Mechanical control of the sense of touch by β-spectrin

Nat Cell Biol. 2014 Mar;16(3):224-33. doi: 10.1038/ncb2915. Epub 2014 Feb 23.

Abstract

The ability to sense and respond to mechanical stimuli emanates from sensory neurons and is shared by most, if not all, animals. Exactly how such neurons receive and distribute mechanical signals during touch sensation remains mysterious. Here, we show that sensation of mechanical forces depends on a continuous, pre-stressed spectrin cytoskeleton inside neurons. Mutations in the tetramerization domain of Caenorhabditis elegans β-spectrin (UNC-70), an actin-membrane crosslinker, cause defects in sensory neuron morphology under compressive stress in moving animals. Through atomic force spectroscopy experiments on isolated neurons, in vivo laser axotomy and fluorescence resonance energy transfer imaging to measure force across single cells and molecules, we show that spectrin is held under constitutive tension in living animals, which contributes to elevated pre-stress in touch receptor neurons. Genetic manipulations that decrease such spectrin-dependent tension also selectively impair touch sensation, suggesting that such pre-tension is essential for efficient responses to external mechanical stimuli.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Biomechanical Phenomena
  • Caenorhabditis elegans
  • Caenorhabditis elegans Proteins / physiology*
  • Cell Shape
  • Mechanoreceptors / metabolism*
  • Mechanoreceptors / physiology
  • Mechanotransduction, Cellular
  • Movement
  • Mutation, Missense
  • Protein Interaction Domains and Motifs / genetics
  • Protein Multimerization
  • Spectrin / physiology*
  • Touch*
  • Vision, Ocular

Substances

  • Caenorhabditis elegans Proteins
  • unc-70 protein, C elegans
  • Spectrin