Stress-Induced Neural Plasticity Mediated by Glial GPCR REMO-1 Promotes C. elegans Adaptive Behavior

Summary: Animal nervous systems remodel following stress. Although global stress-dependent changes are well documented, contributions of individual neuron remodeling events to animal behavior modification are challenging to study. In response to environmental insults, C. elegans become stress-resist...

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Main Authors: In Hae Lee, Carl Procko, Yun Lu, Shai Shaham
Format: Article
Language:English
Published: Elsevier 2021-01-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124720315965
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spelling doaj-9f6de87fbd824c0fada59ac927942a2c2021-01-14T04:17:03ZengElsevierCell Reports2211-12472021-01-01342108607Stress-Induced Neural Plasticity Mediated by Glial GPCR REMO-1 Promotes C. elegans Adaptive BehaviorIn Hae Lee0Carl Procko1Yun Lu2Shai Shaham3Laboratory of Developmental Genetics, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USALaboratory of Developmental Genetics, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USALaboratory of Developmental Genetics, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USALaboratory of Developmental Genetics, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA; Corresponding authorSummary: Animal nervous systems remodel following stress. Although global stress-dependent changes are well documented, contributions of individual neuron remodeling events to animal behavior modification are challenging to study. In response to environmental insults, C. elegans become stress-resistant dauers. Dauer entry induces amphid sensory organ remodeling in which bilateral AMsh glial cells expand and fuse, allowing embedded AWC chemosensory neurons to extend sensory receptive endings. We show that amphid remodeling correlates with accelerated dauer exit upon exposure to favorable conditions and identify a G protein-coupled receptor, REMO-1, driving AMsh glia fusion, AWC neuron remodeling, and dauer exit. REMO-1 is expressed in and localizes to AMsh glia tips, is dispensable for other remodeling events, and promotes stress-induced expression of the remodeling receptor tyrosine kinase VER-1. Our results demonstrate how single-neuron structural changes affect animal behavior, identify key glial roles in stress-induced nervous system plasticity, and demonstrate that remodeling primes animals to respond to favorable conditions.http://www.sciencedirect.com/science/article/pii/S2211124720315965REMO-1C. elegansglianervous system remodelingdauerAWC neuron
collection DOAJ
language English
format Article
sources DOAJ
author In Hae Lee
Carl Procko
Yun Lu
Shai Shaham
spellingShingle In Hae Lee
Carl Procko
Yun Lu
Shai Shaham
Stress-Induced Neural Plasticity Mediated by Glial GPCR REMO-1 Promotes C. elegans Adaptive Behavior
Cell Reports
REMO-1
C. elegans
glia
nervous system remodeling
dauer
AWC neuron
author_facet In Hae Lee
Carl Procko
Yun Lu
Shai Shaham
author_sort In Hae Lee
title Stress-Induced Neural Plasticity Mediated by Glial GPCR REMO-1 Promotes C. elegans Adaptive Behavior
title_short Stress-Induced Neural Plasticity Mediated by Glial GPCR REMO-1 Promotes C. elegans Adaptive Behavior
title_full Stress-Induced Neural Plasticity Mediated by Glial GPCR REMO-1 Promotes C. elegans Adaptive Behavior
title_fullStr Stress-Induced Neural Plasticity Mediated by Glial GPCR REMO-1 Promotes C. elegans Adaptive Behavior
title_full_unstemmed Stress-Induced Neural Plasticity Mediated by Glial GPCR REMO-1 Promotes C. elegans Adaptive Behavior
title_sort stress-induced neural plasticity mediated by glial gpcr remo-1 promotes c. elegans adaptive behavior
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2021-01-01
description Summary: Animal nervous systems remodel following stress. Although global stress-dependent changes are well documented, contributions of individual neuron remodeling events to animal behavior modification are challenging to study. In response to environmental insults, C. elegans become stress-resistant dauers. Dauer entry induces amphid sensory organ remodeling in which bilateral AMsh glial cells expand and fuse, allowing embedded AWC chemosensory neurons to extend sensory receptive endings. We show that amphid remodeling correlates with accelerated dauer exit upon exposure to favorable conditions and identify a G protein-coupled receptor, REMO-1, driving AMsh glia fusion, AWC neuron remodeling, and dauer exit. REMO-1 is expressed in and localizes to AMsh glia tips, is dispensable for other remodeling events, and promotes stress-induced expression of the remodeling receptor tyrosine kinase VER-1. Our results demonstrate how single-neuron structural changes affect animal behavior, identify key glial roles in stress-induced nervous system plasticity, and demonstrate that remodeling primes animals to respond to favorable conditions.
topic REMO-1
C. elegans
glia
nervous system remodeling
dauer
AWC neuron
url http://www.sciencedirect.com/science/article/pii/S2211124720315965
work_keys_str_mv AT inhaelee stressinducedneuralplasticitymediatedbyglialgpcrremo1promotescelegansadaptivebehavior
AT carlprocko stressinducedneuralplasticitymediatedbyglialgpcrremo1promotescelegansadaptivebehavior
AT yunlu stressinducedneuralplasticitymediatedbyglialgpcrremo1promotescelegansadaptivebehavior
AT shaishaham stressinducedneuralplasticitymediatedbyglialgpcrremo1promotescelegansadaptivebehavior
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