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    Area of Science:

    • Immunology
    • Cell Biology
    • Microbiology

    Background:

    • Pathogens manipulate host cell signaling, specifically cyclic adenosine monophosphate (cAMP) surges in macrophages, to evade phagolysosomal killing.
    • This cAMP dysregulation is implicated in inflammatory conditions like refractory colitis.

    Purpose of the Study:

    • To identify the host-encoded molecular mechanisms controlling cAMP surges during pathogen interaction.
    • To investigate the therapeutic potential of modulating this pathway in colitis.

    Main Methods:

    • Structural, biochemical, and ultrastructural analyses of protein interactions.
    • Pharmacogenomic perturbations to identify key signaling components.
    • Functional studies using primary macrophages and human gut organoid co-cultures.

    Main Results:

    • A three-protein 'toggle switch' involving NOD2, GIV, and Gαi was identified, regulating cAMP levels.
    • This axis enforces a biphasic cAMP program: an initial rise followed by a rapid plunge, crucial for phagolysosomal fusion.
    • Dysfunction in this pathway leads to cAMP-PKA hyperactivation, impairing microbial clearance.
    • Modulating the NOD2•GIV•Gαi axis restored microbicidal activity and gut barrier integrity in organoid models.

    Conclusions:

    • The NOD2•GIV•Gαi axis represents a critical host-pathogen interaction checkpoint controlling macrophage function.
    • Targeting this druggable cAMP-control pathway holds therapeutic promise for infectious diseases and inflammatory bowel disease (IBD), including colitis.