Muscle thick filaments are rigid coupled tubules, not flexible ropes.

Understanding the structures of thick filaments and their relation to muscle contraction has been an important problem in muscle biology. The flexural rigidity of natural thick filaments isolated from Caenorhabditis elegans as determined by statistical analysis of their electron microscopic images shows that they are considerably more rigid (persistence length=263 microm) than similarly analyzed synthetic actin filaments (6 microm) or duplex DNA (0.05 microm), which are known to be helical ropes. Indeed, cores of C. elegans thick filaments, having only 11% of the mass per unit length of intact thick filaments, are quite rigid (85 microm) compared with the thick filaments. Cores comprise the backbones of the thick filaments and are composed of tubules containing seven subfilaments cross-linked by non-myosin proteins. Microtubules reconstituted from tubulin and microtubule-associated proteins are nearly as rigid (55 microm) as the cores. We propose a model of coupled tubules as the structural basis for the observed rigidity of natural thick filaments and other linear structures such as microtubules. A similar model was recently presented for microtubules [Felgner et al., 1997]. This coupled tubule model may also explain the differences in flexural rigidity between natural rabbit skeletal muscle thick filaments (27 microm) or synthetic thick filaments reconstituted from myosin and myosin binding protein C (36 microm) and those reconstituted from purified myosin (9 microm). The more flexible myosin structures may be helical ropes like F-actin or DNA, whereas the more rigid muscle or synthetic thick filaments which contain myosin and myosin binding protein C may be constructed of subfilaments coupled into tubules as in C. elegans cores. The observed thick filament rigidity is necessary for the incompressibility and lack of flexure observed with thick filaments in contracting skeletal muscle.