, Apinya organization: Centre for Research and Development of Medical Diagnostic Laboratories, Faculty of Associated Medical Sciences, Khon Kaen University, Khon Kaen, Thailand – sequence: 37 givenname: Watcharin surname: Loilome fullname: Loilome, Watcharin organization: Cholangiocarcinoma Research Institute, Khon Kaen University, Khon Kaen, Thailand – sequence: 38 givenname: Patrick orcidid: 0000-0002-0179-8048 surname: Tan fullname: Tan, Patrick organization: Cancer Science Institute of Singapore, National University of Singapore, Singapore – sequence: 39 givenname: Jing orcidid: 0000-0002-4605-4624 surname: Tan fullname: Tan, Jing organization: State Key Laboratory of Oncology, Collaborative Innovation Center of Cancer Medicine, Sun Yat-sen University Cancer Center, Guangzhou, China – sequence: 40 givenname: Bin Tean orcidid: 0000-0003-1514-1124 surname: Teh fullname: Teh, Bin Tean email: teh.bin.tean@singhealth.com.sg organization: Institute of Molecular and Cell Biology, Agency for Science Technology and Research (ASTAR), Singapore |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38050079$$D View this record in MEDLINE/PubMed |
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| DOI | 10.1136/gutjnl-2023-330483 |
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| Keywords | CHOLANGIOCARCINOMA CANCER MOLECULAR ONCOLOGY |
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10;73(6):888-889. doi: 10.1136/gutjnl-2023-331480 |
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| Snippet | ObjectivesCholangiocarcinoma (CCA) is a heterogeneous malignancy with high mortality and dismal prognosis, and an urgent clinical need for new therapies.... Cholangiocarcinoma (CCA) is a heterogeneous malignancy with high mortality and dismal prognosis, and an urgent clinical need for new therapies. Knowledge of... |
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| SubjectTerms | Animals Aristolochic acid Bile Duct Neoplasms - drug therapy Bile Duct Neoplasms - genetics Bile Duct Neoplasms - metabolism Bile Duct Neoplasms - pathology CANCER Cancer therapies Carcinogenesis Cell Line, Tumor Chemotherapy CHOLANGIOCARCINOMA Cholangiocarcinoma - drug therapy Cholangiocarcinoma - genetics Cholangiocarcinoma - metabolism Cholangiocarcinoma - pathology DNA methylation Epigenetics Estrogens Etiology Gene expression Gene Expression Profiling - methods Hepatology Humans Immunogenicity Immunohistochemistry Infections Liver Malignancy Mice MOLECULAR ONCOLOGY Multiomics Mutation Oxidative phosphorylation Phosphorylation Population studies Signal transduction Therapeutic targets TOR protein Transcriptomics Tumorigenesis Tumors |
| Title | Integrative multiomics enhancer activity profiling identifies therapeutic vulnerabilities in cholangiocarcinoma of different etiologies |
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