Temperature controls oxidative phosphorylation and reactive oxygen species production through uncoupling in rat skeletal muscle mitochondria

Jarmuszkiewicz, Wiesława; Woyda-Płoszczyca, Andrzej; Kozieł, Agnieszka; Majerczak, Joanna; Zoladz, Jerzy A.

doi:10.1016/j.freeradbiomed.2015.02.012

Cited by 63 publications

(68 citation statements)

References 34 publications

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“…These results indicate that the mitochondrial energy transduction system has to consume more oxygen (+ 20 ± 11% at 25 • C and + 37 ± 13% at 30 • C) so as to oxidize more substrates to sustain the production of a given amount of ATP. The negative impact of temperature on mitochondrial coupling efficiency is likely explained by a thermal effect on the fluidity of the inner membrane and a subsequent increase in proton permeability at high temperature (Chamberlin, 2004;Brown et al, 2007Brown et al, , 2012Monternier et al, 2014;Power et al, 2014;Chung and Schulte, 2015;Jarmuszkiewicz et al, 2015;Zoladz et al, 2016). Nevertheless, our data also indicate that the loss of efficiency is also partly ascribed to a thermal stimulation of the activity of the ETS (Figure 2B).…”

Section: Discussionmentioning

confidence: 45%

Mitochondrial Costs of Being Hot: Effects of Acute Thermal Change on Liver Bioenergetics in Toads (Bufo bufo)

Roussel

Voituron

2020

Front. Physiol.

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Global climatic warming is predicted to drive extreme thermal events, especially in temperate terrestrial environments. Hence, describing how physiological parameters are affected by acute temperature changes would allow us to understand the energy management of organisms facing such non-predictable and constraining events. As mitochondria play a key role in the conversion of energy from food into ATP but also produce harmful reactive oxygen species, the understanding of its functioning is crucial to determine the proximal causes of potential decline in an animal's performance.Here we studied the effects of acute temperature changes (between 20 and 30 • C) on mitochondrial respiration, ATP synthesis rate, oxidative phosphorylation efficiency (ATP/O), and H 2 O 2 generation in isolated liver mitochondria of a terrestrial ectotherm, the common toad (Bufo bufo). Using succinate as the respiratory substrate, we found that the mitochondrial rates of oxygen consumption, ATP synthesis, and H 2 O 2 generation increased as the temperature increased, being 65, 52, and 66% higher at 30 • C than at 20 • C, respectively. We also found that the mitochondrial coupling efficiency (ATP/O) decreased, while the oxidative cost of ATP production (H 2 O 2 /ATP ratio) increased. The present results further indicate that between 40 and 60% of temperature effects on mitochondrial ATP production and H 2 O 2 generation was at minima driven by an action on the oxidative capacity of the mitochondria. These results suggest that B. bufo may need to allocate extra energy to maintain ATP production and protect cells from oxidative stress, reducing the energy allocable performances.

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Section: Discussionmentioning

confidence: 45%

Mitochondrial Costs of Being Hot: Effects of Acute Thermal Change on Liver Bioenergetics in Toads (Bufo bufo)

Roussel

Voituron

2020

Front. Physiol.

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“…Indeed, a temperature‐dependent increase in metabolic flux can increase the potential for oxidative stress via increased cellular respiration and mitochondrial proton leak (Jarmuszkiewicz et al . ), which will in turn exacerbate the heat‐induced pro‐inflammatory response (Bouchama & Knochel, ). In this respect, the brain is particularly vulnerable given its high mitochondrial density, abundance of auto‐oxidizable neurotransmitters (e.g.…”

Section: Introductionmentioning

confidence: 99%

“…However, while the metabolic response to moderate hyperthermia can be beneficial, it can also be deleterious in some conditions, particularly when hyperthermia becomes severe (>2°C increase in core temperature). Indeed, a temperature-dependent increase in metabolic flux can increase the potential for oxidative stress via increased cellular respiration and mitochondrial proton leak (Jarmuszkiewicz et al 2015), which will in turn exacerbate the heat-induced pro-inflammatory response (Bouchama & Knochel, 2002). In this respect, the brain is particularly vulnerable given its high mitochondrial density, abundance of auto-oxidizable neurotransmitters (e.g.…”

Section: Introductionmentioning

confidence: 99%

Cerebral metabolism, oxidation and inflammation in severe passive hyperthermia with and without respiratory alkalosis

