SQR mediates therapeutic effects of H<sub>2</sub>S by targeting mitochondrial electron transport to induce mitochondrial uncoupling.

Jia, Jia; Wang, Zichuang; Zhang, Minjie; Huang, Caiyun; Song, Yanmei; Xu, Fuyou; Zhang, Jingyu; Li, Jie et al. · Sci Adv · 2020

basic_science · Level V

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Abstract

Hydrogen sulfide (H<sub>2</sub>S) is a gasotransmitter and a potential therapeutic agent. However, molecular targets relevant to its therapeutic actions remain enigmatic. Sulfide-quinone oxidoreductase (SQR) irreversibly oxidizes H<sub>2</sub>S. Therefore, SQR is assumed to inhibit H<sub>2</sub>S signaling. We now report that SQR-mediated oxidation of H<sub>2</sub>S drives reverse electron transport (RET) at mitochondrial complex I, which, in turn, repurposes mitochondrial function to superoxide production. Unexpectedly, complex I RET, a process dependent on high mitochondrial membrane potential, induces superoxide-dependent mitochondrial uncoupling and downstream activation of adenosine monophosphate-activated protein kinase (AMPK). SQR-induced mitochondrial uncoupling is separated from the inhibition of mitochondrial complex IV by H<sub>2</sub>S. Moreover, deletion of SQR, complex I, or AMPK abolishes therapeutic effects of H<sub>2</sub>S following intracerebral hemorrhage. To conclude, SQR mediates H<sub>2</sub>S signaling and therapeutic effects by targeting mitochondrial electron transport to induce mitochondrial uncoupling. Moreover, SQR is a previously unrecognized target for developing non-protonophore uncouplers with broad clinical implications.