Landscape and Dynamics of Single Immune Cells in Hepatocellular Carcinoma
The immune microenvironment of hepatocellular carcinoma (HCC) is poorly characterized. Combining two single-cell RNA sequencing technologies, we produced transcriptomes of CD45+ immune cells for HCC patients from five immune-relevant sites: tumor, adjacent liver, hepatic lymph node (LN), blood, and...
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| Published in | Cell Vol. 179; no. 4; pp. 829 - 845.e20 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
31.10.2019
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| Subjects | |
| Online Access | Get full text |
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| Abstract | The immune microenvironment of hepatocellular carcinoma (HCC) is poorly characterized. Combining two single-cell RNA sequencing technologies, we produced transcriptomes of CD45+ immune cells for HCC patients from five immune-relevant sites: tumor, adjacent liver, hepatic lymph node (LN), blood, and ascites. A cluster of LAMP3+ dendritic cells (DCs) appeared to be the mature form of conventional DCs and possessed the potential to migrate from tumors to LNs. LAMP3+ DCs also expressed diverse immune-relevant ligands and exhibited potential to regulate multiple subtypes of lymphocytes. Of the macrophages in tumors that exhibited distinct transcriptional states, tumor-associated macrophages (TAMs) were associated with poor prognosis, and we established the inflammatory role of SLC40A1 and GPNMB in these cells. Further, myeloid and lymphoid cells in ascites were predominantly linked to tumor and blood origins, respectively. The dynamic properties of diverse CD45+ cell types revealed by this study add new dimensions to the immune landscape of HCC.
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•Two scRNA-seq platforms reveal a high-resolution dynamic immune landscape in HCC•LAMP3+ DCs, arising from cDCs, can migrate from tumors to hepatic lymph nodes•Paired ligand-receptor analyses implicate the regulation of lymphocytes by LAMP3+ DCs•Macrophage subsets in tumors show distinct states and potentials to egress to ascites
Integrated single-cell RNA sequencing technologies and bioinformatics approaches reveal a high-resolution immune landscape of hepatocellular carcinoma, identifying inflammatory signatures and functional states of myeloid cells as well as predictions of complex cell-cell interactions. |
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| AbstractList | The immune microenvironment of hepatocellular carcinoma (HCC) is poorly characterized. Combining two single-cell RNA sequencing technologies, we produced transcriptomes of CD45⁺ immune cells for HCC patients from five immune-relevant sites: tumor, adjacent liver, hepatic lymph node (LN), blood, and ascites. A cluster of LAMP3⁺ dendritic cells (DCs) appeared to be the mature form of conventional DCs and possessed the potential to migrate from tumors to LNs. LAMP3⁺ DCs also expressed diverse immune-relevant ligands and exhibited potential to regulate multiple subtypes of lymphocytes. Of the macrophages in tumors that exhibited distinct transcriptional states, tumor-associated macrophages (TAMs) were associated with poor prognosis, and we established the inflammatory role of SLC40A1 and GPNMB in these cells. Further, myeloid and lymphoid cells in ascites were predominantly linked to tumor and blood origins, respectively. The dynamic properties of diverse CD45⁺ cell types revealed by this study add new dimensions to the immune landscape of HCC. The immune microenvironment of hepatocellular carcinoma (HCC) is poorly characterized. Combining two single-cell RNA sequencing technologies, we produced transcriptomes of CD45 immune cells for HCC patients from five immune-relevant sites: tumor, adjacent liver, hepatic lymph node (LN), blood, and ascites. A cluster of LAMP3 dendritic cells (DCs) appeared to be the mature form of