Distinct functions of a cGMP-dependent protein kinase in nerve terminal growth and synaptic vesicle cycling

Dason, Jeffrey S.; Allen, Annette D.; Vasquez, Oscar; Sokolowski, Marla B.

doi:10.1242/jcs.227165

Cited by 18 publications

(26 citation statements)

References 107 publications

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“…Together, these data suggest that FOR is required for activation of pr1 cells to induce the nociceptive-like escape response. Presynaptic Drosophila FOR and mammalian PKG maintain sustained neurotransmitter release by facilitating SV endocytosis (32,50,51). The inability of for 0 null mutants to maintain sustained neurotransmitter release in pr1 neurons, which are downstream of cIV multidendritic sensory neurons, may reduce the likelihood of larvae curling and rolling in response to thermal nociception.…”

Section: Discussionmentioning

confidence: 99%

“…UAS-chrimson was used to express a red-light-activated channelrhodopsin, chrimson (40). UAS-for-flag-4c was used to express FOR with a flag-4c tag on the C terminus in selected tissues or cells (32). FOR-flag-4c was previously shown to be a functional FOR protein that recapitulates FOR function (32).…”

Section: Methodsmentioning

confidence: 99%

“…UAS-for-flag-4c was used to express FOR with a flag-4c tag on the C terminus in selected tissues or cells (32). FOR-flag-4c was previously shown to be a functional FOR protein that recapitulates FOR function (32). UAS-Dcr, UAS-forRNAi was used to knock down for in selected cells.…”

Section: Methodsmentioning

confidence: 99%

“…The Drosophila foraging (for) gene encodes a guanosine 3′,5′cyclic monophosphate-dependent protein kinase (PKG) (20) and affects numerous behaviors (20)(21)(22)(23)(24)(25), several types of plasticity (26)(27)(28)(29), and synaptic function (30)(31)(32). Allelic variants of for (rover and sitter) differ in for messenger RNA (mRNA) levels, foraging behavior (20)(21)(22), and their susceptibility to predation by parasitoid wasps (33)(34)(35).…”

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confidence: 99%

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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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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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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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“…In C. elegans, PKG functions in a limited number of neurons 24 . PKG has been shown to regulate syn- www.nature.com/scientificreports/ aptic vesicle cycling, Ca 2+ influx via G-protein signaling, and axon guidance in certain neuron types 80,[82][83][84][85] . The endogenous and ectopic expression of PKG in specific neurons and functional analysis of PKG suggest that PKG modulates multifractal kinetics of animal behaviors in single neurons or small numbers of neurons.…”

Section: Molecular and System-level Mechanisms For Multifractal Episomentioning

confidence: 99%

C. elegans episodic swimming is driven by multifractal kinetics

Ikeda

Jurica

Kimura

et al. 2020

Sci Rep

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Fractal scaling is a common property of temporal change in various modes of animal behavior. The molecular mechanisms of fractal scaling in animal behaviors remain largely unexplored. The nematode C. elegans alternates between swimming and resting states in a liquid solution. Here, we report that C. elegans episodic swimming is characterized by scale-free kinetics with long-range temporal correlation and local temporal clusterization, namely consistent with multifractal kinetics. Residence times in actively-moving and inactive states were distributed in a power law-based scale-free manner. Multifractal analysis showed that temporal correlation and temporal clusterization were distinct between the actively-moving state and the inactive state. These results indicate that C. elegans episodic swimming is driven by transition between two behavioral states, in which each of two transition kinetics follows distinct multifractal kinetics. We found that a conserved behavioral modulator, cyclic GMP dependent kinase (PKG) may regulate the multifractal kinetics underlying an animal behavior. Our combinatorial analysis approach involving molecular genetics and kinetics provides a platform for the molecular dissection of the fractal nature of physiological and behavioral phenomena.

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