Campylobacter jejuni regulates cell cycle progression to potentiate host cell invasion

Abstract Background Campylobacter jejuni is associated with enteritis in humans and domestic animals. Acute C. jejuni-mediated enteritis requires bacterial invasion of intestinal cells with an ensuing host inflammatory response. Known is that C. jejuni invasion of human epithelial cells is dependent...

Full description

Saved in:
Bibliographic Details
Main Authors: Prabhat K. Talukdar, Megan C. Dines, Eric A. Shelden, Brandon A. Toy, Amruta Suresh Kale, Ryan R. Driskell, Lisa M. Gloss, Michael E. Konkel
Format: Article
Language:English
Published: BMC 2025-07-01
Series:Cell Communication and Signaling
Subjects:
Online Access:https://doi.org/10.1186/s12964-025-02348-z
Tags: Add Tag
No Tags, Be the first to tag this record!
Description
Summary:Abstract Background Campylobacter jejuni is associated with enteritis in humans and domestic animals. Acute C. jejuni-mediated enteritis requires bacterial invasion of intestinal cells with an ensuing host inflammatory response. Known is that C. jejuni invasion of human epithelial cells is dependent on host cell-focal adhesion components, which link the extracellular matrix to the actin cytoskeleton of a cell. Based on the observation that C. jejuni cell invasion engages many of the same components involved in regulating the cell cycle, we hypothesized that C. jejuni regulates the host cell cycle. Methods Flow cytometry was used to detect the cell cycle phases (G1, S, G2 and M). Single-cell RNA-sequencing (scRNA-seq) and reverse transcriptase quantitative PCR (RT-qPCR) were used to determine the differential gene expressions of uninfected and C. jejuni-infected cells. Infection assays and confocal microscopy were employed to determine the rate of bacterial invasion and intracellular localization of C. jejuni-infected cells. Quantification of Interleukin-8 (IL-8) was determined by the ELISAs. Results INT 407 cells infected with C. jejuni showed a slower rate of cell cycle progression and a greater percentage of cells in the G1 cell cycle phase. scRNA-seq and RT-qPCR analysis of C. jejuni-infected cells corroborated the result, revealing host genes responsive to C. jejuni infection, including genes associated with cell cycle regulation, focal adhesions, inflammatory cytokines, and oxidative stress. Cell cycle synchronization coupled with the gentamicin-protection revealed that C. jejuni preferentially invades cells in the G1 phase. Moreover, an increase was observed in the number of bacteria colocalized with paxillin, a critical component of focal adhesion complexes, during the G1 phase. The infection of INT 407 cells in the G1 phase also increased the secretion of the proinflammatory cytokine IL-8 from cells. Conclusions Based on the data, we propose that acute C. jejuni-mediated enteritis (campylobacteriosis) alters the cell cycle phase of enterocytes, cytokine production, and immune cell recruitment, disrupting the intestinal permeability barrier.
ISSN:1478-811X