Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

A TRPV family ion channel required for hearing in Drosophila

Nature volume 424, pages 81–84 (2003)Cite this article

Abstract

The many types of insect ear share a common sensory element, the chordotonal organ, in which sound-induced antennal or tympanal vibrations are transmitted to ciliated sensory neurons and transduced to receptor potentials1,2. However, the molecular identity of the transducing ion channels in chordotonal neurons, or in any auditory system, is still unknown3,4. Drosophila that are mutant for NOMPC, a transient receptor potential (TRP) superfamily ion channel, lack receptor potentials and currents in tactile bristles5,6 but retain most of the antennal sound-evoked response7, suggesting that a different channel is the primary transducer in chordotonal organs. Here we describe the Drosophila Nanchung (Nan) protein, an ion channel subunit similar to vanilloid-receptor-related (TRPV) channels of the TRP superfamily. Nan mediates hypo-osmotically activated calcium influx and cation currents in cultured cells. It is expressed in vivo exclusively in chordotonal neurons and is localized to their sensory cilia. Antennal sound-evoked potentials are completely absent in mutants lacking Nan, showing that it is an essential component of the chordotonal mechanotransducer.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Molecular analysis of nan.
Figure 2: Nan mediates cation influx in response to hypo-osmotic stress.
Figure 3: Expression of Nan in chordotonal organs.
Figure 4: Behavioural and electrophysiological defects in nan mutants.

References

  1. Yager, D. D. Structure, development, and evolution of insect auditory systems. Microsc. Res. Tech. 47, 380–400 (1999)

    Article  CAS  Google Scholar 

  2. Eberl, D. F. Feeling the vibes: chordotonal mechanisms in insect hearing. Curr. Opin. Neurobiol. 9, 389–393 (1999)

    Article  CAS  Google Scholar 

  3. Caldwell, J. C. & Eberl, D. F. Towards a molecular understanding of Drosophila hearing. J. Neurobiol. 53, 172–189 (2002)

    Article  CAS  Google Scholar 

  4. Strassmaier, M. & Gillespie, P. G. The hair cell's transduction channel. Curr. Opin. Neurobiol. 12, 380–386 (2002)

    Article  CAS  Google Scholar 

  5. Kernan, M. J., Cowan, D. & Zuker, C. Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron 12, 1195–1206 (1994)

    Article  CAS  Google Scholar 

  6. Walker, R., Willingham, A. & Zuker, C. A Drosophila mechanosensory transduction channel. Science 287, 2229–2234 (2000)

    Article  ADS  CAS  Google Scholar 

  7. Eberl, D., Hardy, R. & Kernan, M. J. Genetically similar transduction mechanisms for touch and hearing in Drosophila. J. Neurosci. 20, 5981–5988 (2000)

    Article  CAS  Google Scholar 

  8. Gunthorpe, M. J., Benham, C. D., Randall, A. & Davis, J. B. The diversity in the vanilloid (TRPV) receptor family of ion channels. Trends Pharmacol. Sci. 23, 183–191 (2002)

    Article  CAS  Google Scholar 

  9. Benham, C. D., Davis, J. B. & Randall, A. D. Vanilloid and TRP channels: a family of lipid-gated cation channels. Neuropharmacology 42, 873–888 (2002)

    Article  CAS  Google Scholar 

  10. Colbert, H., Smith, T. & Bargmann, C. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J. Neurosci. 17, 8259–8369 (1997)

    Article  CAS  Google Scholar 

  11. Tobin, D. et al. Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35, 307–318 (2002)

    Article  CAS  Google Scholar 

  12. Caterina, M. et al. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816–824 (1997)

    Article  ADS  CAS  Google Scholar 

  13. Caterina, M. J. et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288, 306–313 (2000)

    Article  ADS  CAS  Google Scholar 

  14. Caterina, M. J., Rosen, T. A., Tominaga, M., Brake, A. J. & Julius, D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398, 436–441 (1999)

    Article  ADS  CAS  Google Scholar 

  15. Liedtke, W. et al. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103, 525–535 (2000)

    Article  CAS  Google Scholar 

  16. Adams, M. et al. The genome sequence of Drosophila melanogaster. Science 287, 2185–2195 (2000)

    Article  Google Scholar 

  17. Littleton, J. T. & Ganetzky, B. Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 26, 35–43 (2000)

    Article  CAS  Google Scholar 

  18. Strotmann, R., Harteneck, C., Nunnenmacher, K., Schultz, G. & Plant, T. D. OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nature Cell. Biol. 2, 695–702 (2000)

