Blockade of the co-inhibitory molecule PD-1 unleashes ILC2-dependent antitumor immunity in melanoma
Group 2 innate lymphoid cells (ILC2s) are essential to maintain tissue homeostasis. In cancer, ILC2s can harbor both pro-tumorigenic and anti-tumorigenic functions, but we know little about their underlying mechanisms or whether they could be clinically relevant or targeted to improve patient outcom...
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| Published in | Nature immunology Vol. 22; no. 7; pp. 851 - 864 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.07.2021
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1529-2908 1529-2916 1529-2916 |
| DOI | 10.1038/s41590-021-00943-z |
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| Abstract | Group 2 innate lymphoid cells (ILC2s) are essential to maintain tissue homeostasis. In cancer, ILC2s can harbor both pro-tumorigenic and anti-tumorigenic functions, but we know little about their underlying mechanisms or whether they could be clinically relevant or targeted to improve patient outcomes. Here, we found that high ILC2 infiltration in human melanoma was associated with a good clinical prognosis. ILC2s are critical producers of the cytokine granulocyte-macrophage colony-stimulating factor, which coordinates the recruitment and activation of eosinophils to enhance antitumor responses. Tumor-infiltrating ILC2s expressed programmed cell death protein-1, which limited their intratumoral accumulation, proliferation and antitumor effector functions. This inhibition could be overcome in vivo by combining interleukin-33-driven ILC2 activation with programmed cell death protein-1 blockade to significantly increase antitumor responses. Together, our results identified ILC2s as a critical immune cell type involved in melanoma immunity and revealed a potential synergistic approach to harness ILC2 function for antitumor immunotherapies.
Group 2 innate lymphoid cells (ILC2s) are generally considered to have pro-tumor functions. However, Belz and colleagues demonstrate that ILC2s have anti-melanoma effects due to their high production of the inflammatory cytokine granulocyte-macrophage colony-stimulating factor in the tumor microenvironment. |
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| AbstractList | Group 2 innate lymphoid cells (ILC2s) are essential to maintain tissue homeostasis. In cancer, ILC2s can harbor both pro-tumorigenic and anti-tumorigenic functions, but we know little about their underlying mechanisms or whether they could be clinically relevant or targeted to improve patient outcomes. Here, we found that high ILC2 infiltration in human melanoma was associated with a good clinical prognosis. ILC2s are critical producers of the cytokine granulocyte-macrophage colony-stimulating factor, which coordinates the recruitment and activation of eosinophils to enhance antitumor responses. Tumor-infiltrating ILC2s expressed programmed cell death protein-1, which limited their intratumoral accumulation, proliferation and antitumor effector functions. This inhibition could be overcome in vivo by combining interleukin-33-driven ILC2 activation with programmed cell death protein-1 blockade to significantly increase antitumor responses. Together, our results identified ILC2s as a critical immune cell type involved in melanoma immunity and revealed a potential synergistic approach to harness ILC2 function for antitumor immunotherapies. Group 2 innate lymphoid cells (ILC2s) are essential to maintain tissue homeostasis. In cancer, ILC2s can harbor both pro-tumorigenic and anti-tumorigenic functions, but we know little about their underlying mechanisms or whether they could be clinically relevant or targeted to improve patient outcomes. Here, we found that high ILC2 infiltration in human melanoma was associated with a good clinical prognosis. ILC2s are critical producers of the cytokine granulocyte-macrophage colony-stimulating factor, which coordinates the recruitment and activation of eosinophils to enhance antitumor responses. Tumor-infiltrating ILC2s expressed programmed cell death protein-1, which limited their intratumoral accumulation, proliferation and antitumor effector functions. This inhibition could be overcome in vivo by combining interleukin-33-driven ILC2 activation with programmed cell death protein-1 blockade to significantly increase antitumor responses. Together, our results identified ILC2s as a critical immune cell type involved in melanoma immunity and revealed a potential synergistic approach to harness ILC2 function for antitumor immunotherapies. Group 2 innate lymphoid cells (ILC2s) are generally considered to have pro-tumor functions. However, Belz and colleagues demonstrate that ILC2s have anti-melanoma effects due to their high production of the inflammatory cytokine granulocyte-macrophage colony-stimulating factor in the tumor microenvironment. Group 2 innate lymphoid cells (ILC2s) are essential to maintain tissue homeostasis. In cancer, ILC2s can harbor both pro-tumorigenic and anti-tumorigenic functions, but we know little about their underlying mechanisms or whether they could be clinically relevant or targeted to improve patient outcomes. Here, we found that high ILC2 infiltration in human melanoma was associated with a good clinical prognosis. ILC2s are critical producers of the cytokine granulocyte-macrophage colony-stimulating factor, which coordinates the recruitment and activation of eosinophils to enhance antitumor responses. Tumor-infiltrating ILC2s expressed programmed cell death protein-1, which limited their intratumoral accumulation, proliferation and antitumor effector functions. This inhibition could be overcome in vivo by combining interleukin-33-driven ILC2 activation with programmed cell death protein-1 