Single-Cell Transcriptomics of Human and Mouse Lung Cancers Reveals Conserved Myeloid Populations across Individuals and Species
Tumor-infiltrating myeloid cells (TIMs) comprise monocytes, macrophages, dendritic cells, and neutrophils, and have emerged as key regulators of cancer growth. These cells can diversify into a spectrum of states, which might promote or limit tumor outgrowth but remain poorly understood. Here, we use...
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| Published in | Immunity (Cambridge, Mass.) Vol. 50; no. 5; pp. 1317 - 1334.e10 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
21.05.2019
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1074-7613 1097-4180 1097-4180 |
| DOI | 10.1016/j.immuni.2019.03.009 |
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| Abstract | Tumor-infiltrating myeloid cells (TIMs) comprise monocytes, macrophages, dendritic cells, and neutrophils, and have emerged as key regulators of cancer growth. These cells can diversify into a spectrum of states, which might promote or limit tumor outgrowth but remain poorly understood. Here, we used single-cell RNA sequencing (scRNA-seq) to map TIMs in non-small-cell lung cancer patients. We uncovered 25 TIM states, most of which were reproducibly found across patients. To facilitate translational research of these populations, we also profiled TIMs in mice. In comparing TIMs across species, we identified a near-complete congruence of population structures among dendritic cells and monocytes; conserved neutrophil subsets; and species differences among macrophages. By contrast, myeloid cell population structures in patients’ blood showed limited overlap with those of TIMs. This study determines the lung TIM landscape and sets the stage for future investigations into the potential of TIMs as immunotherapy targets.
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•Human dendritic cell and monocyte subsets show one-to-one equivalence in mouse•Neutrophils exhibit tumor-associated phenotypes that are conserved across species•Myeloid subsets in patient blood only partially overlap with those in their tumors•Unique markers define myeloid cell subsets and associate with clinical prognosis
Tumor-infiltrating myeloid cells (TIMs) have emerged as key cancer regulators and potential next-generation immunotherapy targets, yet they remain incompletely understood. Using scRNA-seq, Zilionis et al. map the TIM landscape in human and murine lung tumors and systematically compare cell states, revealing conserved myeloid populations across individuals and species. |
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| AbstractList | Tumor-infiltrating myeloid cells (TIMs) comprise monocytes, macrophages, dendritic cells, and neutrophils, and have emerged as key regulators of cancer growth. These cells can diversify into a spectrum of states, which might promote or limit tumor outgrowth but remain poorly understood. Here, we used single-cell RNA sequencing (scRNA-seq) to map TIMs in non-small-cell lung cancer patients. We uncovered 25 TIM states, most of which were reproducibly found across patients. To facilitate translational research of these populations, we also profiled TIMs in mice. In comparing TIMs across species, we identified a near-complete congruence of population structures among dendritic cells and monocytes; conserved neutrophil subsets; and species differences among macrophages. By contrast, myeloid cell population structures in patients' blood showed limited overlap with those of TIMs. This study determines the lung TIM landscape and sets the stage for future investigations into the potential of TIMs as immunotherapy targets.Tumor-infiltrating myeloid cells (TIMs) comprise monocytes, macrophages, dendritic cells, and neutrophils, and have emerged as key regulators of cancer growth. These cells can diversify into a spectrum of states, which might promote or limit tumor outgrowth but remain poorly understood. Here, we used single-cell RNA sequencing (scRNA-seq) to map TIMs in non-small-cell lung cancer patients. We uncovered 25 TIM states, most of which were reproducibly found across patients. To facilitate translational research of these populations, we also profiled TIMs in mice. In comparing TIMs across species, we identified a near-complete congruence of population structures among dendritic cells and monocytes; conserved neutrophil subsets; and species differences among macrophages. By contrast, myeloid cell population structures in patients' blood showed limited overlap with those of TIMs. This study determines the lung TIM landscape and sets the stage for future investigations into the potential of TIMs as immunotherapy targets. Tumor-infiltrating myeloid cells (TIMs) comprise monocytes, macrophages, dendritic cells and neutrophils, and have emerged as key regulators of cancer growth. These cells can diversify into a