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Subversion of GBP-mediated host defense by E3 ligases acquired during Yersinia pestis evolution

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  • Shiyang Cao

    (Beijing Institute of Microbiology and Epidemiology)

  • Yang Jiao

    (Beijing Institute of Microbiology and Epidemiology)

  • Wei Jiang

    (National Institute of Biological Sciences)

  • Yarong Wu

    (Beijing Institute of Microbiology and Epidemiology)

  • Si Qin

    (Beijing Institute of Microbiology and Epidemiology)

  • Yifan Ren

    (Beijing Institute of Microbiology and Epidemiology)

  • Yang You

    (Beijing Institute of Microbiology and Epidemiology)

  • Yafang Tan

    (Beijing Institute of Microbiology and Epidemiology)

  • Xiao Guo

    (Beijing Institute of Microbiology and Epidemiology)

  • Hongyan Chen

    (Beijing Institute of Microbiology and Epidemiology)

  • Yuan Zhang

    (Beijing Institute of Microbiology and Epidemiology)

  • Gengshan Wu

    (Beijing Institute of Microbiology and Epidemiology)

  • Tong Wang

    (Beijing Institute of Microbiology and Epidemiology)

  • Yazhou Zhou

    (Beijing Institute of Microbiology and Epidemiology)

  • Yajun Song

    (Beijing Institute of Microbiology and Epidemiology)

  • Yujun Cui

    (Beijing Institute of Microbiology and Epidemiology)

  • Feng Shao

    (National Institute of Biological Sciences)

  • Ruifu Yang

    (Beijing Institute of Microbiology and Epidemiology)

  • Zongmin Du

    (Beijing Institute of Microbiology and Epidemiology)

Abstract

Plague has caused three worldwide pandemics in history, including the Black Death in medieval ages. Yersinia pestis, the etiological agent of plague, has evolved a powerful arsenal to disrupt host immune defenses during evolution from enteropathogenic Y. pseudotuberculosis. Here, we find that two functionally redundant E3 ligase of Y. pestis, YspE1 and YspE2, can be delivered via type III secretion injectisome into host cytosol where they ubiquitinate multiple guanylate-binding proteins (GBPs) for proteasomal degradation. However, Y. pseudotuberculosis has no such capability due to lacking functional YspE1/2 homologs. YspE1/2-mediated GBP degradations significantly promote the survival of Y. pestis in macrophages and strongly inhibit inflammasome activation. By contrast, Gbpchr3−/−, chr5−/− macrophages exhibit much lowered inflammasome activation independent of YspE1/2, accompanied with an enhanced replication of Y. pestis. Accordingly, Gbpchr3−/−, chr5−/− mice are more susceptible to Y. pestis. We demonstrate that Y. pestis utilizes E3 ligases to subvert GBP-mediated host defense, which appears to be newly acquired by Y. pestis during evolution.

Suggested Citation

  • Shiyang Cao & Yang Jiao & Wei Jiang & Yarong Wu & Si Qin & Yifan Ren & Yang You & Yafang Tan & Xiao Guo & Hongyan Chen & Yuan Zhang & Gengshan Wu & Tong Wang & Yazhou Zhou & Yajun Song & Yujun Cui & F, 2022. "Subversion of GBP-mediated host defense by E3 ligases acquired during Yersinia pestis evolution," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32218-y
    DOI: 10.1038/s41467-022-32218-y
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    References listed on IDEAS

    as
    1. Daniel L. Zimbler & Jay A. Schroeder & Justin L. Eddy & Wyndham W. Lathem, 2015. "Early emergence of Yersinia pestis as a severe respiratory pathogen," Nature Communications, Nature, vol. 6(1), pages 1-10, November.
    2. Peng Li & Wei Jiang & Qin Yu & Wang Liu & Ping Zhou & Jun Li & Junjie Xu & Bo Xu & Fengchao Wang & Feng Shao, 2017. "Ubiquitination and degradation of GBPs by a Shigella effector to suppress host defence," Nature, Nature, vol. 551(7680), pages 378-383, November.
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