Abstract
BackgroundSkeletal muscle is able to react in a rapid, dynamic way to metabolic and mechanical stimuli. In particular, exposure to either prolonged starvation or disuse results in muscle atrophy. At variance, in hibernating animals muscle atrophy may be scarce or absent after bouts of hibernation i.e., periods of prolonged (months) inactivity and food deprivation, and muscle function is fully preserved at arousal. In this study, myocytes from the quadriceps muscle of euthermic and hibernating edible dormice were investigated by a combination of morphological, morphometrical and immunocytochemical analyses at the light and electron microscopy level. The focus was on cell nuclei and mitochondria, which are highly sensitive markers of changing metabolic rate.ResultsFindings presented herein demonstrate that: 1) the general histology of the muscle, inclusive of muscle fibre shape and size, and the ratio of fast and slow fibre types are not affected by hibernation; 2) the fine structure of cytoplasmic and nuclear constituents is similar in euthermia and hibernation but for lipid droplets, which accumulate during lethargy; 3) during hibernation, mitochondria are larger in size with longer cristae, and 4) myonuclei maintain the same amount and distribution of transcripts and transcription factors as in euthermia.ConclusionIn this study we demonstrate that skeletal muscle cells of the hibernating edible dormouse maintain their structural and functional integrity in full, even after months in the nest. A twofold explanation for that is envisaged: 1) the maintenance, during hibernation, of low-rate nuclear and mitochondrial activity counterbalancing myofibre wasting, 2) the intensive muscle stimulation (shivering) during periodic arousals in the nest, which would mimic physical exercise. These two factors would prevent muscle atrophy usually occurring in mammals after prolonged starvation and/or inactivity as a consequence of prevailing catabolism. Understanding the mechanisms responsible for skeletal muscle preservation in hibernators could pave the way to prevention and treatment of muscle wasting associated with pathological conditions or ageing as well as life in extreme environments, such as ocean deeps or spaceflights.
Highlights
Skeletal muscle is able to react in a rapid, dynamic way to metabolic and mechanical stimuli
Multiple, elongated myonuclei occurred at the periphery of the cell, close to the plasma membrane: they generally showed finely irregular borders, condensed chromatin clumps at both the nuclear and nucleolar periphery, and one roundish nucleolus characterized by a few fibrillar centre (FC), and abundant dense fibrillar component (DFC) and granular component (GC) (Fig. 1f)
All the usual RNP structural constituents involved in pre-mRNA transcription and processing were clearly recognizable: perichromatin fibrils (PF) i.e. the in situ form of pre-mRNA transcription and early splicing [19]; http://www.biomedcentral.com/1471-2121/10/19 was negligible in all immunolabelling experiments
Summary
Skeletal muscle is able to react in a rapid, dynamic way to metabolic and mechanical stimuli. Starvation activates intense lipolysis and proteolysis in several tissues inclusive of skeletal muscle, with increased muscle protein breakdown and final loss of muscle mass (reviewed in [1]); disuse induces muscle atrophy characterised by loss of muscle mass, decreased cross-sectional area of muscle fibre and lower amounts of contractile protein – especially myosin heavy-chain proteins – mainly due to the unbalanced regulation of protein catabolism and anabolism [2,3]. This phenomenon affects skeletal muscle after prolonged inactivity, whether by immobilization, spaceflight, spinal cord isolation, or denervation, with variable effects depending upon muscle type and fibre type Hibernators provide a fascinating model for investigating muscle atrophy associated with disuse
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