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The molecular basis for water taste in Drosophila

Nature volume 465, pages 91–95 (2010)Cite this article

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Abstract

The detection of water and the regulation of water intake are essential for animals to maintain proper osmotic homeostasis1. Drosophila and other insects have gustatory sensory neurons that mediate the recognition of external water sources2,3,4, but little is known about the underlying molecular mechanism for water taste detection. Here we identify a member of the degenerin/epithelial sodium channel family5, PPK28, as an osmosensitive ion channel that mediates the cellular and behavioural response to water. We use molecular, cellular, calcium imaging and electrophysiological approaches to show that ppk28 is expressed in water-sensing neurons, and that loss of ppk28 abolishes water sensitivity. Moreover, ectopic expression of ppk28 confers water sensitivity to bitter-sensing gustatory neurons in the fly and sensitivity to hypo-osmotic solutions when expressed in heterologous cells. These studies link an osmosensitive ion channel to water taste detection and drinking behaviour, providing the framework for examining the molecular basis for water detection in other animals.

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Figure 1: ppk28-Gal4 labels neurons that respond to water.
Figure 2: The ppk28 gene is necessary for cellular and behavioural water responses.
Figure 3: Ectopic expression of ppk28 confers water sensitivity.
Figure 4: Heterologous cells expressing PPK28 respond to hypo-osmolarity.

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References

  1. Bourque, C. W. Central mechanisms of osmosensation and systemic osmoregulation. Nature Rev. Neurosci. 9, 519–531 (2008)

    Article  CAS  Google Scholar 

  2. Evans, D. R. & Mellon, D. Electrophysiological studies of a water receptor associated with the taste sensilla of the blow-fly. J. Gen. Physiol. 45, 487–500 (1962)

    Article  CAS  Google Scholar 

  3. Meunier, N., Ferveur, J. F. & Marion-Poll, F. Sex-specific non-pheromonal taste receptors in Drosophila. Curr. Biol. 10, 1583–1586 (2000)

    Article  CAS  Google Scholar 

  4. Inoshita, T. & Tanimura, T. Cellular identification of water gustatory receptor neurons and their central projection pattern in Drosophila. Proc. Natl Acad. Sci. USA 103, 1094–1099 (2006)

    Article  ADS  CAS  Google Scholar 

  5. Kellenberger, S. & Schild, L. Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol. Rev. 82, 735–767 (2002)

    Article  CAS  Google Scholar 

  6. Awasaki, T. & Kimura, K. pox-neuro is required for development of chemosensory bristles in Drosophila. J. Neurobiol. 32, 707–721 (1997)

    Article  CAS  Google Scholar 

  7. Boll, W. & Noll, M. The Drosophila Pox neuro gene: control of male courtship behavior and fertility as revealed by a complete dissection of all enhancers. Development 129, 5667–5681 (2002)

    Article  CAS  Google Scholar 

  8. Yarmolinsky, D. A., Zuker, C. S. & Ryba, N. J. Common sense about taste: from mammals to insects. Cell 139, 234–244 (2009)

    Article  CAS  Google Scholar 

  9. Chyb, S., Dahanukar, A., Wickens, A. & Carlson, J. R. Drosophila Gr5a encodes a taste receptor tuned to trehalose. Proc. Natl Acad. Sci. USA 100 (suppl. 2). 14526–14530 (2003)

    Article  ADS  CAS  Google Scholar 

  10. Thorne, N., Chromey, C., Bray, S. & Amrein, H. Taste perception and coding in Drosophila. Curr. Biol. 14, 1065–1079 (2004)

    Article  CAS  Google Scholar 

  11. Wang, Z., Singhvi, A., Kong, P. & Scott, K. Taste representations in the Drosophila brain. Cell 117, 981–991 (2004)

    Article  CAS  Google Scholar 

  12. Marella, S. et al. Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49, 285–295 (2006)

    Article  CAS  Google Scholar 

  13. Moon, S. J., Kottgen, M., Jiao, Y., Xu, H. & Montell, C. A taste receptor required for the caffeine response in vivo. Curr. Biol. 16, 1812–1817 (2006)

    Article  CAS  Google Scholar 

  14. Fischler, W., Kong, P., Marella, S. & Scott, K. The detection of carbonation by the Drosophila gustatory system. Nature 448, 1054–1057 (2007)

