Self-Maintaining CD103 + Cancer-Specific T Cells Are Highly Energetic with Rapid Cytotoxic and Effector Responses

Enrichment of CD103 tumor-infiltrating T lymphocytes (TIL) is associated with improved outcomes in patients. However, the characteristics of human CD103 cytotoxic CD8 T cells (CTL) and their role in tumor control remain unclear. We investigated the features and antitumor mechanisms of CD103 CTLs by...

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Veröffentlicht in:Cancer immunology research Jg. 8; H. 2; S. 203
Hauptverfasser: Abd Hamid, Megat, Colin-York, Huw, Khalid-Alham, Nasullah, Browne, Molly, Cerundolo, Lucia, Chen, Ji-Li, Yao, Xuan, Rosendo-Machado, Samara, Waugh, Craig, Maldonado-Perez, David, Bowes, Emma, Verrill, Clare, Cerundolo, Vincenzo, Conlon, Christopher P, Fritzsche, Marco, Peng, Yanchun, Dong, Tao
Format: Journal Article
Sprache:Englisch
Veröffentlicht: United States 01.02.2020
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ISSN:2326-6074, 2326-6074
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Abstract Enrichment of CD103 tumor-infiltrating T lymphocytes (TIL) is associated with improved outcomes in patients. However, the characteristics of human CD103 cytotoxic CD8 T cells (CTL) and their role in tumor control remain unclear. We investigated the features and antitumor mechanisms of CD103 CTLs by assessing T-cell receptor (TCR)-matched CD103 and CD103 cancer-specific CTL immunity and its immunophenotype Interestingly, we found that differentiated CD103 cancer-specific CTLs expressed the active form of TGFβ1 to continually self-regulate CD103 expression, without relying on external TGFβ1-producing cells. The presence of CD103 on CTLs improved TCR antigen sensitivity, which enabled faster cancer recognition and rapid antitumor cytotoxicity. These CD103 CTLs had elevated energetic potential and faster migration capacity. However, they had increased inhibitory receptor coexpression and elevated T-cell apoptosis following prolonged cancer exposure. Our data provide fundamental insights into the properties of matured human CD103 cancer-specific CTLs, which could have important implications for future designs of tissue-localized cancer immunotherapy strategies.
AbstractList Enrichment of CD103+ tumor-infiltrating T lymphocytes (TIL) is associated with improved outcomes in patients. However, the characteristics of human CD103+ cytotoxic CD8+ T cells (CTL) and their role in tumor control remain unclear. We investigated the features and antitumor mechanisms of CD103+ CTLs by assessing T-cell receptor (TCR)-matched CD103+ and CD103- cancer-specific CTL immunity in vitro and its immunophenotype ex vivo Interestingly, we found that differentiated CD103+ cancer-specific CTLs expressed the active form of TGFβ1 to continually self-regulate CD103 expression, without relying on external TGFβ1-producing cells. The presence of CD103 on CTLs improved TCR antigen sensitivity, which enabled faster cancer recognition and rapid antitumor cytotoxicity. These CD103+ CTLs had elevated energetic potential and faster migration capacity. However, they had increased inhibitory receptor coexpression and elevated T-cell apoptosis following prolonged cancer exposure. Our data provide fundamental insights into the properties of matured human CD103+ cancer-specific CTLs, which could have important implications for future designs of tissue-localized cancer immunotherapy strategies.Enrichment of CD103+ tumor-infiltrating T lymphocytes (TIL) is associated with improved outcomes in patients. However, the characteristics of human CD103+ cytotoxic CD8+ T cells (CTL) and their role in tumor control remain unclear. We investigated the features and antitumor mechanisms of CD103+ CTLs by assessing T-cell receptor (TCR)-matched CD103+ and CD103- cancer-specific CTL immunity in vitro and its immunophenotype ex vivo Interestingly, we found that differentiated CD103+ cancer-specific CTLs expressed the active form of TGFβ1 to continually self-regulate CD103 expression, without relying on external TGFβ1-producing cells. The presence of CD103 on CTLs improved TCR antigen sensitivity, which enabled faster cancer recognition and rapid antitumor cytotoxicity. These CD103+ CTLs had elevated energetic potential and faster migration capacity. However, they had increased inhibitory receptor coexpression and elevated T-cell apoptosis following prolonged cancer exposure. Our data provide fundamental insights into the properties of matured human CD103+ cancer-specific CTLs, which could have important implications for future designs of tissue-localized cancer immunotherapy strategies.
