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 rate of oxygen consumption likely increase the overall generation of ROS in vivo. Temperature-induced increases in muscle 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 muscles and small non-jumping muscles undergo atrophy seemingly commensurate with their rate of oxygen consumption during aestivation. However, since 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 the biochemical response to temperature would be muscle-specific. We examined the effect of temperature on the antioxidant and heat shock protein systems and evidence of oxidative damage to lipids and proteins in two functionally different skeletal muscles, gastrocnemius (jumping muscle) and iliofibularis (non-jumping muscle), by aestivating frogs at 24 and 30oC for six months. We assayed small molecule antioxidant capacity, mitochondrial and cytosolic SOD and Hsp70 to show that protective mechanisms in disused muscles are differentially regulated both with respect to temperature and aestivation. High aestivation temperature results in an antioxidant response in the metabolically temperature-sensitive 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 of the different strategies muscles may use in regulating their oxidative environment during extended disuse and disuse at high temperature.