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Context-dependent regulation of feeding behaviour by the insulin receptor, DAF-2, in Caenorhabditis elegans

Context-dependent regulation of feeding behaviour by the insulin receptor, DAF-2, in Caenorhabditis elegans
Context-dependent regulation of feeding behaviour by the insulin receptor, DAF-2, in Caenorhabditis elegans
Insulin signalling plays a significant role in both developmental programmes and pathways modulating the neuronal signalling that controls adult behaviour. Here, we have investigated insulin signalling in food-associated behaviour in adult C. elegans by scoring locomotion and feeding on and off bacteria, the worm’s food. This analysis used mutants (daf-2, daf-18) of the insulin signalling pathway, and we provide evidence for an acute role for insulin signalling in the adult nervous system distinct from its impact on developmental programmes. Insulin receptor daf-2 mutants move slower than wild type both on and off food and showed impaired locomotory responses to food deprivation. This latter behaviour is manifest as a failure to instigate dispersal following prolonged food deprivation and suggests a role for insulin signalling in this adaptive response. Insulin receptor daf-2 mutants are also deficient in pharyngeal pumping on food and off food. Pharmacological analysis showed the pharynx of daf-2 is selectively compromised in its response to 5-HT compared to the excitatory neuropeptide FLP-17. By comparing the adaptive pharyngeal behaviour in intact worms and isolated pharyngeal preparations, we determined that an insulin-dependent signal extrinsic to the pharyngeal system is involved in feeding adaptation. Hence, we suggest that reactive insulin signalling modulates both locomotory foraging and pharyngeal pumping as the animal adapts to the absence of food. We discuss this in the context of insulin signalling directing a shift in the sensitivity of neurotransmitter systems to regulate the worm’s response to changes in food availability in the environment.
1354-2516
1-10
Dillon, James
f406e30a-3ad4-4a53-80db-6694bab5e3ed
Holden-Dye, Linda
8032bf60-5db6-40cb-b71c-ddda9d212c8e
O'connor, Vincent
8021b06c-01a0-4925-9dde-a61c8fe278ca
Hopper, Neil
61835569-6272-4233-b6b2-a69d2bbecb43
Dillon, James
f406e30a-3ad4-4a53-80db-6694bab5e3ed
Holden-Dye, Linda
8032bf60-5db6-40cb-b71c-ddda9d212c8e
O'connor, Vincent
8021b06c-01a0-4925-9dde-a61c8fe278ca
Hopper, Neil
61835569-6272-4233-b6b2-a69d2bbecb43

Dillon, James, Holden-Dye, Linda, O'connor, Vincent and Hopper, Neil (2016) Context-dependent regulation of feeding behaviour by the insulin receptor, DAF-2, in Caenorhabditis elegans. Invertebrate Neuroscience, 16 (4), 1-10. (doi:10.1007/s10158-016-0187-2).

Record type: Article

Abstract

Insulin signalling plays a significant role in both developmental programmes and pathways modulating the neuronal signalling that controls adult behaviour. Here, we have investigated insulin signalling in food-associated behaviour in adult C. elegans by scoring locomotion and feeding on and off bacteria, the worm’s food. This analysis used mutants (daf-2, daf-18) of the insulin signalling pathway, and we provide evidence for an acute role for insulin signalling in the adult nervous system distinct from its impact on developmental programmes. Insulin receptor daf-2 mutants move slower than wild type both on and off food and showed impaired locomotory responses to food deprivation. This latter behaviour is manifest as a failure to instigate dispersal following prolonged food deprivation and suggests a role for insulin signalling in this adaptive response. Insulin receptor daf-2 mutants are also deficient in pharyngeal pumping on food and off food. Pharmacological analysis showed the pharynx of daf-2 is selectively compromised in its response to 5-HT compared to the excitatory neuropeptide FLP-17. By comparing the adaptive pharyngeal behaviour in intact worms and isolated pharyngeal preparations, we determined that an insulin-dependent signal extrinsic to the pharyngeal system is involved in feeding adaptation. Hence, we suggest that reactive insulin signalling modulates both locomotory foraging and pharyngeal pumping as the animal adapts to the absence of food. We discuss this in the context of insulin signalling directing a shift in the sensitivity of neurotransmitter systems to regulate the worm’s response to changes in food availability in the environment.

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Accepted/In Press date: 13 April 2016
e-pub ahead of print date: 21 May 2016
Published date: June 2016
Organisations: Biomedicine

Identifiers

Local EPrints ID: 402109
URI: http://eprints.soton.ac.uk/id/eprint/402109
ISSN: 1354-2516
PURE UUID: c9f5ad75-9cc6-413e-90ff-5aab0e63e697
ORCID for James Dillon: ORCID iD orcid.org/0000-0003-3244-7483
ORCID for Linda Holden-Dye: ORCID iD orcid.org/0000-0002-9704-1217
ORCID for Vincent O'connor: ORCID iD orcid.org/0000-0003-3185-5709

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Date deposited: 02 Nov 2016 11:56
Last modified: 16 Mar 2024 03:13

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Author: James Dillon ORCID iD
Author: Neil Hopper

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