Chronic stress, energy transduction, and free-radical production in a reptile

Abstract

Stress hormones, such as corticosterone, play a crucial role in orchestrating physiological reaction patterns shaping adapted responses to stressful environments. Concepts aiming at predicting individual and population responses to environmental stress typically consider that stress hormones and their effects on metabolic rate provide appropriate proxies for the energy budget. However, uncoupling between the biochemical processes of respiration, ATP production, and free-radical production in mitochondria may play a fundamental role in the stress response and associated life histories. In this study, we aim at dissecting sub-cellular mechanisms that link these three processes by investigating both whole-organism metabolism, liver mitochondrial oxidative phosphorylation processes (O consumption and ATP production) and ROS emission in Zootoca vivipara individuals exposed 21 days to corticosterone relative to a placebo. Corticosterone enhancement had no effect on mitochondrial activity and efficiency. In parallel, the corticosterone treatment increased liver mass and mitochondrial protein content suggesting a higher liver ATP production. We also found a negative correlation between mitochondrial ROS emission and plasma corticosterone level. These results provide a proximal explanation for enhanced survival after chronic exposure to corticosterone in this species. Importantly, none of these modifications affected resting whole-body metabolic rate. Oxygen consumption, ATP, and ROS emission were thus independently affected in responses to corticosterone increase suggesting that concepts and models aiming at linking environmental stress and individual responses may misestimate energy allocation possibilities.

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

“…The role of mitochondrial uncoupling ( i.e . decreased efficiency) as a potential mechanism of oxidative stress prevention during chronic stress exposure deserves further investigation, especially in the light of a recent study showing a reduced ROS production in response to CORT treatment despite no effect on mitochondrial bioenergetics in captive lizards 65 . Experimental manipulations of GC levels ( e.g .…”

Is there an oxidative cost of acute stress? Characterization, implication of glucocorticoids and modulation by prior stress experience

“…Since mitochondria, which are the main sources of cellular ROS [31], possess glucocorticoid receptors [32], one possibility is that during acute stress, mitochondrial oxygen consumption and total energy expenditure increase, leading to a higher production of ROS [33]. However, these effects may be taxon-dependent, since a recent study in lizards showed that exogenous corticosterone supplementation was actually able to decrease mitochondrial ROS production [34]. The effect of glucocorticoids on mitochondria is still under extensive research and may be just one of several mechanisms behind how glucocorticoids could cause a shift into a state of oxidative stress.…”

Chronic elevation of glucorticoids late in life generates long lasting changes in physiological state without a life history switch

“…In the common lizard, the effect of the corticosterone on metabolism can be condition-dependent as well. Indeed, Meylan et al (2010) found an increase of the SMR after 21 days of corticosterone application in pregnant females; whereas SMR decreased after 10 days of treatment in adult males (Cote et al 2010a) and did not change in yearlings (Voituron et al, 2017).…”

“…In our study, the standard metabolic rate of lizards did not change between treatment groups, implying that the decrease of oxidative damage during the laboratory manipulation was not due to changes in basal metabolism. However, we recently demonstrated that the liver mitochondria from corticosterone-treated lizards produced less reactive oxygen species without change in the metabolic rate or oxygen consumption (Voituron et al, 2017). The persistent difference between treatment groups in the field one month after the end of the laboratory manipulation, despite no differences in the immune response, corticosterone concentration or antioxidant barrier, suggests a short-lasting carryover effect on blood oxidative damage.…”

“…In the common lizard, a prolonged corticosterone elevation promotes behaviours associated with food intake including exploratory activity, foraging and basking (Cote et al 2010a). Corticosterone can also induce lipid storage in non-fasted state by activating lipogenesis and adipogenesis (Peckett et al, 2011;Voituron et al, 2017). The body mass gain during the laboratory experiment could thus result from an increase of both food intake and lipid storage.…”