Role of ZBP1 in pathogenesis of Salmonella biofilms

NIH RePORTER · AI · R01 · $834,784 · view on reporter.nih.gov ↗

Abstract

PROJECT SUMMARY Infections with enteric pathogens such as Salmonella, Campylobacter, Shigella, or Yersinia are leading causes of morbidity and mortality worldwide. Although in most individuals the infection resolves, approximately 5% of patients subsequently develop a painful chronic inflammatory condition known as Reactive Arthritis (ReA). How Salmonella infections trigger ReA is not well understood. Using Salmonella enterica serovar Typhimurium (STm) as a model organism, we discovered that a Salmonella protein, curli, is a dominant instigator of inflammation following Salmonella infection. Curli is a secreted protein and major component of the STm biofilm in the gastrointestinal tract. Curli fibrils bind extruded bacterial DNA within the biofilm. It is these curli:DNA complexes, rather than curli alone, that are potent triggers of type I interferon, IL-17, and anti-double stranded DNA autoantibody production, leading to ReA. Unknown, however, is why curli:DNA complexes are so inflammatory. We report in this proposal the remarkable discovery that the DNA present within curli:DNA complexes is not solely B-DNA, the classic right-handed (Watson-Crick) double-helix, but includes copious amounts of left-handed Z-DNA as well. Z-form nucleic acids, such as Z-DNA and Z-RNA, were thought not to readily occur in nature, until we showed last year that Z-RNA is indeed produced during virus infections and is a ligand for the necroptosis-activating host sensor protein ZBP1. Our preliminary results now show that the Z-DNA within curli:DNA complexes activates ZBP1 in intestinal epithelial cells (IECs) and fibroblasts, resulting in RIPK3- dependent necroptosis of these cells. These findings allow us to put forward the hypothesis that Z-DNA within curli:DNA fibrils in Salmonella biofilms activates ZBP1 to instigate RIPK3-dependent necroptosis in intestinal epithelial cells (IECs) and other cell types. Necroptosis, in turn, causes cell loss and disrupts gut barrier integrity, releasi

Key facts

NIH application ID
11325302
Project number
5R01AI171568-04
Recipient
RESEARCH INST OF FOX CHASE CAN CTR
Principal Investigator
SIDDHARTH BALACHANDRAN; Cagla Tukel
Activity code
R01
Funding institute
AI
Fiscal year
2026
Award amount
$834,784
Award type
5
Project period
2023-05-11T00:00:00 → 2028-04-30T00:00:00