conventional DCs and possessed the potential to migrate from tumors to LNs. LAMP3 DCs also expressed diverse immune-relevant ligands and exhibited potential to regulate multiple subtypes of lymphocytes. Of the macrophages in tumors that exhibited distinct transcriptional states, tumor-associated macrophages (TAMs) were associated with poor prognosis, and we established the inflammatory role of SLC40A1 and GPNMB in these cells. Further, myeloid and lymphoid cells in ascites were predominantly linked to tumor and blood origins, respectively. The dynamic properties of diverse CD45 cell types revealed by this study add new dimensions to the immune landscape of HCC. The immune microenvironment of hepatocellular carcinoma (HCC) is poorly characterized. Combining two single-cell RNA sequencing technologies, we produced transcriptomes of CD45+ immune cells for HCC patients from five immune-relevant sites: tumor, adjacent liver, hepatic lymph node (LN), blood, and ascites. A cluster of LAMP3+ dendritic cells (DCs) appeared to be the mature form of conventional DCs and possessed the potential to migrate from tumors to LNs. LAMP3+ DCs also expressed diverse immune-relevant ligands and exhibited potential to regulate multiple subtypes of lymphocytes. Of the macrophages in tumors that exhibited distinct transcriptional states, tumor-associated macrophages (TAMs) were associated with poor prognosis, and we established the inflammatory role of SLC40A1 and GPNMB in these cells. Further, myeloid and lymphoid cells in ascites were predominantly linked to tumor and blood origins, respectively. The dynamic properties of diverse CD45+ cell types revealed by this study add new dimensions to the immune landscape of HCC.The immune microenvironment of hepatocellular carcinoma (HCC) is poorly characterized. Combining two single-cell RNA sequencing technologies, we produced transcriptomes of CD45+ immune cells for HCC patients from five immune-relevant sites: tumor, adjacent liver, hepatic lymph node (LN), blood, and ascites. A cluster of LAMP3+ dendritic cells (DCs) appeared to be the mature form of conventional DCs and possessed the potential to migrate from tumors to LNs. LAMP3+ DCs also expressed diverse immune-relevant ligands and exhibited potential to regulate multiple subtypes of lymphocytes. Of the macrophages in tumors that exhibited distinct transcriptional states, tumor-associated macrophages (TAMs) were associated with poor prognosis, and we established the inflammatory role of SLC40A1 and GPNMB in these cells. Further, myeloid and lymphoid cells in ascites were predominantly linked to tumor and blood origins, respectively. The dynamic properties of diverse CD45+ cell types revealed by this study add new dimensions to the immune landscape of HCC. The immune microenvironment of hepatocellular carcinoma (HCC) is poorly characterized. Combining two single-cell RNA sequencing technologies, we produced transcriptomes of CD45+ immune cells for HCC patients from five immune-relevant sites: tumor, adjacent liver, hepatic lymph node (LN), blood, and ascites. A cluster of LAMP3+ dendritic cells (DCs) appeared to be the mature form of conventional DCs and possessed the potential to migrate from tumors to LNs. LAMP3+ DCs also expressed diverse immune-relevant ligands and exhibited potential to regulate multiple subtypes of lymphocytes. Of the macrophages in tumors that exhibited distinct transcriptional states, tumor-associated macrophages (TAMs) were associated with poor prognosis, and we established the inflammatory role of SLC40A1 and GPNMB in these cells. Further, myeloid and lymphoid cells in ascites were predominantly linked to tumor and blood origins, respectively. The dynamic properties of diverse CD45+ cell types revealed by this study add new dimensions to the immune landscape of HCC. [Display omitted] •Two scRNA-seq platforms reveal a high-resolution dynamic immune landscape in HCC•LAMP3+ DCs, arising from cDCs, can migrate from tumors to hepatic lymph nodes•Paired ligand-receptor analyses implicate the regulation of lymphocytes by LAMP3+ DCs•Macrophage subsets in tumors show distinct states and potentials to egress to ascites Integrated single-cell RNA sequencing technologies and bioinformatics approaches reveal a high-resolution immune landscape of hepatocellular carcinoma, identifying inflammatory signatures and functional states of myeloid cells as well as predictions of complex cell-cell interactions. |
