Enterohemorrhagic Escherichia coli Tir inhibits TAK1 activation and mediates immune evasion

Many pathogens infect hosts through various immune evasion strategies. However, the molecular mechanisms by which pathogen proteins modulate and evade the host immune response remain unclear. Enterohemorrhagic Escherichia coli (EHEC) is a pathological strain that can induce mitogen-activated protein...

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Main Authors: Ruixue Zhou, Zijuan Chen, Doudou Hao, Yu Wang, Yihua Zhang, Xianfu Yi, Liang-Dong Lyu, Haipeng Liu, Quanming Zou, Yiwei Chu, Baoxue Ge, Dapeng Yan
Format: Article
Language:English
Published: Taylor & Francis Group 2019-01-01
Series:Emerging Microbes and Infections
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Online Access:https://www.tandfonline.com/doi/10.1080/22221751.2019.1620589
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author Ruixue Zhou
Zijuan Chen
Doudou Hao
Yu Wang
Yihua Zhang
Xianfu Yi
Liang-Dong Lyu
Haipeng Liu
Quanming Zou
Yiwei Chu
Baoxue Ge
Dapeng Yan
author_facet Ruixue Zhou
Zijuan Chen
Doudou Hao
Yu Wang
Yihua Zhang
Xianfu Yi
Liang-Dong Lyu
Haipeng Liu
Quanming Zou
Yiwei Chu
Baoxue Ge
Dapeng Yan
author_sort Ruixue Zhou
collection DOAJ
description Many pathogens infect hosts through various immune evasion strategies. However, the molecular mechanisms by which pathogen proteins modulate and evade the host immune response remain unclear. Enterohemorrhagic Escherichia coli (EHEC) is a pathological strain that can induce mitogen-activated protein (MAP) kinase (Erk, Jnk and p38 MAPK) and NF-κB pathway activation and proinflammatory cytokine production, which then causes diarrheal diseases such as hemorrhagic colitis and hemolytic uremic syndrome. Transforming growth factor β-activated kinase-1 (TAK1) is a key regulator involved in distinct innate immune signalling pathways. Here we report that EHEC translocated intimin receptor (Tir) protein inhibits the expression of EHEC-induced proinflammatory cytokines by interacting with the host tyrosine phosphatase SHP-1, which is dependent on the phosphorylation of immunoreceptor tyrosine-based inhibition motifs (ITIMs). Mechanistically, the association of EHEC Tir with SHP-1 facilitated the recruitment of SHP-1 to TAK1 and inhibited TAK1 phosphorylation, which then negatively regulated K63-linked polyubiquitination of TAK1 and downstream signal transduction. Taken together, these results suggest that EHEC Tir negatively regulates proinflammatory responses by inhibiting the activation of TAK1, which is essential for immune evasion and could be a potential target for the treatment of bacterial infection.
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spelling doaj-art-9ae96192bf31483494a8b7ee9a4bdb452025-08-20T03:17:32ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512019-01-018173474810.1080/22221751.2019.1620589Enterohemorrhagic Escherichia coli Tir inhibits TAK1 activation and mediates immune evasionRuixue Zhou0Zijuan Chen1Doudou Hao2Yu Wang3Yihua Zhang4Xianfu Yi5Liang-Dong Lyu6Haipeng Liu7Quanming Zou8Yiwei Chu9Baoxue Ge10Dapeng Yan11Department of Immunology, School of Basic Medical Sciences & Shanghai Public Health Clinical Center, Key Laboratory of Medical Molecular Virology of MOE/MOH, Fudan University, Shanghai, People’s Republic of ChinaDepartment of Immunology, School of Basic Medical Sciences & Shanghai Public Health Clinical Center, Key Laboratory of Medical Molecular Virology of MOE/MOH, Fudan University, Shanghai, People’s Republic of ChinaDepartment of Immunology, School of Basic Medical Sciences & Shanghai Public Health Clinical Center, Key Laboratory of Medical Molecular Virology of MOE/MOH, Fudan University, Shanghai, People’s Republic of ChinaDepartment of Microbiology and Biochemical Pharmacy, National Engineering Research Centre of Immunological Products, College of Pharmacy, Army Medical University, Chongqing, People’s Republic of ChinaDepartment of Immunology, School of Basic