A NOD2-Encoded Toggle Switch Resolves the Host–Microbe Battle Over Cyclic AMP Control

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AI-generated deep summary by claude@2026-07, 2026-07-04 · read from full text

This paper investigates how pathogens hijack macrophages by inducing pathological cyclic AMP (cAMP) surges that impair phagolysosomal killing, a defect related to refractory colitis. Using structural, biochemical, and ultrastructural analyses in primary macrophages and human gut organoid co-cultures, the authors identify a host-encoded NOD2–GIV–Gαi “toggle switch” that enforces a biphasic cAMP program: an early NOD2•GIV assembly allows a brief tolerogenic rise, followed by GIV•Gαi engagement that collapses cAMP to promote phagolysosomal fusion and microbial clearance; they also report that pharmacogenomic perturbations attribute the key lesion in GIV-deficient macrophages to cAMP–PKA hyperactivation rather than EPAC. A stated limitation is that the license selected for the preprint version prevents archiving in PMC, though the full text is available from the preprint server. Relevance to endometriosis: the study focuses on macrophage cAMP control in infection/colitis rather than endometriosis/adenomyosis, and endometriosis or adenomyosis are not explicitly discussed in the provided text.

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Abstract

SUMMARY Pathogens hijack macrophages by triggering pathological cAMP surges that block phagolysosomal killing—a defect mirrored in phagocytes from refractory colitis. We identify a host-encoded, pathogen-specific surge-protector comprised of a three-protein toggle: The innate sensor NOD2 binds and masks an evolutionarily conserved motif in GIV that activates trimeric-GTPase Gαi , enforcing a biphasic surge-to-plunge cAMP-program : early, NOD2•GIV assembly permits a brief, tolerogenic cAMP rise, whereas subsequent GIV•Gαi engagement collapses cAMP to drive phagolysosomal fusion and microbial clearance. Structural, biochemical, and ultrastructural analyses reveal how molecular toggling imposes precise spatial and temporal control. Pharmacogenomic perturbations pinpoint cAMP–PKA hyperactivation as the defining lesion in GIV-deficient macrophages. Functional studies in primary macrophages and human gut organoid co-cultures show that toggling the NOD2•GIV•Gαi-axis is necessary and sufficient to convert tolerant macrophages into microbicidal machines that preserve mucosal barrier integrity. These findings uncover a druggable cAMP-control pathway with therapeutic promise in colitis. GRAPHIC ABSTRACT eTOC Blurb Pathogens hijack macrophages by inducing cAMP surges that help them evade clearance. Anandachar et al. identify a host “toggle switch” in which NOD2 and G proteins compete for GIV, driving a rapid and robust surge-to-plunge transition in cAMP. This temporal switch limits tolerogenic signaling, restores microbial clearance and barrier integrity, and unveils a targetable host pathway in infection and IBD. Highlights Pathogens exploit cAMP surges in macrophages to block phagolysosomal killing of microbes GIV acts as a molecular “toggle” linking NOD2 sensing to Gαi-mediated cAMP control Structural and mutagenesis studies reveal mutually exclusive binding of NOD2 and Gαi to GIV Pharmacogenomic perturbations pinpoint PKA, not EPAC, as the critical downstream effector Organoid co-cultures show NOD2-GIV-PKA crosstalk safeguards microbial clearance and gut barrier integrity
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SUMMARY Pathogens hijack macrophages by triggering pathological cAMP surges that block phagolysosomal killing—a defect mirrored in phagocytes from refractory colitis. We identify a host-encoded, pathogen-specific surge-protector comprised of a three-protein toggle: The innate sensor NOD2 binds and masks an evolutionarily conserved motif in GIV that activates trimeric-GTPase Gαi , enforcing a biphasic surge-to-plunge cAMP-program : early, NOD2•GIV assembly permits a brief, tolerogenic cAMP rise, whereas subsequent GIV•Gαi engagement collapses cAMP to drive phagolysosomal fusion and microbial clearance. Structural, biochemical, and ultrastructural analyses reveal how molecular toggling imposes precise spatial and temporal control. Pharmacogenomic perturbations pinpoint cAMP–PKA hyperactivation as the defining lesion in GIV-deficient macrophages. Functional studies in primary macrophages and human gut organoid co-cultures show that toggling the NOD2•GIV•Gαi-axis is necessary and sufficient to convert tolerant macrophages into microbicidal machines that preserve mucosal barrier integrity. These findings uncover a druggable cAMP-control pathway with therapeutic promise in colitis. GRAPHIC ABSTRACT eTOC Blurb Pathogens hijack macrophages by inducing cAMP surges that help them evade clearance. Anandachar et al. identify a host “toggle switch” in which NOD2 and G proteins compete for GIV, driving a rapid and robust surge-to-plunge transition in cAMP. This temporal switch limits tolerogenic signaling, restores microbial clearance and barrier integrity, and unveils a targetable host pathway in infection and IBD. Highlights Pathogens exploit cAMP surges in macrophages to block phagolysosomal killing of microbes GIV acts as a molecular “toggle” linking NOD2 sensing to Gαi-mediated cAMP control Structural and mutagenesis studies reveal mutually exclusive binding of NOD2 and Gαi to GIV Pharmacogenomic perturbations pinpoint PKA, not EPAC, as the critical downstream effector Organoid co-cultures show NOD2-GIV-PKA crosstalk safeguards microbial clearance and gut barrier integrity Full Text Availability The license terms selected by the author(s) for this preprint version do not permit archiving in PMC. The full text is available from the preprint server.

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