PDF receptor expression reveals direct interactions between circadian oscillators in <i>drosophila</i>

Im, Seol Hee; Taghert, Paul H.

doi:10.1002/cne.22311

Cited by 165 publications

(217 citation statements)

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“…2). Indeed, not all members of a particular subset of clock neurons express the receptor (Im and Taghert, 2010) or respond to PDF application (Shafer et al, 2008). Given the behavioral importance of this peptide and the impracticality of biochemical experiments on such small subsets of cells, investigators have used genetic and behavioral strategies in vivo to examine PDFR signaling mechanisms.…”

Section: Animal Models To Discover and Validate Molecular Conceptsmentioning

confidence: 99%

Model Organisms in G Protein–Coupled Receptor Research

et al. 2015

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The study of G protein-coupled receptors (GPCRs) has benefited greatly from experimental approaches that interrogate their functions in controlled, artificial environments. Working in vitro, GPCR receptorologists discovered the basic biologic mechanisms by which GPCRs operate, including their eponymous capacity to couple to G proteins; their molecular makeup, including the famed serpentine transmembrane unit; and ultimately, their three-dimensional structure. Although the insights gained from working outside the native environments of GPCRs have allowed for the collection of low-noise data, such approaches cannot directly address a receptor's native (in vivo) functions. An in vivo approach can complement the rigor of in vitro approaches: as studied in model organisms, it imposes physiologic constraints on receptor action and thus allows investigators to deduce the most salient features of receptor function. Here, we briefly discuss specific examples in which model organisms have successfully contributed to the elucidation of signals controlled through GPCRs and other surface receptor systems. We list recent examples that have served either in the initial discovery of GPCR signaling concepts or in their fuller definition. Furthermore, we selectively highlight experimental advantages, shortcomings, and tools of each model organism.

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Section: Animal Models To Discover and Validate Molecular Conceptsmentioning

confidence: 99%

Model Organisms in G Protein–Coupled Receptor Research

et al. 2015

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“…Pfaff and his colleagues pioneered the strategy of using sites of hormone binding as a guide to mapping behavioral circuits: By determining the principal sites of estrogen binding in female rat brains they elucidated the network underlying the rodent lordosis response (Pfaff and Keiner 1973;Pfaff et al 1994). Receptor mapping has similarly provided key insights into the networks underlying other behaviors in both vertebrates and invertebrates, such as feeding (Wu et al 2003;Scott et al 2009), sleep and circadian rhythms (Marcus et al 2001;Im and Taghert 2010), offspring care (Insel 1990), and pair bonding (Young et al 1997). In general, however, the labor-intensive nature of receptor mapping and the complexity of most hormonally governed neural networks has made them difficult to fully unravel.…”

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confidence: 99%

The Splice Isoforms of the Drosophila Ecdysis Triggering Hormone Receptor Have Developmentally Distinct Roles

et al. 2015

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To grow, insects must periodically shed their exoskeletons. This process, called ecdysis, is initiated by the endocrine release of Ecdysis Trigger Hormone (ETH) and has been extensively studied as a model for understanding the hormonal control of behavior. Understanding how ETH regulates ecdysis behavior, however, has been impeded by limited knowledge of the hormone's neuronal targets. An alternatively spliced gene encoding a G-protein-coupled receptor (ETHR) that is activated by ETH has been identified, and several lines of evidence support a role in ecdysis for its A-isoform. The function of a second ETHR isoform (ETHRB) remains unknown. Here we use the recently introduced "Trojan exon" technique to simultaneously mutate the ETHR gene and gain genetic access to the neurons that express its two isoforms. We show that ETHRA and ETHRB are expressed in largely distinct subsets of neurons and that ETHRA-but not ETHRB-expressing neurons are required for ecdysis at all developmental stages. However, both genetic and neuronal manipulations indicate an essential role for ETHRB at pupal and adult, but not larval, ecdysis. We also identify several functionally important subsets of ETHR-expressing neurons including one that coexpresses the peptide Leucokinin and regulates fluid balance to facilitate ecdysis at the pupal stage. The general strategy presented here of using a receptor gene as an entry point for genetic and neuronal manipulations should be useful in establishing patterns of functional connectivity in other hormonally regulated networks.

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“…Restoring PDFR in both morning and evening cells in a pdfr − genetic background restores wild-type activity in flies, while restoring PDFR only in the LNvs results in loss of morning anticipation similar to that of pdfr − or pdf 01 flies (Renn et al 1999;Lear et al 2009;Im and Taghert 2010). Because there is a reported lack of synaptic connections between the LNvs and the LNds (Kim et al 2013), the LNd response is dependent on PDF diffusion, which is sufficient for signaling (Jan and Jan 1982;Nässel and Wegener 2011).…”

Section: The Dorsal Lateral Neurons and The Fifth S-lnvmentioning

confidence: 95%

“…Later work involving epitope tagging PDFR, measuring pdfr mRNA expression, and critically, testing neuronal response to exogenous PDF injection led to the conclusion that s-LNvs express PDFR and the l-LNvs do not ( Fig. 1E) (Shafer et al 2008;Im and Taghert 2010;Kula-Eversole et al 2010;Im et al 2011;Klose et al 2016). Thus, PDF released from both LNvs impacts only the s-LNvs (and other pdfrexpressing neurons in the CCNN), activating the cellular response leading to light-mediated arousal (Sheeba et al 2002(Sheeba et al , 2008aKula et al 2006;Parisky et al 2008;Shang et al 2008;Im et al 2011;Guo et al 2014;Schlichting et al 2016).…”

Section: Input From the Eyementioning

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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PDF receptor expression reveals direct interactions between circadian oscillators in drosophila

Cited by 165 publications

References 74 publications

Model Organisms in G Protein–Coupled Receptor Research

Model Organisms in G Protein–Coupled Receptor Research

The Splice Isoforms of the Drosophila Ecdysis Triggering Hormone Receptor Have Developmentally Distinct Roles

Coordination between Differentially Regulated Circadian Clocks Generates Rhythmic Behavior

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