Cargando…

Oxygen-sensing neurons reciprocally regulate peripheral lipid metabolism via neuropeptide signaling in Caenorhabditis elegans

The mechanisms by which the sensory environment influences metabolic homeostasis remains poorly understood. In this report, we show that oxygen, a potent environmental signal, is an important regulator of whole body lipid metabolism. C. elegans oxygen-sensing neurons reciprocally regulate peripheral...

Descripción completa

Detalles Bibliográficos
Autores principales: Hussey, Rosalind, Littlejohn, Nicole K., Witham, Emily, Vanstrum, Erik, Mesgarzadeh, Jaleh, Ratanpal, Harkaranveer, Srinivasan, Supriya
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5886693/
https://www.ncbi.nlm.nih.gov/pubmed/29579048
http://dx.doi.org/10.1371/journal.pgen.1007305
_version_ 1783312177432625152
author Hussey, Rosalind
Littlejohn, Nicole K.
Witham, Emily
Vanstrum, Erik
Mesgarzadeh, Jaleh
Ratanpal, Harkaranveer
Srinivasan, Supriya
author_facet Hussey, Rosalind
Littlejohn, Nicole K.
Witham, Emily
Vanstrum, Erik
Mesgarzadeh, Jaleh
Ratanpal, Harkaranveer
Srinivasan, Supriya
author_sort Hussey, Rosalind
collection PubMed
description The mechanisms by which the sensory environment influences metabolic homeostasis remains poorly understood. In this report, we show that oxygen, a potent environmental signal, is an important regulator of whole body lipid metabolism. C. elegans oxygen-sensing neurons reciprocally regulate peripheral lipid metabolism under normoxia in the following way: under high oxygen and food absence, URX sensory neurons are activated, and stimulate fat loss in the intestine, the major metabolic organ for C. elegans. Under lower oxygen conditions or when food is present, the BAG sensory neurons respond by repressing the resting properties of the URX neurons. A genetic screen to identify modulators of this effect led to the identification of a BAG-neuron-specific neuropeptide called FLP-17, whose cognate receptor EGL-6 functions in URX neurons. Thus, BAG sensory neurons counterbalance the metabolic effect of tonically active URX neurons via neuropeptide communication. The combined regulatory actions of these neurons serve to precisely tune the rate and extent of fat loss to the availability of food and oxygen, and provides an interesting example of the myriad mechanisms underlying homeostatic control.
format Online
Article
Text
id pubmed-5886693
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-58866932018-04-20 Oxygen-sensing neurons reciprocally regulate peripheral lipid metabolism via neuropeptide signaling in Caenorhabditis elegans Hussey, Rosalind Littlejohn, Nicole K. Witham, Emily Vanstrum, Erik Mesgarzadeh, Jaleh Ratanpal, Harkaranveer Srinivasan, Supriya PLoS Genet Research Article The mechanisms by which the sensory environment influences metabolic homeostasis remains poorly understood. In this report, we show that oxygen, a potent environmental signal, is an important regulator of whole body lipid metabolism. C. elegans oxygen-sensing neurons reciprocally regulate peripheral lipid metabolism under normoxia in the following way: under high oxygen and food absence, URX sensory neurons are activated, and stimulate fat loss in the intestine, the major metabolic organ for C. elegans. Under lower oxygen conditions or when food is present, the BAG sensory neurons respond by repressing the resting properties of the URX neurons. A genetic screen to identify modulators of this effect led to the identification of a BAG-neuron-specific neuropeptide called FLP-17, whose cognate receptor EGL-6 functions in URX neurons. Thus, BAG sensory neurons counterbalance the metabolic effect of tonically active URX neurons via neuropeptide communication. The combined regulatory actions of these neurons serve to precisely tune the rate and extent of fat loss to the availability of food and oxygen, and provides an interesting example of the myriad mechanisms underlying homeostatic control. Public Library of Science 2018-03-26 /pmc/articles/PMC5886693/ /pubmed/29579048 http://dx.doi.org/10.1371/journal.pgen.1007305 Text en © 2018 Hussey et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Hussey, Rosalind
Littlejohn, Nicole K.
Witham, Emily
Vanstrum, Erik
Mesgarzadeh, Jaleh
Ratanpal, Harkaranveer
Srinivasan, Supriya
Oxygen-sensing neurons reciprocally regulate peripheral lipid metabolism via neuropeptide signaling in Caenorhabditis elegans
title Oxygen-sensing neurons reciprocally regulate peripheral lipid metabolism via neuropeptide signaling in Caenorhabditis elegans
title_full Oxygen-sensing neurons reciprocally regulate peripheral lipid metabolism via neuropeptide signaling in Caenorhabditis elegans
title_fullStr Oxygen-sensing neurons reciprocally regulate peripheral lipid metabolism via neuropeptide signaling in Caenorhabditis elegans
title_full_unstemmed Oxygen-sensing neurons reciprocally regulate peripheral lipid metabolism via neuropeptide signaling in Caenorhabditis elegans
title_short Oxygen-sensing neurons reciprocally regulate peripheral lipid metabolism via neuropeptide signaling in Caenorhabditis elegans
title_sort oxygen-sensing neurons reciprocally regulate peripheral lipid metabolism via neuropeptide signaling in caenorhabditis elegans
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5886693/
https://www.ncbi.nlm.nih.gov/pubmed/29579048
http://dx.doi.org/10.1371/journal.pgen.1007305
work_keys_str_mv AT husseyrosalind oxygensensingneuronsreciprocallyregulateperipherallipidmetabolismvianeuropeptidesignalingincaenorhabditiselegans
AT littlejohnnicolek oxygensensingneuronsreciprocallyregulateperipherallipidmetabolismvianeuropeptidesignalingincaenorhabditiselegans
AT withamemily oxygensensingneuronsreciprocallyregulateperipherallipidmetabolismvianeuropeptidesignalingincaenorhabditiselegans
AT vanstrumerik oxygensensingneuronsreciprocallyregulateperipherallipidmetabolismvianeuropeptidesignalingincaenorhabditiselegans
AT mesgarzadehjaleh oxygensensingneuronsreciprocallyregulateperipherallipidmetabolismvianeuropeptidesignalingincaenorhabditiselegans
AT ratanpalharkaranveer oxygensensingneuronsreciprocallyregulateperipherallipidmetabolismvianeuropeptidesignalingincaenorhabditiselegans
AT srinivasansupriya oxygensensingneuronsreciprocallyregulateperipherallipidmetabolismvianeuropeptidesignalingincaenorhabditiselegans