spectrum of states, which may promote or limit tumor outgrowth, but remain poorly understood. Here, we used single-cell RNA sequencing to map TIMs in non-small cell lung cancer patients. We uncovered 25 TIM states, most of which were reproducibly found across patients. To facilitate translational research of these populations, we also profiled TIMs in mice. In comparing TIMs across species, we identified a near-complete congruence of population structures among dendritic cells and monocytes; conserved neutrophil subsets; and species differences among macrophages. By contrast, myeloid cell population structures in patients’ blood showed limited overlap with those of TIMs. This study determines the lung TIM landscape and sets the stage for future investigations into the potential of TIMs as immunotherapy targets. Tumor-infiltrating myeloid cells (TIM) have emerged as key cancer regulators and potential next-generation immunotherapy targets, yet they remain incompletely understood. Using single cell RNA-seq, Zilionis et al. map the TIM landscape in human and murine lung tumors and systematically compare cell states, revealing conserved myeloid populations across individuals and species. SummaryTumor-infiltrating myeloid cells (TIMs) comprise monocytes, macrophages, dendritic cells, and neutrophils, and have emerged as key regulators of cancer growth. These cells can diversify into a spectrum of states, which might promote or limit tumor outgrowth but remain poorly understood. Here, we used single-cell RNA sequencing (scRNA-seq) to map TIMs in non-small-cell lung cancer patients. We uncovered 25 TIM states, most of which were reproducibly found across patients. To facilitate translational research of these populations, we also profiled TIMs in mice. In comparing TIMs across species, we identified a near-complete congruence of population structures among dendritic cells and monocytes; conserved neutrophil subsets; and species differences among macrophages. By contrast, myeloid cell population structures in patients’ blood showed limited overlap with those of TIMs. This study determines the lung TIM landscape and sets the stage for future investigations into the potential of TIMs as immunotherapy targets. Tumor-infiltrating myeloid cells (TIMs) comprise monocytes, macrophages, dendritic cells, and neutrophils, and have emerged as key regulators of cancer growth. These cells can diversify into a spectrum of states, which might promote or limit tumor outgrowth but remain poorly understood. Here, we used single-cell RNA sequencing (scRNA-seq) to map TIMs in non-small-cell lung cancer patients. We uncovered 25 TIM states, most of which were reproducibly found across patients. To facilitate translational research of these populations, we also profiled TIMs in mice. In comparing TIMs across species, we identified a near-complete congruence of population structures among dendritic cells and monocytes; conserved neutrophil subsets; and species differences among macrophages. By contrast, myeloid cell population structures in patients' blood showed limited overlap with those of TIMs. This study determines the lung TIM landscape and sets the stage for future investigations into the potential of TIMs as immunotherapy targets. Tumor-infiltrating myeloid cells (TIMs) comprise monocytes, macrophages, dendritic cells, and neutrophils, and have emerged as key regulators of cancer growth. These cells can diversify into a spectrum of states, which might promote or limit tumor outgrowth but remain poorly understood. Here, we used single-cell RNA sequencing (scRNA-seq) to map TIMs in non-small-cell lung cancer patients. We uncovered 25 TIM states, most of which were reproducibly found across patients. To facilitate translational research of these populations, we also profiled TIMs in mice. In comparing TIMs across species, we identified a near-complete congruence of population structures among dendritic cells and monocytes; conserved neutrophil subsets; and species differences among macrophages. By contrast, myeloid cell population structures in patients’ blood showed limited overlap with those of TIMs. This study determines the lung TIM landscape and sets the stage for future investigations into the potential of TIMs as immunotherapy targets. [Display omitted] •Human dendritic cell and monocyte subsets show one-to-one equivalence in mouse•Neutrophils exhibit tumor-associated phenotypes that are conserved across species•Myeloid subsets in patient blood only partially overlap with those in their tumors•Unique markers define myeloid cell subsets and associate with clinical prognosis Tumor-infiltrating myeloid cells (TIMs) have emerged as key cancer regulators and potential next-generation immunotherapy targets, yet they remain incompletely understood. Using scRNA-seq, Zilionis et al. map the TIM landscape in human and murine lung tumors and systematically compare cell states, revealing conserved myeloid populations across individuals and species. |
