Metabotropic glutamate receptors: modulators of context-dependent feeding behaviour in C. elegans
Metabotropic glutamate receptors: modulators of context-dependent feeding behaviour in C. elegans
Glutamatergic neurotransmission is evolutionarily conserved across animal phyla. A major class of glutamate receptors consists of the metabotropic glutamate receptors (mGluRs). In C. elegans, three mGluR genes, mgl-1, mgl-2, and mgl-3, are organized into three subgroups, similar to their mammalian counterparts. Cellular reporters identified expression of the mgls in the nervous system of C. elegans and overlapping expression in the pharyngeal microcircuit that controls pharyngeal muscle activity and feeding behavior. The overlapping expression of mgls within this circuit allowed the investigation of receptor signaling per se and in the context of receptor interactions within a neural network that regulates feeding. We utilized the pharmacological manipulation of neuronally regulated pumping of the pharyngeal muscle in the wild-type and mutants to investigate MGL function. This defined a net mgl-1-dependent inhibition of pharyngeal pumping that is modulated by mgl-3 excitation. Optogenetic activation of the pharyngeal glutamatergic inputs combined with electrophysiological recordings from the isolated pharyngeal preparations provided further evidence for a presynaptic mgl-1-dependent regulation of pharyngeal activity. Analysis of mgl-1, mgl-2, and mgl-3 mutant feeding behavior in the intact organism after acute food removal identified a significant role for mgl-1 in the regulation of an adaptive feeding response. Our data describe the molecular and cellular organization of mgl-1, mgl-2, and mgl-3. Pharmacological analysis identified that, in these paradigms, mgl-1 and mgl-3, but not mgl-2, can modulate the pharyngeal microcircuit. Behavioral analysis identified mgl-1 as a significant determinant of the glutamate-dependent modulation of feeding, further highlighting the significance of mGluRs in complex C. elegans behavior.
15052-15065
Dillon, James
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Franks, Christopher
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Murray, Caitriona
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Edwards, Richard J.
e953181d-0c68-4149-a56d-72f026c86c19
Calahorro, Fernando
ffbe5fad-188c-4a9e-9948-087d9fbcc1a5
Ishihara, Takeshi
685a8ceb-cdd3-4290-ad2c-af4b48004257
Katsura, Isao
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Holden-Dye, Lindy
8032bf60-5db6-40cb-b71c-ddda9d212c8e
O’Connor, Vincent
23982c73-d98d-48a3-9797-c9506da04a83
12 June 2015
Dillon, James
f85e4734-297f-4b16-90b2-22122455e778
Franks, Christopher
9842534b-4d3f-4ee8-a07e-3b050f748593
Murray, Caitriona
a6c5d211-d09b-431e-a923-69c6eab3a1d3
Edwards, Richard J.
e953181d-0c68-4149-a56d-72f026c86c19
Calahorro, Fernando
ffbe5fad-188c-4a9e-9948-087d9fbcc1a5
Ishihara, Takeshi
685a8ceb-cdd3-4290-ad2c-af4b48004257
Katsura, Isao
04949a6e-17fd-4ef7-b27f-301e58a1720f
Holden-Dye, Lindy
8032bf60-5db6-40cb-b71c-ddda9d212c8e
O’Connor, Vincent
23982c73-d98d-48a3-9797-c9506da04a83
Dillon, James, Franks, Christopher, Murray, Caitriona, Edwards, Richard J., Calahorro, Fernando, Ishihara, Takeshi, Katsura, Isao, Holden-Dye, Lindy and O’Connor, Vincent
(2015)
Metabotropic glutamate receptors: modulators of context-dependent feeding behaviour in C. elegans.
The Journal of Biological Chemistry, 290 (24), .
(doi:10.1074/jbc.M114.606608).
Abstract
Glutamatergic neurotransmission is evolutionarily conserved across animal phyla. A major class of glutamate receptors consists of the metabotropic glutamate receptors (mGluRs). In C. elegans, three mGluR genes, mgl-1, mgl-2, and mgl-3, are organized into three subgroups, similar to their mammalian counterparts. Cellular reporters identified expression of the mgls in the nervous system of C. elegans and overlapping expression in the pharyngeal microcircuit that controls pharyngeal muscle activity and feeding behavior. The overlapping expression of mgls within this circuit allowed the investigation of receptor signaling per se and in the context of receptor interactions within a neural network that regulates feeding. We utilized the pharmacological manipulation of neuronally regulated pumping of the pharyngeal muscle in the wild-type and mutants to investigate MGL function. This defined a net mgl-1-dependent inhibition of pharyngeal pumping that is modulated by mgl-3 excitation. Optogenetic activation of the pharyngeal glutamatergic inputs combined with electrophysiological recordings from the isolated pharyngeal preparations provided further evidence for a presynaptic mgl-1-dependent regulation of pharyngeal activity. Analysis of mgl-1, mgl-2, and mgl-3 mutant feeding behavior in the intact organism after acute food removal identified a significant role for mgl-1 in the regulation of an adaptive feeding response. Our data describe the molecular and cellular organization of mgl-1, mgl-2, and mgl-3. Pharmacological analysis identified that, in these paradigms, mgl-1 and mgl-3, but not mgl-2, can modulate the pharyngeal microcircuit. Behavioral analysis identified mgl-1 as a significant determinant of the glutamate-dependent modulation of feeding, further highlighting the significance of mGluRs in complex C. elegans behavior.
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Published date: 12 June 2015
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Local EPrints ID: 456205
URI: http://eprints.soton.ac.uk/id/eprint/456205
ISSN: 1083-351X
PURE UUID: 77ee3d59-f365-464c-ad61-759ee0f18e7b
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Date deposited: 26 Apr 2022 16:55
Last modified: 17 Mar 2024 02:43
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Author:
James Dillon
Author:
Caitriona Murray
Author:
Richard J. Edwards
Author:
Fernando Calahorro
Author:
Takeshi Ishihara
Author:
Isao Katsura
Author:
Vincent O’Connor
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