Ring bands in fish skeletal muscle: reorienting the myofibrils and microtubule cytoskeleton within a single cell

Skeletal muscle cells (fibers) contract by shortening their parallel subunits, the myofibrils. Here we show a novel pattern of myofibril orientation in white muscle fibers of large black sea bass, Centropristis striata. Up to 48% of the white fibers in fish >1168 g had peripheral myofibrils undergoing an ∼90(o) shift in orientation. The resultant ring band wrapped the middle of the muscle fibers and was easily detected with polarized light microscopy. Transmission electron microscopy showed that the reoriented myofibrils shared the cytoplasm with the central longitudinal myofibrils. A microtubule network seen throughout the fibers surrounded nuclei but was mostly parallel to the long-axis of the myofibrils. In the ring band portion of the fibers the microtubule cytoskeleton also shifted orientation. Sarcolemmal staining with anti-synapsin was the same in fibers with or without ring bands, suggesting that fibers with ring bands have normal innervation and contractile function. The ring bands appear to be related to body-mass or age, not fiber size, and also vary along the body, being more frequent at the midpoint of the anteroposterior axis. Similar structures have been reported in different taxa and appear to be associated with hypercontraction of fibers not attached to a rigid structure (bone) or with fibers with unusually weak links between the sarcolemma and cytoskeleton, as in muscular dystrophy. Fish muscle fibers are attached to myosepta, which are flexible and may allow for fibers to hypercontract and thus form ring bands. The consequences of such a ring band pattern might be to restrict the further expansion of the sarcolemma and protect it from further mechanical stress.