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A G-protein-coupled neuropeptide Y-like receptor suppresses behavioral and sensory response to multiple stressful stimuli in Drosophila.

ABSTRACT: Recent studies suggest that human neuropeptide Y (NPY) plays a prominent role in management of stress response and emotion, and higher NPY levels observed in combat-exposed veterans may help coping with posttraumatic stress. Neuropeptide F (NPF), the counterpart of NPY in Drosophila melanogaster, also displays parallel activities, including promotion of resilience to diverse stressors and prevention of uncontrolled aggressive behavior. However, it remains unclear how NPY family peptides modulate physical and emotional responses to various stressors. Here we show that NPFR1, a G-protein-coupled NPF receptor, exerts an inhibitory effect on larval aversion to diverse stressful stimuli mediated by different subtypes of fly and mammalian transient receptor potential (TRP) family channels. Imaging analysis in larval sensory neurons and cultured human cells showed that NPFR1 attenuates Ca(2+) influx mediated by fly TRPA and rat TRPV1 channels. Our findings suggest that suppression of TRP channel-mediated neural excitation by the conserved NPF/NPFR1 system may be a major mechanism for attaining its broad anti-stress function.

SUBMITTER: Xu J

PROVIDER: S-EPMC2849674 | biostudies-literature | 2010 Feb

REPOSITORIES: biostudies-literature

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A G-protein-coupled neuropeptide Y-like receptor suppresses behavioral and sensory response to multiple stressful stimuli in Drosophila.

Xu Jie J Li Mo M Shen Ping P

The Journal of neuroscience : the official journal of the Society for Neuroscience 20100201 7

Recent studies suggest that human neuropeptide Y (NPY) plays a prominent role in management of stress response and emotion, and higher NPY levels observed in combat-exposed veterans may help coping with posttraumatic stress. Neuropeptide F (NPF), the counterpart of NPY in Drosophila melanogaster, also displays parallel activities, including promotion of resilience to diverse stressors and prevention of uncontrolled aggressive behavior. However, it remains unclear how NPY family peptides modulate ...[more]

PMID: 20164335

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Project description:Insects respond to the spatial and temporal dynamics of a pheromone plume, which implies not only a strong response to 'odor on', but also to 'odor off'. This requires mechanisms geared toward a fast signal termination. Several mechanisms may contribute to signal termination, among which odorant-degrading enzymes. These enzymes putatively play a role in signal dynamics by a rapid inactivation of odorants in the vicinity of the sensory receptors, although direct in vivo experimental evidences are lacking. Here we verified the role of an extracellular carboxylesterase, esterase-6 (Est-6), in the sensory physiological and behavioral dynamics of Drosophila melanogaster response to its pheromone, cis-vaccenyl acetate (cVA). Est-6 was previously linked to post-mating effects in the reproductive system of females. As Est-6 is also known to hydrolyze cVA in vitro and is expressed in the main olfactory organ, the antenna, we tested here its role in olfaction as a putative odorant-degrading enzyme.We first confirm that Est-6 is highly expressed in olfactory sensilla, including cVA-sensitive sensilla, and we show that expression is likely associated with non-neuronal cells. Our electrophysiological approaches show that the dynamics of olfactory receptor neuron (ORN) responses is strongly influenced by Est-6, as in Est-6° null mutants (lacking the Est-6 gene) cVA-sensitive ORN showed increased firing rate and prolonged activity in response to cVA. Est-6° mutant males had a lower threshold of behavioral response to cVA, as revealed by the analysis of two cVA-induced behaviors. In particular, mutant males exhibited a strong decrease of male-male courtship, in association with a delay in courtship initiation.Our study presents evidence that Est-6 plays a role in the physiological and behavioral dynamics of sex pheromone response in Drosophila males and supports a role of Est-6 as an odorant-degrading enzyme (ODE) in male antennae. Our results also expand the role of Est-6 in Drosophila biology, from reproduction to olfaction, and highlight the role of ODEs in insect olfaction.

Project description:BackgroundNociception evokes a rapid withdrawal behavior designed to protect the animal from potential danger. C. elegans performs a reflexive reversal or forward locomotory response when presented with noxious stimuli at the head or tail, respectively. Here, we have developed an assay with precise spatial and temporal control of an infrared laser stimulus that targets one-fifth of the worm's body and quantifies multiple aspects of the worm's escape response.ResultsWhen stimulated at the head, we found that the escape response can be elicited by changes in temperature as small as a fraction of a degree Celsius, and that aspects of the escape behavior such as the response latency and the escape direction change advantageously as the amplitude of the noxious stimulus increases. We have mapped the behavioral receptive field of thermal nociception along the entire body of the worm, and show a midbody avoidance behavior distinct from the head and tail responses. At the midbody, the worm is sensitive to a change in the stimulus location as small as 80 ?m. This midbody response is probabilistic, producing either a backward, forward or pause state after the stimulus. The distribution of these states shifts from reverse-biased to forward-biased as the location of the stimulus moves from the middle towards the anterior or posterior of the worm, respectively. We identified PVD as the thermal nociceptor for the midbody response using calcium imaging, genetic ablation and laser ablation. Analyses of mutants suggest the possibility that TRPV channels and glutamate are involved in facilitating the midbody noxious response.ConclusionThrough high resolution quantitative behavioral analysis, we have comprehensively characterized the C. elegans escape response to noxious thermal stimuli applied along its body, and found a novel midbody response. We further identified the nociceptor PVD as required to sense noxious heat at the midbody and can spatially differentiate localized thermal stimuli.

Dataset Information

A G-protein-coupled neuropeptide Y-like receptor suppresses behavioral and sensory response to multiple stressful stimuli in Drosophila.

Publications

A G-protein-coupled neuropeptide Y-like receptor suppresses behavioral and sensory response to multiple stressful stimuli in Drosophila.

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