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Phosphoribosyl modification of poly-ubiquitin chains at the Legionella-containing vacuole prohibiting autophagy adaptor recognition

Author

Listed:
  • Min Wan

    (Cornell University
    Cornell University)

  • Marena E. Minelli

    (Cornell University
    Cornell University)

  • Qiuye Zhao

    (Cornell University)

  • Shannon Marshall

    (Cornell University)

  • Haiyuan Yu

    (Cornell University
    Cornell University)

  • Marcus Smolka

    (Cornell University
    Cornell University)

  • Yuxin Mao

    (Cornell University
    Cornell University)

Abstract

Ubiquitination is a posttranslational modification in eukaryotes that plays a significant role in the infection of intracellular microbial pathogens, such as Legionella pneumophila. While the Legionella-containing vacuole (LCV) is coated with ubiquitin (Ub), it avoids recognition by autophagy adaptors. Here, we report that the Sdc and Sde families of effectors work together to build ubiquitinated species around the LCV. The Sdc effectors catalyze canonical polyubiquitination directly on host targets or on phosphoribosyl-Ub conjugated to host targets by Sde. Remarkably, Ub moieties within poly-Ub chains are either modified with a phosphoribosyl group by PDE domain-containing effectors or covalently attached to other host substrates via Sde-mediated phosphoribosyl-ubiquitination. Furthermore, these modifications prevent the recognition by Ub adaptors and therefore exclude host autophagy adaptors from the LCV. In this work, we shed light on the nature of the poly-ubiquitinated species present at the surface of the LCV and provide a molecular mechanism for the avoidance of autophagy adaptors by the Ub-decorated LCV.

Suggested Citation

  • Min Wan & Marena E. Minelli & Qiuye Zhao & Shannon Marshall & Haiyuan Yu & Marcus Smolka & Yuxin Mao, 2024. "Phosphoribosyl modification of poly-ubiquitin chains at the Legionella-containing vacuole prohibiting autophagy adaptor recognition," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51273-1
    DOI: 10.1038/s41467-024-51273-1
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    References listed on IDEAS

    as
    1. Jiazhang Qiu & Michael J. Sheedlo & Kaiwen Yu & Yunhao Tan & Ernesto S. Nakayasu & Chittaranjan Das & Xiaoyun Liu & Zhao-Qing Luo, 2016. "Ubiquitination independent of E1 and E2 enzymes by bacterial effectors," Nature, Nature, vol. 533(7601), pages 120-124, May.
    2. Anil Akturk & David J. Wasilko & Xiaochun Wu & Yao Liu & Yong Zhang & Jiazhang Qiu & Zhao-Qing Luo & Katherine H. Reiter & Peter S. Brzovic & Rachel E. Klevit & Yuxin Mao, 2018. "Mechanism of phosphoribosyl-ubiquitination mediated by a single Legionella effector," Nature, Nature, vol. 557(7707), pages 729-733, May.
    3. Sissy Kalayil & Sagar Bhogaraju & Florian Bonn & Donghyuk Shin & Yaobin Liu & Ninghai Gan & Jérôme Basquin & Paolo Grumati & Zhao-Qing Luo & Ivan Dikic, 2018. "Insights into catalysis and function of phosphoribosyl-linked serine ubiquitination," Nature, Nature, vol. 557(7707), pages 734-738, May.
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