Aversive Behavior in the Nematode C. elegans Is Modulated by cGMP and a Neuronal Gap Junction Network

Krzyzanowski, Michelle; Woldemariam, Sarah; Wood, John J.; Chaubey, Aditi H.; Brueggemann, Chantal; Bowitch, Alexander; Bethke, Mary; L’Étoile, Noëlle D.; Ferkey, Denise M.

doi:10.1371/journal.pgen.1006153

Cited by 51 publications

(34 citation statements)

References 121 publications

(192 reference statements)

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“…These neurons use cGMP-based sensory transduction pathways (36), as do vertebrate photoreceptors, where RD3 is known to be expressed. We used DiI staining (37) to identify two classes of ciliated sensory neuron that are not known to use cGMP signaling in sensory transduction: the ASH and ADL sensory neurons (36,(38)(39)(40)(41). We did not detect expression of rdl-1::gfp in ASH and ADL neurons ( Fig.…”

Section: Resultsmentioning

confidence: 95%

Antagonistic regulation of trafficking to Caenorhabditis elegans sensory cilia by a Retinal Degeneration 3 homolog and retromer

Martínez-Velázquez

Ringstad

2017

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

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Sensory neurons often possess cilia with elaborate membrane structures that are adapted to the sensory modality of the host cell. Mechanisms that target sensory transduction proteins to these specialized membrane domains remain poorly understood. Here, we show that a homolog of the human retinal dystrophy gene () is a Golgi-associated protein required for efficient trafficking of a sensory receptor, the receptor-type guanylate cyclase GCY-9, to cilia in chemosensory neurons of the nematode The trafficking defect caused by mutation of the nematode homolog is suppressed in vivo by mutation of key components of the retromer complex, which mediates recycling of cargo from endosomes to the Golgi. Our data show that there exists a critical balance in sensory neurons between the rates of anterograde and retrograde trafficking of cargo destined for the sensory cilium and this balance requires molecular specialization at an early stage of the secretory pathway.

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Section: Resultsmentioning

confidence: 95%

Antagonistic regulation of trafficking to Caenorhabditis elegans sensory cilia by a Retinal Degeneration 3 homolog and retromer

Martínez-Velázquez

Ringstad

2017

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

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“…The wild-type phenotype of a regulatory allele tax-2(p694), which only affects a subset of the TAX-2 neurons [30], narrows down the cells required for the ascr#3 response to just six pairs-ASGs, ASIs, ASJs, ASKs, AWBs, and AWCs ( Figure 4B). Using strains in which pairs of specific neurons were genetically ablated [13,[31][32][33], we found that the functions of the ASJ, AWB, and AWC pairs were each required for ascr#3 to counter the effect of ascr#10 ( Figures 4B and S4). We were surprised to discover that, although the ASIs express tax-2/tax-4 and were thus expected to mediate the A B Figure 4.…”

Section: Cgmp-mediated Signaling In Several Neurons Is Required For Amentioning

confidence: 99%

Counteracting Ascarosides Act through Distinct Neurons to Determine the Sexual Identity of C. elegans Pheromones

Aprison

Ruvinsky

2017

Current Biology

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Sex pheromones facilitate reproduction by attracting potential mates and altering their behavior and physiology. In C. elegans, males and hermaphrodites secrete similar blends of pheromone molecules, two of which are present in different relative concentrations: ascr#3, which is more abundant in hermaphrodites, and ascr#10, which is more abundant in males. It is not currently understood how this compositional difference results in sex-specific effects, for example, the slower aging of the hermaphrodite germline in the presence of physiologically relevant concentrations of male pheromones. Here we report three key elements of the mechanism responsible for this phenomenon. First, ascr#3 counters the activity of ascr#10. This antagonism decreases the magnitude and the sensitivity of the hermaphrodite response to the male pheromone, restricting it to situations in which the presence of a male could be inferred with high confidence. Second, hermaphrodites recognize pheromone as male if the concentration of ascr#10 is higher than that of ascr#3. Third, the response to ascr#10 requires TRPV channel function in the ADL neurons and the daf-7 signaling from the ASI neurons, whereas the response to ascr#3 relies on cyclic guanosine monophosphate (cGMP)-gated channels and activity of the ASJ, AWB, and AWC neurons. These results argue that the counteracting activities of distinct neuronal circuits determine the sexual identity of the pheromone. The parallels between this mechanism and other signaling systems suggest that diverse organisms may perform particular neuronal computations using similar general principles.

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“…However, it is not known if for is involved in the nociceptive-like escape response. PKG has been shown to regulate nociception in several organisms (36)(37)(38). Here, we use an optogenetic screen to show that activation of a subset of for neurons induces a nociceptive-like escape response.…”

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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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Aversive Behavior in the Nematode C. elegans Is Modulated by cGMP and a Neuronal Gap Junction Network

Cited by 51 publications

References 121 publications

Antagonistic regulation of trafficking to Caenorhabditis elegans sensory cilia by a Retinal Degeneration 3 homolog and retromer

Antagonistic regulation of trafficking to Caenorhabditis elegans sensory cilia by a Retinal Degeneration 3 homolog and retromer

Counteracting Ascarosides Act through Distinct Neurons to Determine the Sexual Identity of C. elegans Pheromones

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

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