Drosophila TRPA channel modulates sugar-stimulated neural excitation, avoidance and social response

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Abstract

Drosophila melanogaster postfeeding larvae show food-averse migration toward food-free habitats before metamorphosis. This developmental switching from food attraction to aversion is regulated by a neuropeptide Y (NPY)-related brain signaling peptide. We used the fly larva model to delineate the neurobiological basis of age-restricted response to environmental stimuli. Here we provide evidence for a fructose-responsive chemosensory pathway that modulates food-averse migratory and social behaviors. We found that fructose potently elicited larval food-averse behaviors, and painless (pain), a transient receptor potential channel that is responsive to noxious stimuli, was required for the fructose response. A subset of pain-expressing sensory neurons have been identified that show pain-dependent excitation by fructose. Although evolutionarily conserved avoidance mechanisms are widely appreciated for their roles in stress coping and survival, their biological importance in animal physiology and development remains unknown. Our findings demonstrate how an avoidance mechanism is recruited to facilitate animal development.

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Figure 1: Behavioral procedures for larval response to aversive food chemicals.
Figure 2: pain is involved in larval aversion to fruit juice and fructose.
Figure 3: Conditional disruption of pain-expressing neuronal signaling attenuates larval food aversion.
Figure 4: Larvae expressing a mammalian vanilloid receptor show capsaicin-averse behaviors.
Figure 5: Imaging and SOARS analysis of excitation of thoracic PAIN neurons by fructose with the cameleon Ca2+ indicator.
Figure 6: Ablation of fructose-responsive PAIN-expressing neurons in the thoracic segments disrupts larval food aversion.

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Acknowledgements

The authors thank S. Benzer, W.D. Tracey, L. Liu, M. Welsch, K. Scott and H. Kitamoto for fly strains. This work is supported by grants from the US National Institutes of Health (AA014348 and DK058348 to P.S. and EB005432 to A.T.S.).

Author information

J.X. carried out the behavioral and imaging experiments. J.K.L. contributed to the behavioral assays and immunostaining. A.T.S. supervised the design of the imaging experiments and data analysis. A.T.S. and J.X. performed imaging data analysis, and helped with writing the manuscript. P.S. supervised the project and wrote the manuscript.

Correspondence to Ping Shen.

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Xu, J., Sornborger, A., Lee, J. et al. Drosophila TRPA channel modulates sugar-stimulated neural excitation, avoidance and social response. Nat Neurosci 11, 676–682 (2008) doi:10.1038/nn.2119

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