Surviving the drought: burrowing frogs save energy by increasing mitochondrial coupling

Kayes, Sara M.; Cramp, Rebecca L.; Hudson, Nicholas J.; Franklin, Craig E.

doi:10.1242/jeb.028233

Cited by 28 publications

(24 citation statements)

References 31 publications

(42 reference statements)

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“…However, if such a feedback loop were in operation, the degree to which this would reduce ROS via mitochondrial uncoupling is also uncertain because during aestivation C. alboguttata are reported to increase mitochondrial coupling (Kayes et al, 2009). The accumulation of lipid peroxidation during aestivation despite antioxidant regulation is consistent with aestivating spadefoot toads (Grundy and Storey, 1998), land snails (Hermes-Lima and Storey, 1995), freshwater snails (Ferreira et al, 2003) and hibernating little susliks (L'vova and Gasangadzhieva, 2003).…”

Section: Oxidative Damage Lipid Peroxidationmentioning

confidence: 99%

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

Young

Cramp

Franklin

2012

Journal of Experimental Biology

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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.

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Section: Oxidative Damage Lipid Peroxidationmentioning

confidence: 99%

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

Young

Cramp

Franklin

2012

Journal of Experimental Biology

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“…The suppression of skeletal muscle mitochondrial-and whole-animal respiration clearly maximises energy savings for aestivating frogs. These results are in agreement with previous work on C. alboguttata, which demonstrated suppression of skeletal muscle mitochondrial and whole-animal respiration during aestivation by more than 80% (Kayes et al, 2009b). The greater magnitude of metabolic depression in that study may be related to a longer period of aestivation and/or differences in the preparation of isolated mitochondria.…”

Section: Mitochondrial Respirationsupporting

confidence: 92%

“…The reduction in gastrocnemius mitochondrial respiration is consistent with previous work on C. alboguttata (Kayes et al, 2009b) and correlates well with the ~70% reduction in whole animal oxygen consumption measured in the current study. The reduction in skeletal muscle mitochondrial H2O2 production is important given the paucity of information about rates of free radical production during metabolic depression.…”

Section: Effect Of Aestivation On Ros Production and Calpains In C Asupporting

confidence: 92%

“…Given that mitochondrial function underpins not only cellular but also tissue and whole animal aerobic metabolic rate, a decrease in mitochondrial energy expenditure (oxygen consumption) would result in substantial energy savings during metabolic depression. Indeed, in the green-striped burrowing frog (Cyclorana alboguttata) the rate of skeletal muscle mitochondrial oxygen consumption has been shown to be reduced by more than 80% following seven months of aestivation (Kayes et al, 2009b). Furthermore, aestivating C. alboguttata were shown to increase mitochondrial coupling efficiency (i.e.…”

Section: The Physiology Of Aestivating Amphibiansmentioning

confidence: 99%

“…Furthermore, aestivating C. alboguttata were shown to increase mitochondrial coupling efficiency (i.e. the ratio of ATP synthesis to proton leak) which is likely to be associated with an increase in energy savings (Kayes et al, 2009b).…”

Section: The Physiology Of Aestivating Amphibiansmentioning

confidence: 99%

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

Reilly¹

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In most mammals, extended inactivity or immobilisation of skeletal muscle (e.g. bedrest, limb-casting or hindlimb unloading) results in muscle disuse atrophy, a process which is characterised by the loss of skeletal muscle mass and function. In stark contrast, animals that experience natural bouts of prolonged muscle inactivity, such as hibernating mammals and aestivating frogs, consistently exhibit limited or no change in either skeletal muscle size or contractile performance. While many of the factors regulating skeletal muscle mass are known, little information exists as to what mechanisms protect against muscle atrophy in some species.Green-striped burrowing frogs (Cyclorana alboguttata) survive in arid environments by burrowing underground and entering into a deep, prolonged metabolic depression known as aestivation. Throughout aestivation, C. alboguttata is immobilised within a cast-like cocoon of shed skin and ceases feeding and moving. Remarkably, these frogs exhibit very little muscle atrophy despite extended disuse and fasting. The overall aim of the current research study was to gain a better understanding of the physiological, cellular and molecular basis underlying resistance to muscle disuse atrophy in C. alboguttata.The first aim of this study was to develop a genomic resource for C. alboguttata by sequencing and functionally characterising its skeletal muscle transcriptome, and to conduct gene expression profiling to identify transcriptional pathways associated with metabolic depression and maintenance of muscle function in aestivating burrowing frogs. A transcriptome was assembled using next-generation short read sequencing followed by a comparison of gene expression patterns between active and four-month aestivating C.alboguttata. This identified a complex suite of gene expression changes that occur in muscle during aestivation and provides evidence that aestivation in burrowing frogs involves transcriptional regulation of genes associated with cytoskeletal remodelling, avoidance of oxidative stress, energy metabolism, the cell stress response, cell death and survival and epigenetic modification. In particular, the expression levels of genes encoding cell cycle regulatory-, pro-survival and chromatin remodelling proteins, such as serine/threonine-protein kinase Chk1, cell division protein kinase 2, survivin, vesicular overexpressed in cancer prosurvival protein 1 and histone-binding protein RBBP4, were upregulated in aestivators.The second aim of this study was to examine the potential role of mitochondrial ROS in the regulation of muscle mass and function during aestivation in C. alboguttata. In III mammals, muscle disuse atrophy has been associated with oxidative damage due to increased mitochondrial ROS production. C. alboguttata reduced skeletal muscle mitochondrial respiration by approximately 50% following four months of aestivation, while mitochondrial ROS production was more than 80% lower in aestivating skeletal muscle relative to controls when mitochondrial substrates were pre...