    Article  ADS  CAS  Google Scholar 

  15. Meunier, N., Marion-Poll, F. & Lucas, P. Water taste transduction pathway is calcium dependent in Drosophila. Chem. Senses 34, 441–449 (2009)

    Article  CAS  Google Scholar 

  16. Parks, A. L. et al. Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nature Genet. 36, 288–292 (2004)

    Article  CAS  Google Scholar 

  17. Hiroi, M., Meunier, N., Marion-Poll, F. & Tanimura, T. Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. J. Neurobiol. 61, 333–342 (2004)

    Article  Google Scholar 

  18. 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 

  19. Werner-Reiss, U., Galun, R., Crnjar, R. & Liscia, A. Sensitivity of the mosquito Aedes aegypti (Culicidae) labral apical chemoreceptors to blood plasma components. J. Insect Physiol. 45, 485–491 (1999)

    Article  CAS  Google Scholar 

  20. Lindemann, B. Taste reception. Physiol. Rev. 76, 718–766 (1996)

    Article  Google Scholar 

  21. Gilbertson, T. A. Hypoosmotic stimuli activate a chloride conductance in rat taste cells. Chem. Senses 27, 383–394 (2002)

    Article  CAS  Google Scholar 

  22. Colbert, H. A., Smith, T. L. & Bargmann, C. I. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J. Neurosci. 17, 8259–8269 (1997)

    Article  CAS  Google Scholar 

  23. Muraki, K. et al. TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes. Circ. Res. 93, 829–838 (2003)

    Article  CAS  Google Scholar 

  24. Liu, L. et al. Drosophila hygrosensation requires the TRP channels water witch and nanchung. Nature 450, 294–298 (2007)

    Article  ADS  CAS  Google Scholar 

  25. Hummel, T., Krukkert, K., Roos, J., Davis, G. & Klambt, C. Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26, 357–370 (2000)

    Article  CAS  Google Scholar 

  26. Hiroi, M., Marion-Poll, F. & Tanimura, T. Differentiated response to sugars among labellar chemosensilla in Drosophila. Zoolog. Sci. 19, 1009–1018 (2002)

    Article  Google Scholar 

  27. Liu, L., Johnson, W. A. & Welsh, M. J. Drosophila DEG/ENaC pickpocket genes are expressed in the tracheal system, where they may be involved in liquid clearance. Proc. Natl Acad. Sci. USA 100, 2128–2133 (2003)

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We thank K. Vranizan for assistance with microarray analyses. K. Gerhold and D. Bautista provided the TRPV4 construct, protocols and advice for HEK293 experiments; the Roelink laboratory provided tissue culture facilities and advice. G. Agarwaal generated heat map images in Matlab for data presentation. W. Fischler generated the NP1017 G-CaMP data in Supplementary Information. We are grateful to C. Zuker and members of the Scott laboratory for comments on the manuscript. This work was supported by a grant from the NIH (NIDCD), a Burroughs-Wellcome CAREER Award and a John Merck Award to K.S. and a NIH predoctoral fellowship to P.C. K.S. is an HHMI Early Career Scientist.

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Authors and Affiliations

  1. Department of Molecular and Cell Biology and Helen Wills Neuroscience Institute, 16 Barker Hall,

    Peter Cameron, Makoto Hiroi & Kristin Scott

  2. Department of Molecular and Cell Biology, Helen Wills Neuroscience Institute and Functional Genomics Laboratory, 142 Life Sciences Addition,

    John Ngai

  3. Howard Hughes Medical Institute, University of California-Berkeley, Berkeley, California 94720, USA,

    Kristin Scott

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  1. Peter Cameron
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  2. Makoto Hiroi
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  4. Kristin Scott
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Contributions

P.C. performed most experiments and co-wrote the manuscript. M.H. performed the electrophysiological recordings and the HEK293 heterologous experiments. J.N. provided expertise on the microarray experiments. K.S. co-wrote the manuscript and supervised the project.

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Correspondence to Kristin Scott.

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The authors declare no competing financial interests.

Supplementary information

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This file contains Supplementary Figures S1-S6 with legends and Supplementary Table S1. (PDF 8415 kb)

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Cameron, P., Hiroi, M., Ngai, J. et al. The molecular basis for water taste in Drosophila. Nature 465, 91–95 (2010). https://doi.org/10.1038/nature09011

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