Document Detail


A Yersinia effector with enhanced inhibitory activity on the NF-κB pathway activates the NLRP3/ASC/caspase-1 inflammasome in macrophages.
MedLine Citation:
PMID:  21533069     Owner:  NLM     Status:  MEDLINE    
Abstract/OtherAbstract:
A type III secretion system (T3SS) in pathogenic Yersinia species functions to translocate Yop effectors, which modulate cytokine production and regulate cell death in macrophages. Distinct pathways of T3SS-dependent cell death and caspase-1 activation occur in Yersinia-infected macrophages. One pathway of cell death and caspase-1 activation in macrophages requires the effector YopJ. YopJ is an acetyltransferase that inactivates MAPK kinases and IKKβ to cause TLR4-dependent apoptosis in naïve macrophages. A YopJ isoform in Y. pestis KIM (YopJ(KIM)) has two amino acid substitutions, F177L and K206E, not present in YopJ proteins of Y. pseudotuberculosis and Y. pestis CO92. As compared to other YopJ isoforms, YopJ(KIM) causes increased apoptosis, caspase-1 activation, and secretion of IL-1β in Yersinia-infected macrophages. The molecular basis for increased apoptosis and activation of caspase-1 by YopJ(KIM) in Yersinia-infected macrophages was studied. Site directed mutagenesis showed that the F177L and K206E substitutions in YopJ(KIM) were important for enhanced apoptosis, caspase-1 activation, and IL-1β secretion. As compared to YopJ(CO92), YopJ(KIM) displayed an enhanced capacity to inhibit phosphorylation of IκB-α in macrophages and to bind IKKβ in vitro. YopJ(KIM) also showed a moderately increased ability to inhibit phosphorylation of MAPKs. Increased caspase-1 cleavage and IL-1β secretion occurred in IKKβ-deficient macrophages infected with Y. pestis expressing YopJ(CO92), confirming that the NF-κB pathway can negatively regulate inflammasome activation. K+ efflux, NLRP3 and ASC were important for secretion of IL-1β in response to Y. pestis KIM infection as shown using macrophages lacking inflammasome components or by the addition of exogenous KCl. These data show that caspase-1 is activated in naïve macrophages in response to infection with a pathogen that inhibits IKKβ and MAPK kinases and induces TLR4-dependent apoptosis. This pro-inflammatory form of apoptosis may represent an early innate immune response to highly virulent pathogens such as Y. pestis KIM that have evolved an enhanced ability to inhibit host signaling pathways.
Authors:
Ying Zheng; Sarit Lilo; Igor E Brodsky; Yue Zhang; Ruslan Medzhitov; Kenneth B Marcu; James B Bliska
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Publication Detail:
Type:  Journal Article; Research Support, N.I.H., Extramural     Date:  2011-04-21
Journal Detail:
Title:  PLoS pathogens     Volume:  7     ISSN:  1553-7374     ISO Abbreviation:  PLoS Pathog.     Publication Date:  2011 Apr 
Date Detail:
Created Date:  2011-05-02     Completed Date:  2011-08-12     Revised Date:  2012-05-10    
Medline Journal Info:
Nlm Unique ID:  101238921     Medline TA:  PLoS Pathog     Country:  United States    
Other Details:
Languages:  eng     Pagination:  e1002026     Citation Subset:  IM    
Affiliation:
Department of Molecular Genetics and Microbiology, Center for Infectious Diseases, Stony Brook University, Stony Brook, New York, United States of America.
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MeSH Terms
Descriptor/Qualifier:
Amino Acid Substitution
Animals
Apoptosis / genetics,  immunology
Bacterial Proteins / genetics,  immunology,  metabolism*
Carrier Proteins / genetics,  immunology,  metabolism*
Caspase 1 / genetics,  immunology,  metabolism*
Cytoskeletal Proteins / genetics,  immunology,  metabolism*
Enzyme Activation / genetics,  immunology
Female
Inflammasomes / genetics,  immunology,  metabolism*
Interleukin-1beta / genetics,  immunology,  metabolism
Macrophages / immunology,  metabolism*,  microbiology
Mice
Mice, Knockout
Mutation, Missense
NF-kappa B / genetics,  immunology,  metabolism*
Toll-Like Receptor 4 / genetics,  immunology,  metabolism
Yersinia pestis / genetics,  immunology,  metabolism*
Yersinia pseudotuberculosis / genetics,  immunology,  metabolism*
Grant Support
ID/Acronym/Agency:
GM066882/GM/NIGMS NIH HHS; P01-AI055621/AI/NIAID NIH HHS; R01 AI043389/AI/NIAID NIH HHS; R01-AI04338/AI/NIAID NIH HHS; R56-AI043389/AI/NIAID NIH HHS; U54-AI057158/AI/NIAID NIH HHS
Chemical
Reg. No./Substance:
0/Bacterial Proteins; 0/CIAS1 protein, mouse; 0/Carrier Proteins; 0/Cytoskeletal Proteins; 0/Inflammasomes; 0/Interleukin-1beta; 0/NF-kappa B; 0/Pycard protein, mouse; 0/Tlr4 protein, mouse; 0/Toll-Like Receptor 4; 0/YopP protein, Yersinia; EC 3.4.22.36/Caspase 1
Comments/Corrections

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