E3 ubiquitin ligase Cbl-b negatively regulates C-type lectin receptor–mediated antifungal innate immunity
Activation of various C-type lectin receptors (CLRs) initiates potent proinflammatory responses against various microbial infections. However, how activated CLRs are negatively regulated remains unknown. In this study, we report that activation of CLRs Dectin-2 and Dectin-3 by fungi infections trigg...
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| Published in | The Journal of experimental medicine Vol. 213; no. 8; pp. 1555 - 1570 |
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| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The Rockefeller University Press
25.07.2016
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0022-1007 1540-9538 1540-9538 |
| DOI | 10.1084/jem.20151932 |
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| Abstract | Activation of various C-type lectin receptors (CLRs) initiates potent proinflammatory responses against various microbial infections. However, how activated CLRs are negatively regulated remains unknown. In this study, we report that activation of CLRs Dectin-2 and Dectin-3 by fungi infections triggers them for ubiquitination and degradation in a Syk-dependent manner. Furthermore, we found that E3 ubiquitin ligase Casitas B–lineage lymphoma protein b (Cbl-b) mediates the ubiquitination of these activated CLRs through associating with each other via adapter protein FcR-γ and tyrosine kinase Syk, and then the ubiquitinated CLRs are sorted into lysosomes for degradation by an endosomal sorting complex required for transport (ESCRT) system. Therefore, the deficiency of either Cbl-b or ESCRT subunits significantly decreases the degradation of activated CLRs, thereby resulting in the higher expression of proinflammatory cytokines and inflammation. Consistently, Cbl-b–deficient mice are more resistant to fungi infections compared with wild-type controls. Together, our study indicates that Cbl-b negatively regulates CLR-mediated antifungal innate immunity, which provides molecular insight for designing antifungal therapeutic agents. |
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| AbstractList | Activation of various C-type lectin receptors (CLRs) initiates potent proinflammatory responses against various microbial infections. However, how activated CLRs are negatively regulated remains unknown. In this study, we report that activation of CLRs Dectin-2 and Dectin-3 by fungi infections triggers them for ubiquitination and degradation in a Syk-dependent manner. Furthermore, we found that E3 ubiquitin ligase Casitas B-lineage lymphoma protein b (Cbl-b) mediates the ubiquitination of these activated CLRs through associating with each other via adapter protein FcR-γ and tyrosine kinase Syk, and then the ubiquitinated CLRs are sorted into lysosomes for degradation by an endosomal sorting complex required for transport (ESCRT) system. Therefore, the deficiency of either Cbl-b or ESCRT subunits significantly decreases the degradation of activated CLRs, thereby resulting in the higher expression of proinflammatory cytokines and inflammation. Consistently, Cbl-b-deficient mice are more resistant to fungi infections compared with wild-type controls. Together, our study indicates that Cbl-b negatively regulates CLR-mediated antifungal innate immunity, which provides molecular insight for designing antifungal therapeutic agents. Activation of various C-type lectin receptors (CLRs) initiates potent proinflammatory responses against various microbial infections. However, how activated CLRs are negatively regulated remains unknown. In this study, we report that activation of CLRs Dectin-2 and Dectin-3 by fungi infections triggers them for ubiquitination and degradation in a Syk-dependent manner. Furthermore, we found that E3 ubiquitin ligase Casitas B-lineage lymphoma protein b (Cbl-b) mediates the ubiquitination of these activated CLRs through associating with each other via adapter protein FcR-γ and tyrosine kinase Syk, and then the ubiquitinated CLRs are sorted into lysosomes for degradation by an endosomal sorting