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Regulation of the pharynx of Caenorhabditis elegans by 5-HT, octopamine, and FMRFamide-like neuropeptides

Regulation of the pharynx of Caenorhabditis elegans by 5-HT, octopamine, and FMRFamide-like neuropeptides
Regulation of the pharynx of Caenorhabditis elegans by 5-HT, octopamine, and FMRFamide-like neuropeptides
More than fifty FMRFamide-like neuropeptides have been identified in nematodes. We addressed the role of a subset of these in the control of nematode feeding by electrophysiological recording of the activity of C. elegans pharynx. AF1 (KNEFIRFamide), AF2 (KHEYLRFamide), AF8 (KSAYMRFamide), and GAKFIRFamide (encoded by the C. elegans genes flp-8, flp-14, flp-6, and flp-5, respectively) increased pharyngeal action potential frequency, in a manner similar to 5-HT. In contrast, SDPNFLRFamide, SADPNFLRFamide, SAEPFGTMRFamide, KPSVRFamide, APEASPFIRFamide, and AQTVRFamide (encoded by the C. elegans genes flp-1; flp-1; flp-3; flp-9; flp-13, and flp-16, respectively) inhibited the pharynx in a manner similar to octopamine. Only three of the neuropeptides had potent effects at low nanomolar concentrations, consistent with a physiological role in pharyngeal regulation. Therefore, we assessed whether these three peptides mediated their actions either directly on the pharynx or indirectly via the neural circuit controlling its activity by comparing actions between wild-type and mutants with deficits in synaptic signaling. Our data support the conclusion that AF1 and SAEPFGTMRFamide regulate the activity of the pharynx indirectly, whereas APEASPFIRFamide exerts its action directly. These results are in agreement with the expression pattern for the genes encoding the neuropeptides (Kim and Li, 1999) as both flp-8 and flp-3 are expressed in extrapharyngeal neurons, whereas flp-13 is expressed in I5, a neuron with synaptic output to the pharyngeal muscle. These results provide the first, direct, functional information on the action of neuropeptides in C. elegans. Furthermore, we provide evidence for a putative inhibitory peptidergic synapse, which is likely to have a role in the control of feeding. © 2001 John Wiley & Sons, Inc. J Neurobiol 49: 235-244, 2001
Caenorhabditis elegans, neuropeptides, electrophysiology, nematode, pharynx
0022-3034
235-244
Rogers, Candida M.
e6b70fdf-ae92-4324-bbb1-8dfb9578d435
Franks, Christopher J.
9842534b-4d3f-4ee8-a07e-3b050f748593
Walker, Robert J.
9368ac2d-f1e9-4bd9-a4b4-4a161c4aa140
Burke, Julian F.
cd32edea-d47d-48a0-837e-ac936cf217d9
Holden-Dye, Lindy
8032bf60-5db6-40cb-b71c-ddda9d212c8e
Rogers, Candida M.
e6b70fdf-ae92-4324-bbb1-8dfb9578d435
Franks, Christopher J.
9842534b-4d3f-4ee8-a07e-3b050f748593
Walker, Robert J.
9368ac2d-f1e9-4bd9-a4b4-4a161c4aa140
Burke, Julian F.
cd32edea-d47d-48a0-837e-ac936cf217d9
Holden-Dye, Lindy
8032bf60-5db6-40cb-b71c-ddda9d212c8e

Rogers, Candida M., Franks, Christopher J., Walker, Robert J., Burke, Julian F. and Holden-Dye, Lindy (2001) Regulation of the pharynx of Caenorhabditis elegans by 5-HT, octopamine, and FMRFamide-like neuropeptides. Journal of Neurobiology, 49 (3), 235-244. (doi:10.1002/neu.1078).

Record type: Article

Abstract

More than fifty FMRFamide-like neuropeptides have been identified in nematodes. We addressed the role of a subset of these in the control of nematode feeding by electrophysiological recording of the activity of C. elegans pharynx. AF1 (KNEFIRFamide), AF2 (KHEYLRFamide), AF8 (KSAYMRFamide), and GAKFIRFamide (encoded by the C. elegans genes flp-8, flp-14, flp-6, and flp-5, respectively) increased pharyngeal action potential frequency, in a manner similar to 5-HT. In contrast, SDPNFLRFamide, SADPNFLRFamide, SAEPFGTMRFamide, KPSVRFamide, APEASPFIRFamide, and AQTVRFamide (encoded by the C. elegans genes flp-1; flp-1; flp-3; flp-9; flp-13, and flp-16, respectively) inhibited the pharynx in a manner similar to octopamine. Only three of the neuropeptides had potent effects at low nanomolar concentrations, consistent with a physiological role in pharyngeal regulation. Therefore, we assessed whether these three peptides mediated their actions either directly on the pharynx or indirectly via the neural circuit controlling its activity by comparing actions between wild-type and mutants with deficits in synaptic signaling. Our data support the conclusion that AF1 and SAEPFGTMRFamide regulate the activity of the pharynx indirectly, whereas APEASPFIRFamide exerts its action directly. These results are in agreement with the expression pattern for the genes encoding the neuropeptides (Kim and Li, 1999) as both flp-8 and flp-3 are expressed in extrapharyngeal neurons, whereas flp-13 is expressed in I5, a neuron with synaptic output to the pharyngeal muscle. These results provide the first, direct, functional information on the action of neuropeptides in C. elegans. Furthermore, we provide evidence for a putative inhibitory peptidergic synapse, which is likely to have a role in the control of feeding. © 2001 John Wiley & Sons, Inc. J Neurobiol 49: 235-244, 2001

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Published date: November 2001
Keywords: Caenorhabditis elegans, neuropeptides, electrophysiology, nematode, pharynx

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Local EPrints ID: 56082
URI: http://eprints.soton.ac.uk/id/eprint/56082
ISSN: 0022-3034
PURE UUID: 546da81d-d037-44f0-bc15-27c40abebe37
ORCID for Christopher J. Franks: ORCID iD orcid.org/0000-0002-5412-7037
ORCID for Robert J. Walker: ORCID iD orcid.org/0000-0002-9031-7671
ORCID for Lindy Holden-Dye: ORCID iD orcid.org/0000-0002-9704-1217

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Date deposited: 07 Aug 2008
Last modified: 16 Mar 2024 04:37

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Contributors

Author: Candida M. Rogers
Author: Julian F. Burke

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