Fasting ameliorates oxidative stress: A review of physiological strategies across life history events in wild vertebrates

Ensminger, David C.; Salvador‐Pascual, Andrea; Arango, B. Gabriela; Allen, Kaitlin; Vázquez‐Medina, José Pablo

doi:10.1016/j.cbpa.2021.110929

Cited by 33 publications

(28 citation statements)

References 199 publications

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“…Of the genes evaluated in this study, none varied significantly with the duration of fasting that the animals experienced prior to sample collection. This was surprising due to the potential oxidative cost of fasting and previous reports of adaptive antioxidant responses in fasting NES ( Ensminger et al, 2021 ). Our ability to detect differences in gene expression between early and late fasted seals may have been limited by a small sample size and warrants further investigation.…”

Section: Discussionmentioning

confidence: 92%

“…Under basal conditions, antioxidant enzyme activity was more than fourfold higher in skeletal muscle of adult hooded seals compared to newborn and weaned pups ( Vázquez-Medina et al, 2011c ). High antioxidant expression and activity have also been reported in northern NES, specifically in the context of adaptive responses to apneas and prolonged fasting ( Allen and Vázquez-Medina, 2019 ; Ensminger et al, 2021 ), but have not been extensively profiled across ontogeny.…”

Section: Introductionmentioning

confidence: 99%

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Ontogeny of Carbon Monoxide-Related Gene Expression in a Deep-Diving Marine Mammal

et al. 2021

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Marine mammals such as northern elephant seals (NES) routinely experience hypoxemia and ischemia-reperfusion events to many tissues during deep dives with no apparent adverse effects. Adaptations to diving include increased antioxidants and elevated oxygen storage capacity associated with high hemoprotein content in blood and muscle. The natural turnover of heme by heme oxygenase enzymes (encoded by HMOX1 and HMOX2) produces endogenous carbon monoxide (CO), which is present at high levels in NES blood and has been shown to have cytoprotective effects in laboratory systems exposed to hypoxia. To understand how pathways associated with endogenous CO production and signaling change across ontogeny in diving mammals, we measured muscle CO and baseline expression of 17 CO-related genes in skeletal muscle and whole blood of three age classes of NES. Muscle CO levels approached those of animals exposed to high exogenous CO, increased with age, and were significantly correlated with gene expression levels. Muscle expression of genes associated with CO production and antioxidant defenses (HMOX1, BVR, GPX3, PRDX1) increased with age and was highest in adult females, while that of genes associated with protection from lipid peroxidation (GPX4, PRDX6, PRDX1, SIRT1) was highest in adult males. In contrast, muscle expression of mitochondrial biogenesis regulators (PGC1A, ESRRA, ESRRG) was highest in pups, while genes associated with inflammation (HMOX2, NRF2, IL1B) did not vary with age or sex. Blood expression of genes involved in regulation of inflammation (IL1B, NRF2, BVR, IL10) was highest in pups, while HMOX1, HMOX2 and pro-inflammatory markers (TLR4, CCL4, PRDX1, TNFA) did not vary with age. We propose that ontogenetic upregulation of baseline HMOX1 expression in skeletal muscle of NES may, in part, underlie increases in CO levels and expression of genes encoding antioxidant enzymes. HMOX2, in turn, may play a role in regulating inflammation related to ischemia and reperfusion in muscle and circulating immune cells. Our data suggest putative ontogenetic mechanisms that may enable phocid pups to transition to a deep-diving lifestyle, including high baseline expression of genes associated with mitochondrial biogenesis and immune system activation during postnatal development and increased expression of genes associated with protection from lipid peroxidation in adulthood.

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Section: Discussionmentioning

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Ontogeny of Carbon Monoxide-Related Gene Expression in a Deep-Diving Marine Mammal

et al. 2021

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“…Rodent mitochondria and the brown trout ( Salmo trutta ) exhibited higher levels of released H 2 O 2 when subjected to fasting (Menezes-Filho et al, 2019; Salin et al, 2018; Sorensen et al, 2006). The reduced H 2 O 2 of fasting boas may be due to the low energetic demand during fasting in snakes (Ensminger et al, 2021) and may be related to the remarkable capacity of metabolic regulation in such animals (McCue, 2007). Nevertheless, a two-month period fasting in B. constrictor may not be sufficient time to induce detrimental effects in mitochondria.…”