complex required for transport (ESCRT) system. Therefore, the deficiency of either Cbl-b or ESCRT subunits significantly decreases the degradation of activated CLRs, thereby resulting in the higher expression of proinflammatory cytokines and inflammation. Consistently, Cbl-b-deficient mice are more resistant to fungi infections compared with wild-type controls. Together, our study indicates that Cbl-b negatively regulates CLR-mediated antifungal innate immunity, which provides molecular insight for designing antifungal therapeutic agents.Activation of various C-type lectin receptors (CLRs) initiates potent proinflammatory responses against various microbial infections. However, how activated CLRs are negatively regulated remains unknown. In this study, we report that activation of CLRs Dectin-2 and Dectin-3 by fungi infections triggers them for ubiquitination and degradation in a Syk-dependent manner. Furthermore, we found that E3 ubiquitin ligase Casitas B-lineage lymphoma protein b (Cbl-b) mediates the ubiquitination of these activated CLRs through associating with each other via adapter protein FcR-γ and tyrosine kinase Syk, and then the ubiquitinated CLRs are sorted into lysosomes for degradation by an endosomal sorting complex required for transport (ESCRT) system. Therefore, the deficiency of either Cbl-b or ESCRT subunits significantly decreases the degradation of activated CLRs, thereby resulting in the higher expression of proinflammatory cytokines and inflammation. Consistently, Cbl-b-deficient mice are more resistant to fungi infections compared with wild-type controls. Together, our study indicates that Cbl-b negatively regulates CLR-mediated antifungal innate immunity, which provides molecular insight for designing antifungal therapeutic agents. Innate immune responses mediated by C-type lectin receptors Dectin-2 and Dectin-3 against fungal infections are negatively regulated by Cbl-b ubiquitination. Activation of various C-type lectin receptors (CLRs) initiates potent proinflammatory responses against various microbial infections. However, how activated CLRs are negatively regulated remains unknown. In this study, we report that activation of CLRs Dectin-2 and Dectin-3 by fungi infections triggers them for ubiquitination and degradation in a Syk-dependent manner. Furthermore, we found that E3 ubiquitin ligase Casitas B–lineage lymphoma protein b (Cbl-b) mediates the ubiquitination of these activated CLRs through associating with each other via adapter protein FcR-γ and tyrosine kinase Syk, and then the ubiquitinated CLRs are sorted into lysosomes for degradation by an endosomal sorting complex required for transport (ESCRT) system. Therefore, the deficiency of either Cbl-b or ESCRT subunits significantly decreases the degradation of activated CLRs, thereby resulting in the higher expression of proinflammatory cytokines and inflammation. Consistently, Cbl-b–deficient mice are more resistant to fungi infections compared with wild-type controls. Together, our study indicates that Cbl-b negatively regulates CLR-mediated antifungal innate immunity, which provides molecular insight for designing antifungal therapeutic agents. Innate immune responses mediated by C-type lectin receptors Dectin-2 and Dectin-3 against fungal infections are negatively regulated by Cbl-b ubiquitination. Activation of various C-type lectin receptors (CLRs) initiates potent proinflammatory responses against various microbial infections. However, how activated CLRs are negatively regulated remains unknown. In this study, we report that activation of CLRs Dectin-2 and Dectin-3 by fungi infections triggers them for ubiquitination and degradation in a Syk-dependent manner. Furthermore, we found that E3 ubiquitin ligase Casitas B-lineage lymphoma protein b (Cbl-b) mediates the ubiquitination of these activated CLRs through associating with each other via adapter protein FcR- gamma and tyrosine kinase Syk, and then the ubiquitinated CLRs are sorted into lysosomes for degradation by an endosomal sorting complex required for transport (ESCRT) system. Therefore, the deficiency of either Cbl-b or ESCRT subunits significantly decreases the degradation of activated CLRs, thereby resulting in the higher expression of proinflammatory cytokines and inflammation. Consistently, Cbl-b-deficient mice are more resistant to fungi infections compared with wild-type controls. Together, our study indicates that Cbl-b negatively regulates CLR-mediated antifungal innate immunity, which provides molecular insight for designing antifungal therapeutic agents. |
