Desmin integrates the three-dimensional mechanical properties of muscles.
Striated muscle is a linear motor whose properties have been defined in terms of uniaxial structures. The question addressed here is what contribution is made to the properties of this motor by extramyofilament cytoskeletal structures that are not aligned in parallel with the myofilaments. This question arose from observations that transverse loads increase muscle force production in diaphragm but not in the hindlimb muscle, thereby indicating the presence of structures that couple longitudinal and transverse properties of diaphragmatic muscle. Furthermore, we find that the diaphragms of null mutants for the cytoskeletal protein desmin show 1) significant reductions in coupling between the longitudinal and transverse properties, indicating for the first time a role for a specific protein in integrating the three-dimensional mechanical properties of muscle, 2) significant reductions in the stiffness and viscoelasticity of muscle, and 3) significant increases in tetanic force production. Thus desmin serves a complex mechanical function in diaphragm muscle by contributing both to passive stiffness and viscoelasticity and to modulation of active force production in a three-dimensional structural network. Our finding changes the paradigm of force transmission among cells by placing our understanding of the function of the cytoskeleton in the context of the structural and mechanical complexity of muscles.
Boriek
A M
AM
Department of Medicine, Baylor College of Medicine, Houston, Texas 77030, USA. boriek@bcm.tmc.edu
Capetanaki
Y
Y
Hwang
W
W
Officer
T
T
Badshah
M
M
Rodarte
J
J
Tidball
J G
JG
D000818:Animals; D001696:Biomechanical Phenomena; D003599:Cytoskeleton / Q000378:metabolism / Q000648:ultrastructure; D003893:Desmin / Q000378:metabolism*; D003964:Diaphragm / Q000378:metabolism / Q000648:ultrastructure; D006614:Hindlimb / Q000502:physiology; D051379:Mice; D018345:Mice, Knockout; D009119:Muscle Contraction / Q000502:physiology*; D018485:Muscle Fibers, Skeletal / Q000378:metabolism* / Q000648:ultrastructure; D018482:Muscle, Skeletal / Q000378:metabolism* / Q000648:ultrastructure; D013314:Stress, Mechanical; D016474:Weight-Bearing / Q000502:physiology*
D003893:Desmin