| Author | He, Yao Zhu, Weihua Hu, Xueda Carotta, Sebastian Modak, Madhura Bergmann, Michael Gao, Ranran Kerkar, Sid P. Zhong, Guojie Luo, Nan Peet, Gregory W. Han, Yanjie Haslinger, Christian Pflanz, Stefan Zhang, Qiming Zhang, Zemin Ren, Xianwen Peng, Jirun Vogt, Anne B. Patel, Shashank J. Lu, Shuangjia Xiao, Mengmeng Kind, David Liu, Kang Mao, Yilei |
| Author_xml | – sequence: 1 givenname: Qiming surname: Zhang fullname: Zhang, Qiming organization: BIOPIC, Beijing Advanced Innovation Center for Genomics, School of Life Sciences, Peking University, Beijing 100871, China – sequence: 2 givenname: Yao surname: He fullname: He, Yao organization: Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China – sequence: 3 givenname: Nan surname: Luo fullname: Luo, Nan organization: Department of Surgery, Beijing Shijitan Hospital, Capital Medical University, Beijing 100038, China – sequence: 4 givenname: Shashank J. surname: Patel fullname: Patel, Shashank J. organization: Department of Cancer Immunology and Immune Modulation, Boehringer Ingelheim Pharmaceuticals, Inc., 900 Ridgebury Road, Ridgefield, CT 06877, USA – sequence: 5 givenname: Yanjie surname: Han fullname: Han, Yanjie organization: BIOPIC, Beijing Advanced Innovation Center for Genomics, School of Life Sciences, Peking University, Beijing 100871, China – sequence: 6 givenname: Ranran surname: Gao fullname: Gao, Ranran organization: BIOPIC, Beijing Advanced Innovation Center for Genomics, School of Life Sciences, Peking University, Beijing 100871, China – sequence: 7 givenname: Madhura surname: Modak fullname: Modak, Madhura organization: Department of Cancer Immunology and Immune Modulation, Boehringer Ingelheim Pharma, Birkendorfer Str. 65, 88400 Biberach, Germany – sequence: 8 givenname: Sebastian surname: Carotta fullname: Carotta, Sebastian organization: Department of Cancer Cell Signaling, Boehringer Ingelheim RCV GmBH & Co KG., Dr. Boehringer Gasse 5–11, 1120 Vienna, Austria – sequence: 9 givenname: Christian surname: Haslinger fullname: Haslinger, Christian organization: Department of Computational Biology and Genomics, Boehringer Ingelheim Pharma, Birkendorfer Str. 65, 88400 Biberach, Germany – sequence: 10 givenname: David surname: Kind fullname: Kind, David organization: Department of Computational Biology and Genomics, Boehringer Ingelheim Pharma, Birkendorfer Str. 65, 88400 Biberach, Germany – sequence: 11 givenname: Gregory W. surname: Peet fullname: Peet, Gregory W. organization: Department of Cancer Immunology and Immune Modulation, Boehringer Ingelheim Pharmaceuticals, Inc., 900 Ridgebury Road, Ridgefield, CT 06877, USA – sequence: 12 givenname: Guojie surname: Zhong fullname: Zhong, Guojie organization: BIOPIC, Beijing Advanced Innovation Center for Genomics, School of Life Sciences, Peking University, Beijing 100871, China – sequence: 13 givenname: Shuangjia surname: Lu fullname: Lu, Shuangjia organization: BIOPIC, Beijing Advanced Innovation Center for Genomics, School of Life Sciences, Peking University, Beijing 100871, China – sequence: 14 givenname: Weihua surname: Zhu fullname: Zhu, Weihua organization: Department of Hepatobiliary Surgery, Peking University People’s Hospital, Beijing 100044, China – sequence: 15 givenname: Yilei surname: Mao fullname: Mao, Yilei organization: Department of Liver Surgery, Peking Union Medical College Hospital, Beijing 100730, China – sequence: 16 givenname: Mengmeng surname: