Deletion of ripA alleviates suppression of the inflammasome and MAPK by Francisella tularensis

Francisella tularensis is a facultative intracellular pathogen and potential biothreat agent. Evasion of the immune response contributes to the extraordinary virulence of this organism although the mechanism is unclear. Whereas wild-type strains induced low levels of cytokines, an F. tularensis ripA...

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Published inThe Journal of immunology (1950) Vol. 185; no. 9; pp. 5476 - 5485
Main Authors Huang, Max Tze-Han, Mortensen, Brittany L, Taxman, Debra J, Craven, Robin R, Taft-Benz, Sharon, Kijek, Todd M, Fuller, James R, Davis, Beckley K, Allen, Irving Coy, Brickey, Willie June, Gris, Denis, Wen, Haitao, Kawula, Thomas H, Ting, Jenny Pan-Yun
Format Journal Article
LanguageEnglish
Published United States 01.11.2010
Subjects
Animals
Bacterial Proteins - genetics
Bacterial Proteins - immunology
Bacterial Proteins - metabolism
Blotting, Western
Cytokines - biosynthesis
Enzyme-Linked Immunosorbent Assay
Female
Francisella tularensis - genetics
Francisella tularensis - immunology
Francisella tularensis - pathogenicity
Genes, Bacterial - genetics
Genes, Bacterial - immunology
Humans
Immune Evasion - genetics
Immune Evasion - immunology
Inflammation - genetics
Inflammation - immunology
Macrophages - immunology
Mice
Mice, Inbred C57BL
Mice, Knockout
Mitogen-Activated Protein Kinases - genetics
Mitogen-Activated Protein Kinases - immunology
Signal Transduction - genetics
Signal Transduction - immunology
Tularemia - genetics
Tularemia - immunology
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Abstract Francisella tularensis is a facultative intracellular pathogen and potential biothreat agent. Evasion of the immune response contributes to the extraordinary virulence of this organism although the mechanism is unclear. Whereas wild-type strains induced low levels of cytokines, an F. tularensis ripA deletion mutant (LVSΔripA) provoked significant release of IL-1β, IL-18, and TNF-α by resting macrophages. IL-1β and IL-18 secretion was dependent on inflammasome components pyrin-caspase recruitment domain/apoptotic speck-containing protein with a caspase recruitment domain and caspase-1, and the TLR/IL-1R signaling molecule MyD88 was required for inflammatory cytokine synthesis. Complementation of LVSΔripA with a plasmid encoding ripA restored immune evasion. Similar findings were observed in a human monocytic line. The presence of ripA nearly eliminated activation of MAPKs including ERK1/2, JNK, and p38, and pharmacologic inhibitors of these three MAPKs reduced cytokine induction by LVSΔripA. Animals infected with LVSΔripA mounted a stronger IL-1β and TNF-α response than that of mice infected with wild-type live vaccine strain. This analysis revealed novel immune evasive mechanisms of F. tularensis.
AbstractList Francisella tularensis is a facultative intracellular pathogen and potential biothreat agent. Evasion of the immune response contributes to the extraordinary virulence of this organism although the mechanism is unclear. Whereas wild-type strains induced low levels of cytokines, an F. tularensis ripA deletion mutant (LVSΔripA) provoked significant release of IL-1β, IL-18, and TNF-α by resting macrophages. IL-1β and IL-18 secretion was dependent on inflammasome components pyrin-caspase recruitment domain/apoptotic speck-containing protein with a caspase recruitment domain and caspase-1, and the TLR/IL-1R signaling molecule MyD88 was required for inflammatory cytokine synthesis. Complementation of LVSΔripA with a plasmid encoding ripA restored immune evasion. Similar findings were observed in a human monocytic line. The presence of ripA nearly eliminated activation of MAPKs including ERK1/2, JNK, and p38, and pharmacologic inhibitors of these three MAPKs reduced cytokine induction by LVSΔripA. Animals infected with LVSΔripA mounted a stronger IL-1β and TNF-α response than that of mice infected with wild-type live vaccine strain. This analysis revealed novel immune evasive mechanisms of F. tularensis.