Section: Discussionmentioning

confidence: 99%

“…However, an excess can exhaust the antioxidant system and promote damage to proteins, lipids, and DNA, leading to oxidative stress (Hamanaka and Chandel, 2010). However, in species adapted to prolonged fasting, including mammalian hibernators, there seem to be mechanisms that allow the mitigation of oxidative stress (Ensminger et al, 2021). Nevertheless, although a robust body of literature exists for the physiological effects of fasting and feeding in snakes (McCue, 2008; Secor, 2009), knowledge of the optimization of metabolism at the subcellular level during periods of fasting or during the metabolic increment after meal intake are lacking (Butler et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Feeding effects on liver mitochondrial bioenergetics of Boa constrictor (Serpentes: Boidae)

Araujo

Sartori

Navarro

et al. 2021

Preprint

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Snakes are interesting examples of overcoming energy metabolism challenges as many species can endure long periods without feeding, and their eventual meals are of reasonably large sizes, thus exhibiting dual extreme adaptations. Consequently, metabolic rate increases considerably to attend to the energetic demand of digestion, absorption and, protein synthesis. These animals should be adapted to transition from these two opposite states of energy fairly quickly, and therefore we investigated mitochondrial function plasticity in these states. Herein we compared liver mitochondrial bioenergetics of the boid snake Boa constrictor during fasting and after meal intake. We fasted the snakes for 60 days, then we fed a subgroup with 30% of their body size and evaluated their maximum postprandial response. We measured liver respiration rates from permeabilized tissue and isolated mitochondria, and from isolated mitochondria, we also measured Ca2+ retention capacity, the release of H2O2, and NAD(P) redox state. Mitochondrial respiration rates were maximized after feeding, reaching until 60% increase from fasting levels when energized with complex I-linked substrates. Interestingly, fasting and fed snakes exhibited similar respiratory control ratios and citrate synthase activity. Furthermore, we found no differences in Ca2+ retention capacity, indicating no increase in susceptibility to mitochondrial permeability transition pore (PTP), or redox state of NAD(P), although fed animals exhibited increases in the release of H2O2. Thus, we conclude that liver mitochondria from B. constrictor snakes increase the maintenance costs during the postprandial period and quickly improve the mitochondrial bioenergetics capacity without compromising the redox balance.

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“…Some results support this idea [15][16][17], while others refute it [18,19]. Increased reproductive effort can promote susceptibility to oxidative stress derived from either exhaustion of antioxidant defenses or dysregulated oxidant generation due to increased metabolic activity, but work with laboratory versus wild animals often yields conflicting results [42]. Moreover, differences in reproductive strategies within wild vertebrates likely result in differential susceptibility to oxidative stress [20][21][22].…”

Section: Oxidative Damage Is a Potential Trade-off Of The Fitness Benefits Associated With Arribada Nestingmentioning

confidence: 99%

Oxidative stress is a potential cost of synchronous nesting in olive ridley sea turtles

Harfush-Melendez

Ensminger

et al. 2021

Preprint

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Olive ridley sea turtles, Lepidochelys olivacea, exhibit a polymorphic reproductive behaviour nesting in solitary or in mass aggregations termed "arribadas", where thousands of turtles nest at once. Arribadas may provide fitness benefits including mate finding during nearshore aggregations and predator satiation at the time of hatching, but the potential costs of arribada nesting remain understudied. To explore the potential trade-offs of the fitness benefits associated with arribada nesting, we collected blood from olive ridley turtles nesting in arribada and solitary. We measured reproductive and metabolic hormones (progesterone, estradiol, testosterone, thyroxine, and triiodothyronine), triglycerides (TG), non-esterified fatty acids (NEFA) and markers of oxidative damage (4-hydroxynonenal, malondialdehyde, protein carbonyls, and nitrotyrosine). Arribada nesters were bigger and had higher levels of progesterone than solitary nesters. Similarly, thyroid hormones were higher in individuals nesting in arribada than in solitary nesters, while TG and NEFA were positively correlated in arribada but not in solitary nesters. Nesting in arribada was associated with increased lipid peroxidation and protein carbonyls compared to solitary nesting. These results suggest that nesting in arribada is potentially more energetically expensive than nesting solitarily, and that oxidative stress may be a trade-off of the fitness benefits associated with arribada nesting.

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Fasting ameliorates oxidative stress: A review of physiological strategies across life history events in wild vertebrates

Cited by 33 publications

References 199 publications

Ontogeny of Carbon Monoxide-Related Gene Expression in a Deep-Diving Marine Mammal

Ontogeny of Carbon Monoxide-Related Gene Expression in a Deep-Diving Marine Mammal

Feeding effects on liver mitochondrial bioenergetics of Boa constrictor (Serpentes: Boidae)

Oxidative stress is a potential cost of synchronous nesting in olive ridley sea turtles

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