Freshwater turtles (Trachemys scripta) are among the very few vertebrates capable of tolerating severe hypoxia and reoxygenation without suffering from damage to the heart. As myocardial ischemia and reperfusion causes a burst of mitochondrial reactive oxygen species (ROS) in mammals, the question arises as to whether, and if so how, this ROS burst is prevented in the turtle heart. We find here that heart mitochondria isolated from turtles acclimated to anoxia produce less ROS than mitochondria from normoxic turtles when consuming succinate. As succinate accumulates in the hypoxic heart and is oxidised when oxygen returns this suggest an adaptation to lessen ROS production. Specific S-nitrosation of complex I can lower ROS in mammals and here we show that turtle complex I activity and ROS production can also be strongly depressed in vitro by S-nitrosation. While we can detect in vivo endogenous S-nitrosated complex I in turtle heart mitochondria, these levels are unaffected upon anoxia acclimation. Thus while heart mitochondria from anoxia-acclimated turtles generate less ROS and have a lower aerobic capacity than those from normoxic turtles, this is not due to decreases in complex I activity or expression levels. Interestingly, in-gel activity staining reveals that most complex I of heart mitochondria from normoxic and anoxic turtles forms stable supercomplexes with other respiratory enzymes and, in contrast to mammals, these are not disrupted by dodecyl maltoside. Taken together, these results show that, although S-nitrosation of complex I is a potent mechanism to prevent ROS formation upon reoxygenation after anoxia in vitro, this is not a major cause of the suppression of ROS production by anoxic turtle heart mitochondria.
Suppression of reactive oxygen species generation in heart mitochondria from anoxic turtles: the role of complex I S-nitrosation
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Amanda Bundgaard, Andrew M. James, William Joyce, Michael P. Murphy, Angela Fago; Suppression of reactive oxygen species generation in heart mitochondria from anoxic turtles: the role of complex I S-nitrosation. J Exp Biol 2018; jeb.174391. doi: https://doi.org/10.1242/jeb.174391
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