Intermittent Fasting Results in Tissue-Specific Changes in Bioenergetics and Redox State

Chausse, Bruno; Vieira-Lara, Marcel A.; Sanchez, Angélica Bianchini; Medeiros, Marisa H. G.; Kowaltowski, Alicia J.

doi:10.1371/journal.pone.0120413

Cited by 63 publications

(62 citation statements)

References 39 publications

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“…The increase in state 3 mitochondrial respiration combined with a decrease in state 4 respiration suggests a selective upregulation of the capacity to produce ATP without a concomitant increase in energy expended via proton leak (Kadenbach, ). The state‐specific responses of the mitochondria that we observed during fasting contrast with many studies that show comparable directional changes in state 3 and state 4 respiratory capacities (Brown & Staples, , ; Chausse et al., ). Those studies were in mammals that experience much briefer periods of food limitation in comparison with the fish in this study, which may help explain the differences observed.…”

Section: Discussioncontrasting

confidence: 99%

“…To meet that challenge, animals utilize physiological responses that reduce their metabolic requirements and thus enhance their chance of survival (Secor & Carey, ). A central component of such responses is the alteration of mitochondrial energy metabolism (Bermejo‐Nogales, Calduch‐Giner, & Pérez‐Sánchez, ; Chausse, Vieira‐Lara, Sanchez, Medeiros, & Kowaltowski, ; Monternier, Marmillot, Rouanet, & Roussel, ). However, mitochondria are also a major source of reactive oxygen species (ROS) that have the potential to cause oxidative damage (Brand, ).…”

Section: Introductionmentioning

confidence: 99%

“…Temporary reductions in mitochondrial energy requirements, while providing short‐term energetic benefits, could potentially lead to associated increases in ROS levels, resulting in the long‐term costs of oxidative stress (Schull et al., ; Sorensen et al., ), potentially faster organismal senescence and hence constraints on future life history (Dowling & Simmons, ; Midwood, Larsen, Aarestrup, & Cooke, ; Monaghan, Metcalfe, & Torres, ; Selman, Blount, Nussey, & Speakman, ; Speakman et al., ). However, surprisingly little is known about these interactions as studies of mitochondrial energetics are generally conducted separately from those of ROS production (Sorensen et al., ; Zhang, Wu, & Klaassen, ; but see Brown & Staples, ; Chausse et al., ).…”

Section: Introductionmentioning

confidence: 99%

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Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost

et al. 2018

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Summary Many animals experience periods of food shortage in their natural environment. It has been hypothesised that the metabolic responses of animals to naturally‐occurring periods of food deprivation may have long‐term negative impacts on their subsequent life‐history.In particular, reductions in energy requirements in response to fasting may help preserve limited resources but potentially come at a cost of increased oxidative stress. However, little is known about this trade‐off since studies of energy metabolism are generally conducted separately from those of oxidative stress.Using a novel approach that combines measurements of mitochondrial function with in vivo levels of hydrogen peroxide (H2O2) in brown trout (Salmo trutta), we show here that fasting induces energy savings in a highly metabolically active organ (the liver) but at the cost of a significant increase in H2O2, an important form of reactive oxygen species (ROS).After a 2‐week period of fasting, brown trout reduced their whole‐liver mitochondrial respiratory capacities (state 3, state 4 and cytochrome c oxidase activity), mainly due to reductions in liver size (and hence the total mitochondrial content). This was compensated for at the level of the mitochondrion, with an increase in state 3 respiration combined with a decrease in state 4 respiration, suggesting a selective increase in the capacity to produce ATP without a concomitant increase in energy dissipated through proton leakage. However, the reduction in total hepatic metabolic capacity in fasted fish was associated with an almost two‐fold increase in in vivo mitochondrial H2O2 levels (as measured by the MitoB probe).The resulting increase in mitochondrial ROS, and hence potential risk of oxidative damage, provides mechanistic insight into the trade‐off between the short‐term energetic benefits of reducing metabolism in response to fasting and the potential long‐term costs to subsequent life‐history traits.

