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A tyramine-gated chloride channel coordinates distinct motor programs of a Caenorhabditis elegans escape response.

ABSTRACT: A key feature of escape responses is the fast translation of sensory information into a coordinated motor output. In C. elegans, anterior touch initiates a backward escape response in which lateral head movements are suppressed. Here, we show that tyramine inhibits head movements and forward locomotion through the activation of a tyramine-gated chloride channel, LGC-55. lgc-55 mutant animals have defects in reversal behavior and fail to suppress head oscillations in response to anterior touch. lgc-55 is expressed in neurons and muscle cells that receive direct synaptic inputs from tyraminergic motor neurons. Therefore, tyramine can act as a classical inhibitory neurotransmitter. Activation of LGC-55 by tyramine coordinates the output of two distinct motor programs, locomotion and head movements that are critical for a C. elegans escape response.

SUBMITTER: Pirri JK

PROVIDER: S-EPMC2804440 | biostudies-literature | 2009 May

REPOSITORIES: biostudies-literature

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A tyramine-gated chloride channel coordinates distinct motor programs of a Caenorhabditis elegans escape response.

Pirri Jennifer K JK McPherson Adam D AD Donnelly Jamie L JL Francis Michael M MM Alkema Mark J MJ

Neuron 20090501 4

A key feature of escape responses is the fast translation of sensory information into a coordinated motor output. In C. elegans, anterior touch initiates a backward escape response in which lateral head movements are suppressed. Here, we show that tyramine inhibits head movements and forward locomotion through the activation of a tyramine-gated chloride channel, LGC-55. lgc-55 mutant animals have defects in reversal behavior and fail to suppress head oscillations in response to anterior touch. l ...[more]

PMID: 19477154

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Project description:BackgroundTyramine, known as a "trace amine" in mammals, modulates a wide range of behavior in invertebrates; however, the underlying cellular and circuit mechanisms are not well understood. In the nematode Caenorhabditis elegans (C. elegans), tyramine affects key behaviors, including foraging, feeding, and escape responses. The touch-evoked backward escape response is often coupled with a sharp omega turn that allows the animal to navigate away in the opposite direction. Previous studies have showed that a metabotropic tyramine receptor, SER-2, in GABAergic body motor neurons controls deep body bending in omega turns. In this study, we focused on the role of tyramine in GABAergic head motor neurons. Our goal is to understand the mechanism by which tyraminergic signaling alters neural circuit activity to control escape behavior.ResultsUsing calcium imaging in freely moving C. elegans, we found that GABAergic RME motor neurons in the head had high calcium levels during forward locomotion but low calcium levels during spontaneous and evoked backward locomotion. This calcium decrease was also observed during the omega turn. Mutant analyses showed that tbh-1 mutants lacking only octopamine had normal calcium responses, whereas tdc-1 mutants lacking both tyramine and octopamine did not exhibit the calcium decrease in RME. This neuromodulation was mediated by SER-2. Moreover, tyraminergic RIM neuron activity was negatively correlated with RME activity in the directional switch from forward to backward locomotion. These results indicate that tyramine released from RIM inhibits RME via SER-2 signaling. The omega turn is initiated by a sharp head bend when the animal reinitiates forward movement. Interestingly, ser-2 mutants exhibited shallow head bends and often failed to execute deep-angle omega turns. The behavioral defect and the abnormal calcium response in ser-2 mutants could be rescued by SER-2 expression in RME. These results suggest that tyraminergic inhibition of RME is involved in the control of omega turns.ConclusionWe demonstrate that endogenous tyramine downregulates calcium levels in GABAergic RME motor neurons in the head via the tyramine receptor SER-2 during backward locomotion and omega turns. Our data suggest that this neuromodulation allows deep head bending during omega turns and plays a role in the escape behavior in C. elegans.

Project description:Anthelmintic resistance is a major problem in livestock farming, especially of small ruminants, but our understanding of it has been limited by the difficulty in carrying out functional genetic studies on parasitic nematodes. An important nematode infecting sheep and goats is Haemonchus contortus; in many parts of the world this species is resistant to almost all the currently available drugs, including ivermectin. It is extremely polymorphic and to date it has proved impossible to relate any sequence polymorphisms to its ivermectin resistance status. Expression of candidate drug-resistance genes in Caenorhabditis elegans could provide a convenient means to study the effects of polymorphisms found in resistant parasites, but may be complicated by differences between the gene families of target and model organisms. We tested this using the glutamate-gated chloride channel (GluCl) gene family, which forms the ivermectin drug target and are candidate resistance genes. We expressed GluCl subunits from C. elegans and H. contortus in a highly resistant triple mutant C. elegans strain (DA1316) under the control of the avr-14 promoter; expression of GFP behind this promoter recapitulated the pattern previously reported for avr-14. Expression of ivermectin-sensitive subunits from both species restored drug sensitivity to transgenic worms, though some quantitative differences were noted between lines. Expression of an ivermectin-insensitive subunit, Hco-GLC-2, had no effect on drug sensitivity. Expression of a previously uncharacterised parasite-specific subunit, Hco-GLC-6, caused the transgenic worms to become ivermectin sensitive, suggesting that this subunit also encodes a GluCl that responds to the drug. These results demonstrate that both orthologous and paralogous subunits from C. elegans and H. contortus are able to rescue the ivermectin sensitivity of mutant C. elegans, though some quantitative differences were observed between transgenic lines in some assays. C. elegans is a suitable system for studying parasitic nematode genes that may be involved in drug resistance.

Dataset Information

A tyramine-gated chloride channel coordinates distinct motor programs of a Caenorhabditis elegans escape response.

Publications

A tyramine-gated chloride channel coordinates distinct motor programs of a Caenorhabditis elegans escape response.

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