Abstract
We show that the level of the core protein of the circadian clock Period (PER) expressed by glial peripheral oscillators depends on their location in the Drosophila optic lobe. It appears to be controlled by the ventral lateral neurons (LNvs) that release the circadian neurotransmitter Pigment Dispersing Factor (PDF). We demonstrate that glial cells of the distal medulla neuropil (dMnGl) that lie in the vicinity of the PDF-releasing terminals of the LNvs possess receptors for PDF (PDFRs) and express PER at significantly higher level than other types of glia. Surprisingly, the amplitude of PER molecular oscillations in dMnGl is increased twofold in PDF-free environment, that is in Pdf0 mutants. The Pdf0 mutants also reveal an increased level of glia-specific protein REPO in dMnGl. The photoreceptors of the compound eye (R-cells) of the PDF-null flies, on the other hand, exhibit de-synchrony of PER molecular oscillations, which manifests itself as increased variability of PER-specific immunofluorescence among the R-cells. Moreover, the daily pattern of expression of the presynaptic protein Bruchpilot (BRP) in the lamina terminals of the R-cells is changed in Pdf0 mutant. Considering that PDFRs are also expressed by the marginal glia of the lamina that surround the R-cell terminals, the LNv pacemakers appear to be the likely modulators of molecular cycling in the peripheral clocks of both the glial cells and the photoreceptors of the compound eye. Consequently, some form of PDF-based coupling of the glial clocks and the photoreceptors of the eye with the central LNv pacemakers must be operational.
Highlights
The circadian clocks, displaying molecular oscillations of canonical clock molecules Period (PER) and Timeless (TIM) with a period of ∼24 h, are endogenous pacemakers that lay cellular foundation for biological timekeeping (Tataroglu and Emery, 2015)
They send projections to the optic lobe and densely arborize on the surface of the second optic neuropil, the medulla (Helfrich-Förster, 1998; Helfrich-Förster et al, 2007). They are, anatomically well-situated to receiving the light input from the retina of the compound eye and conveying circadian signals to the optic lobe. They control the output by the paracrine release of the main circadian transmitter - the neuropeptide Pigment Dispersing Factor (PDF) (HelfrichFörster, 1997; Park et al, 2000), and by signaling via its receptor— PDFR (Renn et al, 1999; Lin et al, 2004; Lear et al, 2005; Shafer et al, 2008; Im and Taghert, 2010; Im et al, 2011)
It was detected in the nuclei of circadian pacemaker neurons, compound eye photoreceptors, and numerous glial cells (Figure 1A)
Summary
The circadian clocks, displaying molecular oscillations of canonical clock molecules Period (PER) and Timeless (TIM) with a period of ∼24 h, are endogenous pacemakers that lay cellular foundation for biological timekeeping (Tataroglu and Emery, 2015). Even though the oscillatory pattern of the glia was similar to that of the neuronal oscillators (cf Figure 2), the average daily level of nuclear immunofluorescence in dMnGl was 52% lower than in the LNvs and 65% lower than in the R-cells (Kruskal–Wallis Test: H [2, N = 210] = 59.7, p = 0.00001, followed by Multiple Comparison Test, p = 0.00002 and p = 0.000001, respectively).
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