Abstract
Our bodies are in constant motion and so are the neurons that invade each tissue. Motion-induced neuron deformation and damage are associated with several neurodegenerative conditions. Here, we investigated the question of how the neuronal cytoskeleton protects axons and dendrites from mechanical stress, exploiting mutations in UNC-70 β-spectrin, PTL-1 tau/MAP2-like and MEC-7 β-tubulin proteins in Caenorhabditis elegans. We found that mechanical stress induces supercoils and plectonemes in the sensory axons of spectrin and tau double mutants. Biophysical measurements, super-resolution, and electron microscopy, as well as numerical simulations of neurons as discrete, elastic rods provide evidence that a balance of torque, tension, and elasticity stabilizes neurons against mechanical deformation. We conclude that the spectrin and microtubule cytoskeletons work in combination to protect axons and dendrites from mechanical stress and propose that defects in β-spectrin and tau may sensitize neurons to damage.
Highlights
Neurons play a central role in receiving and distributing information and depend on long, slender axons and dendrites for their function
We focused on the six touch receptor neurons (TRNs) required for sensing gentle touch (Chalfie et al, 1985) because they are among the best characterized neurons in the C. elegans nervous system
B-tubulin, and tau are highly conserved from C. elegans to humans and constitute the major protein content in the mammalian central nervous system, our results provide a mechanistic framework for understanding how neurons remain resilient in the face of mechanical stress
Summary
Neurons play a central role in receiving and distributing information and depend on long, slender axons and dendrites for their function. Vertebrate peripheral neurons can be meters long and less than 1 mm in diameter: the peripheral neurons of Cetaceans have aspect ratios exceeding a factor of 10,000,000 (Wedel, 2012). Despite their slender construction, peripheral neurons have axons that bend without breaking—that is they are robust enough to withstand the mechanical deformations generated during body movements under most conditions. It is of central importance to understand how neurons maintain their shape and function in the mechanically active environment of our bodies
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