Each to their own: skeletal muscles of different function use different biochemical strategies during aestivation at high temperature

Abstract

SUMMARYPreservation of muscle morphology depends on a continuing regulatory balance between molecules that protect and molecules that damage muscle structural integrity. Excessive disruption of the biochemical balance that favours reactive oxygen species (ROS) in disused muscles may lead to oxidative stress, which in turn is associated with increased atrophic or apoptotic signalling and/or oxidative damage to the muscle and thus muscle disuse atrophy. Increases in the rate of oxygen consumption likely increase the overall generation of ROS in vivo. Temperature-induced increases in oxygen consumption rate occur in some muscles of ectotherms undergoing prolonged muscular disuse during aestivation. In the green-striped burrowing frog, Cyclorana alboguttata, both large jumping and small non-jumping muscles undergo atrophy seemingly commensurate with their rate of oxygen consumption during aestivation. However, because the extent of atrophy in these muscles is not enhanced at higher temperatures, despite a temperature-sensitive rate of oxygen consumption in the jumping muscle, we proposed that muscles are protected by biochemical means that, when mobilised at higher temperatures, inhibit atrophy. We proposed that the biochemical response to temperature would be muscle-specific. We examined the effect of temperature on the antioxidant and heat shock protein systems and determined the extent of oxidative damage to lipids and proteins in two functionally different skeletal muscles, the gastrocnemius (jumping muscle) and the iliofibularis (non-jumping muscle), by aestivating frogs at 24 and 30°C for 6months. We assayed small molecule antioxidant capacity, mitochondrial and cytosolic superoxide dismutase activities and Hsp70 concentrations to show that protective mechanisms in disused muscles are differentially regulated with respect to both temperature and aestivation. High aestivation temperature results in an antioxidant response in the metabolically temperaturesensitive jumping muscle. We assayed lipid peroxidation and protein oxidation to show that oxidative damage is apparent during aestivation and its pattern is muscle-specific, but unaffected by temperature. Consideration is given to how the complex responses of muscle biochemistry inform the different strategies muscles may use in regulating their oxidative environment during extended disuse and disuse at high temperature.

Mechanisms underlying inhibition of muscle disuse atrophy during aestivation in the green-striped burrowing frog, Cyclorana alboguttata

“…Consistent with our gene expression data, a recent study demonstrated an increase in levels of heat shock 70 kDa protein (HSP70) in the gastrocnemius of C. alboguttata during aestivation (Young et al, 2013). Interestingly, there is a decline in expression of various HSPs in atrophied muscles of rats subjected to hindlimb unloading, which is predicted to be associated with impairment of muscle mass recovery (Lawler et al, 2006;Sakurai et al, 2005;Stevenson et al, 2003).…”

“…Consistent with this hypothesis is the finding that levels of antioxidants (catalase and glutathione peroxidase 4) were maintained at control levels in aestivating muscle of C. alboguttata, whilst the total antioxidant capacity increases (when standardised to the oxygen consumption rate of the animal or tissue) (Hudson et al, 2006;Mantle et al, 2009;Young et al, 2013). There is some evidence that oxidative damage occurs in muscle during aestivation, but this appears to be confined to the iliofibularis muscle (Young et al, 2013).…”

“…The induction of heat shock proteins may also play an important role in countering muscle wasting during hibernation and aestivation (Lee et al, 2008;Young et al, 2013), especially given that heat shock protein overexpression improves structural and functional recovery of skeletal muscle following immobilisation-induced atrophy in mice (Miyabara et al, 2012). Despite such advances in understanding the biochemical regulation associated with dormancy, overall little is known about the modulation of cell mechanisms (e.g.…”

“…These studies indicate that modulation of antioxidants in aestivating muscle might decrease the susceptibility of muscle fibres to the atrophic effects of oxidative stress. As direct measurements of ROS are complicated and often exposed to errors, redox balance during dormancy has been typically studied indirectly by examination of lipid peroxidation and/or protein carbonylation (Grundy and Storey, 1998;Young et al, 2013). In one of the few studies that measured ROS production directly, there was generally no difference observed in mitochondrial ROS production in skeletal muscle of dormant vs.…”

Modulation of Antioxidant Status of Erythrocyte of In Vivo Heat Exposed Rats Fed on Altered Dietary Protein Level

“…Bernabucci et al suggested that erythrocytes are an appropriate and sensitive model to study the oxidative status of transition dairy cows exposed to hot environment [3]. On the other hand, studies demonstrated that heat stress induces oxidative stress in the body [4,5,6]. It has been demonstrated that heat stress is one of the most important stressors in the hot regions of the world (Altan, 2003).It results the generation of free radicals and other reactive oxygen species(ROS) (Chihuailaf et al, 2002) which leads to cellular and tissue damage (Tkaczyk andVizek, 2007).…”