Enrichment of CD103 tumor-infiltrating T lymphocytes (TIL) is associated with improved outcomes in patients. However, the characteristics of human CD103 cytotoxic CD8 T cells (CTL) and their role in tumor control remain unclear. We investigated the features and antitumor mechanisms of CD103 CTLs by assessing T-cell receptor (TCR)-matched CD103 and CD103 cancer-specific CTL immunity and its immunophenotype Interestingly, we found that differentiated CD103 cancer-specific CTLs expressed the active form of TGFβ1 to continually self-regulate CD103 expression, without relying on external TGFβ1-producing cells. The presence of CD103 on CTLs improved TCR antigen sensitivity, which enabled faster cancer recognition and rapid antitumor cytotoxicity. These CD103 CTLs had elevated energetic potential and faster migration capacity. However, they had increased inhibitory receptor coexpression and elevated T-cell apoptosis following prolonged cancer exposure. Our data provide fundamental insights into the properties of matured human CD103 cancer-specific CTLs, which could have important implications for future designs of tissue-localized cancer immunotherapy strategies.
Author Conlon, Christopher P
Rosendo-Machado, Samara
Chen, Ji-Li
Peng, Yanchun
Verrill, Clare
Fritzsche, Marco
Colin-York, Huw
Bowes, Emma
Cerundolo, Vincenzo
Abd Hamid, Megat
Maldonado-Perez, David
Dong, Tao
Yao, Xuan
Browne, Molly
Cerundolo, Lucia
Waugh, Craig
Khalid-Alham, Nasullah
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  givenname: Huw
  surname: Colin-York
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  organization: Medical Research Council (MRC) Human Immunology Unit, MRC Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom
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  surname: Rosendo-Machado
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  organization: Medical Research Council (MRC) Human Immunology Unit, MRC Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom
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  fullname: Waugh, Craig
  organization: Flow Cytometry Facility, Weatherall Institute of Molecular Medicine, University of Oxford, Oxford, United Kingdom
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  organization: Nuffield Department of Surgical Sciences, University of Oxford, John Radcliffe Hospital, Oxford, United Kingdom
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  orcidid: 0000-0002-4905-8233
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  orcidid: 0000-0002-3531-2464
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  organization: Chinese Academy of Medical Sciences (CAMS) Oxford Institute, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
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  surname: Fritzsche
  fullname: Fritzsche, Marco
  organization: Kennedy Institute of Rheumatology, University of Oxford, Oxford, United Kingdom
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  givenname: Yanchun
  surname: Peng
  fullname: Peng, Yanchun
  organization: Medical Research Council (MRC) Human Immunology Unit, MRC Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom
– sequence: 17
  givenname: Tao
  surname: Dong
  fullname: Dong, Tao
  email: tao.dong@imm.ox.ac.uk
  organization: Medical Research Council (MRC) Human Immunology Unit, MRC Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom
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Snippet Enrichment of CD103 tumor-infiltrating T lymphocytes (TIL) is associated with improved outcomes in patients. However, the characteristics of human CD103...
Enrichment of CD103+ tumor-infiltrating T lymphocytes (TIL) is associated with improved outcomes in patients. However, the characteristics of human CD103+...
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SubjectTerms Antigens, CD - immunology
Antigens, CD - metabolism
CD8-Positive T-Lymphocytes - immunology
Humans
Immunophenotyping - methods
Integrin alpha Chains - immunology
Integrin alpha Chains - metabolism
Lung Neoplasms - immunology
Lung Neoplasms - metabolism
Lung Neoplasms - pathology
Lymphocytes, Tumor-Infiltrating - immunology
Neoplasms - immunology
Neoplasms - metabolism
Neoplasms - pathology
Prognosis
Receptors, Antigen, T-Cell - genetics
Receptors, Antigen, T-Cell - immunology
T-Lymphocytes, Cytotoxic - immunology
Transforming Growth Factor beta1 - immunology
Transforming Growth Factor beta1 - metabolism
Title Self-Maintaining CD103 + Cancer-Specific T Cells Are Highly Energetic with Rapid Cytotoxic and Effector Responses
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