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

Hermann, Christiane; Yoshii, Taishi; Dusik, Verena; Helfrich‐Förster, Charlotte

doi:10.1002/cne.22742

Cited by 89 publications

(107 citation statements)

References 41 publications

(93 reference statements)

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“…Locomotor activity of individual flies was recorded using the Drosophila Activity Monitoring (DAM) System (Trikinetics) as previously described [67]. Briefly, to investigate locomotor behavior 3–7 day old male flies were monitored in LD 12∶12 for 7 days (with a light intensity of 100 lux in the light phase) followed by additional 14 days in constant darkness (DD).…”

Section: Methodsmentioning

confidence: 99%

The MAP Kinase p38 Is Part of Drosophila melanogaster's Circadian Clock

et al. 2014

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All organisms have to adapt to acute as well as to regularly occurring changes in the environment. To deal with these major challenges organisms evolved two fundamental mechanisms: the p38 mitogen-activated protein kinase (MAPK) pathway, a major stress pathway for signaling stressful events, and circadian clocks to prepare for the daily environmental changes. Both systems respond sensitively to light. Recent studies in vertebrates and fungi indicate that p38 is involved in light-signaling to the circadian clock providing an interesting link between stress-induced and regularly rhythmic adaptations of animals to the environment, but the molecular and cellular mechanisms remained largely unknown. Here, we demonstrate by immunocytochemical means that p38 is expressed in Drosophila melanogaster's clock neurons and that it is activated in a clock-dependent manner. Surprisingly, we found that p38 is most active under darkness and, besides its circadian activation, additionally gets inactivated by light. Moreover, locomotor activity recordings revealed that p38 is essential for a wild-type timing of evening activity and for maintaining ∼24 h behavioral rhythms under constant darkness: flies with reduced p38 activity in clock neurons, delayed evening activity and lengthened the period of their free-running rhythms. Furthermore, nuclear translocation of the clock protein Period was significantly delayed on the expression of a dominant-negative form of p38b in Drosophila's most important clock neurons. Western Blots revealed that p38 affects the phosphorylation degree of Period, what is likely the reason for its effects on nuclear entry of Period. In vitro kinase assays confirmed our Western Blot results and point to p38 as a potential “clock kinase” phosphorylating Period. Taken together, our findings indicate that the p38 MAP Kinase is an integral component of the core circadian clock of Drosophila in addition to playing a role in stress-input pathways.

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Section: Methodsmentioning

confidence: 99%

The MAP Kinase p38 Is Part of Drosophila melanogaster's Circadian Clock

et al. 2014

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“…However, in R. pedestris, the circadian clock has been shown to be involved in the photoperiodic response (Ikeno et al, 2010;Ikeno et al, 2011a;Ikeno et al, 2011b;Ikeno et al, 2011c;Ikeno et al, 2013), suggesting that these neurons would also be the circadian clock neurons. Such PDFimmunonegative circadian clock neurons are indeed observed in D. melanogaster (Rieger et al, 2006;Picot et al, 2007;Hermann et al, 2012). To interpret the effects of Site 1 removal at a cellular level, a neuroanatomical study of this region will be necessary.…”

Section: Research Articlementioning

confidence: 98%

The involvement of the brain region containing pigment-dispersing factor-immunoreactive neurons in the photoperiodic response of the bean bugRiptortus pedestris

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et al. 2013

Journal of Experimental Biology

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The concept of insect photoperiodism based on a circadian clock has been supported by many studies demonstrating that the behavioural circadian rhythm and the photoperiodic response are driven by the same circadian clock genes. However, the neuronal mechanism of the circadian clock underlying photoperiodism is poorly understood. To examine whether circadian rhythm and photoperiodism share a neuronal mechanism, we focused on the neurons that express neuropeptide pigment-dispersing factor (PDF) in the bean bug, Riptortus pedestris. PDF has been identified as an important regulator of the insect circadian rhythm and is expressed in circadian clock neurons of various insect species. In R. pedestris, PDF immunoreactivity was detected in some clusters of cells and their fibres in the optic lobe and the protocerebrum. cDNA encoding a PDF precursor protein was highly conserved between R. pedestris and many other insects. Differences between day and night were not observed in the immunolabelling intensity in cell bodies of PDFimmunoreactive neurons and pdf mRNA expression levels in the head. Surgical removal of the region containing PDF-immunoreactive cell bodies at the medulla disrupted the photoperiodic regulation of diapause. However, gene suppression of pdf by RNA interference did not affect the photoperiodic response. These results suggest that the region containing PDF-immunoreactive somata is important for the photoperiodic response in R. pedestris, but pdf mRNA expression is probably not required for the response.

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“…Neuropeptide F (NPF) and its receptor NPFR1, help regulate evening anticipation. NPF is produced in two to three l-LNvs, three LNds, and the fifth s-LNv (Hermann et al 2012;Kim et al 2013), with one study reporting production in all four s-LNvs (He et al 2013), although not consistently observed by others (Fig. 1D) (Hermann et al 2012;Kim et al 2013).…”

Section: Other Neuropeptides and Evening Anticipationmentioning

confidence: 80%

“…NPF is produced in two to three l-LNvs, three LNds, and the fifth s-LNv (Hermann et al 2012;Kim et al 2013), with one study reporting production in all four s-LNvs (He et al 2013), although not consistently observed by others (Fig. 1D) (Hermann et al 2012;Kim et al 2013). The s-LNvs do express NPFR1 however, which associates with Gi to inhibit cAMP production (Garczynski et al 2002;Kim et al 2013) that may antagonize PDFR or D1-like DA receptor production of cAMP in these neurons (Fig.…”

Section: Other Neuropeptides and Evening Anticipationmentioning

confidence: 81%

“…Loss of pdf modestly shortens rhythmic behavior in constant darkness, while loss of npf modestly lengthens it, suggesting an antagonistic relationship between the morning and evening clocks ( Fig. 1F) (Renn et al 1999;Shafer and Taghert 2009;Hermann et al 2012). The proposed antagonistic mechanism mirrors the advances and delays exhibited by morning and evening anticipation to light, discussed above (Pittendrigh and Daan 1976).…”

Section: Other Neuropeptides and Evening Anticipationmentioning

confidence: 98%

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

Cited by 89 publications

References 41 publications

The MAP Kinase p38 Is Part of Drosophila melanogaster's Circadian Clock

The MAP Kinase p38 Is Part of Drosophila melanogaster's Circadian Clock

The involvement of the brain region containing pigment-dispersing factor-immunoreactive neurons in the photoperiodic response of the bean bugRiptortus pedestris

Coordination between Differentially Regulated Circadian Clocks Generates Rhythmic Behavior

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