Changes in striated muscle fibres during contraction and growth with particular reference to myofibril splitting

Abstract

Ultrastructural measurements were carried out on the mouse biceps brachii and soleus muscles fixed at different states of contraction and stretch. At a sarcomere length of 2·7–2·9 μm the more peripheral actin filaments ran slightly obliquely from the Z-disk to the A-band. This is due to a mismatch between the rhombic actin lattice at the Z-disk and the hexagonal lattice at the M-line. For a perfect transformation of a rhombic lattice into a hexagonal lattice the ratio of the lattice spacings has to be 1:1·51. However, at this sarcomere length the ratio is about 1:2·0 (Z:M). During contraction the angle of the peripheral actin filaments remains approxi-mately the same because the expansion of the M lattice is compensated for, partly by an increase in the Z-lattice spacing and partly by the bowing of the peripheral myosin filaments. When the sarcomeres are stretched beyond 3·0 μm the myosin filaments straighten out and the Z:M ratio decreases. The ratio of 1:1·51 is almost attained when there is no overlap of the actin and myosin filaments. Ultrastructural measurements were also carried out on biceps brachii muscles of different ages. The lattice spacings for a standard sarcomere length did not change during the post-natal growth period. The amount of myofibrillar material and sarcoplasmic reticulum plus transverse tubular system were estimated using linear analysis for muscles at 3 different stages of growth. It was found that the myofibrillar cross-sectional area in an individual muscle fibre may increase 40-fold during growth and that the transverse tubular and sarcoplasmic reticulum systems increase at about the same rate. In both the biceps brachii and the soleus muscles the myosin and actin filaments are not built into a continuous mass but they are divided into numerous discrete myofibrils. Subdivision of the myofibril mass occurs because the myofibrils split once they attain a certain size. The evidence presented in this paper supports the suggestion that the longitudinal splitting of the myofibrils occurs by the ripping of the Z-disks. When tension is rapidly developed by 2 adjacent sarco-meres a stress is produced at the centre of the Z-disk resulting from the oblique pull of the actin filaments. This causes some of the Z-disk filaments to rip and the rip then extends across the disk with the direction of the weave of the lattice. Evidence for the mechanism includes electron-micrographs showing Z-disks that are apparently just commencing to split; in these cases a hole can be seen in the centre of the disk. A model experiment is described which demonstrates the importance of the rate of tension development in causing myofibril splitting. Rapid tension development produces a snatch effect which causes the Z-disk filaments to break more readily. This may explain why the myofibrils in fast muscles tend to be small and discrete whilst those in slow muscles are larger and more irregular in shape.