Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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The Mosquito Repellent Citronellal Directly Potentiates Drosophila TRPA1, Facilitating Feeding Suppression

  • Du, Eun Jo (Samsung Biomedical Research Institute, School of Medicine, Sungkyunkwan University) ;
  • Ahn, Tae Jung (Samsung Biomedical Research Institute, School of Medicine, Sungkyunkwan University) ;
  • Choi, Min Sung (Department of Biological Sciences, Sungkyunkwan University) ;
  • Kwon, Ilmin (Samsung Biomedical Research Institute, School of Medicine, Sungkyunkwan University) ;
  • Kim, Hyung-Wook (College of Life Sciences, Sejong University) ;
  • Kwon, Jae Young (Department of Biological Sciences, Sungkyunkwan University) ;
  • Kang, KyeongJin (Samsung Biomedical Research Institute, School of Medicine, Sungkyunkwan University)
  • Received : 2015.08.07
  • Accepted : 2015.08.26
  • Published : 2015.10.31
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Abstract

Citronellal, a well-known plant-derived mosquito repellent, was previously reported to repel Drosophila melanogaster via olfactory pathways involving but not directly activating Transient Receptor Potential Ankyrin 1 (TRPA1). Here, we show that citronellal is a direct agonist for Drosophila and human TRPA1s (dTRPA1 and hTRPA1) as well as Anopheles gambiae TRPA1 (agTRPA1). Citronellal-induced activity is isoform-dependent for Drosophila and Anopheles gambiae TRPA1s. The recently identified dTRPA1(A) and ag-TRPA1(A) isoforms showed citronellal-provoked currents with EC50s of $1.0{\pm}0.2$ and $0.1{\pm}0.03mM$, respectively, in Xenopus oocytes, while the sensitivities of TRPA1(B)s were much inferior to those of TRPA1(A)s. Citronellal dramatically enhanced the feeding-inhibitory effect of the TRPA1 agonist N-methylmaleimide (NMM) in Drosophila at an NMM concentration that barely repels flies. Thus, citronellal can promote feeding deterrence of fruit flies through direct action on gustatory dTRPA1, revealing the first isoform-specific function for TRPA1(A).

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References

  1. Carlson, L.H.C., Machado, R.aF., Spricigo, C.B., Pereira, L.K., and Bolzan, A. (2001). Extraction of lemongrass essential oil with dense carbon dioxide. J. Supercrit. Fluids 21, 33-39. https://doi.org/10.1016/S0896-8446(01)00085-7
  2. Choi, S.H., Lee, B.H., Kim, H.J., Jung, S.W., Kim, H.S., Shin, H.C., Lee, J.H., Kim, H.C., Rhim, H., Hwang, S.H., et al. (2014). Ginseng gintonin activates the human cardiac delayed rectifier $K^+$ channel: involvement of $Ca^{2+}$/calmodulin binding sites. Mol. Cells 37, 656-663. https://doi.org/10.14348/molcells.2014.0087
  3. Dunipace, L., Meister, S., McNealy, C., and Amrein, H. (2001). Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr. Biol. 11, 822-835. https://doi.org/10.1016/S0960-9822(01)00258-5
  4. Goldman-Huertas, B., Mitchell, R.F., Lapoint, R.T., Faucher, C.P., Hildebrand, J.G., and Whiteman, N.K. (2015). Evolution of herbivory in Drosophilidae linked to loss of behaviors, antennal responses, odorant receptors, and ancestral diet. Proc. Natl. Acad. Sci. USA 112, 201424656.
  5. Hamada, F.N., Rosenzweig, M., Kang, K., Pulver, S.R., Ghezzi, A., Jegla, T.J., and Garrity, P.A. (2008). An internal thermal sensor controlling temperature preference in Drosophila. Nature 454, 217-220. https://doi.org/10.1038/nature07001
  6. Ja, W.W., Carvalho, G.B., Mak, E.M., de la Rosa, N.N., Fang, A.Y., Liong, J.C., Brummel, T., and Benzer, S. (2007). Prandiology of Drosophila and the CAFE assay. Proc. Natl. Acad. Sci. USA 104, 8253-8256. https://doi.org/10.1073/pnas.0702726104
  7. Kang, K., Pulver, S.R., Panzano, V.C., Chang, E.C., Griffith, L.C., Theobald, D.L., and Garrity, P.A. (2010). Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception. Nature 464, 597-600. https://doi.org/10.1038/nature08848
  8. Kang, K., Panzano, V.C., Chang, E.C., Ni, L., Dainis, A.M., Jenkins, A.M., Regna, K., Muskavitch, M.A.T., and Garrity, P.A. (2012). Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature 481, 76-80. https://doi.org/10.1038/nature10715
  9. Kwon, Y., Kim, S.H., Ronderos, D.S., Lee, Y., Akitake, B., Woodward, O.M., Guggino, W.B., Smith, D.P., and Montell, C. (2010). Drosophila TRPA1 channel is required to avoid the naturally occurring insect repellent citronellal. Curr. Biol. 20, 1672-1678. https://doi.org/10.1016/j.cub.2010.08.016
  10. Larsson, M.C., Domingos, A.I., Jones, W.D., Chiappe, M.E., Amrein, H., and Vosshall, L.B. (2004). Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703-714. https://doi.org/10.1016/j.neuron.2004.08.019
  11. Macpherson, L.J., Dubin, A.E., Evans, M.J., Marr, F., Schultz, P.G., Cravatt, B.F., and Patapoutian, A. (2007). Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445, 541-545. https://doi.org/10.1038/nature05544
  12. Meunier, N., Rospars, J., Tanimura, T., and Marion-Poll, F. (2003). Peripheral coding of bitter taste in Drosophila. J. Neurobiol. 56, 139-152. https://doi.org/10.1002/neu.10235
  13. Ni, L., Bronk, P., Chang, E.C., Lowell, A.M., Flam, J.O., Panzano, V.C., Theobald, D.L., Griffith, L.C., and Garrity, P.A. (2013). A gustatory receptor paralogue controls rapid warmth avoidance in Drosophila. Nature 500, 580-584. https://doi.org/10.1038/nature12390
  14. Sakulku, U., Nuchuchua, O., Uawongyart, N., Puttipipatkhachorn, S., Soottitantawat, A., and Ruktanonchai, U. (2009). Characterization and mosquito repellent activity of citronella oil nanoemulsion. Int. J. Pharm. 372, 105-111. https://doi.org/10.1016/j.ijpharm.2008.12.029
  15. Weiss, L.a, Dahanukar, A., Kwon, J.Y., Banerjee, D., and Carlson, J.R. (2011). The molecular and cellular basis of bitter taste in Drosophila. Neuron 69, 258-272. https://doi.org/10.1016/j.neuron.2011.01.001
  16. Zhou, Y., Suzuki, Y., Uchida, K., and Tominaga, M. (2013). Identification of a splice variant of mouse TRPA1 that regulates TRPA1 activity. Nat. Commun. 4, 2399.

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