Dataset Information

Regulation of sleep by neuropeptide Y-like system in Drosophila melanogaster.

ABSTRACT: Sleep is important for maintenance of normal physiology in animals. In mammals, neuropeptide Y (NPY), a homolog of Drosophila neuropeptide F (NPF), is involved in sleep regulation, with different effects in human and rat. However, the function of NPF on sleep in Drosophila melanogaster has not yet been described. In this study, we investigated the effects of NPF and its receptor-neuropeptide F receptor (NPFR1) on Drosophila sleep. Male flies over-expressing NPF or NPFR1 exhibited increased sleep during the nighttime. Further analysis demonstrated that sleep episode duration during nighttime was greatly increased and sleep latency was significantly reduced, indicating that NPF and NPFR1 promote sleep quality, and their action on sleep is not because of an impact of the NPF signal system on development. Moreover, the homeostatic regulation of flies after sleep deprivation was disrupted by altered NPF signaling, since sleep deprivation decreased transcription of NPF in control flies, and there were less sleep loss during sleep deprivation and less sleep gain after sleep deprivation in flies overexpressing NPF and NPFR1 than in control flies, suggesting that NPF system auto-regulation plays an important role in sleep homeostasis. However, these effects did not occur in females, suggesting a sex-dependent regulatory function in sleep for NPF and NPFR1. NPF in D1 brain neurons showed male-specific expression, providing the cellular locus for male-specific regulation of sleep by NPF and NPFR1. This study brings a new understanding into sleep studies of a sexually dimorphic regulatory mode in female and male flies.

SUBMITTER: He C

PROVIDER: S-EPMC3770577 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Regulation of sleep by neuropeptide Y-like system in Drosophila melanogaster.

He Chunxia C Yang Yunyan Y Zhang Mingming M Price Jeffrey L JL Zhao Zhangwu Z

PloS one 20130911 9

Sleep is important for maintenance of normal physiology in animals. In mammals, neuropeptide Y (NPY), a homolog of Drosophila neuropeptide F (NPF), is involved in sleep regulation, with different effects in human and rat. However, the function of NPF on sleep in Drosophila melanogaster has not yet been described. In this study, we investigated the effects of NPF and its receptor-neuropeptide F receptor (NPFR1) on Drosophila sleep. Male flies over-expressing NPF or NPFR1 exhibited increased sleep ...[more]

PMID: 24040211

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Project description:Sleep abnormalities have widespread and costly public health consequences, yet we have only a rudimentary understanding of the events occurring at the cellular level in the brain that regulate sleep. Several key signaling molecules that regulate sleep across taxa come from the family of neuropeptide transmitters. For example, in Drosophila melanogaster, the neuropeptide Y (NPY)-related transmitter short neuropeptide F (sNPF) appears to promote sleep. In this study, we utilized optogenetic activation of neuronal populations expressing sNPF to determine the causal effects of precisely timed activity in these cells on sleep behavior. Combining sNPF-GAL4 and UAS-Chrimson transgenes allowed us to activate sNPF neurons using red light. We found that activating sNPF neurons for as little as 3 s at a time of day when most flies were awake caused a rapid transition to sleep that persisted for another 2+ hours following the stimulation. Changing the timing of red light stimulation to times of day when flies were already asleep caused the control flies to wake up (due to the pulse of light), but the flies in which sNPF neurons were activated stayed asleep through the light pulse, and then showed further increases in sleep at later points when they would have normally been waking up. Video recording of individual fly responses to short-term (0.5-20 s) activation of sNPF neurons demonstrated a clear light duration-dependent decrease in movement during the subsequent 4-min period. These results provide supportive evidence that sNPF-producing neurons promote long-lasting increases in sleep, and show for the first time that even brief periods of activation of these neurons can cause changes in behavior that persist after cessation of activation. We have also presented evidence that sNPF neuron activation produces a homeostatic sleep drive that can be dissipated at times long after the neurons were stimulated. Future studies will determine the specific roles of sub-populations of sNPF-producing neurons, and will also assess how sNPF neurons act in concert with other neuronal circuits to control sleep.

Project description:Animals respond to changes in food availability by adjusting sleep and foraging strategies to optimize their fitness. Wild populations of the fruit fly, Drosophila melanogaster, display highly variable levels of starvation resistance that are dependent on geographic location, food availability and evolutionary history. How behaviors that include sleep and feeding vary in Drosophila with increased starvation resistance is unclear. We have generated starvation-resistant flies through experimental evolution to investigate the relationship between foraging behaviors and starvation resistance. Outbred populations of D. melanogaster were selected for starvation resistance over 60 generations. This selection process resulted in flies with a threefold increase in total lipids that survive up to 18 days without food. We tested starvation-selected (S) flies for sleep and feeding behaviors to determine the effect that selection for starvation resistance has had on foraging behavior. Flies from three replicated starvation-selected populations displayed a dramatic reduction in feeding and prolonged sleep duration compared to fed control (F) populations, suggesting that modified sleep and feeding may contribute to starvation resistance. A prolonged larval developmental period contributes to the elevated energy stores present in starvation-selected flies. By preventing S larvae from feeding longer than F larvae, we were able to reduce energy stores in adult S flies to the levels seen in adult F flies, thus allowing us to control for energy storage levels. However, the reduction of energy stores in S flies fails to generate normal sleep and feeding behavior seen in F flies with similar energy stores. These findings suggest that the behavioral changes observed in S flies are due to genetic regulation of behavior rather than elevated lipid levels. Testing S-F hybrid individuals for both feeding and sleep revealed a lack of correlation between food consumption and sleep duration, indicating further independence in genetic factors underlying the sleep and feeding changes observed in S flies. Taken together, these findings provide evidence that starvation selection results in prolonged sleep and reduced feeding through a mechanism that is independent of elevated energy stores. These findings suggest that changes in both metabolic function and behavior contribute to the increase in starvation resistance seen in flies selected for starvation resistance.

Dataset Information

Regulation of sleep by neuropeptide Y-like system in Drosophila melanogaster.

Publications

Regulation of sleep by neuropeptide Y-like system in Drosophila melanogaster.

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