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The SUMOylation of TAB2 mediated by TRIM60 inhibits MAPK/NF-κB activation and the innate immune response

Activation of the TAK1 signalosome is crucial for mediating the innate immune response to pathogen invasion and is regulated by multiple layers of posttranslational modifications, including ubiquitination, SUMOylation, and phosphorylation; however, the underlying molecular mechanism is not fully und...

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Autores principales: Gu, Zhiwen, Chen, Xueying, Yang, Wenyong, Qi, Yu, Yu, Hui, Wang, Xiaomeng, Gong, Yanqiu, Chen, Qianqian, Zhong, Bo, Dai, Lunzhi, Qi, Shiqian, Zhang, Zhiqiang, Zhang, Huiyuan, Hu, Hongbo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8322076/
https://www.ncbi.nlm.nih.gov/pubmed/33184450
http://dx.doi.org/10.1038/s41423-020-00564-w
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author Gu, Zhiwen
Chen, Xueying
Yang, Wenyong
Qi, Yu
Yu, Hui
Wang, Xiaomeng
Gong, Yanqiu
Chen, Qianqian
Zhong, Bo
Dai, Lunzhi
Qi, Shiqian
Zhang, Zhiqiang
Zhang, Huiyuan
Hu, Hongbo
author_facet Gu, Zhiwen
Chen, Xueying
Yang, Wenyong
Qi, Yu
Yu, Hui
Wang, Xiaomeng
Gong, Yanqiu
Chen, Qianqian
Zhong, Bo
Dai, Lunzhi
Qi, Shiqian
Zhang, Zhiqiang
Zhang, Huiyuan
Hu, Hongbo
author_sort Gu, Zhiwen
collection PubMed
description Activation of the TAK1 signalosome is crucial for mediating the innate immune response to pathogen invasion and is regulated by multiple layers of posttranslational modifications, including ubiquitination, SUMOylation, and phosphorylation; however, the underlying molecular mechanism is not fully understood. In this study, TRIM60 negatively regulated the formation and activation of the TAK1 signalosome. Deficiency of TRIM60 in macrophages led to enhanced MAPK and NF-κB activation, accompanied by elevated levels of proinflammatory cytokines but not IFN-I. Immunoprecipitation-mass spectrometry assays identified TAB2 as the target of TRIM60 for SUMOylation rather than ubiquitination, resulting in impaired formation of the TRAF6/TAB2/TAK1 complex and downstream MAPK and NF-κB pathways. The SUMOylation sites of TAB2 mediated by TRIM60 were identified as K329 and K562; substitution of these lysines with arginines abolished the SUMOylation of TAB2. In vivo experiments showed that TRIM60-deficient mice showed an elevated immune response to LPS-induced septic shock and L. monocytogenes infection. Our data reveal that SUMOylation of TAB2 mediated by TRIM60 is a novel mechanism for regulating the innate immune response, potentially paving the way for a new strategy to control antibacterial immune responses.
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spelling pubmed-83220762021-08-02 The SUMOylation of TAB2 mediated by TRIM60 inhibits MAPK/NF-κB activation and the innate immune response Gu, Zhiwen Chen, Xueying Yang, Wenyong Qi, Yu Yu, Hui Wang, Xiaomeng Gong, Yanqiu Chen, Qianqian Zhong, Bo Dai, Lunzhi Qi, Shiqian Zhang, Zhiqiang Zhang, Huiyuan Hu, Hongbo Cell Mol Immunol Article Activation of the TAK1 signalosome is crucial for mediating the innate immune response to pathogen invasion and is regulated by multiple layers of posttranslational modifications, including ubiquitination, SUMOylation, and phosphorylation; however, the underlying molecular mechanism is not fully understood. In this study, TRIM60 negatively regulated the formation and activation of the TAK1 signalosome. Deficiency of TRIM60 in macrophages led to enhanced MAPK and NF-κB activation, accompanied by elevated levels of proinflammatory cytokines but not IFN-I. Immunoprecipitation-mass spectrometry assays identified TAB2 as the target of TRIM60 for SUMOylation rather than ubiquitination, resulting in impaired formation of the TRAF6/TAB2/TAK1 complex and downstream MAPK and NF-κB pathways. The SUMOylation sites of TAB2 mediated by TRIM60 were identified as K329 and K562; substitution of these lysines with arginines abolished the SUMOylation of TAB2. In vivo experiments showed that TRIM60-deficient mice showed an elevated immune response to LPS-induced septic shock and L. monocytogenes infection. Our data reveal that SUMOylation of TAB2 mediated by TRIM60 is a novel mechanism for regulating the innate immune response, potentially paving the way for a new strategy to control antibacterial immune responses. Nature Publishing Group UK 2020-11-12 2021-08 /pmc/articles/PMC8322076/ /pubmed/33184450 http://dx.doi.org/10.1038/s41423-020-00564-w Text en © The Author(s) 2020 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Gu, Zhiwen
Chen, Xueying
Yang, Wenyong
Qi, Yu
Yu, Hui
Wang, Xiaomeng
Gong, Yanqiu
Chen, Qianqian
Zhong, Bo
Dai, Lunzhi
Qi, Shiqian
Zhang, Zhiqiang
Zhang, Huiyuan
Hu, Hongbo
The SUMOylation of TAB2 mediated by TRIM60 inhibits MAPK/NF-κB activation and the innate immune response
title The SUMOylation of TAB2 mediated by TRIM60 inhibits MAPK/NF-κB activation and the innate immune response
title_full The SUMOylation of TAB2 mediated by TRIM60 inhibits MAPK/NF-κB activation and the innate immune response
title_fullStr The SUMOylation of TAB2 mediated by TRIM60 inhibits MAPK/NF-κB activation and the innate immune response
title_full_unstemmed The SUMOylation of TAB2 mediated by TRIM60 inhibits MAPK/NF-κB activation and the innate immune response
title_short The SUMOylation of TAB2 mediated by TRIM60 inhibits MAPK/NF-κB activation and the innate immune response
title_sort sumoylation of tab2 mediated by trim60 inhibits mapk/nf-κb activation and the innate immune response
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8322076/
https://www.ncbi.nlm.nih.gov/pubmed/33184450
http://dx.doi.org/10.1038/s41423-020-00564-w
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