Glycolysis and Oxidative Phosphorylation Play Critical Roles in Natural Killer Cell Receptor-Mediated Natural Killer Cell Functions
Natural killer (NK) cells are innate lymphocytes that directly kill tumor and pathogen-infected cells upon activation by cytokines and NK cell receptors (NKRs) without previous sensitization. It is known that cell metabolism affects the differentiation and effector functions of immune cells. For ins...
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Published in | Frontiers in immunology Vol. 11; p. 202 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
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Frontiers Media S.A
20.02.2020
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Abstract | Natural killer (NK) cells are innate lymphocytes that directly kill tumor and pathogen-infected cells upon activation by cytokines and NK cell receptors (NKRs) without previous sensitization. It is known that cell metabolism affects the differentiation and effector functions of immune cells. For instance, interleukin-2 and interleukin-15 treatment increases glycolysis and oxidative phosphorylation (OXPHOS) in NK cells to support their effector functions. However, little is known about the metabolic reprogramming of human NK cells upon their activation by NKRs. In this study, we investigated the metabolism of NK cells stimulated via NKRs. We found that NK cells upregulated glycolysis and OXPHOS in response to anti-CD16 antibody or NKG2D ligand engagement. Inhibition of either glycolysis or OXPHOS impaired NK cell production of interferon-γ. Interestingly, inhibition of glycolysis but not OXPHOS decreased NK cell killing and dampened NK cell degranulation and Fas ligand expression, suggesting that glycolysis is more critical for NKR-activated cell cytotoxicity. Thus, our study provides insight into understanding the metabolic requirements underlying different effector functions of human NK cells. |
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AbstractList | Natural killer (NK) cells are innate lymphocytes that directly kill tumor and pathogen-infected cells upon activation by cytokines and NK cell receptors (NKRs) without previous sensitization. It is known that cell metabolism affects the differentiation and effector functions of immune cells. For instance, interleukin-2 and interleukin-15 treatment increases glycolysis and oxidative phosphorylation (OXPHOS) in NK cells to support their effector functions. However, little is known about the metabolic reprogramming of human NK cells upon their activation by NKRs. In this study, we investigated the metabolism of NK cells stimulated via NKRs. We found that NK cells upregulated glycolysis and OXPHOS in response to anti-CD16 antibody or NKG2D ligand engagement. Inhibition of either glycolysis or OXPHOS impaired NK cell production of interferon-γ. Interestingly, inhibition of glycolysis but not OXPHOS decreased NK cell killing and dampened NK cell degranulation and Fas ligand expression, suggesting that glycolysis is more critical for NKR-activated cell cytotoxicity. Thus, our study provides insight into understanding the metabolic requirements underlying different effector functions of human NK cells. Natural killer (NK) cells are innate lymphocytes that directly kill tumor and pathogen-infected cells upon activation by cytokines and NK cell receptors (NKRs) without previous sensitization. It is known that cell metabolism affects the differentiation and effector functions of immune cells. For instance, interleukin−2 and interleukin−15 treatment increases glycolysis and oxidative phosphorylation (OXPHOS) in NK cells to support their effector functions. However, little is known about the metabolic reprogramming of human NK cells upon their activation by NKRs. In this study, we investigated the metabolism of NK cells stimulated via NKRs. We found that NK cells upregulated glycolysis and OXPHOS in response to anti-CD16 antibody or NKG2D ligand engagement. Inhibition of either glycolysis or OXPHOS impaired NK cell production of interferon-γ. Interestingly, inhibition of glycolysis but not OXPHOS decreased NK cell killing and dampened NK cell degranulation and Fas ligand expression, suggesting that glycolysis is more critical for NKR-activated cell cytotoxicity. Thus, our study provides insight into understanding the metabolic requirements underlying different effector functions of human NK cells. |
Author | Guan, Di Wang, Shu Xu, Shengli Wang, Zixi Chai, Louis Yi Ann Lam, Kong-Peng |
