Evidence for increased myofibrillar mobility in desmin-null mouse skeletal muscle

Abstract

SUMMARY Quantitative electron microscopy was used to characterize the longitudinal mobility of myofibrils during muscle extension to investigate the functional roles of skeletal muscle intermediate filaments. Extensor digitorum longus fifth toe muscles from wild-type (+/+) and desmin-null (des –/–) animals were passively stretched to varying lengths, and the horizontal displacement of adjacent Z-disks in neighboring myofibrils (Δxmyo) and average sarcomere length (SL) were calculated. At short SL (<2.20 μm), wild-type and desmin-null Δxmyo were not significantly different, although there was a trend towards greater Z-disk misalignment in muscles from knockout animals (Δxmyo 0.34±0.04 μm versus 0.22±0.09 μm; P>0.2; means ± s.e.m.). However, at higher SL (>2.90 μm), muscles from knockout animals displayed a dramatically increased Δxmyo relative to wild-type muscles (0.49±0.10 μm versus 0.25±0.07 μm; P<0.05). The results, which establish a maximum extension of the desmin network surrounding the Z-disk, provide what we believe to be the first quantitative estimation of the functional limits of the desmin intermediate filament system in the presence of an intact myofibrillar lattice. The existence of a limit on the extension of desmin suggests a mechanism for the recruitment of desmin into a network of force transmission, whether as a longitudinal load bearer or as a component in a radial force-transmission system.