The cytoskeletal lattice of muscle cells

Abstract

By modulating the level of structural organization of two primary components, actin and myosin, nature has devised a wide range of actin-based motile systems. At one extreme is the cross-striated muscle cell with its highly ordered and stable arrangement of filaments, specialised for rapid contractions. And at the other are non-muscle cells, like fibroblasts and amoebae, whose dynamic protrusive movements depend on the continual growth and breakdown of less organised actin filament arrays coupled, in some way, with the shearing of monomeric, tailless myosin molecules.Left to their own devices, in vitro, actin and myosin filaments can form contractile threads [268] but these are poorly organized and inefficient. Order in contractile assemblies must therefore be brought about by other components, accessory molecules, whose function is to link filaments with each other and with the cell membrane. In order to characterise such accessory molecules and gain insight into assembly principles, efforts have been mainly concentrated on vertebrate skeletal muscle. This system has been favoured, first, because it readily facilitates a combined biochemical and microscopic approach and, second, because early data (reviewed in [261 I) had already pointed to the existence in the sarcomere of structural material distinct from the contractile elements. Results accumulated over the last decade or so from skeletal muscle, together with complementary data from other systems, has now led to the recognition of a complex structural lattice in muscle cells; included in this lattice is an organised membrane skeleton whose components may play roles in maintaining sarcomere integrity. The purpose ofthis review is to survey recent advances in our understanding of the organisation and function of this structural lattice. The starting point is skeletal muscle but we shall also analyse cardiac and smooth muscle as well as other muscle types for which relevant information is available. Previous reviews of this subject have been presented by Obinata et al. [164], Wang [261], Maruyama [139], Price [181] and Trinick [239, 2401. CROSS-STRIATED MUSCLEIt is notable that the first indications of the existence of a structural lattice in striated muscle came in parallel with the discovery of the actin-and myosin-based sliding filament

Desmin and actin alterations in human muscles affected by delayed onset muscle soreness: a high resolution immunocytochemical study

“…In several reviews on the structure and composition of skeletal muscle, longitudinal desmin filaments surrounding successive sarcomeres are suggested to be a common feature of the desmin cytoskeleton (Price 1991;Waterman-Storer 1991;Small et al 1992;Capetanaki and Milner 1998;Stromer 1998;Dalakas et al 2000). This conclusion is based on studies on chicken and rabbit muscles (Price and Sanger 1979;Tokuyasu et al 1983;Wang and Ramirez Mitchell 1983).…”

“…A feature related to the Z-discs is the desmin intermediate filament network, which surrounds and links the Zdiscs to each other and to the sarcolemma (Small et al 1992;Carlsson and Thornell 2001). On the basis of studies on animal models of eccentric contraction-induced injury, it has been proposed that damage to this network is an early event after DOMS-causing exercise, which results in loss of myofibrillar registry, i.e., Z-disc streaming and A-band disorganization, loss of cell integrity, inflammation, and muscle degeneration (Lieber and Friden 2002).…”

Differences in the distribution of synemin, paranemin, and plectin in skeletal muscles of wild-type and desmin knock-out mice

“…Specializations of the cytoskeleton are present at the sarcolemma, especially at the costameres, neuromuscular junctions, and myotendinous junctions (Small et al 1992). Knowledge about the membrane cytoskeleton has 43 Fig.…”

“…Desmin, the major IF protein in adult skeletal muscle, is mainly localized around the myofibrils at the Z-disc level and at the sarcolemma (Small et al 1992). It is also abundant at neuromuscular and myotendinous junctions, where IFs may be involved in the anchoring of myofibrils to the junctional sarcolemma (Askanas et al 1990;Tidball 1992).…”

Eccentric contractions leading to DOMS do not cause loss of desmin nor fibre necrosis in human muscle

“…The most significant structural abnormality that occurs after eccentric exercise in a rabbit model is the selective loss of desmin (Lieber et al 1996;Lieber 1998, 2001), the major intermediate filament protein in muscle. Desmin is thought to act as an extrasarcomeric mechanical stabiliser of myofibrillar regularity and integrity (Small et al 1992). In desmin knockout mice, a cardiomyopathy and a muscular dystrophy can be observed in muscles which are highly solicited, supporting the role of the cytoskeleton in maintaining muscle integrity (Thornell et al 1997;Carlsson and Thornell 2001).…”