Listeria Adhesion Protein Orchestrates Caveolae-Mediated Apical Junctional Remodeling of Epithelial Barrier for Listeria monocytogenes Translocation

Authors

Rishi Drolia, Old Dominion UniversityFollow
Donald B. Bryant, Eastern Kentucky University
Shivendra Tenguria, Purdue University
Zuri A. Jules-Culver, Old Dominion UniversityFollow
Jessie Thind, Eastern Kentucky University
Breanna Amelunke, Eastern Kentucky University
Donqi Liu, Purdue University
Nicholas L. F. Gallina, Purdue University
Krishna K. Mishra, Purdue University
Manalee Samaddar, Purdue University
Manoj R. Sawale, Purdue University
Dharmendra K. Mishra, Purdue University
Abigail D. Cox, Purdue University
Arun K. Bhunia, Purdue University

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

Repository Citation

Drolia, Rishi; Bryant, Donald B.; Tenguria, Shivendra; Jules-Culver, Zuri A.; Thind, Jessie; Amelunke, Breanna; Liu, Donqi; Gallina, Nicholas L. F.; Mishra, Krishna K.; Samaddar, Manalee; Sawale, Manoj R.; Mishra, Dharmendra K.; Cox, Abigail D.; and Bhunia, Arun K., "Listeria Adhesion Protein Orchestrates Caveolae-Mediated Apical Junctional Remodeling of Epithelial Barrier for Listeria monocytogenes Translocation" (2024). Biological Sciences Faculty Publications. 584.
https://digitalcommons.odu.edu/biology_fac_pubs/584

ORCID

0000-0002-8405-2961 (Drolia)