Length-tension relation in Limulus striated muscle.

Abstract

Laser diffraction techniques coupled with simultaneous tension measurements were used to determine the length-tension relation in intact, small (0.5-mm thick, 1 .0-mm wide, 20-25-mm long) bundles of a Limulus (horseshoe crab) striated muscle, the telson levator muscle . This muscle differs from the model vertebrate systems in that the thick filaments are not of a constant length, but shorten from 4.9 to -2 .0 ttm as the sarcomeres shorten from 7 to 3 ttm.In the Limulus muscle, the length-tension relation plateaued to an average maximum tension of 0.34 N/m m 2 at a sarcomere length of 6.5 ,um (Lo) to 8.0 ttm . In the sarcomere length range from 3.8 to 12 .5 ttm, the muscle developed 50% or more of the maximum tension. When the sarcomere lengths are normalized (expressed as L/Lo) and the Limulus data are compared to those from frog muscle, it is apparent that Limulus muscle develops tension over a relatively greater range of sarcomere lengths.Evidence is nearly irrefutable that, in vertebrate striated muscle, shortening of sarcomeres is accompanied structurally by a reduction in 1-band width and by a constancy of the A-band width. This observation, in addition to the evidence for the constancy of lengths of the thick and thin filaments that make up the A-and I-bands, has led to the generally accepted slidingfilament theory of muscle contraction proposed by Huxley and co-workers (10, 11) . Further support ofthis theory is the lengthtension data ofGordon et al. (9), which suggest that the amount of isometric tension developed by a vertebrate striated muscle fiber is determined by the degree of overlap of the thick and thin filaments and thus, presumably, the number of myosin bridges that can interact with actin .In one invertebrate muscle, however, it has been shown that a basic tenet of the sliding-filament model is not followed; in Limulus telson levator muscle the A-bands and constitutive thick filaments change length with sarcomere length. de Villafranca (4) was the first to report extensive changes in A-band length with sarcomere length in glycerinated Limulus muscle . This was confirmed by Dewey et al. (6), who additionally demonstrated by electron microscope observations that the shortening ofthe A-band below 5 ftm resulted from $hortening of the thick filaments. This observation was confirmed by a series of experiments in which thick filaments were isolated from muscle at different sarcomere lengths (8) . Long, thick filaments (-4.2 ttm) were isolated from muscles with long sarcomeres (8 pm), whereas short, thick filaments (-2 .9 /m) were isolated from muscle with short sarcomeres (6 lilm).Given this significant variation from the structural aspect of the vertebrate system and model, the question arises as to its 204 effect on the function of the Limulus muscle. Therefore, we have determined the length-tension diagram for Limulus telson muscle and have correlated it with structural information previously determined. MATERIALS AND METHODSAdult Limulus (20-30 cm across the carapace) were obtained from...

Elastic Properties of Isolated Thick Filaments Measured by Nanofabricated Cantilevers

“…For Limulus, the maximal tension during contraction is reported to be 0.34 N/mm 2 (Walcott and Dewey, 1980). Using a published cross-sectional electron micrograph of Limulus muscle (Eagles et al, 1982) we counted the thick filaments in the same way as described for Mytilus.…”

Invertebrate muscles: Thin and thick filament structure; molecular basis of contraction and its regulation, catch and asynchronous muscle

“…Work in tarantula shows that during cross-bridge cycling myosin heads bind weakly to a peripheral site on actin before binding to a strong binding site ) and that maintaining myosin head helical order on the thick filaments requires that the heads be in a specific conformational state with the so-called γ phosphate pocket closed (Zoghbi et al, 2004) A surprising but persistent observation in Limulus is that thick filament length changes with muscle shortening (de Villafranca, 1961;de Villafranca and Marchhaus, 1963;Stephens, 1965;Dewey et al, 1977;Walcott and Dewey, 1980;Huxley, 1985) (an early report of A-band shortening during contraction in stick insect muscle also exists, von Hehn, 1965). Isolated Limulus thick filaments also shorten when exposed to Ca ++ and ATP, and shortened filaments lengthen when incubated with phosphatase (Brann et al, 1979).…”

Fibre types inLimulus telson muscles: morphology and histochemistry

“…In particular, reexamination of the length-tension curves using single fibres of known morphology seems to be most important. Previous analyses of the length-tension relationship of Limulus telson muscles Walcott & Dewey, 1980) showed that active tension was developed by such bundles over a very great range of muscle and sarcomere lengths. The results of the studies we report here appear to bear on the ability of muscles stretched to 2L0 , or 14.0 l~m sarcomere length, to develop some degree of active tension.…”