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PMID: 20133635 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome.

Miao EA, Mao DP, Yudkovsky N, Bonneau R, Lorang CG, Warren SE, Leaf IA, Aderem A

Abstract

The mammalian innate immune system uses Toll-like receptors (TLRs) and Nod-LRRs (NLRs) to detect microbial components during infection. Often these molecules work in concert; for example, the TLRs can stimulate the production of the proforms of the cytokines IL-1beta and IL-18, whereas certain NLRs trigger their subsequent proteolytic processing via caspase 1. Gram-negative bacteria use type III secretion systems (T3SS) to deliver virulence factors to the cytosol of host cells, where they modulate cell physiology to favor the pathogen. We show here that NLRC4/Ipaf detects the basal body rod component of the T3SS apparatus (rod protein) from S. typhimurium (PrgJ), Burkholderia pseudomallei (BsaK), Escherichia coli (EprJ and EscI), Shigella flexneri (MxiI), and Pseudomonas aeruginosa (PscI). These rod proteins share a sequence motif that is essential for detection by NLRC4; a similar motif is found in flagellin that is also detected by NLRC4. S. typhimurium has two T3SS: Salmonella pathogenicity island-1 (SPI1), which encodes the rod protein PrgJ, and SPI2, which encodes the rod protein SsaI. Although PrgJ is detected by NLRC4, SsaI is not, and this evasion is required for virulence in mice. The detection of a conserved component of the T3SS apparatus enables innate immune responses to virulent bacteria through a single pathway, a strategy that is divergent from that used by plants in which multiple NB-LRR proteins are used to detect T3SS effectors or their effects on cells. Furthermore, the specific detection of the virulence machinery permits the discrimination between pathogenic and nonpathogenic bacteria.

MeSH Terms
Animals Apoptosis Regulatory Proteins/genetics,immunology Bacterial Infections/immunology Bacterial Proteins/genetics,immunology,metabolism Calcium-Binding Proteins/genetics,immunology Caspase 1/immunology,metabolism Immunity, Innate/immunology Membrane Proteins/immunology,metabolism Mice Mice, Inbred C57BL Mice, Knockout Protein Conformation Transfection
Chemicals
Apoptosis Regulatory Proteins Bacterial Proteins Calcium-Binding Proteins Ipaf protein, mouse Membrane Proteins SPI-2 protein, Salmonella Spi1 protein, Salmonella Caspase 1
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Miao Edward A
Institute for Systems Biology, Seattle, WA 98103, USA.
Mao Dat P
Yudkovsky Natalya
Bonneau Richard
Lorang Cynthia G
Warren Sarah E
Leaf Irina A
Aderem Alan
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Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2010-02-16
Epub
2010-00-01
Pages
3076-80
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2840275
Subset
IM
Grants
NIAID NIH HHS · U54 AI057141 · United States
NIAID NIH HHS · R01 AI032972 · United States
NIAID NIH HHS · AI025032 · United States
NIAID NIH HHS · R01 AI052286 · United States
NIAID NIH HHS · U54AI057141 · United States
NIAID NIH HHS · R01 AI025032 · United States
NIAID NIH HHS · K08 AI065878 · United States
NIAID NIH HHS · AI052286 · United States
NIAID NIH HHS · R37 AI025032 · United States
NIAID NIH HHS · AI065878 · United States
NIAID NIH HHS · AI032972 · United States
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