Peptidergic clock neurons in <i>Drosophila</i>: Ion transport peptide and short neuropeptide F in subsets of dorsal and ventral lateral neurons

Johard, Helena A.D.; Yoishii, Taishi; Dircksen, Heinrich; Cusumano, Paola; Rouyer, François; Helfrich‐Förster, Charlotte; Nässel, Dick R.

doi:10.1002/cne.22099

Cited by 196 publications

(228 citation statements)

References 125 publications

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“…For example, sNPF mRNA is substantially more abundant in s-LNvs than in l-LNvs without being enriched ( Fig. 2A), consistent with recent immunohistochemical data (29). The transcription factor Dimmed and the octopamine receptor Oamb are only marginally enriched in l-LNvs but have very low expression in s-LNvs.…”

Section: Discussionsupporting

confidence: 89%

“…1 on the s/l ranking. Consistent with these data, sNPF has very recently been shown by immunohistochemistry to be present in s-LNvs but not in l-LNvs (29). The lack of strong enrichment is almost certainly because there are many other neurons that express sNPF and/or because these other neurons have much higher sNPF mRNA levels than s-LNvs.…”

Section: Resultssupporting

confidence: 65%

“…The lack of strong enrichment is almost certainly because there are many other neurons that express sNPF and/or because these other neurons have much higher sNPF mRNA levels than s-LNvs. There is good evidence in favor of the first possibility (29). To identify circadian genes, we used a panneuronal driver, elav-GAL4.…”

Section: Resultsmentioning

confidence: 99%

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Surprising gene expression patterns within and between PDF-containing circadian neurons in Drosophila

Kula-Eversole

Nagoshi

Shang

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

163

201

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To compare circadian gene expression within highly discrete neuronal populations, we separately purified and characterized two adjacent but distinct groups of Drosophila adult circadian neurons: the 8 small and 10 large PDF-expressing ventral lateral neurons (s-LNvs and l-LNvs, respectively). The s-LNvs are the principal circadian pacemaker cells, whereas recent evidence indicates that the l-LNvs are involved in sleep and light-mediated arousal. Although half of the l-LNv-enriched mRNA population, including core clock mRNAs, is shared between the l-LNvs and s-LNvs, the other half is l-LNv-and s-LNv-specific. The distribution of four specific mRNAs is consistent with prior characterization of the four encoded proteins, and therefore indicates successful purification of the two neuronal types. Moreover, an octopamine receptor mRNA is selectively enriched in l-LNvs, and only these neurons respond to in vitro application of octopamine. Dissection and purification of l-LNvs from flies collected at different times indicate that these neurons contain cycling clock mRNAs with higher circadian amplitudes as well as at least a 10-fold higher fraction of oscillating mRNAs than all previous analyses of head RNA. Many of these cycling l-LNv mRNAs are well expressed but do not cycle or cycle much less well elsewhere in heads. The results suggest that RNA cycling is much more prominent in circadian neurons than elsewhere in heads and may be particularly important for the functioning of these neurons.PDF neurons | microarrays | cycling mRNAs M any biochemical, physiological, and behavioral processes are governed by a circadian clock, which results in daily oscillations with a period of approximately 24 h. Circadian phenomena have been studied in multiple eukaryotic and even prokaryotic systems, and a large body of evidence now indicates that the biochemical underpinnings of eukaryotic molecular clocks include negative feedback loops of transcription (1-3). These cell-autonomous feedback loops also regulate the expression of so-called "output genes," many of which regulate circadian functions other than core timekeeping (1). In addition to this transcriptional regulation, posttranscriptional modifications such as phosphorylation regulate the stability and activity of clock proteins, and therefore also contribute to accurate timing as well as to robust mRNA and protein oscillations (4-8).In Drosophila, there are about 75 clock neurons on each side of the adult brain. They control adult Drosophila locomotor activity, which peaks twice a day in anticipation of the dawn and dusk transitions. The clock neurons are divided into seven classes based on their anatomical locations and characteristics (9, 10). There are three groups of dorsal neurons (DN1, DN2, and DN3), a lateral posterior neuron, and three groups of lateral neurons. These are the dorsal lateral neurons and the two groups of lateral neurons: the small ventral lateral neurons (s-LNvs) and the large ventral lateral neurons (l-LNvs). Although many genes are expressed similar...