Bain

Hoiland

Donnelly

et al. 2020

The Journal of Physiology

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Key points It was unknown whether respiratory alkalosis impacts the global cerebral metabolic response as well as the cerebral pro‐oxidation and inflammatory response in passive hyperthermia. This study demonstrated that the cerebral metabolic rate was increased by ∼20% with passive hyperthermia of up to +2°C oesophageal temperature, and this response was unaffected by respiratory alkalosis. Additionally, the increase in cerebral metabolism did not significantly impact the net cerebral release of oxidative and inflammatory markers. These data indicate that passive heating of up to +2°C core temperature in healthy young men is not enough to confer a major oxidative and inflammatory burden on the brain, but it does markedly increase the cerebral metabolic rate, independently of PnormalaCO2. Abstract There is limited information concerning the impact of arterial PnormalCO2/pH on heat‐induced alteration in cerebral metabolism, as well as on the cerebral oxidative/inflammatory burden of hyperthermia. Accordingly, we sought to address two hypotheses: (1) passive hyperthermia will increase the cerebral metabolic rate of oxygen (CMRO2) consistent with a combined influence of Q10 and respiratory alkalosis; and (2) the net cerebral release of pro‐oxidative and pro‐inflammatory markers will be elevated in hyperthermia, particularly in poikilocapnic hyperthermia. Healthy young men (n = 6) underwent passive heating until an oesophageal temperature of 2°C above resting was reached. At 0.5°C increments in core temperature, CMRO2 was calculated from the product of cerebral blood flow (ultrasound) and the radial artery–jugular venous oxygen content difference (cannulation). Net cerebral glucose/lactate exchange, and biomarkers of oxidative and inflammatory stress were also measured. At +2.0°C oesophageal temperature, arterial PnormalCO2 was restored to normothermic values using end‐tidal forcing. The primary findings were: (1) while CMRO2 was increased (P < 0.05) by ∼20% with hyperthermia of +1.5–2.0°C, this was not influenced by respiratory alkalosis, and (2) although biomarkers of pro‐oxidation and pro‐inflammation were systemically elevated in hyperthermia (P < 0.05), there were no differences in the trans‐cerebral exchange kinetics. These novel data indicate that passive heating of up to +2°C core temperature in healthy young men is not enough to confer a major oxidative and inflammatory burden on the brain, despite it markedly increasing CMRO2, irrespective of arterial pH.

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“…The thermoregulation of oxidative phosphorylation could support our findings. It was reported that increasing temperature increased both respiration and phosphorylation rates in isolated muscle mitochondria of houseflies and rats [42,86]. However, increasing the temperature above 31°C in houseflies or 35°C in rats uncoupled the two processes and reduced mitochondrial oxidative phosphorylation efficiency [42,86].…”

Section: Discussionmentioning

confidence: 99%

“…It was reported that increasing temperature increased both respiration and phosphorylation rates in isolated muscle mitochondria of houseflies and rats [42,86]. However, increasing the temperature above 31°C in houseflies or 35°C in rats uncoupled the two processes and reduced mitochondrial oxidative phosphorylation efficiency [42,86]. Similarly, isolated rat brain mitochondria showed that the respiratory control ratio, which is the product of state 3 (phosphorylating respiration)/state 4 (non-phosphorylating respiration), had a temperature dependent inverted U-shape profile within range with a highest value at (20–25°C) [32].…”

Section: Discussionmentioning

confidence: 99%

Effect of temperature on FAD and NADH-derived signals and neurometabolic coupling in the mouse auditory and motor cortex

Ibrahim

Wang

Lesicko

et al. 2017

Pflugers Arch - Eur J Physiol

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Tight coupling of neuronal metabolism to synaptic activity is critical to ensure that the supply of metabolic substrates meets the demands of neuronal signaling. Given the impact of temperature on metabolism, and the wide fluctuations of brain temperature observed during clinical hypothermia, we examined the effect of temperature on neurometabolic coupling. Intrinsic fluorescence signals of the oxidized form of flavin adenine dinucleotide (FAD) and the reduced form of nicotinamide adenine dinucleotide (NADH), and their ratios, were measured to assess neural metabolic state and local field potentials were recorded to measure synaptic activity in the mouse brain. Brain slice preparations were used to remove the potential impacts of blood flow. Tight coupling between metabolic signals and local field potential amplitudes was observed at a range of temperatures below 29°C. However, above 29 °C, the metabolic and synaptic signatures diverged such that FAD signals were diminished, but local field potentials retained their amplitude. It was also observed that the declines in the FAD signals seen at high temperatures (and hence the decoupling between synaptic and metabolic events), is driven by low FAD availability at high temperatures. These data suggest that neurometabolic coupling, thought to be critical for ensuring the metabolic health of the brain, may show temperature dependence, and is related to temperature-dependent changes in FAD supplies.

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Temperature controls oxidative phosphorylation and reactive oxygen species production through uncoupling in rat skeletal muscle mitochondria

Cited by 63 publications

References 34 publications

Mitochondrial Costs of Being Hot: Effects of Acute Thermal Change on Liver Bioenergetics in Toads (Bufo bufo)

Mitochondrial Costs of Being Hot: Effects of Acute Thermal Change on Liver Bioenergetics in Toads (Bufo bufo)

Cerebral metabolism, oxidation and inflammation in severe passive hyperthermia with and without respiratory alkalosis

Effect of temperature on FAD and NADH-derived signals and neurometabolic coupling in the mouse auditory and motor cortex

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