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Food experience–induced taste desensitization modulated by the Drosophila TRPL channel

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Abstract

Animals tend to reject bitter foods. However, long-term exposure to some unpalatable tastants increases acceptance of these foods. Here we show that dietary exposure to an unappealing but safe additive, camphor, caused the fruit fly Drosophila melanogaster to decrease camphor rejection. The transient receptor potential-like (TRPL) cation channel was a direct target for camphor in gustatory receptor neurons, and long-term feeding on a camphor diet led to reversible downregulation of TRPL protein concentrations. The turnover of TRPL was controlled by an E3 ubiquitin ligase, Ube3a. The decline in TRPL levels and increased acceptance of camphor reversed after returning the flies to a camphor-free diet long term. We propose that dynamic regulation of taste receptors by ubiquitin-mediated protein degradation comprises an important molecular mechanism that allows an animal to alter its taste behavior in response to a changing food environment.

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Figure 1: Behavioral and electrophysiological responses of wild-type flies after feeding on a normal or camphor-containing diet.
Figure 2: Electrophysiological responses of wild-type flies after feeding on a normal or camphor-containing diet.
Figure 3: Requirement for trpl in responding to the taste of camphor.
Figure 4: Camphor directly activates TRPL.
Figure 5: TRPL localizes to GRN dendrites.
Figure 6: Effects of a camphor or normal diet on TRPL protein expression in GRNs.
Figure 7: ube3a is required to form camphor-induced taste desensitization.
Figure 8: Effects of camphor exposure on the number of synaptic boutons formed by trpl-expressing GRNs in the SOG.

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Acknowledgements

We thank J. Fischer (University of Texas at Austin), K. Scott (University of California, Berkeley) and the Bloomington Stock Center for providing fly stocks, FlyBase for genomic information and B. Minke (Hebrew University, Jerusalem) for the pMT-trpl-eGFP construct. This work was supported by grants to C.M. from the US National Institute on Deafness and Other Communication Disorders (DC007864) and the US National Eye Institute (EY010852).

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Y.V.Z. conceived of the project, designed and performed most of the experiments and wrote the manuscript. R.P.R. assisted Y.V.Z. in the behavioral assays. W.L.S. generated the trpl-GAL4 lines. C.M. supervised the experimental design and interpretations and wrote the manuscript.

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Correspondence to Craig Montell.

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Zhang, Y., Raghuwanshi, R., Shen, W. et al. Food experience–induced taste desensitization modulated by the Drosophila TRPL channel. Nat Neurosci 16, 1468–1476 (2013). https://doi.org/10.1038/nn.3513

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