blockade to significantly increase antitumor responses. Together, our results identified ILC2s as a critical immune cell type involved in melanoma immunity and revealed a potential synergistic approach to harness ILC2 function for antitumor immunotherapies. Group 2 innate lymphoid cells (ILC2s) are generally considered to have pro-tumor functions. However, Belz and colleagues demonstrate that ILC2s have anti-melanoma effects due to their high production of the inflammatory cytokine granulocyte-macrophage colony-stimulating factor in the tumor microenvironment. Group 2 innate lymphoid cells (ILC2s) are essential to maintain tissue homeostasis. In cancer, ILC2s can harbor both pro-tumorigenic and anti-tumorigenic functions, but we know little about their underlying mechanisms or whether they could be clinically relevant or targeted to improve patient outcomes. Here, we found that high ILC2 infiltration in human melanoma was associated with a good clinical prognosis. ILC2s are critical producers of the cytokine granulocyte-macrophage colony-stimulating factor, which coordinates the recruitment and activation of eosinophils to enhance antitumor responses. Tumor-infiltrating ILC2s expressed programmed cell death protein-1, which limited their intratumoral accumulation, proliferation and antitumor effector functions. This inhibition could be overcome in vivo by combining interleukin-33-driven ILC2 activation with programmed cell death protein-1 blockade to significantly increase antitumor responses. Together, our results identified ILC2s as a critical immune cell type involved in melanoma immunity and revealed a potential synergistic approach to harness ILC2 function for antitumor immunotherapies.Group 2 innate lymphoid cells (ILC2s) are essential to maintain tissue homeostasis. In cancer, ILC2s can harbor both pro-tumorigenic and anti-tumorigenic functions, but we know little about their underlying mechanisms or whether they could be clinically relevant or targeted to improve patient outcomes. Here, we found that high ILC2 infiltration in human melanoma was associated with a good clinical prognosis. ILC2s are critical producers of the cytokine granulocyte-macrophage colony-stimulating factor, which coordinates the recruitment and activation of eosinophils to enhance antitumor responses. Tumor-infiltrating ILC2s expressed programmed cell death protein-1, which limited their intratumoral accumulation, proliferation and antitumor effector functions. This inhibition could be overcome in vivo by combining interleukin-33-driven ILC2 activation with programmed cell death protein-1 blockade to significantly increase antitumor responses. Together, our results identified ILC2s as a critical immune cell type involved in melanoma immunity and revealed a potential synergistic approach to harness ILC2 function for antitumor immunotherapies. |
| Audience | Academic |
| Author | Thia, Kevin Shi, Wei Munitz, Ariel Nutt, Stephen L. Zhang, Shengbo Chopin, Michael Wicks, Ian P. Gray, Daniel H. D. Neeson, Paul J. de Graaf, Carolyn A. Hansbro, Philip M. Macdonald, Sean Davis, Melissa J. Grisaru-Tal, Sharon Cebon, Jonathan Louis, Cynthia Groom, Joanna R. Trapani, Joseph A. Belz, Gabrielle T. Foster, Paul S. Luong, Kylie Liao, Yang Souza-Fonseca-Guimaraes, Fernando Molden-Hauer, Tristan Behren, Andreas Seillet, Cyril Huang, Qiutong Umansky, Viktor Ciric, Bogoljub Vivier, Eric Camilleri, Mary McKenzie, Andrew N. J. Jacquelot, Nicolas Pizzolla, Angela Hediyeh-zadeh, Soroor Schreuder, Jaring Wang, Minyu |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34099918$$D View this record in MEDLINE/PubMed https://amu.hal.science/hal-03566011$$DView record in HAL |
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| ContentType | Journal Article |
| Copyright | Crown 2021 COPYRIGHT 2021 Nature Publishing Group Crown 2021. Distributed under a Creative Commons Attribution 4.0 International License |
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| DOI | 10.1038/s41590-021-00943-z |
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| SubjectTerms | 631/250/2504/2506 631/67/580/1884 Animals Antibodies - pharmacology Antineoplastic Combined Chemotherapy Protocols - pharmacology Antitumor activity Apoptosis Biomedical and Life Sciences Biomedicine Care and treatment Cell activation Cell death Cell Line, Tumor Cell receptors Chemotaxis, Leukocyte - drug effects Colonies Colony-stimulating factor Cytokines Cytotoxicity, Immunologic - drug effects Development and progression Eosinophils - drug effects Eosinophils - immunology Eosinophils - metabolism Female Genetic aspects Granulocyte-macrophage colony-stimulating factor Granulocyte-Macrophage Colony-Stimulating Factor - genetics Granulocyte-Macrophage Colony-Stimulating Factor - metabolism Granulocytes Health aspects Homeostasis Humans Immune Checkpoint Inhibitors - pharmacology Immune response Immunity Immunology Immunotherapy Infectious Diseases Inflammation Interleukin-33 - pharmacology Leukocytes (eosinophilic) Life Sciences Lymphocytes Lymphocytes - drug effects Lymphocytes - immunology Lymphocytes - metabolism Lymphoid cells Male Melanoma Melanoma, Experimental - drug therapy Melanoma, Experimental - genetics Melanoma, Experimental - immunology Melanoma, Experimental - metabolism Metastases Mice Mice, Inbred C57BL Mice, Knockout PD-1 protein Phenotype Programmed Cell Death 1 Receptor - antagonists & inhibitors Programmed Cell Death 1 Receptor - genetics Programmed Cell Death 1 Receptor - metabolism Skin Neoplasms - drug therapy Skin Neoplasms - genetics Skin Neoplasms - immunology Skin Neoplasms - metabolism Tumor microenvironment |
| Title | Blockade of the co-inhibitory molecule PD-1 unleashes ILC2-dependent antitumor immunity in melanoma |
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