Lessons from an estivating frog: sparing muscle protein despite starvation and disuse

Nicholas J. Hudson, Sigrid A. Lehnert, Aaron B. Ingham, Beth Symonds, Craig E. Franklin, Gregory S. Harper
2006 American Journal of Physiology. Regulatory Integrative and Comparative Physiology  
Long (6-to 9-mo) bouts of estivation in green-striped burrowing frogs lead to 28% atrophy of cruralis oxidative fibers (P Ͻ 0.05) and some impairment of in vitro gastrocnemius endurance (P Ͻ 0.05) but no significant deficit in maximal twitch force production. These data suggest the preferential atrophy of oxidative fibers at a rate slower than, but comparable to, laboratory disuse models. We tested the hypothesis that the frog limits atrophy by modulating oxidative stress. We assayed various
more » ... assayed various proteins at the transcript level and verified these results for antioxidant enzymes at the biochemical level. Transcript data for NADH ubiquinone oxidoreductase subunit 1 (71% downregulated, P Ͻ 0.05) and ATP synthase (67% downregulated, P Ͻ 0.05) are consistent with mitochondrial quiescence and reduced oxidant production. Meanwhile, uncoupling protein type 2 transcription (P ϭ 0.31), which is thought to reduce mitochondrial leakage of reactive oxygen species, was maintained. Total antioxidant defense of watersoluble (22.3 Ϯ 1.7 and 23.8 Ϯ 1.5 M/g total protein in control and estivator, respectively, P ϭ 0.53) and membrane-bound proteins (31.5 Ϯ 1.9 and 42.1 Ϯ 7.3 M/g total protein in control and estivator, respectively, P ϭ 0.18) was maintained, equivalent to a bolstering of defense relative to oxygen insult. This probably decelerates muscle atrophy by preventing accumulation of oxidative damage in static protein reserves. Transcripts of the mitochondrially encoded antioxidant superoxide dismutase type 2 (67% downregulated, P Ͻ 0.05) paralleled mitochondrial activity, whereas nuclearencoded catalase and glutathione peroxidase were maintained at control values (P ϭ 0.42 and P ϭ 0.231), suggesting a dissonance between mitochondrial and nuclear antioxidant expression. Pyruvate dehydrogenase kinase 4 transcription was fourfold lower in estivators (P ϭ 0.11), implying that, in contrast to mammalian hibernators, this enzyme does not drive the combustion of lipids that helps spare hypometabolic muscle. disuse atrophy; antioxidant; mitochondria; gene expression THE GREEN-STRIPED BURROWING frog Cyclorana alboguttata survives extended droughts by burrowing underground, shedding a waterproof cocoon (33), and undergoing a deep metabolic depression called estivation (29). In this capacity, its hindlimbs are fully immobilized, and it has no external food supply. C. alboguttata can withstand short (3-mo) bouts of estivation without suffering the losses in muscle contractile performance and mass (13) normally associated with disuse (23) and starvation (12).
doi:10.1152/ajpregu.00380.2005 pmid:16239372 fatcat:fllattvkvveyrmbn4z6k5dfyvi