Dataset Information

Electron transfer and ROS production in brain mitochondria of intertidal and subtidal triplefin fish (Tripterygiidae).

ABSTRACT: While oxygen is essential for oxidative phosphorylation, O₂ can form reactive species (ROS) when interacting with electrons of mitochondrial electron transport system. ROS is dependent on O₂ pressure (PO₂) and has traditionally been assessed in O₂ saturated media, PO₂ at which mitochondria do not typically function in vivo. Mitochondrial ROS can be significantly elevated by the respiratory complex II substrate succinate, which can accumulate within hypoxic tissues, and this is exacerbated further with reoxygenation. Intertidal species are repetitively exposed to extreme O₂ fluctuations, and have likely evolved strategies to avoid excess ROS production. We evaluated mitochondrial electron leakage and ROS production in permeabilized brain of intertidal and subtidal triplefin fish species from hyperoxia to anoxia, and assessed the effect of anoxia reoxygenation and the influence of increasing succinate concentrations. At typical intracellular PO₂, net ROS production was similar among all species; however at elevated PO₂, brain tissues of the intertidal triplefin fish released less ROS than subtidal species. In addition, following in vitro anoxia reoxygenation, electron transfer mediated by succinate titration was better directed to respiration, and not to ROS production for intertidal species. Overall, these data indicate that intertidal triplefin fish species better manage electrons within the ETS, from hypoxic-hyperoxic transitions.

SUBMITTER: Devaux JBL

PROVIDER: S-EPMC10299943 | biostudies-literature | 2023 Aug

REPOSITORIES: biostudies-literature

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Electron transfer and ROS production in brain mitochondria of intertidal and subtidal triplefin fish (Tripterygiidae).

Devaux Jules B L JBL Hedges Chris P CP Birch Nigel N Herbert Neill N Renshaw Gillian M C GMC Hickey Anthony J R AJR

Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology 20230505 4

While oxygen is essential for oxidative phosphorylation, O2 can form reactive species (ROS) when interacting with electrons of mitochondrial electron transport system. ROS is dependent on O2 pressure (PO2) and has traditionally been assessed in O2 saturated media, PO2 at which mitochondria do not typically function in vivo. Mitochondrial ROS can be significantly elevated by the respiratory complex II substrate succinate, which can accumulate ...[more]

PMID: 37145369

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Project description:The vertebrate brain is generally very sensitive to acidosis, so a hypoxia-induced decrease in pH is likely to have an effect on brain mitochondria (mt). Mitochondrial respiration (JO2) is required to generate an electrical gradient (ΔΨm) and a pH gradient to power ATP synthesis, yet the impact of pH modulation on brain mt function remains largely unexplored. As intertidal fishes within rock pools routinely experience hypoxia and reoxygenation, they would most likely experience changes in cellular pH. We hence compared four New Zealand triplefin fish species ranging from intertidal hypoxia-tolerant species (HTS) to subtidal hypoxia-sensitive species (HSS). We predicted that HTS would tolerate acidosis better than HSS in terms of sustaining mt structure and function. Using respirometers coupled to fluorimeters and pH electrodes, we titrated lactic-acid to decrease the pH of the media, and simultaneously recorded JO2, ΔΨm, and H+ buffering capacities within permeabilized brain and swelling of mt isolated from non-permeabilized brains. We then measured ATP synthesis rates in the most HTS (Bellapiscus medius) and the HSS (Forsterygion varium) at pH 7.25 and 6.65. Mitochondria from HTS brain did have greater H+ buffering capacities than HSS mt (∼10 mU pH.mgprotein -1). HTS mt swelled by 40% when exposed to a decrease of 1.5 pH units, and JO2 was depressed by up to 15% in HTS. However, HTS were able to maintain ΔΨm near -120 mV. Estimates of work, in terms of charges moved across the mt inner-membrane, suggested that with acidosis, HTS mt may in part harness extra-mt H+ to maintain ΔΨm, and could therefore support ATP production. This was confirmed with elevated ATP synthesis rates and enhanced P:O ratios at pH 6.65 relative to pH 7.25. In contrast, mt volumes and ΔΨm decreased downward pH 6.9 in HSS mt and paradoxically, JO2 increased (∼25%) but ATP synthesis and P:O ratios were depressed at pH 6.65. This indicates a loss of coupling in the HSS with acidosis. Overall, the mt of these intertidal fish have adaptations that enhance ATP synthesis efficiency under acidic conditions such as those that occur in hypoxic or reoxygenated brain.

Project description:IntroductionIncidents of myocardial infarction and sudden cardiac arrest vary with time of the day, but the mechanism for this effect is not clear. We hypothesized that diurnal changes in the ability of cardiac mitochondria to control calcium homeostasis dictate vulnerability to cardiovascular events.ObjectivesHere we investigate mitochondrial calcium dynamics, respiratory function, and reactive oxygen species (ROS) production in mouse heart during different phases of wake versus sleep periods.MethodsWe assessed time-of-the-day dependence of calcium retention capacity of isolated heart mitochondria from young male C57BL6 mice. Rhythmicity of mitochondrial-dependent oxygen consumption, ROS production and transmembrane potential in homogenates were explored using the Oroboros O2k Station equipped with a fluorescence detection module. Changes in expression of essential clock and calcium dynamics genes/proteins were also determined at sleep versus wake time points.ResultsOur results demonstrate that cardiac mitochondria exhibit higher calcium retention capacity and higher rates of calcium uptake during sleep period. This was associated with higher expression of clock gene Bmal1, lower expression of per2, greater expression of MICU1 gene (mitochondrial calcium uptake 1), and lower expression of the mitochondrial transition pore regulator gene cyclophilin D. Protein levels of mitochondrial calcium uniporter (MCU), MICU2, and sodium/calcium exchanger (NCLX) were also higher at sleep onset relative to wake period. While complex I and II-dependent oxygen utilization and transmembrane potential of cardiac mitochondria were lower during sleep, ROS production was increased presumably due to mitochondrial calcium sequestration.ConclusionsTaken together, our results indicate that retaining mitochondrial calcium in the heart during sleep dissipates membrane potential, slows respiratory activities, and increases ROS levels, which may contribute to increased vulnerability to cardiac stress during sleep-wake transition. This pronounced daily oscillations in mitochondrial functions pertaining to stress vulnerability may at least in part explain diurnal prevalence of cardiac pathologies.

Dataset Information

Electron transfer and ROS production in brain mitochondria of intertidal and subtidal triplefin fish (Tripterygiidae).

Publications

Electron transfer and ROS production in brain mitochondria of intertidal and subtidal triplefin fish (Tripterygiidae).

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