Environmental conditions can modulate the links among oxidative stress, age, and longevity

Marasco, Valeria; Stier, Antoine; Boner, Winnie; Griffiths, Kate; Heidinger, Britt J.; Monaghan, Patricia

doi:10.1016/j.mad.2017.04.012

Cited by 37 publications

(35 citation statements)

References 55 publications

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“…This low-dose exposure resulted in an extended lifespan, comparable to our heat-stress survival assay, showing a slightly increased stress resistance after 0.01 mM PQ exposure, suggesting a mitohormetic effect [61, 62]. Generally, a close relation between elevated reactive oxygen species and shortened lifespan expectancy can be drawn throughout investigations and species [63, 64], which is in line with our findings.…”

Section: Discussionsupporting

confidence: 89%

Mitochondrial Oxidative Stress Impairs Energy Metabolism and Reduces Stress Resistance and Longevity ofC. elegans

Dilberger

Baumanns

Schmitt

et al. 2019

Oxidative Medicine and Cellular Longevity

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Introduction Mitochondria supply cellular energy and are key regulators of intrinsic cell death and consequently affect longevity. The nematode Caenorhabditis elegans is frequently used for lifespan assays. Using paraquat (PQ) as a generator of reactive oxygen species, we here describe its effects on the acceleration of aging and the associated dysfunctions at the level of mitochondria. Methods Nematodes were incubated with various concentrations of paraquat in a heat-stress resistance assay (37°C) using nucleic staining. The most effective concentration was validated under physiological conditions, and chemotaxis was assayed. Mitochondrial membrane potential (ΔΨm) was measured using rhodamine 123, and activity of respiratory chain complexes determined using a Clark-type electrode in isolated mitochondria. Energetic metabolites in the form of pyruvate, lactate, and ATP were determined using commercial kits. Mitochondrial integrity and structure was investigated using transmission electron microscopy. Live imaging after staining with fluorescent dyes was used to measure mitochondrial and cytosolic ROS. Expression of longevity- and mitogenesis-related genes were evaluated using qRT-PCR. Results PQ (5 mM) significantly increased ROS formation in nematodes and reduced the chemotaxis, the physiological lifespan, and the survival in assays for heat-stress resistance. The number of fragmented mitochondria significantly increased. The ∆Ψm, the activities of complexes I-IV of the mitochondrial respiratory chain, and the levels of pyruvate and lactate were significantly reduced, whereas ATP production was not affected. Transcript levels of genetic marker genes, atfs-1, atp-2, skn-1, and sir-2.1, were significantly upregulated after PQ incubation, which implicates a close connection between mitochondrial dysfunction and oxidative stress response. Expression levels of aak-2 and daf-16 were unchanged. Conclusion Using paraquat as a stressor, we here describe the association of oxidative stress, restricted energy metabolism, and reduced stress resistance and longevity in the nematode Caenorhabditis elegans making it a readily accessible in vivo model for mitochondrial dysfunction.

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Section: Discussionsupporting

confidence: 89%

Mitochondrial Oxidative Stress Impairs Energy Metabolism and Reduces Stress Resistance and Longevity ofC. elegans

Dilberger

Baumanns

Schmitt

et al. 2019

Oxidative Medicine and Cellular Longevity

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“…Mitochondrial function was however not affected by acute restraint-stress. King penguins seem therefore well equipped to buffer potential oxidative damage arising from acute stress or high GC exposure, which contrasts to what has been found in many other animals to date 9,11,18,20–22 . Most of our knowledge so far on the mechanisms linking acute/chronic stress or high GC exposure to oxidative stress comes from laboratory animals adapted to unchallenging controlled environments.…”

Section: Discussionmentioning

confidence: 72%

“…However, the relationship between baseline GC levels and fitness is not consistent 8 , and little is known about the physiological pathways relating GCs to individual fitness. Recently, oxidative stress has been suggested as one important down-stream consequence of chronically elevated baseline GC levels, with potential consequences on fitness 9–11 . Oxidative stress is a complex, multi-faceted state that arises in organisms as a consequence of the imbalance between the production of pro-oxidant molecules and antioxidant defences 12,13 .…”

