The Distribution and Arrangement of Microtubules in Mammalian Skeletal Muscle Fibers.

Abstract

ABSTRACT. The distribution and arrangement of microtubules (MTs) in skeletal muscle fibers of the rat and mousediaphragm were examined by thin-section electron microscopy. In the central portion of muscle fibers, most MTsran longitudinally between myofibrils and beneath the sarcolemma, and some MTsran transversely predominantly at the level of the I band, especially of the A-I junction, thus forming a lattice-like arrangement. At the fiber periphery, MTswere aggregated in the perinuclear region, from which they radiated to take a longitudinal course beneath the sarcolemma and to run in a transverse direction at the I-band level. In the end portion of muscle fibers, MTswere abundant and ran longitudinally into sarcoplasmic processes. MTswere often found to be spatially associated with membranousorgandies. Quantitative analyses indicated that the longitudinally running MTswere remarkably more numerous in the peripheral zone of muscle fibers than in the deeper zones. The density of MTsin the central portion was almost the same in both red and white muscle fibers. The density was significantly higher at the fiber ends, though it varied considerably among different fibers. These results are discussed with special reference to the possible involvement of MTsin intracellular transport as well as structural support.Microtubules (MTs) are one of the major components of the cytoskeleton and are believed to primarily provide structural supports in various types of cells. Thus MTs are involved not only in the maintenance of cell shape but also in various cellular movements such as ciliary movement, cell division, and intracellular transport (for reviews see 3, 17, 18, 20).Skeletal muscle fibers are highly specialized cells.Most of the cytoplasm (sarcoplasm) is occupied by the contractile material called cross-striated myofibrils. Membranousorganelles such as the sarcoplasmic reticulum and T-system are also regularly arranged in register around and between the myofibrils. Skeletal muscle fibers contain numerous nuclei, which are usually located at the fiber periphery. It is interesting to ask how the structural integrity, contractile activity, and metabolism are maintained in such multinucleate, giant cells.Of particular interest is the process of intracellular transport, including the nucleus-sarcoplasm interaction, with special reference to the possible functions of MTs. MTsare remarkably abundant in developing muscle cells (1,5,32,33). Thus much attention has been paid to the role of MTsin myogenesis. In definitive myo-* To whomcorrespondance should be addressed. !) Present address:

Cytoskeletal structure of skeletal muscle: identification of an intricate exosarcomeric microtubule lattice in slow- and fast-twitch muscle fibers.

“…However, a consistently higher relative intensity of the microtubules was found in the sarcoplasmic space and in the subsarcolemmal region in Type I fibers of the SOL muscle compared to Type IIb fibers of the SVL muscle. Kano et al (1991), using the rat and mouse diaphragm and electron microscopic quantification, did not observe a higher relative density of microtubules in the subsarcolemmal region of the fibers examined and did not report any quantitative differences with regard to fiber types. It is important to note that these investigators employed mitochondrial volume as a basis for fiber classification.…”

“…Although it has been generally accepted that mature skeletal muscle fibers contain microtubules, the available information has been derived primarily from electron microscopic analysis (Kano et al, 1991;Goldstein and CartWright, 1984). This approach can provide useful information regarding the organization of specific filament structures of the muscle fiber.…”

“…Some information derived from electron microscopy is available concerning the disposition of microtubules in the skeletal muscle fiber (Kano et al, 1991;Cartwright and Goldstein, 1980). These studies suggest that microtubules are found in the intermyofibrillar space and appear to wrap around the myofibrils in a helical fashion, thus displaying a variety of orientations.…”

Muscle-specific RING finger-2 (MURF-2) is important for microtubule, intermediate filament and sarcomeric M-line maintenance in striated muscle development

“…are challenging as their distinct arrays and orientations vary among muscle types, during development, and with disease (Saitoh et al, 1988;Gundersen et al, 1989;Kano et al, 1991;Boudriau et al, 1993;Webster, 1997;Belmadani et al, 2002).…”

Effects of Tissue Protectants on the Kinetics of Lactate Dehydrogenase in Cells

“…However, the cytoskeletal organizations in skeletal muscle fibers and hepatocytes differ, especially concerning F-actin and microtubules. In skeletal muscle fibers, repeated assemblies of the actin-and myosin-based contractile units of myofibrils dominate the sarcoplasm, and microtubules are present mostly longitudinally between myofibrils and beneath the sarcolemma and transversely in a lattice-like arrangement (Parysek et al 1984;Kano et al 1991;Boudriau et al 1993). In hepatocytes, actin microfilaments are present throughout the cytoplasm, particularly beneath the plasma membranes around the bile canaliculi with a contractile function (Katsuma et al 1988;Watanabe et al 1991;Blankson et al 1995).…”