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Section: Discussionsupporting

confidence: 89%

Section: Resultssupporting

confidence: 65%

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Surprising gene expression patterns within and between PDF-containing circadian neurons in Drosophila

Kula-Eversole

Nagoshi

Shang

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

163

201

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“…Interestingly, NPF was also found to be expressed in three of the LN d clock neurons in male flies (Lee et al, 2006). One of these NPF-positive LN d s is also CRY-positive and might be the so-called ''extra LN d ,'' that was shown to be an important E component (Rieger et al, 2006(Rieger et al, , 2009Johard et al, 2009). Lee et al (2006) reported that the expression of uas-reaper with an npfGal4 line leads to the ablation of all NPF neurons, including the three LN d s. In another recent study by Hamasaka et al (2010) the same npfGal4 line was used to ablate the NPF neurons with uas-hid.…”

mentioning

confidence: 95%

Neuropeptide F immunoreactive clock neurons modify evening locomotor activity and free‐running period in Drosophila melanogaster

Hermann

Yoshii

Dusik

et al. 2012

J of Comparative Neurology

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100

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Different subsets of Drosophila melanogaster's clock neurons are characterized by their specific functions in daily locomotor rhythms and the differences in their neurotransmitter composition. We investigated the function of the neuropeptide F (NPF) immunoreactive clock neurons in the rhythmic locomotor behavior of adult flies. We newly identified the fifth s-LN(v) and a subset of the l-LN(v)s as NPF-positive in addition to the three LN(d)s that have been described previously. We then selectively ablated different subsets of NPF-expressing neurons using npfGal4-targeted expression of the cell death gene head involution defective (hid) in combination with cryGal80 and pdfGal80. By analyzing daily locomotor rhythms in these flies, we show that the NPF-positive clock neurons--especially the fifth s-LN(v) and the LN(d)s--are involved in both the control of the free-running period in constant darkness (DD) and the phasing and amplitude of the evening activity in light-dark (LD) cycles. Furthermore, we show that the simultaneous ablation of NPF and pigment dispersing factor (PDF)-immunoreactive neurons has additive effects in LD, resulting in an evening peak phase that is even more advanced in comparison to PDF-ablated flies. We also found that this more advanced evening peak is additionally reduced in amplitude. To putatively assign the observed phenotypes to the action of NPF, we knocked it down in conjunction with PDF using RNA-interference (RNAi) and further suggest a possible role for NPF in the control of the flies' evening activity.

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“…The short-NPF (sNPF) neuropeptide is expressed in the two LNds lacking NPF, as well as in the s-LNvs (Fig. 1D) (Johard et al 2009;Kula-Eversole et al 2010). Although similar in name, the sNPF and NPF neurotransmitters are very different in amino acid sequence and are encoded by different genes.…”

Section: Coordination Between Differentially Regulated Circadian Clocksmentioning

confidence: 99%

Coordination between Differentially Regulated Circadian Clocks Generates Rhythmic Behavior

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Young

2017

Cold Spring Harb Perspect Biol

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Specialized groups of neurons in the brain are key mediators of circadian rhythms, receiving daily environmental cues and communicating those signals to other tissues in the organism for entrainment and to organize circadian physiology. In Drosophila, the "circadian clock" is housed in seven neuronal clusters, which are defined by their expression of the main circadian proteins, Period, Timeless, Clock, and Cycle. These clusters are distributed across the fly brain and are thereby subject to the respective environments associated with their anatomical locations. While these core components are universally expressed in all neurons of the circadian network, additional regulatory proteins that act on these components are differentially expressed, giving rise to "local clocks" within the network that nonetheless converge to regulate coherent behavioral rhythms. In this review, we describe the communication between the neurons of the circadian network and the molecular differences within neurons of this network. We focus on differences in protein-expression patterns and discuss how such variation can impart functional differences in each local clock. Finally, we summarize our current understanding of how communication within the circadian network intersects with intracellular biochemical mechanisms to ultimately specify behavioral rhythms. We propose that additional efforts are required to identify regulatory mechanisms within each neuronal cluster to understand the molecular basis of circadian behavior. C ircadian rhythms are behavioral and physiological responses that allow anticipation of daily changes in the environment, such as day/ night cycles. Indeed, circadian rhythms are entrained by diurnal oscillations in light, temperature, and food availability, each of which can be considered a "zeitgeber," or "time giver." Such anticipatory behavior of daily events confers adaptive advantages on individuals that organize physiology around planetary rhythms, as well as within a species as a whole, for purposes of mating, cooperation, protection, etc. In a sense, rhythmic anticipation can be thought of as a primitive mechanism of planning and cognition.The circadian clock, consisting of transcriptional negative feedback loops, underlies the regulation of a ∼24-h behavioral rhythm. The molecular architecture of this feedback loop is conserved across the majority of multicellular organisms. In animals, the "master clock" is housed in specialized pacemaker neurons in the brain that coordinate various "peripheral clocks" throughout the organism to regulate daily physiological and behavioral changes.

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Peptidergic clock neurons in Drosophila: Ion transport peptide and short neuropeptide F in subsets of dorsal and ventral lateral neurons

Cited by 196 publications

References 125 publications

Surprising gene expression patterns within and between PDF-containing circadian neurons in Drosophila

Surprising gene expression patterns within and between PDF-containing circadian neurons in Drosophila

Neuropeptide F immunoreactive clock neurons modify evening locomotor activity and free‐running period in Drosophila melanogaster

Coordination between Differentially Regulated Circadian Clocks Generates Rhythmic Behavior

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