The Drosophila Small Conductance Calcium-Activated Potassium Channel Negatively Regulates Nociception

K, Walcott; Mauthner, Stephanie E.; Tsubouchi, Asako; Robertson, Jessica; Tracey, W. Daniel

doi:10.1016/j.celrep.2018.08.070

Cited by 14 publications

(16 citation statements)

References 47 publications

(67 reference statements)

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“…Drosophila larvae use class IV (cIV) multidendritic sensory neurons on their cuticle to detect noxious stimuli or an attack by a parasitoid wasp and then escape by eliciting a sequential body bending and corkscrew-like rolling response (8,9). This escape behavior is also seen in response to mechanical or thermal nociception (10)(11)(12)(13)(14)(15)(16). Silencing cIV multidendritic sensory neurons with tetanus toxin eliminates this nociceptive-like escape response (8), whereas optogenetic activation of these neurons induces the curling and rolling escape response (8,17,18).…”

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confidence: 99%

Drosophila melanogaster foraging regulates a nociceptive-like escape behavior through a developmentally plastic sensory circuit

Dason

Cheung

Anreiter

et al. 2019

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

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Painful or threatening experiences trigger escape responses that are guided by nociceptive neuronal circuitry. Although some components of this circuitry are known and conserved across animals, how this circuitry is regulated at the genetic and developmental levels is mostly unknown. To escape noxious stimuli, such as parasitoid wasp attacks, Drosophila melanogaster larvae generate a curling and rolling response. Rover and sitter allelic variants of the Drosophila foraging (for) gene differ in parasitoid wasp susceptibility, suggesting a link between for and nociception. By optogenetically activating cells associated with each of for’s promoters (pr1–pr4), we show that pr1 cells regulate larval escape behavior. In accordance with rover and sitter differences in parasitoid wasp susceptibility, we found that rovers have higher pr1 expression and increased sensitivity to nociception relative to sitters. The for null mutants display impaired responses to thermal nociception, which are rescued by restoring for expression in pr1 cells. Conversely, knockdown of for in pr1 cells phenocopies the for null mutant. To gain insight into the circuitry underlying this response, we used an intersectional approach and activity-dependent GFP reconstitution across synaptic partners (GRASP) to show that pr1 cells in the ventral nerve cord (VNC) are required for the nociceptive response, and that multidendritic sensory nociceptive neurons synapse onto pr1 neurons in the VNC. Finally, we show that activation of the pr1 circuit during development suppresses the escape response. Our data demonstrate a role of for in larval nociceptive behavior. This function is specific to for pr1 neurons in the VNC, guiding a developmentally plastic escape response circuit.

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confidence: 99%

Drosophila melanogaster foraging regulates a nociceptive-like escape behavior through a developmentally plastic sensory circuit

Dason

Cheung

Anreiter

et al. 2019

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

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“…sensory neurons with extensive dendritic arbors that cover the body wall and function in thermal, light and mechanical sensation (Chin & Tracey, 2017;Hwang et al, 2007;Onodera, Baba, Murakami, Uemura, & Usui, 2017;Tracey, Wilson, Laurent, & Benzer, 2003;Walcott, Mauthner, Tsubouchi, Robertson, & Tracey, 2018;Xiang et al, 2010). da neurons elaborate their dendritic arbors two dimensionally between the epidermis and the muscles, and they are easily visualized at high resolution by whole-mount imaging using cell-specific transgenic GFP markers (Grueber, Ye, Moore, Jan, & Jan, 2003;Sugimura et al, 2003).…”

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confidence: 99%

DeTerm: Software for automatic detection of neuronal dendritic branch terminals via an artificial neural network

et al. 2019

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Dendrites of neurons receive and process synaptic or sensory inputs. The Drosophila class IV dendritic arborization (da) neuron is an established model system to explore molecular mechanisms of dendrite morphogenesis. The total number of dendritic branch terminals is one of the frequently employed parameters to characterize dendritic arborization complexity of class IV neurons. This parameter gives a useful phenotypic readout of arborization during neurogenesis, and it is typically determined by laborious manual analyses of numerous images. Ideally, an automated analysis would greatly reduce the workload; however, it is challenging to automatically discriminate dendritic branch terminals from signals of surrounding tissues in whole‐mount live larvae. Here, we describe our newly developed software, called DeTerm, which automatically recognizes and quantifies dendrite branch terminals via an artificial neural network. Once we input an image file of a neuronal dendritic arbor and its region of interest information, DeTerm is capable of labeling terminals of larval class IV neurons with high precision, and it also provides positional data of individual terminals. We further show that DeTerm is applicable to other types of neurons, including mouse cerebellar Purkinje cells. DeTerm is freely available on the web and was successfully tested on Mac, Windows and Linux.

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“…It is noteworthy that prior studies have noted a potential link between the degree of dendrite branching and the sensitivity of nociception behaviors (Honjo et al 2016). In other cases, axonal factors such as the ion channel SK have been found to be important in regulating the cIVda neuron excitability (Walcott et al 2018;Onodera et al 2017).…”

Section: Discussionmentioning

confidence: 98%

Loss of Pseudouridine Synthases in the RluA Family Causes Hypersensitive Nociception inDrosophila

Song

Ressl

Tracey

2020

G3 Genes|Genomes|Genetics

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Nociceptive neurons of Drosophila melanogaster larvae are characterized by highly branched dendritic processes whose proper morphogenesis relies on a large number of RNA-binding proteins. Post-transcriptional regulation of RNA in these dendrites has been found to play an important role in their function. Here, we investigate the neuronal functions of two putative RNA modification genes, RluA-1 and RluA-2, which are predicted to encode pseudouridine synthases. RluA-1 is specifically expressed in larval sensory neurons while RluA-2 expression is ubiquitous. Nociceptor-specific RNAi knockdown of RluA-1 caused hypersensitive nociception phenotypes, which were recapitulated with genetic null alleles. These were rescued with genomic duplication and nociceptor-specific expression of UAS-RluA-1-cDNA. As with RluA-1, RluA-2 loss of function mutants also displayed hyperalgesia. Interestingly, nociceptor neuron dendrites showed a hyperbranched morphology in the RluA-1 mutants. The latter may be a cause or a consequence of heightened sensitivity in mutant nociception behaviors.

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The Drosophila Small Conductance Calcium-Activated Potassium Channel Negatively Regulates Nociception

Cited by 14 publications

References 47 publications

Drosophila melanogaster foraging regulates a nociceptive-like escape behavior through a developmentally plastic sensory circuit

Drosophila melanogaster foraging regulates a nociceptive-like escape behavior through a developmentally plastic sensory circuit

DeTerm: Software for automatic detection of neuronal dendritic branch terminals via an artificial neural network

Loss of Pseudouridine Synthases in the RluA Family Causes Hypersensitive Nociception inDrosophila

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