Molecular Mechanisms of Inflammasome Activation During Salmonella Infections

NIH RePORTER · NIH · R01 · $384,014 · view on reporter.nih.gov ↗

Abstract

PROJECT SUMMARY Mammals have evolved a number of innate immune defense mechanisms to detect microbial infection and protect the host. Previous studies of have demonstrated that intracellular multiprotein complexes, called inflammasomes, are important for host defense against infections. Inflammasomes sense infectious or noxious stimuli and activate effector proteases caspase-1 (casp-1) and caspase-11 (casp-11). Casp-1 processes pro- inflammatory cytokines IL-1band IL-18 to contribute to pathogen control. Casp-11 detects cytosolic lipopolysaccharide (LPS) and activates a pro-inflammatory cell death pathway termed pyroptosis when host cells are infected with Gram-negative pathogens or during septic shock induced by LPS. An increased understanding of how casp-11 is regulated during Gram-negative bacterial infections is necessary in order to develop new therapeutics to treat these infections. We have used Salmonella enterica serovars, which cause diseases ranging from self-limited gastroenteritis (e.g., S. Typhimurium) to systemic infections (e.g., S. Typhi) in humans, as a model Gram-negative pathogen to elucidate the molecular mechanisms of inflammasome activation. We have shown that intracellular S. Typhimurium (Stm) induce casp-11-dependent macrophage death, which is due to leakage of LPS from the Salmonella containing vacuole (SCV) into the macrophage cytosol. In ongoing experiments, we have found that casp-11 is regulated by both host and pathogen factors. Our preliminary data show that: (1) mouse complement factors regulate casp-11 gene expression, (2) two different casp-11 transcript variants, in addition to the full-length transcript, occur in macrophages treated with LPS, and (3) at least one Stm virulence factor that is translocated into host cells by a type 3 secretion system (T3SS) dampens the activation of casp-11 inflammasomes. These data suggest that the innate immune detection of intracellular Gram-negative bacteria and LPS that leads to casp-11 activation is regulated by the host at multiple levels (e.g., gene transcription, multiple casp-11 variants) and by Stm virulence factors. Given these findings, we hypothesize that specific host proteins direct casp-11 cell death and that Salmonella virulence factors modulate casp-11 activation. These hypotheses will be addressed in the experiments of the following Specific Aims: (1) identify host molecules and pathways involved in casp-11-dependent cell death, (2) characterize the expression and function of casp-11 transcript variants in the context of bacterial infection, and (3) identify Salmonella factors that impact casp-11-dependent cell death. The result of this study will lead to the identification and characterization of new host and bacterial factors that regulate casp-11 during bacterial infections. These findings may lead to novel therapeutics for the treatment of infections with Gram-negative pathogens and sepsis.

Key facts

NIH application ID
9961473
Project number
5R01AI095396-09
Recipient
STANFORD UNIVERSITY
Principal Investigator
Denise M Monack
Activity code
R01
Funding institute
NIH
Fiscal year
2020
Award amount
$384,014
Award type
5
Project period
2011-12-01 → 2022-06-30