Document Type

Article

Publication Date

2024

DOI

10.1128/mbio.02821-23

Publication Title

mBio

Volume

15

Issue

3

Pages

e0282123

Abstract

The cellular junctional architecture remodeling by Listeria adhesion protein-heat shock protein 60 (LAP-Hsp60) interaction for Listeria monocytogenes (Lm) passage through the epithelial barrier is incompletely understood. Here, using the gerbil model, permissive to internalin (Inl) A/B-mediated pathways like in humans, we demonstrate that Lm crosses the intestinal villi at 48 h post-infection. In contrast, the single isogenic (lap− or ΔinlA) or double (lap−ΔinlA) mutant strains show significant defects. LAP promotes Lm translocation via endocytosis of cell-cell junctional complex in enterocytes that do not display luminal E-cadherin. In comparison, InlA facilitates Lm translocation at cells displaying apical E-cadherin during cell extrusion and mucus expulsion from goblet cells. LAP hijacks caveolar endocytosis to traffic integral junctional proteins to the early and recycling endosomes. Pharmacological inhibition in a cell line and genetic knockout of caveolin-1 in mice prevents LAP-induced intestinal permeability, junctional endocytosis, and Lm translocation. Furthermore, LAP-Hsp60-dependent tight junction remodeling is also necessary for InlA access to E-cadherin for Lm intestinal barrier crossing in InlA-permissive hosts.

Rights

© 2024 Drolia et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International (CC BY 4.0) License.

Data Availability

Article states: "All strains used in this study will be made publicly available upon request."

Original Publication Citation

Drolia, R., Bryant, D. B., Tenguria, S., Jules-Culver, Z. A., Thind, J., Amelunke, B., Liu, D., Gallina, N. L. F., Mishra, K. K., Samaddar, M., Sawale, M. R., Mishra, D. K., Cox, A. D., & Bhunia, A. K. (2024). Listeria adhesion protein orchestrates caveolae-mediated apical junctional remodeling of epithelial barrier for Listeria monocytogenes translocation. mBio, 15(3), 1-25, Article e0282123. https://doi.org/10.1128/mbio.02821-23

ORCID

0000-0002-8405-2961 (Drolia)

Download

Share

 
COinS