Xiao fullname: Xiao, Mengmeng organization: Department of Retroperitoneal Tumor Surgery, Peking University International Hospital, Beijing 102206, China – sequence: 17 givenname: Michael surname: Bergmann fullname: Bergmann, Michael organization: Department of Surgery and Comprehensive Cancer Center, Medical University of Vienna, Vienna, Austria – sequence: 18 givenname: Xueda surname: Hu fullname: Hu, Xueda organization: BIOPIC, Beijing Advanced Innovation Center for Genomics, School of Life Sciences, Peking University, Beijing 100871, China – sequence: 19 givenname: Sid P. surname: Kerkar fullname: Kerkar, Sid P. organization: Department of Cancer Immunology and Immune Modulation, Boehringer Ingelheim Pharmaceuticals, Inc., 900 Ridgebury Road, Ridgefield, CT 06877, USA – sequence: 20 givenname: Anne B. surname: Vogt fullname: Vogt, Anne B. organization: Department of Human Cancer Immunology, Boehringer Ingelheim RCV GmBH & Co KG., Dr. Boehringer Gasse 5–11, 1120 Vienna, Austria – sequence: 21 givenname: Stefan surname: Pflanz fullname: Pflanz, Stefan organization: Department of Cancer Immunology and Immune Modulation, Boehringer Ingelheim Pharma, Birkendorfer Str. 65, 88400 Biberach, Germany – sequence: 22 givenname: Kang surname: Liu fullname: Liu, Kang email: kang_3.liu@boehringer-ingelheim.com organization: Department of Cancer Immunology and Immune Modulation, Boehringer Ingelheim Pharmaceuticals, Inc., 900 Ridgebury Road, Ridgefield, CT 06877, USA – sequence: 23 givenname: Jirun surname: Peng fullname: Peng, Jirun email: pengjr@medmail.com.cn organization: Department of Surgery, Beijing Shijitan Hospital, Capital Medical University, Beijing 100038, China – sequence: 24 givenname: Xianwen surname: Ren fullname: Ren, Xianwen email: renxwise@pku.edu.cn organization: BIOPIC, Beijing Advanced Innovation Center for Genomics, School of Life Sciences, Peking University, Beijing 100871, China – sequence: 25 givenname: Zemin orcidid: 0000-0003-3789-6536 surname: Zhang fullname: Zhang, Zemin email: zemin@pku.edu.cn organization: BIOPIC, Beijing Advanced Innovation Center for Genomics, School of Life Sciences, Peking University, Beijing 100871, China |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31675496$$D View this record in MEDLINE/PubMed |
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| Snippet | The immune microenvironment of hepatocellular carcinoma (HCC) is poorly characterized. Combining two single-cell RNA sequencing technologies, we produced... |
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| SubjectTerms | ascites Carcinoma, Hepatocellular - genetics Carcinoma, Hepatocellular - immunology Carcinoma, Hepatocellular - pathology Cation Transport Proteins - genetics Cell Communication - genetics Cell Communication - immunology Cell Lineage - genetics Cell Lineage - immunology dendritic cells Dendritic Cells - immunology Dendritic Cells - pathology Gene Expression Regulation, Neoplastic hepatoma Humans immunity Inflammation - genetics Inflammation - immunology Inflammation - pathology Leukocyte Common Antigens - immunology ligands liver Liver - immunology Liver - pathology Liver Neoplasms - genetics Liver Neoplasms - immunology Liver Neoplasms - pathology lymph nodes Lymph Nodes - immunology Lymph Nodes - pathology lymphocytes Lymphocytes - immunology Lymphocytes - pathology Lysosomal Membrane Proteins - genetics macrophages Macrophages - immunology Macrophages - pathology Membrane Glycoproteins - genetics Myeloid Cells - immunology Myeloid Cells - pathology Neoplasm Proteins - genetics patients prognosis sequence analysis Sequence Analysis, RNA Single-Cell Analysis transcription (genetics) transcriptome Transcriptome - genetics Transcriptome - immunology Tumor Microenvironment - genetics Tumor Microenvironment - immunology |
| Title | Landscape and Dynamics of Single Immune Cells in Hepatocellular Carcinoma |
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