High-dimensional single cell analysis identifies stem-like cytotoxic CD8+ T cells infiltrating human tumors
CD8+ T cells infiltrating tumors are largely dysfunctional, but whether a subset maintains superior functionality remains ill defined. By high-dimensional single cell analysis of millions of CD8+ T cells from 53 individuals with lung cancer, we defined those subsets that are enriched in tumors compa...
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| Published in | The Journal of experimental medicine Vol. 215; no. 10; pp. 2520 - 2535 |
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| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Rockefeller University Press
01.10.2018
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| Online Access | Get full text |
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| Abstract | CD8+ T cells infiltrating tumors are largely dysfunctional, but whether a subset maintains superior functionality remains ill defined. By high-dimensional single cell analysis of millions of CD8+ T cells from 53 individuals with lung cancer, we defined those subsets that are enriched in tumors compared with cancer-free tissues and blood. Besides exhausted and activated cells, we identified CXCR5+ TIM-3– CD8+ T cells with a partial exhausted phenotype, while retaining gene networks responsible for stem-like plasticity and cytotoxicity, as revealed by single cell sequencing of the whole transcriptome. Ex vivo, CXCR5+ TIM-3– CD8+ T cells displayed enhanced self-renewal and multipotency compared with more differentiated subsets and were largely polyfunctional. Analysis of inhibitory and costimulatory receptors revealed PD-1, TIGIT, and CD27 as possible targets of immunotherapy. We thus demonstrate a hierarchy of differentiation in the context of T cell exhaustion in human cancer similar to that of chronically infected mice, which is further shown to disappear with disease progression. |
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| AbstractList | CD8+ T cells infiltrating tumors are largely dysfunctional, but whether a subset maintains superior functionality remains ill defined. By high-dimensional single cell analysis of millions of CD8+ T cells from 53 individuals with lung cancer, we defined those subsets that are enriched in tumors compared with cancer-free tissues and blood. Besides exhausted and activated cells, we identified CXCR5+ TIM-3- CD8+ T cells with a partial exhausted phenotype, while retaining gene networks responsible for stem-like plasticity and cytotoxicity, as revealed by single cell sequencing of the whole transcriptome. Ex vivo, CXCR5+ TIM-3- CD8+ T cells displayed enhanced self-renewal and multipotency compared with more differentiated subsets and were largely polyfunctional. Analysis of inhibitory and costimulatory receptors revealed PD-1, TIGIT, and CD27 as possible targets of immunotherapy. We thus demonstrate a hierarchy of differentiation in the context of T cell exhaustion in human cancer similar to that of chronically infected mice, which is further shown to disappear with disease progression.CD8+ T cells infiltrating tumors are largely dysfunctional, but whether a subset maintains superior functionality remains ill defined. By high-dimensional single cell analysis of millions of CD8+ T cells from 53 individuals with lung cancer, we defined those subsets that are enriched in tumors compared with cancer-free tissues and blood. Besides exhausted and activated cells, we identified CXCR5+ TIM-3- CD8+ T cells with a partial exhausted phenotype, while retaining gene networks responsible for stem-like plasticity and cytotoxicity, as revealed by single cell sequencing of the whole transcriptome. Ex vivo, CXCR5+ TIM-3- CD8+ T cells displayed enhanced self-renewal and multipotency compared with more differentiated subsets and were largely polyfunctional. Analysis of inhibitory and costimulatory receptors revealed PD-1, TIGIT, and CD27 as possible targets of immunotherapy. We thus demonstrate a hierarchy of differentiation in the context of T cell exhaustion in human cancer similar to that of chronically infected mice, which is further shown to disappear with disease progression. CD8 + T cells infiltrating tumors are largely dysfunctional. Brummelman and Mazza et al. identify partially exhausted CXCR5 + TIM-3 – CD8 + T cells with enhanced stem-like properties and cytotoxicity infiltrating human solid tumors. These cells express candidate immunotherapeutic targets (PD-1, TIGIT and CD27) for their reinvigoration. CD8 + T cells infiltrating tumors are largely dysfunctional, but whether a subset maintains superior functionality remains ill defined. By high-dimensional single cell analysis of millions of CD8 + T cells from 53 individuals with lung cancer, we defined those subsets that are enriched in tumors compared with cancer-free tissues and blood. Besides exhausted and activated cells, we identified CXCR5 + TIM-3 – CD8 + T cells with a partial exhausted phenotype, while retaining gene networks responsible for stem-like plasticity and cytotoxicity, as revealed by single cell sequencing of the whole transcriptome. Ex vivo, CXCR5 + TIM-3 – CD8 + T cells displayed enhanced self-renewal and multipotency compared with more differentiated subsets and were largely polyfunctional. Analysis of inhibitory and costimulatory receptors revealed PD-1, TIGIT, and CD27 as possible targets of immunotherapy. We thus demonstrate a hierarchy of differentiation in the context of T cell exhaustion in human cancer similar to that of chronically infected mice, which is further shown to disappear with disease progression. CD8 T