All animals and plants, even protozoa, have evolved specialized molecular sensors that convert mechanical stress into behavioral responses. The touch receptor neurons (TRNs) in Caenorhabditis elegans respond to gentle body touch and are especially well characterized on a physiological and ultrastructural level, a knowledge which is unavailable in other animals. Moreover, C. elegans is a unique model organism to study the mechanics of neurons due to their simple shapes, the known wiring diagram and a rich repertoire of simple behaviors, thus permitting a systems perspective on cell function.
As in other animals, neuron morphology is critical for function in C. elegans. Some neurons are highly branched and curved, while others are extremely straight. We have previously shown that a functional, pre-stressed spectrin network is critical for mechanosensation and neuron stability under body-evoked forces (Krieg, Nat Cell Bio, 2014). How the constituent molecules of these different neurons establish a functional organization and how nanometer sized molecules can determine cell shape in the millimeter scale is still not understood. To establish this paradigm, we first compared different neurons and classified their shapes. We then used electron and STED microscopy to investigate how the organization of microtubule bundles and spectrin network determines neuron morphology. We found that TRNs with defective organization in both cytoskeletal elements undergo deformations highly similar to a twisted rod under compression. These experimental results, together with mechanical modeling of the neuron, suggest that spectrin tension and microtubule bundle mechanics are crucial for stabilizing chiral cytoskeletal networks and produce a specialized cell shape that we propose is critical for mechanosensation.
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