    Article  CAS  Google Scholar 

  19. Vandaele, C., Coulon-Bublex, M., Couble, P. & Durand, B. Drosophila regulatory factor X is an embryonic type I sensory neuron marker also expressed in spermatids and in the brain of Drosophila. Mech. Dev. 103, 159–162 (2001)

    Article  CAS  Google Scholar 

  20. Dubruille, R. et al. Drosophila regulatory factor X is necessary for ciliated sensory neuron differentiation. Development 129, 5487–5498 (2002)

    Article  CAS  Google Scholar 

  21. Chung, Y., Zhu, J., Han, Y. & Kernan, M. nompA encodes a PNS-specific, ZP-domain protein required to connect mechanosensory dendrites to sensory structures. Neuron 29, 415–428 (2001)

    Article  CAS  Google Scholar 

  22. Xu, H. et al. Regulation of a TRP channel by tyrosine phosphorylation: Src family kinase-dependent phosphorylation of TRPV4 on Y253 mediates its response to hypotonic stress. J. Biol. Chem. 278, 11520–11527 (2003)

    Article  CAS  Google Scholar 

  23. Guler, A. D. et al. Heat-evoked activation of the ion channel, TRPV4. J. Neurosci. 22, 6408–6414 (2002)

    Article  CAS  Google Scholar 

  24. Watanabe, H. et al. Activation of TRPV4 channels (hVRL-2/mTRP12) by phorbol derivatives. J. Biol. Chem. 277, 13569–13577 (2002)

    Article  CAS  Google Scholar 

  25. Moller, S., Croning, M. D. & Apweiler, R. Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17, 646–653 (2001)

    Article  CAS  Google Scholar 

  26. Schultz, J., Milpetz, F., Bork, P. & Ponting, C. P. SMART, a simple modular architecture research tool: Identification of signalling domains. Proc. Natl Acad. Sci. USA 95, 5857–5864 (1998)

    Article  ADS  CAS  Google Scholar 

  27. Brand, A. H. & Perrimon, N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415 (1993)

    CAS  Google Scholar 

Download references

Acknowledgements

We thank K.-W. Choi and S. Lee for comments on a preliminary version of this manuscript; W. Sullivan for nuf1; and the Korea Basic Science Institute for use of equipment for Ca2+ measurement and electron microscope. This work was supported in part by a National Institute of Deafness and Communicative Disorders grant to M.K., by a Korea Research Foundation Grant to C.S.P. and by a Creative Research Initiatives of the Korean Ministry of Science and Technology grant to J.Y.

Author information

Authors and Affiliations

  1. Department of Genetics, Hanwha Chemical Co. R&D Center, Sinsung-Dong, Yusung-Gu, Daejeon, 305-345, Korea

    Janghwan Kim, Dae-young Park, SooKyung Choi, Dong Wook Shin, Hye Won Lee, Wonseok Son & Changsoo Kim

  2. Department of Microbiology, Chungnam National University, Daejeon, 305-764, Korea

    Janghwan Kim

  3. Department of Neurobiology & Behavior, State University of New York at Stony Brook, New York, 11794, USA

    Yun Doo Chung & Maurice J. Kernan

  4. Behavior, State University of New York at Stony Brook, New York, 11794

    Yun Doo Chung & Maurice J. Kernan

  5. Center for Developmental Genetics, State University of New York at Stony Brook, New York, 11794, USA

    Yun Doo Chung & Maurice J. Kernan

  6. Department of Life Science, K-JIST, Gwangju, 500-712, Korea

    Heun Soh & Chul-Seung Park

  7. National Creative Research Institute for Genetic Reprogramming, Seoul National University, Seoul, 151-742, Korea

    Jeongbin Yim

Authors
  1. Janghwan Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yun Doo Chung
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dae-young Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. SooKyung Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dong Wook Shin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Heun Soh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hye Won Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Wonseok Son
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jeongbin Yim
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Chul-Seung Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Maurice J. Kernan
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Changsoo Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Changsoo Kim.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kim, J., Chung, Y., Park, Dy. et al. A TRPV family ion channel required for hearing in Drosophila. Nature 424, 81–84 (2003). https://doi.org/10.1038/nature01733

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01733

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing