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http://dx.doi.org/10.14348/molcells.2015.0215

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)
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).
Keywords
Anopheles gambiae; citronellal; Drosophila melanogaster; human TRPA1; insect repellent; TRPA1;
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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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
12 Meunier, N., Rospars, J., Tanimura, T., and Marion-Poll, F. (2003). Peripheral coding of bitter taste in Drosophila. J. Neurobiol. 56, 139-152.   DOI   ScienceOn
13 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.
14 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.   DOI   ScienceOn
15 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.   DOI   ScienceOn
16 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.   DOI   ScienceOn