Abstract
Drosophila melanogaster is a common model used to study circadian rhythms in behavior and circadian clocks. However, numerous circadian rhythms have also been detected in non-clock neurons, especially in the first optic neuropil (lamina) of the fly’s visual system. Such rhythms have been observed in the number of synapses and in the structure of interneurons, which exhibit changes in size and shape in a circadian manner. Although the patterns of these changes are known, the mechanism remains unclear. In the present study, we investigated the role of the TOR signaling pathway and autophagy in regulating circadian rhythms based on the behavior and structural plasticity of the lamina L2 monopolar cell dendritic trees. In addition, we examined the cyclic expression of the TOR signaling pathway (Tor, Pi3K class 1, Akt1) and autophagy (Atg5 and Atg7) genes in the fly’s brain. We observed that Tor, Atg5 and Atg7 exhibit rhythmic expressions in the brain of wild-type flies in day/night conditions (LD 12:12) that are abolished in per01 clock mutants. The silencing of Tor in per expressing cells shortens a period of the locomotor activity rhythm of flies. In addition, silencing of the Tor and Atg5 genes in L2 cells disrupts the circadian plasticity of the L2 cell dendritic trees measured in the distal lamina. In turn, silencing of the Atg7 gene in L2 cells changes the pattern of this rhythm. Our results indicate that the TOR signaling pathway and autophagy are involved in the regulation of circadian rhythms in the behavior and plasticity of neurons in the brain of adult flies.
Highlights
Circadian rhythms observed in animal behavior and in the brain are generated by a circadian system composed of central and peripheral clocks
The target of rapamycin (TOR) signaling pathway and autophagy are involved in the regulation of the locomotor activity rhythm, the activity level, sleep and circadian plasticity of L2 monopolar cells
Atg5 and Atg7 genes showed cyclic expressions in the brain of Canton S flies kept in light and 12 hours of darkness (LD 12):12, and these rhythms were abolished in the brain of per01 mutants
Summary
Circadian rhythms observed in animal behavior and in the brain are generated by a circadian system composed of central (pacemaker) and peripheral clocks. The dendrites are longest at the beginning of the day and shorter later during the day and at night in LD 12:12 This rhythm is maintained in constant darkness (DD) but not in continuous light (LL), which indicates that this type of plasticity is controlled by the circadian clock in the brain of D. melanogaster. Because the TOR signaling pathway is responsible for regulating several cellular processes, including translation and autophagy, a process of protein degradation, we hypothesized that these two processes might be involved in the regulation of circadian plasticity of L2 monopolar cells. Since locomotor activity and sleep are relatively easy to measure we used both behaviors to observe effects of the decreased TOR or autophagy protein levels in per-expressing clock cells on the period of the locomotor activity rhythm, the total activity, the day sleep and the night sleep in Drosophila.
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