Chronic stress, energy transduction, and free-radical production in a reptile
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 (O2 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.
KeywordsCorticosterone Reptile Mitochondrial efficiency Allostatic overload ROS emission and ATP production Oxygen consumption
We are thankful to field assistants and technical staff at CEREEP-Ecotron IleDeFrance for their support, especially Hugo Mell. This study was funded by the Centre National de la Recherche Scientifique (CNRS), the Agence Nationale de la Recherche (ANR-13-JSV7-0011-01 to S.M.) and the Région Île-de-France R2DS program (Grant 2013-08 to S.M., J.F.L.G. and R.J.). The authors declare no competing or financial interests.
Author contribution statement
YV, SM, and JFLG conceived, designed the study, and analyzed the data. RJ ensured animal husbandry, hormonal treatment and performed the statistical analyses. CH ensured plasma corticosterone measurements. DR and CR conceived and conducted the bioenergetics studies and performed the ROS production assessment. YV, SM, and JFLG wrote the manuscript; other authors provided editorial advice.
- Arvier M, Lagoutte L, Johnson G, Dumas JF, Sion B, Grizard G, Malthiery Y, Simard G, Ritz P (2007) Adenine nucleotide translocator promotes oxidative phosphorylation and mild uncoupling in mitochondria after dexamethasone treatment. Am J Physiol Endocrinol Metab 293:E1320–E1324CrossRefPubMedGoogle Scholar
- Duclos M, Gouarne C, Martin C, Rocher C, Mormede P, Letellier T (2004) Effects of corticosterone on muscle mitochondria identifying different sensitivity to glucocorticoids in Lewis and Fischer rats. Am J Physiol 286:E159–E167Google Scholar
- Kooijman SALM (2010) Dynamic energy budget theory for metabolic organisation, 3rd edn. Cambridge University Press, CambridgeGoogle Scholar
- Mason RT (1992) Reptilian pheromones. In: Gans C, Crews D (eds) Biology of the Reptilia, vol 18. University of Chicago Press, Chicago, pp 114–228Google Scholar
- Team RDC (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar