Seasonal oxidative capacity of skeletal muscles in hibernating Daurian ground squirrels (Spermophilus dauricus)

Abstract

We investigated the mechanism of high oxidative capacity of skeletal muscles in hibernating Daurian ground squirrels (Spermophilus dauricus Brandt, 1843). Myoglobin (Mb) levels, as well as citrate synthase and lactate dehydrogenase (LDH) activities, were measured by spectrophotometry. Mb content in the soleus (SOL) muscle lasted from the beginning of hibernation to spring. Mb content in SOL was 87% higher in the hibernating group than in the summer group. Mb content in the extensor digitorum longus (EDL) muscle stayed at similar levels during the different periods of the year. Citrate synthase activity in SOL was 30% higher in the hibernating group than in the summer group. Meanwhile, citrate synthase activity in EDL did not change during hibernation. LDH activity in SOL was not different between the hibernating group and the summer active group, whereas LDH activity in EDL increased significantly (up to 11%) in the 2 days arousal after hibernation group compared with the hibernating group. We conclude that high oxidative capacity is provided by increased oxygen storage capacity of slow-twitch muscle fibers rather than from fast-twitch muscle fibers in hibernating animals. Résumé :Nous avons examiné le mécanisme qui sous-tend la capacité oxydative élevée des muscles squelettiques chez des spermophiles de Daourie (Spermophilus dauricus Brandt, 1843) hibernants. Les teneurs en myoglobine (Mb), ainsi que les activités de la citrate-synthase et de la lactate-déshydrogénase (LDH) ont été mesurées par spectrophotométrie. Les teneurs en Mb dans le muscle soléaire (SOL) persistaient du début de l'hibernation jusqu'au printemps. Les teneurs en Mb dans le SOL étaient de 87 % plus grandes dans le groupe hibernant que dans le groupe d'été. La Mb dans le muscle long extenseur du doigt (EDL) se maintenait à des teneurs semblables durant toutes les saisons de l'année. L'activité de la citrate-synthase dans le SOL était de 30 % plus grande dans le groupe hibernant que dans le groupe estival, alors que dans l'EDL, elle ne changeait pas durant l'hibernation. Il n'y avait pas de différence sur le plan de l'activité de la LDH dans le SOL entre le groupe hibernant et le groupe estival, alors que dans l'EDL, l'activité de la LDH augmentait de manière significative (jusqu'à 11 %) dans le groupe observé 2 jours après le réveil suivant l'hibernation par rapport au groupe hibernant. Nous concluons que la capacité oxydative élevée chez les animaux hibernants est assurée par une capacité de stockage d'oxygène accrue dans les fibres musculaires à contraction lente plutôt que par les fibres musculaires à contraction rapide. [Traduit par la Rédaction]

Novel findings on ultrastructural protection of skeletal muscle fibers during hibernation of Daurian ground squirrels: Mitochondria, nuclei, cytoskeleton, glycogen

“…Due to fact that small mammals undergo torpor‐arousal cycle during hibernation, increased expression of ATP synthase suggests higher ATP production, which makes sense when rapid muscle activation is needed in critical situations. Our previous study on citrate synthase activity also showed that the activity of both slow SOL and fast EDL muscles in hibernating Daurian ground squirrels were no less than pre‐hibernation (Jiang et al, ). This also indicates that the mitochondrial aerobic oxidation and energy production capacity of skeletal muscle in hibernating ground squirrels are well preserved.…”

Muscle protection during hibernation of Daurian ground squirrels (Spermophilus dauricus): role of atrogin-1, MuRF1, and fiber-type transition

“…Daurian ground squirrels (Spermophilus dauricus (Brandt, 1843)) are native to the dry plain steppes and deserts of North-Eastern China and Eastern Mongolia (Shar and Lkhagvasuren 2008;Jiang et al 2015). These rodents reach maturity at the age of 2-years and enter hibernation at the end of May while younger ground squirrels may be active until autumn (Shar and Lkhagvasuren 2008).…”

“…While most mammals experience muscle atrophy during hibernation, ground squirrels show little muscle atrophy during prolonged periods of skeletal muscle disuse during hibernation, which suggests that they have developed adaptive mechanisms to preserve skeletal muscle mass (Jiang et al 2015). While most mammals experience muscle atrophy during hibernation, ground squirrels show little muscle atrophy during prolonged periods of skeletal muscle disuse during hibernation, which suggests that they have developed adaptive mechanisms to preserve skeletal muscle mass (Jiang et al 2015).…”