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Neurosensory mechanotransduction

Nature Reviews Molecular Cell Biology volume 10, pages 44–52 (2009)Cite this article

Key Points

  • Neurosensory mechanotransduction is rapid, which suggests that it requires the direct gating of transducing channels, rather than activation through chemical intermediates.

  • Candidate mechanosensory channels have been identified through assays for stretch-activated channels, genetic screens for mechanosensory defective animals and the investigation of proteins that are homologous to those found by the other two approaches.

  • Three families of channel proteins DEG/ENaC (degenerin (also known as ACCN1)/epithelial Na+ channel (ENaC; also known as SCNN1)) proteins, the transient receptor potential (TRP) proteins and the two-pore-domain K+ channel (K2P) proteins) have been implicated in mechanosensation in animals. A fourth family of channel bacterial proteins, the mechanosensitive channel of large conductance (MscS)-like proteins, is also found in plants.

  • Evidence for the involvement of these channel proteins in mechanosensation is variable. Many cannot be gated in heterologous systems and others, although required, might not be directly involved in transduction.

  • Three models have been proposed for the gating of mechanosensory channels. First, changes in forces in the lipid bilayer affect channel conformation (no other proteins are needed); second, stretching between tethered intracellular and extracellular structures opens the channels (membrane forces do not have a role); and third, movement of a single tether to the channel alters the interaction of the channel with the membrane and the forces inside it, thereby opening the channel.

Abstract

Neurons that sense touch, sound and acceleration respond rapidly to specific mechanical signals. The proteins that transduce these signals and underlie these senses, however, are mostly unknown. Research over the past decade has suggested that members of three families of channel proteins are candidate transduction molecules. Current studies are directed towards characterizing these candidates, determining how they are mechanically gated and discovering new molecules that are involved in mechanical sensing.

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Figure 1: A gallery of mechanosensitive cells.
Figure 2: Gentle touch in Caenorhabditis elegans.
Figure 3: Mechanosensory transduction in bacteria.
Figure 4: Dual-tether model.
Figure 5: Single-tether model.

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Acknowledgements

The author thanks J. Árnadóttir for helpful discussions. Research in the author's laboratory has been supported by grant GM30997 from the US Public Health Service.

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Glossary

Spheroplast

A preparation of bacterial membrane that can be recorded electrophysiologically. Spheroplasts are produced by using a bacterial strain that conditionally does not allow cell division, thus allowing the formation of large membrane structures.

Prohibitin domain

(PHB domain). A 150 amino-acid sequence that is found in several proteins in prokayotes and eukaryotes. Human PHB proteins include prohibitin, stomatin and podocin. The PHB domain in C. elegans MEC-2 and mouse podocin allows the binding of cholesterol.

Paraoxonase

A family of proteins in humans, two of which are associated with high-density lipoprotein particles and another is localized to the plasma membrane in a wide range of cells. A similar protein, MEC-6, is needed for touch sensitivity in C. elegans.

Chordotonal organ

The mechanosensory structure that is used in insects for mechanosensation and hearing.

Proprioception

The sense of body position and movement.

Stereocilium

An actin-containing projection in a vertebrate hair cell.

Kinocilum

The single projection in each vertebrate hair cell that contains a microtubule axoneme.

Connexin

A gap junction and hemijunction protein that is found in vertebrates.

Pannexin

A gap junction and hemijunction protein that is found in vertebrates and invertebrates. The invertebrate proteins were originally called innexins.

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Chalfie, M. Neurosensory mechanotransduction. Nat Rev Mol Cell Biol 10, 44–52 (2009). https://doi.org/10.1038/nrm2595

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