Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
Structural origin of the series elastic component in horseshoe crab skeletal muscle fibers
Introduction
The behavior of active skeletal muscle can be explained by postulating an elastic component in series with a contractile component [3]. During the isometric force development, the contractile component shortens internally by stretching the series elastic component (SEC) until the force exerted by the contractile component balances with the force in the SEC. Thus, the degree of extension of the SEC under the maximum isometric force (P0) is equal to the minimum amount of quick release required to drop the isometric force from P0 to zero. By carefully removing the external stray compliance, Jewell and Wilkie [7] showed that SEC in vertebrate skeletal muscle is distributed along the entire muscle length, and its degree of extension under P0 is about 1% of the slack muscle length (L0). This was confirmed by Huxley and Simmons [4] on single muscle fibers, and they put forward a contraction model in which the SEC (or the instantaneous elasticity) largely resides in the cross-bridges; each cross-bridge has an elastic link extending from the thick filament, and the link is extended by about 10 nm, i.e. about 1% of the length of a half-sarcomere, when the cross-bridge exerts its full force.
On the other hand, Suzuki and Sugi [11] presented evidence that the SEC resides not only in the cross-bridges but also in the thin filament in the myofilament nonoverlap region, i.e. the I-band in each sarcomere. Recently, it has been established that, in vertebrate skeletal muscle fibers, about 50% of the SEC extension at P0 (5 nm per half-sarcomere) originates from elastic extension of the thin filaments in the I-band, while the rest 50% of the SEC extension (also 5 nm per half-sarcomere) originates form the cross-bridges [5], [11], [12], [15].
In some arthropod skeletal muscles, the sarcomere length at L0 is very long (5–10 μm) compared to that in vertebrate skeletal muscle fibers (about 2 μm) [6]. If the cross-bridge and thin filament elasticities are assumed to be the same in all types of skeletal muscle, the extension of the cross-bridges at P0 is the same (5 nm per half-sarcomere) irrespective of the sarcomere length, while the extension of the thin filaments in the I-band is 5×I/0.2 nm, where I/0.2 is the I-band length per half-sarcomere at L0 relative to the corresponding value in vertebrate skeletal muscle fibers. In crayfish abdominal extensor muscle fibers, the sarcomere length at L0 is about 9 μm while the A-band length is about 6 μm [13]. The extension of the SEC at P0 is estimated on the above basis to be (5+5×1.5/0.2)=42.5 nm per half-sarcomere, i.e. about 0.9% of L0. Contrary to this estimation, the extension of the SEC at P0 was about 2% of L0, i.e. about 90 nm per half-sarcomere, and this compliant SEC distributed uniformly along the fiber length, indicating that there would be an additional source of the SEC in each sarcomere [9], [13]. Unfortunately, irregular striation patterns of crayfish fibers made it difficult to further study the structural origin of the SEC.
The present experiments were undertaken to investigate the structural origin of the highly compliant SEC in arthropod skeletal muscle fibers, using the telson depressor muscle fibers of a horseshoe crab Tachypleus tridentatus, which exhibited a reasonably uniform striation pattern along their entire length. It will be shown that the highly compliant SEC in the telson depressor muscle fibers largely originates from elastic misalignment of the thick filaments in the A-band.
Section snippets
Intact fiber preparation
Horseshoe crab (T. tridentatus) with carapace of 18–35 cm long were collected at Fukuoka, Japan, and fed in aerated sea-water in the laboratory until used. Telson depressor muscles [1] were isolated from the animals, and were carefully teased to obtain small fiber bundles (major diameter, 0.5–1 mm; slack length L0, 1.6–3.4 cm) with a piece of carapace attached to one end and a piece of tendon left at the other. The fiber bundle preparation was mounted horizontally in a glass experimental
Force-extension curve of the SEC in intact muscle fiber bundle preparations
A typical force-extension curve of the SEC of the intact fiber bundle preparation electrically stimulated at L0 is shown in Fig. 1, in which the force immediately after quick release is plotted against the amount of quick release. The minimum amount of quick release required to reduce the force from P0 to zero was 5.8±0.5% of L0 (mean±S.D., n=15). The above degree of extension of the SEC at P0 (about 6% of L0 or 210 nm per half-sarcomere) is obviously too large for the elastic extension of the
Elastic A-band lengthening as the main source of the compliant SEC
The present experiments have shown that, in electrically stimulated telson depressor muscle fibers, the extension of the SEC at P0 (6% of L0 or 210 nm per half-sarcomere) is too large to be explained by elastic extension of the cross-bridges and the thin filaments (Fig. 1, Fig. 2), and that, in Ca2+-activated myofibril bundles, the A-band length is lengthened transiently by about 10% during the initial sarcomere shortening (Fig. 3, Fig. 4, Fig. 5). The latter results can be taken to indicate
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