Structure and function of the murine muscle–tendon junction

Abstract

The muscle-tendon junctions of the extensor carpi radialis longus and brevis muscles from adult Balb C Bailey/J mice have been examined tensiometrically and ultrastructurally following removal of cellular membrane and soluble cytoplasm by exposure to nonionic detergent. As judged by the ability of the extracted muscle to generate tension upon exposure to ATP and to transmit the generated tension to the tendon, detergent extraction leaves the muscle-tendon junction functionally intact. Electron microscopic analysis of the extracted muscle-tendon junctions reveals that the relationship between the terminal myofilaments and the lamina densa of the basal lamina is retained, despite the extensive extraction of the plasma membrane. Fine filaments (2-7 nm) are seen to connect the lamina densa with an electron-dense intracellular layer into which terminal actin filaments appear to insert. These fine filaments are considered to represent an important component of the structural linkage between myofilaments and connective tissue and hence to be a significant component of the tension transmitting mechanism. Their precise nature is not known, but some part of the filaments must pass through the hydrophobic compartment of the plasma membrane and thus must be a transmembrane component of considerable tensile strength. These studies suggest that detergent-extractable membrane lipids play no significant role in the transmission of tension at the muscle-tendon junction, and that fine filaments, probably protein, are responsible for transmitting tension from myofilaments, through the plasma membrane, to the lamina densa of the basal lamina.

Mechanotransduction in skeletal muscle

“…Force generated by the action of actin and myosin is aggregated by the rigid attachments at the Z-disks, and the Z-disks are tied into the cytoskeleton both along and perpendicular to the fiber axis (30,31). While there are clear morphological specializations at the myotendinous junction that suggest it plays an important role in transmitting that force to the extracellular matrix (ECM) and tendon (32,33), it is also clear that transmission of force by shear, often referred to as "lateral force transmission," contributes to whole muscle force transmission (19,34). The presence of elastic tissue, whether tendon, aponeurosis, or perimysium, in series with the contractile tissue means that active force generation will result in myofiber shortening during fixed endpoint activations (35,36), and potentially during lengthening activations (37,38).…”

Type VI collagen in mouse masseter tendon, from osseous attachment to myotendinous junction

“…The myotendinous 0 1995 WILEY-LISS. INC junction is a highly specialized region where the plasma membrane of the muscle cell is folded and invaginates to form finger-like structures; thus terminal cell processes interdigitate with tendon collagen fibers (Trotter et al, 1981;Tidball et al, 1986;Law, 1993). There were some reports on macromolecular composition at this junction (Trotter et al, 1983;Chiquet and Fambrough, 1984;Tidball et al, 1986;Tidball, 1992).…”

Functional Morphology of Force Transmission in Skeletal Muscle

“…Filamentous con nections are seen between the internal lamina and the lamina densa (e.g., the references in tables 1 and 2). Con necting filaments are also observed connecting the internal lamina with the external lamina after extraction of muscles in the nonionic detergent Triton X-l(X) [Trotter et al, 1981). That these detergent-resistant filaments transmit Model: C =right circular cylinder; P = paraboloid; o>=degree of orientation (not shapespecific) [see Eisenberg andMilton.…”

“…active tension between myofilaments and lamina densa, and ultimately to tendon collagen fibrils, is suggested by the ability of detergent-extracted muscles to exert active ten sion on their tendons [Trotter et al, 1981]. Chemical extraction studies have shown that the filaments are com posed of intracellular, transmembrane, and extracellular domains, which are differentially extractable [Trotter et al.…”