Abstract
Circadian plasticity of the visual system of Drosophila melanogaster depends on functioning of both the neuronal and glial oscillators. The clock function of the former is already quite well-recognized. The latter, however, is much less known and documented. In this study we focus on the glial oscillators that reside in the distal part of the second visual neuropil, medulla (dMnGl), in vicinity of the PIGMENT-DISPERSING FACTOR (PDF) releasing terminals of the circadian clock ventral Lateral Neurons (LNvs). We reveal the heterogeneity of the dMnGl, which express the clock protein PERIOD (PER) and the pan-glial marker REVERSED POLARITY (REPO) at higher (P1) or lower (P2) levels. We show that the cells with stronger expression of PER display also stronger expression of REPO, and that the number of REPO-P1 cells is bigger during the day than during the night. Using a combination of genetic markers and immunofluorescent labeling with anti PER and REPO Abs, we have established that the P1 and P2 cells can be associated with two different types of the dMnGl, the ensheathing (EnGl), and the astrocyte-like glia (ALGl). Surprisingly, the EnGl belong to the P1 cells, whereas the ALGl, previously reported to play the main role in the circadian rhythms, display the characteristics of the P2 cells (express very low level of PER and low level of REPO). Next to the EnGl and ALGl we have also observed another type of cells in the distal medulla that express PER and REPO, although at very low levels. Based on their morphology we have identified them as the T1 interneurons. Our study reveals the complexity of the distal medulla circadian network, which appears to consist of different types of glial and neuronal peripheral clocks, displaying molecular oscillations of higher (EnGl) and lower (ALGl and T1) amplitudes.
Highlights
Glial cells of Drosophila are as diverse as their counterparts in vertebrates, with which they share many morphological and functional features
We focus on PER-expressing glial cells, which are located in the distal part of the second visual neuropil, the medulla, in vicinity of the PIGMENT-DISPERSING FACTOR (PDF) releasing terminals of the circadian clock large Ventral Lateral Neurons (l-Nvs)
In our recent study (Walkowicz et al, 2017) we found that DmMANF is strongly expressed in the epithelial glial cells (EGl) of the first visual neuropil
Summary
Glial cells of Drosophila are as diverse as their counterparts in vertebrates, with which they share many morphological and functional features (for review see Freeman and Doherty, 2006). Glial cells that express the so called clock genes are considered to be the peripheral clocks (oscillators) in the fruit fly circadian (∼24 h) timing system, comparable to photoreceptors and other sensory neurons (reviewed in Jackson et al, 2015; Zwarts et al, 2015; Chi-Castañeda and Ortega, 2016). Studies of mammalian glial cells have likewise demonstrated the presence of functional clocks in astrocytes and microglia, which express e.g., Per and Per in a rhythmic manner (Prolo et al, 2005; Marpegan et al, 2011; Hayashi et al, 2013; Fonken et al, 2015; Brancaccio et al, 2017; Chi-Castañeda and Ortega, 2018). The glial cells in both mammals and in Drosophila appear to be equipped with the same core components of the clock mechanism as the central clocks
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