Section: Introductionmentioning

confidence: 99%

Oxidative stress and mitochondrial responses to stress exposure suggest that king penguins are naturally equipped to resist stress

Stier

Schull

Bize

et al. 2019

Sci Rep

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Exposure to unpredictable environmental stressors could influence animal health and fitness by inducing oxidative stress, potentially through downstream effects of glucocorticoid stress hormones ( e.g . corticosterone) on mitochondrial function. Yet, it remains unclear whether species that have evolved in stochastic and challenging environments may present adaptations to alleviate the effects of stress exposure on oxidative stress. We tested this hypothesis in wild king penguins by investigating mitochondrial and oxidative stress responses to acute restraint-stress, and their relationships with baseline (potentially mirroring exposure to chronic stress) and stress-induced increase in corticosterone levels. Acute restraint-stress did not significantly influence mitochondrial function. However, acute restraint-stress led to a significant increase in endogenous antioxidant defences, while oxidative damage levels were mostly not affected or even decreased. High baseline corticosterone levels were associated with an up-regulation of the glutathione antioxidant system and a decrease in mitochondrial efficiency. Both processes might contribute to prevent oxidative damage, potentially explaining the negative relationship observed between baseline corticosterone and plasma oxidative damage to proteins. While stress exposure can represent an oxidative challenge for animals, protective mechanisms like up-regulating antioxidant defences and decreasing mitochondrial efficiency seem to occur in king penguins, allowing them to cope with their stochastic and challenging environment.

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“…reduced growth rate (Saino et al 2005) and altered immune function (Rubolini et al 2005). Chronic exposure to stress/high glucocorticoid levels can also lead to oxidative stress (imbalance between free radicals and antioxidant defences) (Costantini et al 2011; Marasco et al 2017), and accordingly, predator cues have been shown to induce an oxidative stress response in an amphibian species (Pinya et al 2016). Additionally, parents may reduce their provisioning rates when predators are present (Tilgar et al 2011; Zanette et al 2011; but see Hakkarainen et al 2002; Thomson et al 2010).…”

Section: Introductionmentioning

confidence: 99%

Impact of continuous predator threat on telomere dynamics in parent and nestling pied flycatchers

et al. 2019

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In addition to direct mortality, predators can have indirect effects on prey populations by affecting prey behaviour or physiology. For example, predator presence can increase stress hormone levels, which can have physiological costs. Stress exposure accelerates the shortening of telomeres (i.e. the protective caps of chromosomes) and shorter telomeres have been linked to increased mortality risk. However, the effect of perceived predation risk on telomeres is not known. We investigated the effects of continuous predator threat (nesting Eurasian pygmy owl Glaucidium passerinum) on telomere dynamics of both adult and partially cross-fostered nestling pied flycatchers (Ficedula hypoleuca) in the wild. Females nesting at owl-inhabited sites showed impaired telomere maintenance between incubation and chick rearing compared to controls, and both males and females ended up with shorter telomeres at owl-inhabited sites in the end of chick rearing. On the contrary, both original and cross-fostered chicks reared in owl sites had consistently longer telomeres during growth than chicks reared at control sites. Thus, predation risk may cause a long-term cost in terms of telomeres for parents but not for their offspring. Predators may therefore affect telomere dynamics of their preys, which could have implications for their ageing rate and consequently for population dynamics.Electronic supplementary materialThe online version of this article (10.1007/s00442-019-04529-3) contains supplementary material, which is available to authorized users.

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Environmental conditions can modulate the links among oxidative stress, age, and longevity

Cited by 37 publications

References 55 publications

Mitochondrial Oxidative Stress Impairs Energy Metabolism and Reduces Stress Resistance and Longevity ofC. elegans

Mitochondrial Oxidative Stress Impairs Energy Metabolism and Reduces Stress Resistance and Longevity ofC. elegans

Oxidative stress and mitochondrial responses to stress exposure suggest that king penguins are naturally equipped to resist stress

Impact of continuous predator threat on telomere dynamics in parent and nestling pied flycatchers

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