cells infiltrating tumors are largely dysfunctional, but whether a subset maintains superior functionality remains ill defined. By high-dimensional single cell analysis of millions of CD8 T cells from 53 individuals with lung cancer, we defined those subsets that are enriched in tumors compared with cancer-free tissues and blood. Besides exhausted and activated cells, we identified CXCR5 TIM-3 CD8 T cells with a partial exhausted phenotype, while retaining gene networks responsible for stem-like plasticity and cytotoxicity, as revealed by single cell sequencing of the whole transcriptome. Ex vivo, CXCR5 TIM-3 CD8 T cells displayed enhanced self-renewal and multipotency compared with more differentiated subsets and were largely polyfunctional. Analysis of inhibitory and costimulatory receptors revealed PD-1, TIGIT, and CD27 as possible targets of immunotherapy. We thus demonstrate a hierarchy of differentiation in the context of T cell exhaustion in human cancer similar to that of chronically infected mice, which is further shown to disappear with disease progression. CD8+ T cells infiltrating tumors are largely dysfunctional, but whether a subset maintains superior functionality remains ill defined. By high-dimensional single cell analysis of millions of CD8+ T cells from 53 individuals with lung cancer, we defined those subsets that are enriched in tumors compared with cancer-free tissues and blood. Besides exhausted and activated cells, we identified CXCR5+ TIM-3– CD8+ T cells with a partial exhausted phenotype, while retaining gene networks responsible for stem-like plasticity and cytotoxicity, as revealed by single cell sequencing of the whole transcriptome. Ex vivo, CXCR5+ TIM-3– CD8+ T cells displayed enhanced self-renewal and multipotency compared with more differentiated subsets and were largely polyfunctional. Analysis of inhibitory and costimulatory receptors revealed PD-1, TIGIT, and CD27 as possible targets of immunotherapy. We thus demonstrate a hierarchy of differentiation in the context of T cell exhaustion in human cancer similar to that of chronically infected mice, which is further shown to disappear with disease progression. |
| Author | Brummelman, Jolanda Mazza, Emilia M.C. Colombo, Federico S. Lopci, Egesta Ferrari, Francesco Mikulak, Joanna Mavilio, Domenico Grilli, Andrea Alloisio, Marco Alvisi, Giorgia Veronesi, Giulia Novellis, Pierluigi Lugli, Enrico |
| AuthorAffiliation | 6 Department of Medical Biotechnologies and Translational Medicine, University of Milan, Milan, Italy 7 Division of Thoracic Surgery, Humanitas Clinical and Research Center, Rozzano, Milan, Italy 8 IFOM, the FIRC Institute of Molecular Oncology, Milan, Italy 2 Humanitas Flow Cytometry Core, Humanitas Clinical and Research Center, Rozzano, Milan, Italy 5 Unit of Clinical and Experimental Immunology, Humanitas Clinical and Research Center, Rozzano, Milan, Italy 1 Laboratory of Translational Immunology, Humanitas Clinical and Research Center, Rozzano, Milan, Italy 9 Nuclear Medicine Department, Humanitas Clinical and Research Hospital, Milan, Italy 3 Department of Biological Sciences, University of Modena and Reggio Emilia, Modena, Italy 4 PhD Program of Molecular and Translational Medicine, Department of Medical Biotechnology and Translational Medicine, University of Milan, Segrate, Italy |
| AuthorAffiliation_xml | – name: 1 Laboratory of Translational Immunology, Humanitas Clinical and Research Center, Rozzano, Milan, Italy – name: 2 Humanitas Flow Cytometry Core, Humanitas Clinical and Research Center, Rozzano, Milan, Italy – name: 5 Unit of Clinical and Experimental Immunology, Humanitas Clinical and Research Center, Rozzano, Milan, Italy – name: 7 Division of Thoracic Surgery, Humanitas Clinical and Research Center, Rozzano, Milan, Italy – name: 9 Nuclear Medicine Department, Humanitas Clinical and Research Hospital, Milan, Italy – name: 8 IFOM, the FIRC Institute of Molecular Oncology, Milan, Italy – name: 3 Department of Biological Sciences, University of Modena and Reggio Emilia, Modena, Italy – name: 6 Department of Medical Biotechnologies and Translational Medicine, University of Milan, Milan, Italy – name: 4 PhD Program of Molecular and Translational Medicine, Department of Medical Biotechnology and Translational Medicine, University of Milan, Segrate, Italy |
| Author_xml | – sequence: 1 givenname: Jolanda orcidid: 0000-0003-3581-4816 surname: Brummelman fullname: Brummelman, Jolanda – sequence: 2 givenname: Emilia M.C. surname: Mazza fullname: Mazza, Emilia M.C. – sequence: 3 givenname: Giorgia surname: Alvisi fullname: Alvisi, Giorgia – sequence: 4 givenname: Federico S. orcidid: 0000-0003-4480-3481 surname: Colombo fullname: Colombo, Federico S. – sequence: 5 givenname: Andrea orcidid: 0000-0002-6219-0714 surname: Grilli fullname: Grilli, Andrea – sequence: 6 givenname: Joanna surname: Mikulak fullname: Mikulak, Joanna – sequence: 7 givenname: Domenico orcidid: 0000-0001-6147-0952 surname: Mavilio fullname: Mavilio, Domenico – sequence: 8 givenname: Marco surname: Alloisio fullname: Alloisio, Marco – sequence: 9 givenname: Francesco surname: Ferrari fullname: Ferrari, Francesco – sequence: 10 givenname: Egesta surname: Lopci fullname: Lopci, Egesta – sequence: 11 givenname: Pierluigi surname: Novellis fullname: Novellis, Pierluigi – sequence: 12 givenname: Giulia surname: Veronesi fullname: Veronesi, Giulia – sequence: 13 givenname: Enrico orcidid: 0000-0002-1964-7678 surname: Lugli fullname: Lugli, Enrico |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30154266$$D View this record in MEDLINE/PubMed |
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