An Elongin-Cullin-SOCS Box Complex Regulates Stress-Induced Serotonergic Neuromodulation

Neuromodulatory cells transduce environmental information into long-lasting behavioral responses. However, the mechanisms governing how neuronal cells influence behavioral plasticity are difficult to characterize. Here, we adapted the translating ribosome affinity purification (TRAP) approach in C. ...

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Main Authors: Xicotencatl Gracida, Michael F. Dion, Gareth Harris, Yun Zhang, John A. Calarco
Format: Article
Language:English
Published: Elsevier 2017-12-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124717316790
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spelling doaj-0b1bdfeea47c40259537997aaed579182020-11-24T21:43:41ZengElsevierCell Reports2211-12472017-12-0121113089310110.1016/j.celrep.2017.11.042An Elongin-Cullin-SOCS Box Complex Regulates Stress-Induced Serotonergic NeuromodulationXicotencatl Gracida0Michael F. Dion1Gareth Harris2Yun Zhang3John A. Calarco4FAS Center for Systems Biology, Harvard University, Cambridge, MA 02138, USAFAS Center for Systems Biology, Harvard University, Cambridge, MA 02138, USADepartment of Organismal and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USADepartment of Organismal and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USAFAS Center for Systems Biology, Harvard University, Cambridge, MA 02138, USANeuromodulatory cells transduce environmental information into long-lasting behavioral responses. However, the mechanisms governing how neuronal cells influence behavioral plasticity are difficult to characterize. Here, we adapted the translating ribosome affinity purification (TRAP) approach in C. elegans to profile ribosome-associated mRNAs from three major tissues and the neuromodulatory dopaminergic and serotonergic cells. We identified elc-2, an Elongin C ortholog, specifically expressed in stress-sensing amphid neuron dual ciliated sensory ending (ADF) serotonergic sensory neurons, and we found that it plays a role in mediating a long-lasting change in serotonin-dependent feeding behavior induced by heat stress. We demonstrate that ELC-2 and the von Hippel-Lindau protein VHL-1, components of an Elongin-Cullin-SOCS box (ECS) E3 ubiquitin ligase, modulate this behavior after experiencing stress. Also, heat stress induces a transient redistribution of ELC-2, becoming more nuclearly enriched. Together, our results demonstrate dynamic regulation of an E3 ligase and a role for an ECS complex in neuromodulation and control of lasting behavioral states.http://www.sciencedirect.com/science/article/pii/S2211124717316790neuromodulationheat shock responseElonginCvon Hippel-LindauTRAPserotoninC. elegansfeeding
collection DOAJ
language English
format Article
sources DOAJ
author Xicotencatl Gracida
Michael F. Dion
Gareth Harris
Yun Zhang
John A. Calarco
spellingShingle Xicotencatl Gracida
Michael F. Dion
Gareth Harris
Yun Zhang
John A. Calarco
An Elongin-Cullin-SOCS Box Complex Regulates Stress-Induced Serotonergic Neuromodulation
Cell Reports
neuromodulation
heat shock response
ElonginC
von Hippel-Lindau
TRAP
serotonin
C. elegans
feeding
author_facet Xicotencatl Gracida
Michael F. Dion
Gareth Harris
Yun Zhang
John A. Calarco
author_sort Xicotencatl Gracida
title An Elongin-Cullin-SOCS Box Complex Regulates Stress-Induced Serotonergic Neuromodulation
title_short An Elongin-Cullin-SOCS Box Complex Regulates Stress-Induced Serotonergic Neuromodulation
title_full An Elongin-Cullin-SOCS Box Complex Regulates Stress-Induced Serotonergic Neuromodulation
title_fullStr An Elongin-Cullin-SOCS Box Complex Regulates Stress-Induced Serotonergic Neuromodulation
title_full_unstemmed An Elongin-Cullin-SOCS Box Complex Regulates Stress-Induced Serotonergic Neuromodulation
title_sort elongin-cullin-socs box complex regulates stress-induced serotonergic neuromodulation
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2017-12-01
description Neuromodulatory cells transduce environmental information into long-lasting behavioral responses. However, the mechanisms governing how neuronal cells influence behavioral plasticity are difficult to characterize. Here, we adapted the translating ribosome affinity purification (TRAP) approach in C. elegans to profile ribosome-associated mRNAs from three major tissues and the neuromodulatory dopaminergic and serotonergic cells. We identified elc-2, an Elongin C ortholog, specifically expressed in stress-sensing amphid neuron dual ciliated sensory ending (ADF) serotonergic sensory neurons, and we found that it plays a role in mediating a long-lasting change in serotonin-dependent feeding behavior induced by heat stress. We demonstrate that ELC-2 and the von Hippel-Lindau protein VHL-1, components of an Elongin-Cullin-SOCS box (ECS) E3 ubiquitin ligase, modulate this behavior after experiencing stress. Also, heat stress induces a transient redistribution of ELC-2, becoming more nuclearly enriched. Together, our results demonstrate dynamic regulation of an E3 ligase and a role for an ECS complex in neuromodulation and control of lasting behavioral states.
topic neuromodulation
heat shock response
ElonginC
von Hippel-Lindau
TRAP
serotonin
C. elegans
feeding
url http://www.sciencedirect.com/science/article/pii/S2211124717316790
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