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

Nature volume 440, pages 684687 (30 March 2006) | Download Citation

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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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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.

Author information

Affiliations

  1. Life Sciences Institute, University of Michigan, and

    • Wei Li
    • , Zhaoyang Feng
    •  & X. Z. Shawn Xu
  2. Department of Molecular and Integrative Physiology, University of Michigan Medical School, Ann Arbor, Michigan 48109, USA

    • X. Z. Shawn Xu
  3. Howard Hughes Medical Institute and Division of Biology, California Institute of Technology, Pasadena, California 91125, USA

    • Paul W. Sternberg

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Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Corresponding author

Correspondence to X. Z. Shawn Xu.

Supplementary information

PDF files

  1. 1.

    Supplementary Figure 1

    TRP-4 expression pattern.

  2. 2.

    Supplementary Figure 2

    Representative calcium imaging traces of various mutants.

  3. 3.

    Supplementary Figure 3

    DVA neurons lacking TRP-4 can still respond to membrane depolarization.

  4. 4.

    Supplementary Figure 4

    Amplitude of calcium response versus bending angles.

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    Supplementary Methods

    Additional methods not described in the main text.

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DOI

https://doi.org/10.1038/nature04538

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