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A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue

Nature volume 440, pages 684–687 (2006)Cite this article

Abstract

The nematode Caenorhabditis elegans is commonly used as a genetic model organism for dissecting integration of the sensory and motor systems1. Despite extensive genetic and behavioural analyses that have led to the identification of many genes and neural circuits involved in regulating C. elegans locomotion behaviour1, it remains unclear whether and how somatosensory feedback modulates motor output during locomotion. In particular, no stretch receptors have been identified in C. elegans, raising the issue of whether stretch-receptor-mediated proprioception is used by C. elegans to regulate its locomotion behaviour. Here we have characterized TRP-4, the C. elegans homologue of the mechanosensitive TRPN channel. We show that trp-4 mutant worms bend their body abnormally, exhibiting a body posture distinct from that of wild-type worms during locomotion, suggesting that TRP-4 is involved in stretch-receptor-mediated proprioception. We show that TRP-4 acts in a single neuron, DVA, to mediate its function in proprioception, and that the activity of DVA can be stimulated by body stretch. DVA both positively and negatively modulates locomotion, providing a unique mechanism whereby a single neuron can fine-tune motor activity. Thus, DVA represents a stretch receptor neuron that regulates sensory–motor integration during C. elegans locomotion.

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Figure 1: Defective locomotion in trp-4 mutants.
Figure 2: Dopamine neurons mediate the fast bending phenotype of trp-4 mutants.
Figure 3: TRP-4 functions in DVA to regulate the extent of body bending.
Figure 4: The DVA neuron is stretch-sensitive.

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Acknowledgements

We thank J. Nakai for the G-CaMP plasmid; B. Perry for help with deletion libraries; C. Cronin for assistance with data analysis; G. Schindelman, N. Moghal, C. Montell and A. Ward for comments; and G. Medina, E. Larkspur and R. Mahapatra for technical assistance. Some strains were obtained from the Caenorhabditis Genetics Center. This work was supported by the University of Michigan BSSP Scholar Program (X.Z.S.X.), the Helen Hay Whitney Foundation (X.Z.S.X), and the Howard Hughes Medical Institute, of which P.W.S. is an investigator.

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Authors and Affiliations

  1. Life Sciences Institute, University of Michigan,

    Wei Li, Zhaoyang Feng & X. Z. Shawn Xu

  2. Department of Molecular and Integrative Physiology, University of Michigan Medical School, Michigan, 48109, Ann Arbor, USA

    X. Z. Shawn Xu

  3. Howard Hughes Medical Institute and Division of Biology, California Institute of Technology, California, 91125, Pasadena, USA

    Paul W. Sternberg

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Correspondence to X. Z. Shawn Xu.

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Supplementary information

Supplementary Figure 1

TRP-4 expression pattern. (PDF 150 kb)

Supplementary Figure 2

Representative calcium imaging traces of various mutants. (PDF 166 kb)

Supplementary Figure 3

DVA neurons lacking TRP-4 can still respond to membrane depolarization. (PDF 152 kb)

Supplementary Figure 4

Amplitude of calcium response versus bending angles. (PDF 81 kb)

Supplementary Methods

Additional methods not described in the main text. (DOC 37 kb)

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Li, W., Feng, Z., Sternberg, P. et al. A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 440, 684–687 (2006). https://doi.org/10.1038/nature04538

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