Medical Sciences & Shanghai Public Health Clinical Center, Key Laboratory of Medical Molecular Virology of MOE/MOH, Fudan University, Shanghai, People’s Republic of ChinaSchool of Biomedical Engineering, Tianjin Medical University, Tianjin, People’s Republic of ChinaDepartment of Immunology, School of Basic Medical Sciences & Shanghai Public Health Clinical Center, Key Laboratory of Medical Molecular Virology of MOE/MOH, Fudan University, Shanghai, People’s Republic of ChinaShanghai Key Laboratory of Tuberculosis, Shanghai Pulmonary Hospital, Tongji University School of Medicine, Shanghai, People’s Republic of ChinaDepartment of Microbiology and Biochemical Pharmacy, National Engineering Research Centre of Immunological Products, College of Pharmacy, Army Medical University, Chongqing, People’s Republic of ChinaDepartment of Immunology, School of Basic Medical Sciences & Shanghai Public Health Clinical Center, Key Laboratory of Medical Molecular Virology of MOE/MOH, Fudan University, Shanghai, People’s Republic of ChinaShanghai Key Laboratory of Tuberculosis, Shanghai Pulmonary Hospital, Tongji University School of Medicine, Shanghai, People’s Republic of ChinaDepartment of Immunology, School of Basic Medical Sciences & Shanghai Public Health Clinical Center, Key Laboratory of Medical Molecular Virology of MOE/MOH, Fudan University, Shanghai, People’s Republic of ChinaMany pathogens infect hosts through various immune evasion strategies. However, the molecular mechanisms by which pathogen proteins modulate and evade the host immune response remain unclear. Enterohemorrhagic Escherichia coli (EHEC) is a pathological strain that can induce mitogen-activated protein (MAP) kinase (Erk, Jnk and p38 MAPK) and NF-κB pathway activation and proinflammatory cytokine production, which then causes diarrheal diseases such as hemorrhagic colitis and hemolytic uremic syndrome. Transforming growth factor β-activated kinase-1 (TAK1) is a key regulator involved in distinct innate immune signalling pathways. Here we report that EHEC translocated intimin receptor (Tir) protein inhibits the expression of EHEC-induced proinflammatory cytokines by interacting with the host tyrosine phosphatase SHP-1, which is dependent on the phosphorylation of immunoreceptor tyrosine-based inhibition motifs (ITIMs). Mechanistically, the association of EHEC Tir with SHP-1 facilitated the recruitment of SHP-1 to TAK1 and inhibited TAK1 phosphorylation, which then negatively regulated K63-linked polyubiquitination of TAK1 and downstream signal transduction. Taken together, these results suggest that EHEC Tir negatively regulates proinflammatory responses by inhibiting the activation of TAK1, which is essential for immune evasion and could be a potential target for the treatment of bacterial infection.https://www.tandfonline.com/doi/10.1080/22221751.2019.1620589EHECTirITIMSHP-1TAK1immune evasion
spellingShingle Ruixue Zhou
Zijuan Chen
Doudou Hao
Yu Wang
Yihua Zhang
Xianfu Yi
Liang-Dong Lyu
Haipeng Liu
Quanming Zou
Yiwei Chu
Baoxue Ge
Dapeng Yan
Enterohemorrhagic Escherichia coli Tir inhibits TAK1 activation and mediates immune evasion
Emerging Microbes and Infections
EHEC
Tir
ITIM
SHP-1
TAK1
immune evasion
title Enterohemorrhagic Escherichia coli Tir inhibits TAK1 activation and mediates immune evasion
title_full Enterohemorrhagic Escherichia coli Tir inhibits TAK1 activation and mediates immune evasion
title_fullStr Enterohemorrhagic Escherichia coli Tir inhibits TAK1 activation and mediates immune evasion
title_full_unstemmed Enterohemorrhagic Escherichia coli Tir inhibits TAK1 activation and mediates immune evasion
title_short Enterohemorrhagic Escherichia coli Tir inhibits TAK1 activation and mediates immune evasion
title_sort enterohemorrhagic escherichia coli tir inhibits tak1 activation and mediates immune evasion
topic EHEC
Tir
ITIM
SHP-1
TAK1
immune evasion
url https://www.tandfonline.com/doi/10.1080/22221751.2019.1620589
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