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Microtubules provide force to promote membrane uncoating in vacuolar escape for a cyto-invasive bacterial pathogen

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  • Yuen-Yan Chang

    (and CNRS UMR 3691 Université de Paris Cité
    Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health)

  • Camila Valenzuela

    (and CNRS UMR 3691 Université de Paris Cité)

  • Arthur Lensen

    (and CNRS UMR 3691 Université de Paris Cité)

  • Noelia Lopez-Montero

    (and CNRS UMR 3691 Université de Paris Cité)

  • Saima Sidik

    (Dalhousie University)

  • John Salogiannis

    (University of California San Diego
    Howard Hughes Medical Institute
    University of Vermont)

  • Jost Enninga

    (and CNRS UMR 3691 Université de Paris Cité)

  • John Rohde

    (Dalhousie University)

Abstract

Intracellular bacterial pathogens gain entry to mammalian cells inside a vacuole derived from the host membrane. Some of them escape the bacteria-containing vacuole (BCV) and colonize the cytosol. Bacteria replicating within BCVs coopt the microtubule network to position it within infected cells, whereas the role of microtubules for cyto-invasive pathogens remains obscure. Here, we show that the microtubule motor cytoplasmic dynein-1 and specific activating adaptors are hijacked by the enterobacterium Shigella flexneri. These host proteins were found on infection-associated macropinosomes (IAMs) formed during Shigella internalization. We identified Rab8 and Rab13 as mediators of dynein recruitment and discovered that the Shigella effector protein IpaH7.8 promotes Rab13 retention on moving BCV membrane remnants, thereby facilitating membrane uncoating of the Shigella-containing vacuole. Moreover, the efficient unpeeling of BCV remnants contributes to a successful intercellular spread. Taken together, our work demonstrates how a bacterial pathogen subverts the intracellular transport machinery to secure a cytosolic niche.

Suggested Citation

  • Yuen-Yan Chang & Camila Valenzuela & Arthur Lensen & Noelia Lopez-Montero & Saima Sidik & John Salogiannis & Jost Enninga & John Rohde, 2024. "Microtubules provide force to promote membrane uncoating in vacuolar escape for a cyto-invasive bacterial pathogen," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45182-6
    DOI: 10.1038/s41467-024-45182-6
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    1. Amar R. Bhagwat & Valerie Le Sage & Eric Nturibi & Katarzyna Kulej & Jennifer Jones & Min Guo & Eui Tae Kim & Benjamin A. Garcia & Matthew D. Weitzman & Hari Shroff & Seema S. Lakdawala, 2020. "Quantitative live cell imaging reveals influenza virus manipulation of Rab11A transport through reduced dynein association," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    2. 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.
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