The Monoaminergic Modulation of Sensory-Mediated Aversive Responses in Caenorhabditis elegans Requires Glutamatergic/Peptidergic Cotransmission

Abstract

Monoamines and neuropeptides interact to modulate behavioral plasticity in both vertebrates and invertebrates. In Caenorhabditis elegans behavioral state or "mood" is dependent on food availability and is translated by both monoaminergic and peptidergic signaling in the fine-tuning of most behaviors. In the present study, we have examined the interaction of monoamines and peptides on C. elegans aversive behavior mediated by a pair of polymodal, nociceptive, ASH sensory neurons. Food or serotonin sensitize the ASHs and stimulate aversive responses through a pathway requiring the release of nlp-3-encoded neuropeptides from the ASHs. Peptides encoded by nlp-3 appear to stimulate ASH-mediated aversive behavior through the neuropeptide receptor-17 (NPR-17) receptor. nlp-3-and npr-17-null animals exhibit identical phenotypes and animals overexpressing either nlp-3 or npr-17 exhibit elevated aversive responses off food that are absent when nlp-3 or npr-17 are overexpressed in npr-17-or nlp-3-null animals, respectively. ASH-mediated aversive responses are increased by activating either G␣ q or G␣ s in the ASHs, with G␣ s signaling specifically stimulating the release of nlp-3-encoded peptides. In contrast, octopamine appears to inhibit 5-HT stimulation by activating G␣ o signaling in the ASHs that, in turn, inhibits both G␣ s and G␣ q signaling and the release of nlp-3-encoded peptides. These results demonstrate that serotonin and octopamine reversibly modulate the activity of the ASHs, and highlight the utility of the C. elegans model for defining interactions between monoamines and peptides in individual neurons of complex sensory-mediated circuits.

Succinylated Octopamine Ascarosides and a New Pathway of Biogenic Amine Metabolism in Caenorhabditis elegans

“…S6, see supplemental data for structure elucidation). We only detected trace amounts (1-2% of osas#9) of tsas#9 in starved wild-type L1 medium, suggesting that the great abundance of this compound in tbh-1 medium is a result of the roughly 20-fold increased tyramine levels in this mutant (28). These findings demonstrated that osas ascarosides are synthesized from worm-produced octopamine.…”

“…In C. elegans, octopamine down-regulates pharyngeal pumping (and thereby food intake) as well as egg laying (25,28,30), opposing the effects of serotonin. In addition, octopamine signaling is required for avoidance behavior in response to specific chemical stimuli (29), although octopamine itself is not known to be deterrent.…”

Reciprocal inhibition between sensory ASH and ASI neurons modulates nociception and avoidance in Caenorhabditis elegans

“…Notably, the neurotransmitters, such as neuropeptides, serotonin (5-HT), tyramine (TA) and octopamine (OA), have been increasingly shown to be transmitters or modulators of ASH-mediated aversive behaviours [12][13][14][15] . ASI sensory neurons are reported to mediate dauer formation 16 , enable worms to learn to avoid the smell of pathogenic bacteria after ingestion via INS-6 signalling 17 , suppress male-specific sexual attraction behaviour 18 , respond to temperature stimuli to negatively modulate thermotaxis behaviour 19 , mediate diet-restriction-induced longevity 20 , modulate satiety quiescence 21 , regulate acute CO 2 avoidance 22 , repress exploratory behaviours that comprise spontaneous reversals and omega turns 5 , and inhibit ASH-mediated aversive responses to 100% 1-octanol 23 .…”

Characterizations of kinetic power and propulsion of the nematode Caenorhabditis elegans based on a micro-particle image velocimetry system

“…As a result, the mutant features hyperactive motility and hyper-responses as an adult. 34 A representative trajectory of movement over a cycle based on the worm's body centroid is shown in Fig. 6(a).…”