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The cell nuclei of skeletal muscle cells are transcriptionally active in hibernating edible dormice.

Malatesta M, Perdoni F, Battistelli S, Muller S, Zancanaro C - BMC Cell Biol. (2009)

Bottom Line: In particular, exposure to either prolonged starvation or disuse results in muscle atrophy.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Dipartimento di Scienze Morfologico-Biomediche, Sezione di Anatomia e Istologia, University of Verona, Italy. manuela.malatesta@univr.it

ABSTRACT

Background: Skeletal 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.

Results: Findings 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.

Conclusion: In 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.

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Myonuclei from euthermic (a, e) and hibernating (b-d, f) edible dormice; LRWhite embedding, EDTA staining. a-d. Immunolabelling with anti-DNA/RNA hybrid molecule antibody: the signal occurs in both nucleoplasm, where it is mainly associated to PF (arrows), and in nucleolar DFC (arrowheads). The amorphous body (AB) is unlabelled. e, f. Immunolabelling with anti-phosphorylated polymerase II antibody: a specific signal is present over PF (thick arrows). Bars = 0.2 μm.
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Figure 4: Myonuclei from euthermic (a, e) and hibernating (b-d, f) edible dormice; LRWhite embedding, EDTA staining. a-d. Immunolabelling with anti-DNA/RNA hybrid molecule antibody: the signal occurs in both nucleoplasm, where it is mainly associated to PF (arrows), and in nucleolar DFC (arrowheads). The amorphous body (AB) is unlabelled. e, f. Immunolabelling with anti-phosphorylated polymerase II antibody: a specific signal is present over PF (thick arrows). Bars = 0.2 μm.

Mentions: In all dormice, skeletal muscle cells showed their typical, elongated shape with most of the cytoplasm occupied by the longitudinally arrayed myofibrils composed of thick (myosin) and thin (actin) filaments (Fig. 1c, d). The mitochondria were lined in small, longitudinally oriented cytoplasm areas between myofibrils; they were ovoid in shape with many transverse cristae in both euthermic and hibernating dormice; however, in mitochondria of hibernating animals both size and inner-to-outer membrane ratio significantly increased (Fig 3). Glycogen was more abundant in euthermia, especially close to mitochondria; on the other hand, during hibernation lipid droplets accumulated in the cytoplasm in close proximity to mitochondria (Fig. 1d, e). 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 FC, and abundant DFC and GC (Fig. 1f). In the nucleoplasm, 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]; perichromatin granules (PG), acting as both vector and storage site of already spliced pre-mRNA [19]; interchromatin granules (IG), sites for the storage and/or assembly of pre-splicing complexes [20,21]. In addition, amorphous bodies (Fig. 4c), a nuclear structural constituent found in different tissues during hibernation [22,23], were occasionally observed in myonuclei of hibernating dormice (at least one in about 2% of sectioned myonuclei). Morphometry (Table 1) showed that all the investigated structural parameters in myonuclei were similar in euthermic and hibernating dormice.


The cell nuclei of skeletal muscle cells are transcriptionally active in hibernating edible dormice.

Malatesta M, Perdoni F, Battistelli S, Muller S, Zancanaro C - BMC Cell Biol. (2009)

Myonuclei from euthermic (a, e) and hibernating (b-d, f) edible dormice; LRWhite embedding, EDTA staining. a-d. Immunolabelling with anti-DNA/RNA hybrid molecule antibody: the signal occurs in both nucleoplasm, where it is mainly associated to PF (arrows), and in nucleolar DFC (arrowheads). The amorphous body (AB) is unlabelled. e, f. Immunolabelling with anti-phosphorylated polymerase II antibody: a specific signal is present over PF (thick arrows). Bars = 0.2 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2663540&req=5

Figure 4: Myonuclei from euthermic (a, e) and hibernating (b-d, f) edible dormice; LRWhite embedding, EDTA staining. a-d. Immunolabelling with anti-DNA/RNA hybrid molecule antibody: the signal occurs in both nucleoplasm, where it is mainly associated to PF (arrows), and in nucleolar DFC (arrowheads). The amorphous body (AB) is unlabelled. e, f. Immunolabelling with anti-phosphorylated polymerase II antibody: a specific signal is present over PF (thick arrows). Bars = 0.2 μm.
Mentions: In all dormice, skeletal muscle cells showed their typical, elongated shape with most of the cytoplasm occupied by the longitudinally arrayed myofibrils composed of thick (myosin) and thin (actin) filaments (Fig. 1c, d). The mitochondria were lined in small, longitudinally oriented cytoplasm areas between myofibrils; they were ovoid in shape with many transverse cristae in both euthermic and hibernating dormice; however, in mitochondria of hibernating animals both size and inner-to-outer membrane ratio significantly increased (Fig 3). Glycogen was more abundant in euthermia, especially close to mitochondria; on the other hand, during hibernation lipid droplets accumulated in the cytoplasm in close proximity to mitochondria (Fig. 1d, e). 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 FC, and abundant DFC and GC (Fig. 1f). In the nucleoplasm, 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]; perichromatin granules (PG), acting as both vector and storage site of already spliced pre-mRNA [19]; interchromatin granules (IG), sites for the storage and/or assembly of pre-splicing complexes [20,21]. In addition, amorphous bodies (Fig. 4c), a nuclear structural constituent found in different tissues during hibernation [22,23], were occasionally observed in myonuclei of hibernating dormice (at least one in about 2% of sectioned myonuclei). Morphometry (Table 1) showed that all the investigated structural parameters in myonuclei were similar in euthermic and hibernating dormice.

Bottom Line: In particular, exposure to either prolonged starvation or disuse results in muscle atrophy.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Dipartimento di Scienze Morfologico-Biomediche, Sezione di Anatomia e Istologia, University of Verona, Italy. manuela.malatesta@univr.it

ABSTRACT

Background: Skeletal 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.

Results: Findings 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.

Conclusion: In 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.

Show MeSH
Related in: MedlinePlus