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Section: Discussioncontrasting

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost

et al. 2018

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“…S4b). The discrepancy with previous data could be due to the variation of expression patterns of HDAC isoforms among tissues (Chausse, Vieira‐Lara, Sanchez, Medeiros, & Kowaltowski, 2015). …”

Section: Resultscontrasting

confidence: 88%

Ketone body 3‐hydroxybutyrate mimics calorie restriction via the Nrf2 activator, fumarate, in the retina

et al. 2017

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SummaryCalorie restriction (CR) being the most robust dietary intervention provides various health benefits. D‐3‐hydroxybutyrate (3HB), a major physiological ketone, has been proposed as an important endogenous molecule for CR. To investigate the role of 3HB in CR, we investigated potential shared mechanisms underlying increased retinal 3HB induced by CR and exogenously applied 3HB without CR to protect against ischemic retinal degeneration. The repeated elevation of retinal 3HB, with or without CR, suppressed retinal degeneration. Metabolomic analysis showed that the antioxidant pentose phosphate pathway and its limiting enzyme, glucose‐6‐phosphate dehydrogenase (G6PD), were concomitantly preserved. Importantly, the upregulation of nuclear factor erythroid 2 p45‐related factor 2 (Nrf2), a regulator of G6PD, and elevation of the tricarboxylic acid cycle's Nrf2 activator, fumarate, were also shared. Together, our findings suggest that CR provides retinal antioxidative defense by 3HB through the antioxidant Nrf2 pathway via modification of a tricarboxylic acid cycle intermediate during 3HB metabolism.

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“…Because mitochondria are cornerstone organelles implicated in metabolic responses to fasting (Monternier et al, 2014), but also the first site of production of damaging reactive oxygen species (ROS) (Andreyev et al, 2005), direct oxidative costs to prolonged fasting may be expected (e.g. Chausse et al, 2015;Geiger et al, 2012;Sorensen et al, 2006;Wasselin et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

The oxidative debt of fasting: evidence for short to medium-term costs of advanced fasting in adult king penguins

Schull

Viblanc

Stier

et al. 2016

Journal of Experimental Biology

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In response to prolonged periods of fasting, animals have evolved metabolic adaptations helping to mobilize body reserves and/or reduce metabolic rate to ensure a longer usage of reserves. However, those metabolic changes can be associated with higher exposure to oxidative stress, raising the question of how species that naturally fast during their life cycle avoid an accumulation of oxidative damage over time. King penguins repeatedly cope with fasting periods of up to several weeks. Here, we investigated how adult male penguins deal with oxidative stress after an experimentally induced moderate fasting period (PII) or an advanced fasting period (PIII). After fasting in captivity, birds were released to forage at sea. We measured plasmatic oxidative stress on the same individuals at the start and end of the fasting period and when they returned from foraging at sea. We found an increase in activity of the antioxidant enzyme superoxide dismutase along with fasting. However, PIII individuals showed higher oxidative damage at the end of the fast compared with PII individuals. When they returned from re-feeding at sea, all birds had recovered their initial body mass and exhibited low levels of oxidative damage. Notably, levels of oxidative damage after the foraging trip were correlated to the rate of mass gain at sea in PIII individuals but not in PII individuals. Altogether, our results suggest that fasting induces a transitory exposure to oxidative stress and that effort to recover in body mass after an advanced fasting period may be a neglected carryover cost of fasting.

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Intermittent Fasting Results in Tissue-Specific Changes in Bioenergetics and Redox State

Cited by 63 publications

References 39 publications

Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost

Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost

Ketone body 3‐hydroxybutyrate mimics calorie restriction via the Nrf2 activator, fumarate, in the retina

The oxidative debt of fasting: evidence for short to medium-term costs of advanced fasting in adult king penguins

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