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Tumor necrosis factor induces pathogenic mitochondrial ROS in tuberculosis through reverse electron transport

Francisco J. Roca, Laura Whitworth, Hiran A. Prag, Michael P. Murphy, Lalita Ramakrishnan

2022Science161 citationsDOIOpen Access PDF

Abstract

Tumor necrosis factor (TNF) is a critical host resistance factor against tuberculosis. However, excess TNF produces susceptibility by increasing mitochondrial reactive oxygen species (mROS), which initiate a signaling cascade to cause pathogenic necrosis of mycobacterium-infected macrophages. In zebrafish, we identified the mechanism of TNF-induced mROS in tuberculosis. Excess TNF in mycobacterium-infected macrophages elevates mROS production by reverse electron transport (RET) through complex I. TNF-activated cellular glutamine uptake leads to an increased concentration of succinate, a Krebs cycle intermediate. Oxidation of this elevated succinate by complex II drives RET, thereby generating the mROS superoxide at complex I. The complex I inhibitor metformin, a widely used antidiabetic drug, prevents TNF-induced mROS and necrosis of Mycobacterium tuberculosis –infected zebrafish and human macrophages; metformin may therefore be useful in tuberculosis therapy.

Topics & Concepts

Tumor necrosis factor alphaReactive oxygen speciesNecrosisGlutamineZebrafishMitochondrionMycobacterium tuberculosisChemistryMitochondrial ROSTuberculosisBiologyMicrobiologyBiochemistryImmunologyMedicinePathologyAmino acidGeneticsGeneNeutrophil, Myeloperoxidase and Oxidative MechanismsImmune Response and InflammationImmune cells in cancer
Tumor necrosis factor induces pathogenic mitochondrial ROS in tuberculosis through reverse electron transport | Litcius