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Vertebrate Respiration and Circulation in Extreme Conditions

Lillywhite¹

2021

Encyclopedia of Life Sciences

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The, acquisition and internal transport of respiratory gases and metabolic fuels depend on linked processes, with design and function related to energetic demands and attributes of the environment. Environmental challenges to these processes reflect variation in the density of gases, temperature and the pressures that prevail in the environmental medium. The limits of vertebrate survival and performance are tested in environments of low oxygen such as soil, mud or water in which animals overwinter sometimes at freezing temperatures; high altitude where the atmospheric density of oxygen is low; and the deeper reaches of ocean where pressure and distance challenge the physiology of air‐breathing vertebrates. Cardiorespiratory functions are also limited by the metabolic demands of animals related to body size, temperature, activity and gravity, which also impacts features of morphology and behaviour. Responses of vertebrates to physical environmental challenges are related to phylogenetic evolutionary changes and include both plasticity of adjustments and genetic/genomic changes influencing form and function, including molecular underpinnings. Key Concepts Aerobic cellular respiration requires internal transport of fuels, oxygen and carbon dioxide, which are exchanged with the external environment and at greater rates during exercise or activity involving muscles. The rate of energy expenditure, or metabolism, per unit of body mass decreases with increasing body size, while increasing with temperature and level of activity. The functional capacities of each step in oxygen transport are matched to each other, and the upper limits to aerobic capacity depend on the integrated function of the linked steps in oxygen transport, rather than any single factor. Saving of energy is related to lowering of body temperature, suppression of metabolism, behavioural reduction of activity and molecular adjustments in fuel usage, among other factors. Countermeasures to gravity's ‘pull’ on blood circulation include tight tissues, relatively nondistending blood vessels, effective neurogenic control of heart and blood vessels and anatomical or behavioural reduction in the vertical length of blood vessels. Increasing altitude reduces the density of oxygen, reduces temperature, increases the diffusion of gases and increases evaporative water loss. The pressure in a fluid column increases with depth as a result of gravity, and increasing pressures in deep water columns compress air spaces, alter the structure of proteins and function of enzymes and decrease the fluidity of membranes. Atmospheric hypoxia limits the distributional range and performance of vertebrates at higher altitudes. Responses to hypoxia may increase the cardiac output and blood flow to tissues, increase the growth of blood vessels, increase blood oxygen capacity and circulating blood volume and adjust metabolic pathways to favour increased efficiency of ATP production. Compared with mammals, birds have superior ability to acquire O 2 and to maintain blood flow to the brain during hypoxia when levels of CO 2 in the blood are reduced. The survival of overwintering ectothermic vertebrates at subzero temperatures is aided by behavioural, physiological and biochemical adaptations that enable animals either to avoid freezing or to tolerate some portion of their body fluids being converted to ice, which is managed by cryoprotectants and antifreeze proteins. Routine dives of diving vertebrates are aerobic, but glycolysis supplements the energy requirements during prolonged submergence or repetitive dives of some species, as well as the low metabolic needs of turtles and frogs hibernating at low temperatures. Vertebrate adaptations for diving deeply include enhanced oxygen reserves primarily in blood, circulation of blood principally to brain and heart, smaller volumes and collapse of the lung to minimize problems associated with buoyancy and the entry into blood of pressurized pulmonary nitrogen, which leads to embolism and the debilitating condition known as the bends. In sea snakes, cardiovascular shunts ‘meter’ the lung oxygen store, lower the partial pressure of oxygen in blood and enable the loss of nitrogen while minimizing the loss of oxygen across the skin.

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Surviving the drought: burrowing frogs save energy by increasing mitochondrial coupling

Cited by 28 publications

References 31 publications

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

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

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

Vertebrate Respiration and Circulation in Extreme Conditions

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