AuthorAffiliation | 5 Division of Infectious Diseases, University Medicine Cluster, National University Health System , Singapore , Singapore 7 Department of Physiology, Yong Loo Lin School of Medicine, National University of Singapore , Singapore , Singapore 4 Department of Biological Sciences, National University of Singapore , Singapore , Singapore 1 Department of Microbiology and Immunology, Yong Loo Lin School of Medicine, National University of Singapore , Singapore , Singapore 3 NUS Graduate School for Integrative Sciences & Engineering (NGS), National University of Singapore , Singapore , Singapore 6 Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore , Singapore , Singapore 2 Bioprocessing Technology Institute, Agency for Science, Technology and Research , Singapore , Singapore |
AuthorAffiliation_xml | – name: 4 Department of Biological Sciences, National University of Singapore , Singapore , Singapore – name: 1 Department of Microbiology and Immunology, Yong Loo Lin School of Medicine, National University of Singapore , Singapore , Singapore – name: 2 Bioprocessing Technology Institute, Agency for Science, Technology and Research , Singapore , Singapore – name: 7 Department of Physiology, Yong Loo Lin School of Medicine, National University of Singapore , Singapore , Singapore – name: 5 Division of Infectious Diseases, University Medicine Cluster, National University Health System , Singapore , Singapore – name: 6 Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore , Singapore , Singapore – name: 3 NUS Graduate School for Integrative Sciences & Engineering (NGS), National University of Singapore , Singapore , Singapore |
Author_xml | – sequence: 1 givenname: Zixi surname: Wang fullname: Wang, Zixi organization: Bioprocessing Technology Institute, Agency for Science, Technology and Research, Singapore, Singapore – sequence: 2 givenname: Di surname: Guan fullname: Guan, Di organization: NUS Graduate School for Integrative Sciences & Engineering (NGS), National University of Singapore, Singapore, Singapore – sequence: 3 givenname: Shu surname: Wang fullname: Wang, Shu organization: Department of Biological Sciences, National University of Singapore, Singapore, Singapore – sequence: 4 givenname: Louis Yi Ann surname: Chai fullname: Chai, Louis Yi Ann organization: Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore – sequence: 5 givenname: Shengli surname: Xu fullname: Xu, Shengli organization: Department of Physiology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore – sequence: 6 givenname: Kong-Peng surname: Lam fullname: Lam, Kong-Peng organization: Bioprocessing Technology Institute, Agency for Science, Technology and Research, Singapore, Singapore |
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Copyright | Copyright © 2020 Wang, Guan, Wang, Chai, Xu and Lam. Copyright © 2020 Wang, Guan, Wang, Chai, Xu and Lam. 2020 Wang, Guan, Wang, Chai, Xu and Lam |
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Keywords | anti-tumor natural killer cells CD16 NKG2D cell metabolism glycolysis |
Language | English |
License | Copyright © 2020 Wang, Guan, Wang, Chai, Xu and Lam. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by: Eleanor Riley, University of Edinburgh, United Kingdom Reviewed by: Alexander Steinle, Goethe University Frankfurt, Germany; Subramaniam Malarkannan, Medical College of Wisconsin, United States This article was submitted to NK and Innate Lymphoid Cell Biology, a section of the journal Frontiers in Immunology |
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SubjectTerms | anti-tumor Antibodies - immunology Antibodies - pharmacology Blood Donors CD16 Cell Degranulation cell metabolism Cells, Cultured Cytotoxicity, Immunologic - drug effects Fas Ligand Protein - metabolism glycolysis Glycolysis - drug effects GPI-Linked Proteins - immunology Humans Immunology Interferon-gamma - biosynthesis Killer Cells, Natural - immunology Killer Cells, Natural - metabolism Ligands Lymphocyte Activation - drug effects natural killer cells NK Cell Lectin-Like Receptor Subfamily K - metabolism NKG2D Oxidative Phosphorylation - drug effects Receptors, IgG - immunology Receptors, Natural Killer Cell - metabolism |
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Title | Glycolysis and Oxidative Phosphorylation Play Critical Roles in Natural Killer Cell Receptor-Mediated Natural Killer Cell Functions |
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