| Author | Levantini, Elena Kerwin, Clara M. Savova, Virginia Saatcioglu, Hatice D. Choi, Sun Krishnan, Indira Richards, William G. Bueno, Raphael Engblom, Camilla Zemmour, David Tenen, Daniel G. Zilionis, Rapolas Maroni, Giorgia Pfirschke, Christina Pittet, Mikael J. Meyerovitz, Claire V. De Rienzo, Assunta Klein, Allon M. |
| AuthorAffiliation | 2 Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, Lithuania 4 Graduate Program in Immunology, Harvard Medical School, Boston, MA, USA 5 Precision Immunology, Immunology and Inflammation Therapeutic Area, Sanofi, US 8 Harvard Stem Cell Institute, Harvard Medical School, Boston, MA, USA 12 Cancer Science Institute of Singapore, National University of Singapore, Singapore City, Singapore 3 Center for Systems Biology, Massachusetts General Hospital Research Institute and Harvard Medical School, Boston, MA, USA 7 Pediatric Surgical Research Laboratories, Massachusetts General Hospital and Department of Surgery, Harvard Medical School, Boston, MA 9 Beth Israel Deaconess Medical Center, Boston, MA, USA 11 Division of Thoracic Surgery, The Lung Center and the International Mesothelioma Program, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA 10 Institute of Biomedical Technologies, National Research Council (CNR), Pisa, Italy 1 Department of System |
| AuthorAffiliation_xml | – name: 9 Beth Israel Deaconess Medical Center, Boston, MA, USA – name: 4 Graduate Program in Immunology, Harvard Medical School, Boston, MA, USA – name: 11 Division of Thoracic Surgery, The Lung Center and the International Mesothelioma Program, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA – name: 5 Precision Immunology, Immunology and Inflammation Therapeutic Area, Sanofi, US – name: 6 Division of Immunology, Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA, USA – name: 8 Harvard Stem Cell Institute, Harvard Medical School, Boston, MA, USA – name: 10 Institute of Biomedical Technologies, National Research Council (CNR), Pisa, Italy – name: 12 Cancer Science Institute of Singapore, National University of Singapore, Singapore City, Singapore – name: 1 Department of Systems Biology, Harvard Medical School, Boston, MA, USA – name: 2 Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, Lithuania – name: 3 Center for Systems Biology, Massachusetts General Hospital Research Institute and Harvard Medical School, Boston, MA, USA – name: 7 Pediatric Surgical Research Laboratories, Massachusetts General Hospital and Department of Surgery, Harvard Medical School, Boston, MA |
| Author_xml | – sequence: 1 givenname: Rapolas surname: Zilionis fullname: Zilionis, Rapolas organization: Department of Systems Biology, Harvard Medical School, Boston, MA, USA – sequence: 2 givenname: Camilla surname: Engblom fullname: Engblom, Camilla organization: Center for Systems Biology, Massachusetts General Hospital Research Institute and Harvard Medical School, Boston, MA, USA – sequence: 3 givenname: Christina surname: Pfirschke fullname: Pfirschke, Christina organization: Center for Systems Biology, Massachusetts General Hospital Research Institute and Harvard Medical School, Boston, MA, USA – sequence: 4 givenname: Virginia surname: Savova fullname: Savova, Virginia email: virginia.savova@sanofi.com organization: Department of Systems Biology, Harvard Medical School, Boston, MA, USA – sequence: 5 givenname: David surname: Zemmour fullname: Zemmour, David organization: Graduate Program in Immunology, Harvard Medical School, Boston, MA, USA – sequence: 6 givenname: Hatice D. surname: Saatcioglu fullname: Saatcioglu, Hatice D. organization: Pediatric Surgical Research Laboratories, Massachusetts General Hospital and Department of Surgery, Harvard Medical School, Boston, MA, USA – sequence: 7 givenname: Indira surname: Krishnan fullname: Krishnan, Indira organization: Harvard Stem Cell Institute, Harvard Medical School, Boston, MA, USA – sequence: 8 givenname: Giorgia surname: Maroni fullname: Maroni, Giorgia organization: Harvard Stem Cell Institute, Harvard Medical School, Boston, MA, USA – sequence: 9 givenname: Claire V. surname: Meyerovitz fullname: Meyerovitz, Claire V. organization: Division of Thoracic Surgery, The Lung Center and the International Mesothelioma Program, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA – sequence: 10 givenname: Clara M. surname: Kerwin fullname: Kerwin, Clara M. organization: Division of Thoracic Surgery, The Lung Center and the International Mesothelioma Program, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA – sequence: 11 givenname: Sun surname: Choi fullname: Choi, Sun organization: Division of Thoracic Surgery, The Lung Center and the International Mesothelioma Program, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA – sequence: 12 givenname: William G. surname: Richards fullname: