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bioRxiv · 10.1101/2023.03.15.532774

Coxiella burnetii actively blocks IL-17-induced oxidative stress in macrophages

Abstract

Coxiella burnetii is a highly infectious, aerosol-transmitted obligate intracellular bacterium that causes human Q fever and replicates within alveolar macrophages during pulmonary infection. Successful infection requires the C. burnetii Type IVB secretion system (T4BSS), which delivers bacterial effector proteins into the host cytoplasm to remodel host processes and suppress the innate immune response. In the lung, IL-17 promotes antibacterial immunity by activating ACT1-TRAF6-dependent pathways that drive inflammatory gene expression, reactive oxygen species production, and neutrophil recruitment. However, how intracellular pathogens subvert IL-17 signaling pathways to promote survival within macrophages remains poorly understood. Here, we show that C. burnetii evades IL-17-mediated host defense by targeting TRAF6, a central ubiquitin-dependent regulator of innate immune signaling. IL-17 signaling through ACT1-TRAF6 restricts C. burnetii viability in macrophages; however, C. burnetii impairs IL-17-induced NF-{kappa}B and MAPK activation, particularly JNK phosphorylation. C. burnetii T4BSS activity suppresses IL-17-driven reactive oxygen species production and neutrophil recruitment. We identify the C. burnetii T4BSS effector EmcB as a TRAF6-targeting deubiquitinase that disrupts IL-17-dependent antimicrobial and chemotactic responses. Together these findings reveal that C. burnetii downregulates intracellular innate immune signaling by targeting TRAF6, enabling evasion of the macrophage antimicrobial response and limiting neutrophil-mediated immunity. Significance StatementCoxiella burnetii causes Q fever and survives inside macrophages, immune cells that normally help eliminate inhaled pathogens. This study identifies a mechanism by which C. burnetii weakens macrophage defenses. We show that the bacterium disrupts macrophage IL-17 signaling, an immune pathway that promotes inflammatory gene expression, reactive oxygen species production, and neutrophil recruitment. Mechanistically, C. burnetii uses the secreted enzyme EmcB to target TRAF6, a central signaling protein required for IL-17-dependent antimicrobial responses. These findings reveal how an intracellular bacterial pathogen disables a key immune signaling hub to promote survival and limit innate immune activation, providing broader insight into how pathogens manipulate host immunity.

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Clemente, T. M., Augusto, L., Angara, R. K., Gilk, S. D.. 2023-03-15. Coxiella burnetii actively blocks IL-17-induced oxidative stress in macrophages. https://doi.org/10.1101/2023.03.15.532774

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