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.
Highlights
Sleep, consisting of a period of sustained quiescence that is associated with an increased arousal threshold, is a common phenomenon that widely exists in animals from vertebrates to invertebrates [1]
The npf-gal4, UAS-npf, npfr1-gal4, UAS-npfr1, UAS-npf dsRNAi and UAS-NPFRdsRNAi lines have been widely used for regulation of npf and npfr1 expression [18,27]
The sleep increase at nighttime was due to a significant increase in sleep episode duration in the males of overexpressing npf (p < 0.001) but not in sleep bout number (Figure 3A, C) and the males of overexpressing npfr1 (p < 0.001) (Figure 3B & D)
Summary
Sleep, consisting of a period of sustained quiescence that is associated with an increased arousal threshold, is a common phenomenon that widely exists in animals from vertebrates to invertebrates [1]. Sleep regulation in Drosophila melanogaster is anatomically located in the mushroom body, known to be involved in learning and memory [3], while approximately 150 clock neurons in the central nervous system are involved in setting circadian rhythms. These clock neurons are divided into three lateral neuron groups - dorsolateral neurons (LN ds), PDF-positive ventrolateral neurons (LN Vs) and the fifth small ventrolateral neuron (5th small LNv) - and three dorsal neuron groups - dorsal neurons 1, 2, and 3 (DN1, DN2, DN3). Dorsal neurons function in modulating sleep suppression during starvation [7]
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