Francisella tularensis is a facultative intracellular pathogen and potential biothreat agent. Evasion of the immune response contributes to the extraordinary virulence of this organism although the mechanism is unclear. Whereas wild-type strains induced low levels of cytokines, an F. tularensis ripA deletion mutant (LVSΔ ripA ) provoked significant release of IL-1β, IL-18, and TNF-α by resting macrophages. IL-1β and IL-18 secretion was dependent on inflammasome components pyrin-caspase recruitment domain/apoptotic speck-containing protein with a caspase recruitment domain and caspase-1, and the TLR/IL-1R signaling molecule MyD88 was required for inflammatory cytokine synthesis. Complementation of LVSΔ ripA with a plasmid encoding ripA restored immune evasion. Similar findings were observed in a human monocytic line. The presence of ripA nearly eliminated activation of MAPKs including ERK1/2, JNK, and p38, and pharmacologic inhibitors of these three MAPKs reduced cytokine induction by LVSΔ ripA . Animals infected with LVSΔ ripA mounted a stronger IL-1β and TNF-α response than that of mice infected with wild-type live vaccine strain. This analysis revealed novel immune evasive mechanisms of F. tularensis .
Author Ting, Jenny Pan-Yun
Taxman, Debra J
Mortensen, Brittany L
Davis, Beckley K
Huang, Max Tze-Han
Fuller, James R
Kawula, Thomas H
Kijek, Todd M
Brickey, Willie June
Craven, Robin R
Taft-Benz, Sharon
Allen, Irving Coy
Gris, Denis
Wen, Haitao
AuthorAffiliation Lineberger Comprehensive Cancer Center, Institute of Inflammatory Diseases, University of North Carolina, Chapel Hill, NC 27599
Center for Translational Immunology, Institute of Inflammatory Diseases, University of North Carolina, Chapel Hill, NC 27599
Department of Microbiology and Immunology, Institute of Inflammatory Diseases, University of North Carolina, Chapel Hill, NC 27599
AuthorAffiliation_xml – name: Center for Translational Immunology, Institute of Inflammatory Diseases, University of North Carolina, Chapel Hill, NC 27599
– name: Lineberger Comprehensive Cancer Center, Institute of Inflammatory Diseases, University of North Carolina, Chapel Hill, NC 27599
– name: Department of Microbiology and Immunology, Institute of Inflammatory Diseases, University of North Carolina, Chapel Hill, NC 27599
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  article-title: Immunologic consequences of Francisella tularensis live vaccine strain infection: role of the innate immune response in infection and immunity.
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  doi: 10.4049/jimmunol.176.11.6888
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Snippet Francisella tularensis is a facultative intracellular pathogen and potential biothreat agent. Evasion of the immune response contributes to the extraordinary...
Francisella tularensis is a facultative intracellular pathogen and potential biothreat agent. Evasion of the immune response contributes to the extraordinary...
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SubjectTerms Animals
Bacterial Proteins - genetics
Bacterial Proteins - immunology
Bacterial Proteins - metabolism
Blotting, Western
Cytokines - biosynthesis
Enzyme-Linked Immunosorbent Assay
Female
Francisella tularensis - genetics
Francisella tularensis - immunology
Francisella tularensis - pathogenicity
Genes, Bacterial - genetics
Genes, Bacterial - immunology
Humans
Immune Evasion - genetics
Immune Evasion - immunology
Inflammation - genetics
Inflammation - immunology
Macrophages - immunology
Mice
Mice, Inbred C57BL
Mice, Knockout
Mitogen-Activated Protein Kinases - genetics
Mitogen-Activated Protein Kinases - immunology
Signal Transduction - genetics
Signal Transduction - immunology
Tularemia - genetics
Tularemia - immunology
Title Deletion of ripA alleviates suppression of the inflammasome and MAPK by Francisella tularensis
URI https://www.ncbi.nlm.nih.gov/pubmed/20921527
https://search.proquest.com/docview/759874390
https://pubmed.ncbi.nlm.nih.gov/PMC4671501
Volume 185
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