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 are the metabotropic glutamate receptors (mGluRs). In C. elegans three mGluR genes mgl-1, mgl-2 and mgl-3 are organised into three sub-groups, 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 behaviour. The overlapping expression of mgls within this circuit allowed investigation of receptor signalling 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 wild type and mutants to investigate mgl function. This defined a net mgl-1 dependent inhibition of pharyngeal pumping which 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 behaviour 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 describes the molecular and cellular organisation 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. Behavioural 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 behaviour.
metabotropic glutamate receptors (mGluR), optogenetics, Caenorhabditis elegans (C. elegans), electrophysiology, invertebrate
15052-15065
Dillon, James
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Franks, Christopher J
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Murray, Caitriona
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Edwards, Richard J
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Calahorro, Fernando
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Ishihara, Takeshi
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Katsura, Isao
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Holden-Dye, Lindy
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O'Connor, Vincent
8021b06c-01a0-4925-9dde-a61c8fe278ca
12 June 2015
Dillon, James
f406e30a-3ad4-4a53-80db-6694bab5e3ed
Franks, Christopher J
4927f50e-1b16-42f1-bc4c-760ff3548417
Murray, Caitriona
6fcb874d-75d7-49aa-9219-8f9723d862fe
Edwards, Richard J
9d25e74f-dc0d-455a-832c-5f363d864c43
Calahorro, Fernando
dddfa373-d3cc-433f-8851-9ca37f2f3950
Ishihara, Takeshi
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Katsura, Isao
31c65a0a-2d8e-430b-9e51-8f03b972f1ce
Holden-Dye, Lindy
8032bf60-5db6-40cb-b71c-ddda9d212c8e
O'Connor, Vincent
8021b06c-01a0-4925-9dde-a61c8fe278ca
Dillon, James, Franks, Christopher J, 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).
(PMID:25869139)
Abstract
Glutamatergic neurotransmission is evolutionarily conserved across animal phyla. A major class of glutamate receptors are the metabotropic glutamate receptors (mGluRs). In C. elegans three mGluR genes mgl-1, mgl-2 and mgl-3 are organised into three sub-groups, 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 behaviour. The overlapping expression of mgls within this circuit allowed investigation of receptor signalling 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 wild type and mutants to investigate mgl function. This defined a net mgl-1 dependent inhibition of pharyngeal pumping which 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 behaviour 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 describes the molecular and cellular organisation 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. Behavioural 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 behaviour.
Text
J. Biol. Chem.-2015-Dillon-jbc.M114.606608.pdf
- Accepted Manuscript
More information
e-pub ahead of print date: 13 April 2015
Published date: 12 June 2015
Keywords:
metabotropic glutamate receptors (mGluR), optogenetics, Caenorhabditis elegans (C. elegans), electrophysiology, invertebrate
Organisations:
Biomedicine
Identifiers
Local EPrints ID: 377230
URI: http://eprints.soton.ac.uk/id/eprint/377230
ISSN: 0021-9258
PURE UUID: 9151f7e0-64d9-4b79-9784-0851cb758eb1
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Date deposited: 08 Jun 2015 10:02
Last modified: 15 Mar 2024 03:46
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Contributors
Author:
Christopher J Franks
Author:
Caitriona Murray
Author:
Richard J Edwards
Author:
Takeshi Ishihara
Author:
Isao Katsura
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