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Mitochondria from the systemic heart of Pacific hagfish (Eptatretus stoutii) are insensitive to one hour of anoxia followed by reoxygenation

Pacific hagfish (Eptatretus stoutii) are an ancient agnathan vertebrate known to be anoxia tolerant. To study their metabolic organization and the role of the mitochondria in anoxia tolerance we developed a novel protocol to measure mitochondrial function in permeabilized cardiomyocytes and how this...

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Published in:Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 2025-01, Vol.275, p.111022, Article 111022
Main Authors: Yutsyschyna, Maria A., Shaftoe, Jared B., Gillis, Todd E.
Format: Article
Language:English
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Summary:Pacific hagfish (Eptatretus stoutii) are an ancient agnathan vertebrate known to be anoxia tolerant. To study their metabolic organization and the role of the mitochondria in anoxia tolerance we developed a novel protocol to measure mitochondrial function in permeabilized cardiomyocytes and how this is affected by one hour of anoxia followed by reoxygenation. When measured at 10 °C the mitochondria had a respiration rate of 2.1 ± 0.1pmol/s/mg WW during OXPHOS with saturating concentrations of glutamate, malate, and succinate. This is comparatively low compared to other ectothermic species. The functional characteristics of the mitochondria were quantified with mitochondrial control ratios. These demonstrated that proton leak contributed to just under 50% of the oxygen flux, with the remainder going towards ATP phosphorylation. Finally, when the preparations were exposed to an anoxia-reoxygenation protocol there was no difference in respiration compared to that of a heart sample from the same animal maintained under normoxia for the same time. When Complex I alone or Complex I and II were stimulated following one hour of anoxia there was no decline in oxygen flux observed. However, if Complex II was activated alone there was a significant decline in respiration. This decrease was however also observed in the mitochondria maintained in normoxia for one hour. In conclusion, Pacific hagfish cardiac mitochondria demonstrated a low rate of oxygen consumption, a loosely coupled electron transfer system, and a resistance to one hour of anoxia. [Display omitted] •First time that mitochondrial function has been measured in hagfish.•The respiration rate of mitochondria in permeabilized hagfish heart tissue is comparatively low compared to that of other ectothermic species.•Mitochondrial proton leak contributed to just under 40% of the O2 flux, with the remainder going towards ATP phosphorylation.•There was no difference in respiration between control preparations and those exposed to one hour of anoxia followed by reoxygenation.
ISSN:1096-4959
1879-1107
1879-1107
DOI:10.1016/j.cbpb.2024.111022