| Author | Lin, Xin Jia, Xin-Ming Zhu, Le-Le Zhao, Xue-Qiang Jiang, Yuan-Ying Wang, Ting-Ting Xu, Xia Tang, Bing Luo, Tian-Ming Guo, Ya-Hui Xu, Jin-Fu |
| AuthorAffiliation | 2 Clinical Translational Research Center, Shanghai Pulmonary Hospital, Tongji University School of Medicine, Shanghai 200433, China 3 Department of Respiratory Medicine, Shanghai Pulmonary Hospital, Tongji University School of Medicine, Shanghai 200433, China 6 School of Pharmacy, Second Military Medical University, Shanghai 200433, China 5 Department of Burns, The First Affiliated Hospital of Sun Yat-sen University, Guangzhou 510080, China 4 Department of Molecular and Cellular Oncology, University of Texas MD Anderson Cancer Center, Houston, TX 77030 1 Institute for Immunology, Department of Basic Medical Sciences, Tsinghua University School of Medicine, Beijing 100084, China |
| AuthorAffiliation_xml | – name: 2 Clinical Translational Research Center, Shanghai Pulmonary Hospital, Tongji University School of Medicine, Shanghai 200433, China – name: 5 Department of Burns, The First Affiliated Hospital of Sun Yat-sen University, Guangzhou 510080, China – name: 6 School of Pharmacy, Second Military Medical University, Shanghai 200433, China – name: 4 Department of Molecular and Cellular Oncology, University of Texas MD Anderson Cancer Center, Houston, TX 77030 – name: 3 Department of Respiratory Medicine, Shanghai Pulmonary Hospital, Tongji University School of Medicine, Shanghai 200433, China – name: 1 Institute for Immunology, Department of Basic Medical Sciences, Tsinghua University School of Medicine, Beijing 100084, China |
| Author_xml | – sequence: 1 givenname: Le-Le surname: Zhu fullname: Zhu, Le-Le – sequence: 2 givenname: Tian-Ming orcidid: 0000-0002-6263-7854 surname: Luo fullname: Luo, Tian-Ming – sequence: 3 givenname: Xia surname: Xu fullname: Xu, Xia – sequence: 4 givenname: Ya-Hui orcidid: 0000-0003-1587-4619 surname: Guo fullname: Guo, Ya-Hui – sequence: 5 givenname: Xue-Qiang surname: Zhao fullname: Zhao, Xue-Qiang – sequence: 6 givenname: Ting-Ting surname: Wang fullname: Wang, Ting-Ting – sequence: 7 givenname: Bing surname: Tang fullname: Tang, Bing – sequence: 8 givenname: Yuan-Ying surname: Jiang fullname: Jiang, Yuan-Ying – sequence: 9 givenname: Jin-Fu orcidid: 0000-0002-8039-8973 surname: Xu fullname: Xu, Jin-Fu – sequence: 10 givenname: Xin orcidid: 0000-0003-0956-3654 surname: Lin fullname: Lin, Xin – sequence: 11 givenname: Xin-Ming surname: Jia fullname: Jia, Xin-Ming |
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| Snippet | Activation of various C-type lectin receptors (CLRs) initiates potent proinflammatory responses against various microbial infections. However, how activated... Innate immune responses mediated by C-type lectin receptors Dectin-2 and Dectin-3 against fungal infections are negatively regulated by Cbl-b ubiquitination.... |
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| SubjectTerms | Adaptor Proteins, Signal Transducing - genetics Adaptor Proteins, Signal Transducing - immunology Animals Candida albicans - immunology Candidiasis - genetics Candidiasis - immunology Humans Immunity, Innate Lectins, C-Type - genetics Lectins, C-Type - immunology Mice Mice, Knockout Proteolysis Proto-Oncogene Proteins c-cbl - genetics Proto-Oncogene Proteins c-cbl - immunology Receptors, Immunologic - genetics Receptors, Immunologic - immunology Syk Kinase - genetics Syk Kinase - immunology Ubiquitination - genetics Ubiquitination - immunology |
| Title | E3 ubiquitin ligase Cbl-b negatively regulates C-type lectin receptor–mediated antifungal innate immunity |
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