Richards, William G. organization: Division of Thoracic Surgery, The Lung Center and the International Mesothelioma Program, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA – sequence: 13 givenname: Assunta surname: De Rienzo fullname: De Rienzo, Assunta organization: Division of Thoracic Surgery, The Lung Center and the International Mesothelioma Program, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA – sequence: 14 givenname: Daniel G. surname: Tenen fullname: Tenen, Daniel G. organization: Harvard Stem Cell Institute, Harvard Medical School, Boston, MA, USA – sequence: 15 givenname: Raphael surname: Bueno fullname: Bueno, Raphael organization: Division of Thoracic Surgery, The Lung Center and the International Mesothelioma Program, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA – sequence: 16 givenname: Elena surname: Levantini fullname: Levantini, Elena organization: Harvard Stem Cell Institute, Harvard Medical School, Boston, MA, USA – sequence: 17 givenname: Mikael J. surname: Pittet fullname: Pittet, Mikael J. email: mpittet@mgh.harvard.edu organization: Center for Systems Biology, Massachusetts General Hospital Research Institute and Harvard Medical School, Boston, MA, USA – sequence: 18 givenname: Allon M. surname: Klein fullname: Klein, Allon M. email: allon_klein@hms.harvard.edu organization: Department of Systems Biology, Harvard Medical School, Boston, MA, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30979687$$D View this record in MEDLINE/PubMed |
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| Issue | 5 |
| Keywords | macrophage heterogeneity tumor immunology myeloid cells neutrophil heterogeneity dendritic cell heterogeneity mouse-human comparison tumor microenvironment single-cell analysis |
| Language | English |
| License | Copyright © 2019 Elsevier Inc. All rights reserved. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Lead Contact: Allon M. Klein RZ, CE, CP, VS, MJP and AMK initiated the study, performed the analyses, prepared the figures and wrote the manuscript. CE and CP carried out mouse experiments and prepared mouse samples. RZ and VS carried out scRNA-Seq experiments and computational analyses. DZ developed the Bayesian classifier and assisted in data analysis. HDS performed RNA in situ hybridization and immunohistochemical analysis on patient tumor sections. CVM, CMK, SC, WGR, ADR, IK, GM, EL, DGT, and RB obtained and prepared human patient samples, specifically: CVM, CMK and SC consented patients, maintained IRB approval, obtained blood, gathered clinical data and provided the specimens; WGR, ADR helped in the design of sample collection, provided infrastructure and quality assurance; RB supervised human sample collection and processing, initiated the collaboration, reviewed the work and provided clinical context. IK and GM processed patient samples; EL and DGT initiated the collaboration and coordinated patient sample experiments. AMK and MJP supervised the study. These authors contributed equally Author contributions |
| OpenAccessLink | http://www.cell.com/article/S1074761319301268/pdf |
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| PublicationTitle | Immunity (Cambridge, Mass.) |
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| Snippet | Tumor-infiltrating myeloid cells (TIMs) comprise monocytes, macrophages, dendritic cells, and neutrophils, and have emerged as key regulators of cancer growth.... SummaryTumor-infiltrating myeloid cells (TIMs) comprise monocytes, macrophages, dendritic cells, and neutrophils, and have emerged as key regulators of cancer... Tumor-infiltrating myeloid cells (TIMs) comprise monocytes, macrophages, dendritic cells and neutrophils, and have emerged as key regulators of cancer growth.... |
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| SubjectTerms | Animals Base Sequence Carcinoma, Non-Small-Cell Lung - immunology Carcinoma, Non-Small-Cell Lung - pathology Cell Line, Tumor Collaboration dendritic cell heterogeneity Dendritic cells Dendritic Cells - immunology Dendritic structure Experiments Gene expression Gene Expression Profiling Gene sequencing Grants Granulocytes Histology Humans Immunotherapy Laboratory animals Leukocytes (neutrophilic) Lung - immunology Lung - pathology Lung cancer Lung Neoplasms - immunology Lung Neoplasms - pathology macrophage heterogeneity Macrophages Macrophages - immunology Male Mice Mice, Inbred C57BL Monocytes Monocytes - immunology mouse-human comparison Myeloid cells neutrophil heterogeneity Neutrophils Neutrophils - immunology Patients Populations Regulators Ribonucleic acid RNA Sequence Analysis, RNA single-cell analysis Species Studies tumor immunology tumor microenvironment Tumors |
| Title | Single-Cell Transcriptomics of Human and Mouse Lung Cancers Reveals Conserved Myeloid Populations across Individuals and Species |
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