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ENVIRONMENTAL, EXERCISE AND RESPIRATORY PHYSIOLOGY

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

¹Commonwealth Scientific and Industrial Research Organization Livestock Industries and ²School of Integrative Biology, University of Queensland, Brisbane, Queensland, Australia

Submitted 31 May 2005 ; accepted in final form 19 October 2005

Long (6- to 9-mo) bouts of estivation in green-striped burrowing frogs lead to 28% atrophy of cruralis oxidative fibers (P < 0.05) and some impairment of in vitro gastrocnemius endurance (P < 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 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 < 0.05) and ATP synthase (67% downregulated, P < 0.05) are consistent with mitochondrial quiescence and reduced oxidant production. Meanwhile, uncoupling protein type 2 transcription (P = 0.31), which is thought to reduce mitochondrial leakage of reactive oxygen species, was maintained. Total antioxidant defense of water-soluble (22.3 ± 1.7 and 23.8 ± 1.5 µM/µg total protein in control and estivator, respectively, P = 0.53) and membrane-bound proteins (31.5 ± 1.9 and 42.1 ± 7.3 µM/µg total protein in control and estivator, respectively, P = 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 < 0.05) paralleled mitochondrial activity, whereas nuclear-encoded catalase and glutathione peroxidase were maintained at control values (P = 0.42 and P = 0.231), suggesting a dissonance between mitochondrial and nuclear antioxidant expression. Pyruvate dehydrogenase kinase 4 transcription was fourfold lower in estivators (P = 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

This article has been cited by other articles:

				B. L. Mantle, N. J. Hudson, G. S. Harper, R. L. Cramp, and C. E. Franklin Skeletal muscle atrophy occurs slowly and selectively during prolonged aestivation in Cyclorana alboguttata (Gunther 1867) J. Exp. Biol., November 15, 2009; 212(22): 3664 - 3672. [Abstract] [Full Text] [PDF]

				S. M. Kayes, R. L. Cramp, N. J. Hudson, and C. E. Franklin Surviving the drought: burrowing frogs save energy by increasing mitochondrial coupling J. Exp. Biol., July 15, 2009; 212(14): 2248 - 2253. [Abstract] [Full Text] [PDF]