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Three-dimensional structural analysis of mitochondria composing each subtype of fast-twitch muscle fibers in chicken.

ABSTRACT: In a previous study, the three-dimensional structures of mitochondria in type I and type IIb muscle fibers of chicken were analyzed. The study reported differences in the shape of the mitochondria and the distribution of lipid droplets. In this study, we three-dimensionally analyzed mitochondria and lipid droplets of type II muscle fiber subtypes IIa, IIb, and IIc of chicken lateral iliotibial muscle in the same field of view using correlative light electron microscopy (CLEM) and array tomography methods. The reconstructed images showed that the mitochondria of type IIa muscle fiber were thick and aligned along the myofibrils, and many lipid droplets were embedded in the mitochondria. The mitochondria of type IIb muscle fibers were intermittent, aligned along the myofibrils, and showed contact between adjacent horizontal mitochondria. No lipid droplets were observed in type IIb muscle fiber. In type IIc muscle fiber, we observed irregularly shaped mitochondria with small diameters aligned along the myofibrils. Lipid droplets not only were embedded in the mitochondria but also existed independently in some cases. The combination of array tomography and CLEM methods enabled three-dimensional electron microscopic observation of mitochondria in different subtypes of type II muscle fibers. The subtypes of type II muscle fibers differed in mitochondrial occupancy and morphology and in lipid droplet distribution, and characteristics that had been demonstrated biochemically were also demonstrated ultrastructurally.

SUBMITTER: Makida S

PROVIDER: S-EPMC9246695 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The contractile properties of fast-twitch and slow-twitch skeletal muscles are primarily determined by the myosin isoform content and modulated by a variety of sarcomere proteins. X-ray diffraction studies of regulatory mechanisms in muscle contraction have focused predominately on fast- or mixed-fibre muscle with slow muscle being much less studied. Here, we used time-resolved X-ray diffraction to investigate the dynamic behaviour of the myofilament proteins in relatively pure slow-twitch-fibre rat soleus (SOL) and pure fast-twitch-fibre rat extensor digitorum longus (EDL) muscle during twitch and tetanic contractions at optimal length. During twitch contractions the diffraction signatures indicating a transition in the myosin heads from ordered OFF states, where heads are held close to the thick filament backbone, to disordered ON states, where heads are free to bind to thin filaments, were found in EDL and not in SOL muscle. During tetanic contraction, changes in the disposition of myosin heads as active tension develops is a quasi-stepwise process in EDL muscle whereas in SOL muscle this relationship appears to be linear. The observed reduced extensibility of the thick filaments in SOL muscle as compared to EDL muscles indicates a molecular basis for this behaviour. These data indicate that for the EDL, thick filament activation is a cooperative strain-induced mechano-sensing mechanism, whereas for the SOL, thick filament activation has a more graded response. These different approaches to thick filament regulation in fast- and slow-twitch muscles may be adaptations for short-duration, strong contractions versus sustained, finely controlled contractions, respectively. KEY POINTS: Fast-twitch muscle and slow-twitch muscle are optimized for strong, short-duration contractions and for tonic postural activity, respectively. Structural events (OFF to ON transitions) in the myosin-containing thick filaments in fast muscle help determine the timing and strength of contractions, but these have not been studied in slow-twitch muscle. The X-ray diffraction signatures of structural OFF to ON transitions are different in fast extensor digitorum longus (EDL) and slow soleus (SOL) muscle, being completely absent during twitches in soleus muscle and blunted during tetanic contractions SOL as compared to EDL Quasi-stepwise thick filament structural OFF to ON transitions in fast twitch muscle may be an adaptation for rapid, ballistic movements, whereas more graded OFF to ON structural transitions in slow-twitch muscle may be an adaptation for slower, finer motions.

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Three-dimensional structural analysis of mitochondria composing each subtype of fast-twitch muscle fibers in chicken.

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