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Du EJ
,
Ahn TJ
,
Choi MS
,
Kwon I
,
Kim HW
,
Kwon JY
,
Kang K
.
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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 B1 0.2 and 0.1 B1 0.03 mM, 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).
Fig. 1. dTRPA1(A), and not dTRPA1(B), heterologously expressed in Xenopus oocytes is activated by citronellal. (AâC) Left, Representative current recordings at â60 and +60 mV from (A) dTRPA1(A)-, (B) dTRPA1(B)-, or (C) dTRPA1(A)2C-expressing oocytes. Right, Current-voltage (IV) relationship observed at the indicated citronellal concentrations ranging from 0 to 10 mM. (D) Dose dependence of indicated Drosophila TRPA1 variants of TRPA1(A), TRPA1(A)2C and TRPA1(B) in Xenopus oocytes (n = 5â6). Mean±standard error of mean (SEM) is shown. ***: p < 0.001, Tukey tests.
Fig. 2. hTRPA1 exhibits functional parameters intermediate to agTRPA1(A) and dTRPA1(A) when heterologously expressed in Xenopus oocytes. (AâD) Indicated TRPA1 channels were heterologously expressed in oocytes and subjected to electrophysiological characterization upon exposure to different doses of citronellal. Responses at +60 and â60 mV are shown in the left panels and IV relationships in the right panels. RR: 0.05 mM ruthenium red, a TRPA1 inhibitor. (E) Citronellal dose-dependence of Anopheles gambiae TRPA1 (agTRPA1) isoforms and human TRPA1 (hTRPA1) in oocytes. Letters indicate statistically distinct groups (Tukey, p < 0.01, n = 6â7). ***: p < 0.001, Studentâs t-test. (F) Maximal citronellal responses normalized to those of NMM. Citronellal concentrations used for maximal responses: 10 mM for dTRPA1s, agTRPA1(B), hTRPA1, and 1 mM for agTRPA1(A) channels (n = 6â7). ***: p < 0.001, all comparisons. ###: p < 0.001, comparisons between dTRPA1s and agTRPA1(B) that show means lower than 1.0. ANOVA Tukey test.
Fig. 3. Citronellal facilitates activation of TrpA1-positive gustatory neurons by NMM at the suboptimal concentration of 1 mM. (A) Typical examples of extracellular action potential recordings of taste neurons in I-type sensilla. The viability of non-responding neurons in WT and TrpA1ins was examined by exposure to 1 mM berberine that stimulates TrpA1-independent bitter signaling in the same neuron as shown in (C). (B) Bar graphs represent averages of spiking frequencies from in (A). (C) Reintroduction of Drosophila TrpA1 cDNAs differentially restored the neuronal responses to a mixture of 2 mM citronellal and 1 mM NMM. (D) A summary of experiments in (C). (E) Neuronal responses to berberine and caffeine were not enhanced by citronellal, unlike NMM. The number of experiments is presented in grey on each bar (B, D, and E). p < 0.001, ANOVA Tukey test.
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