Regulation of host innate and adaptive immunity by bacterial type III effectors

NIH RePORTER · NIH · R01 · $361,861 · view on reporter.nih.gov ↗

Abstract

Type III secretion (T3S) systems are used by bacterial pathogens to translocate effectors into infected host cells to promote virulence. T3S can also trigger compensatory innate immune responses that can protect the infected host. For example, T3S can trigger inflammasome assembly in infected host cells, resulting in cell death and secretion of cytokines. Virulent pathogens must therefore inhibit protective compensatory host immune responses triggered by T3S. The long-term objective of this project is to understand how a T3S system in the bacterial pathogen Yersinia initially triggers and subsequently inhibits host inflammasomes. A possible link between a human genetic autoinflammatory disease and resistance to Yersinia infection is also explored. The T3S effector YopE is a GTPase-activation protein (GAP) that promotes Yersinia virulence by deactivating RhoA to inhibit phagocytosis. YopE RhoA GAP activity was recently shown to trigger the pyrin inflammasome in macrophages. Bacterial toxins that covalently inactivate RhoA are known to trigger the pryin inflammasome, via a regulatory mechanism that uses the kinase PRK. Specifically, active RhoA positively regulates PRK by allosteric interaction and PRK negatively controls pyrin by phosphorylation. Triggering of the pryin inflammasome by the YopE GAP is unexpected because published data indicated that this response required covalent inactivation of RhoA. It is unknown if YopE triggers the pyrin inflammasome by the same mechanism as toxins that covalently inactivate RhoA, and it is unclear if other bacterial RhoA GAPs induce this response. Aim 1 will test the hypothesis that YopE, other bacterial GAPs, and toxins that covalently modify RhoA, trigger the pryin inflammasome by a conserved allosteric mechanism of PRK inactivation. The T3S effector YopM promotes Yersinia virulence by inhibiting inflammasomes. It has recently been discovered that YopM inhibits pyrin, allowing Yersinia to bypass YopE-triggered inflammasomes. Mechanistically, YopM hijacks PRK to maintain pyrin in a phosphorylated and inactive state. Published data obtained using knock out mouse lines in Yersinia infection assays suggest that YopM targets inflammatory monocytes to promote Yersinia virulence. Aim 2 will test the hypothesis that Yersinia virulence requires YopM to inhibit activation of pyrin in inflammatory monocytes. Codon changes in the gene Mefv, which encodes pyrin, are responsible for the human autoinflammatory disease Familial Mediterranean Fever (FMF). It has been suggested that the high carrier frequency of FMF in Mediterranean and Middle Eastern populations has resulted from a selective advantage in resistance to an unknown infection. Aim 3 will test the hypothesis that FMF pyrin variants, which trigger constitutive inflammasome activation, provide host resistance to Yersinia pestis infection.

Key facts

NIH application ID
10137878
Project number
5R01AI099222-10
Recipient
DARTMOUTH COLLEGE
Principal Investigator
James B Bliska
Activity code
R01
Funding institute
NIH
Fiscal year
2021
Award amount
$361,861
Award type
5
Project period
2012-05-01 → 2022-09-19