IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45182-6.html
   My bibliography  Save this article

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

Author

Listed:
  • 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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45182-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-45182-6?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    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. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Xiangkai Zhen & Yongyu Wu & Jinli Ge & Jiaqi Fu & Le Ye & Niannian Lin & Zhijie Huang & Zihe Liu & Zhao-qing Luo & Jiazhang Qiu & Songying Ouyang, 2022. "Molecular mechanism of toxin neutralization in the HipBST toxin-antitoxin system of Legionella pneumophila," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Zhengrui Zhang & Jiaqi Fu & Johannes Gregor Matthias Rack & Chuang Li & Jim Voorneveld & Dmitri V. Filippov & Ivan Ahel & Zhao-Qing Luo & Chittaranjan Das, 2024. "Legionella metaeffector MavL reverses ubiquitin ADP-ribosylation via a conserved arginine-specific macrodomain," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Michael Adams & Rahul Sharma & Thomas Colby & Felix Weis & Ivan Matic & Sagar Bhogaraju, 2021. "Structural basis for protein glutamylation by the Legionella pseudokinase SidJ," Nature Communications, Nature, vol. 12(1), pages 1-12, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45182-6. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.