Cargando…

The stress-responsive gene GDPGP1/mcp-1 regulates neuronal glycogen metabolism and survival

Maladaptive responses to stress might play a role in the sensitivity of neurons to stress. To identify novel cellular responses to stress, we performed transcriptional analysis in acutely stressed mouse neurons, followed by functional characterization in Caenorhabditis elegans. In both contexts, we...

Descripción completa

Detalles Bibliográficos
Autores principales: Schulz, Alexander, Sekine, Yuichi, Oyeyemi, Motunrayo J., Abrams, Alexander J., Basavaraju, Manasa, Han, Sung Min, Groth, Marco, Morrison, Helen, Strittmatter, Stephen M., Hammarlund, Marc
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7041677/
https://www.ncbi.nlm.nih.gov/pubmed/31968056
http://dx.doi.org/10.1083/jcb.201807127
_version_ 1783501184918618112
author Schulz, Alexander
Sekine, Yuichi
Oyeyemi, Motunrayo J.
Abrams, Alexander J.
Basavaraju, Manasa
Han, Sung Min
Groth, Marco
Morrison, Helen
Strittmatter, Stephen M.
Hammarlund, Marc
author_facet Schulz, Alexander
Sekine, Yuichi
Oyeyemi, Motunrayo J.
Abrams, Alexander J.
Basavaraju, Manasa
Han, Sung Min
Groth, Marco
Morrison, Helen
Strittmatter, Stephen M.
Hammarlund, Marc
author_sort Schulz, Alexander
collection PubMed
description Maladaptive responses to stress might play a role in the sensitivity of neurons to stress. To identify novel cellular responses to stress, we performed transcriptional analysis in acutely stressed mouse neurons, followed by functional characterization in Caenorhabditis elegans. In both contexts, we found that the gene GDPGP1/mcp-1 is down-regulated by a variety of stresses. Functionally, the enzyme GDPGP1/mcp-1 protects against stress. Knockdown of GDPGP1 in mouse neurons leads to widespread neuronal cell death. Loss of mcp-1, the single homologue of GDPGP1 in C. elegans, leads to increased degeneration of GABA neurons as well as reduced survival of animals following environmental stress. Overexpression of mcp-1 in neurons enhances survival under hypoxia and protects against neurodegeneration in a tauopathy model. GDPGP1/mcp-1 regulates neuronal glycogen levels, indicating a key role for this metabolite in neuronal stress resistance. Together, our data indicate that down-regulation of GDPGP1/mcp-1 and consequent loss of neuronal glycogen is a maladaptive response that limits neuronal stress resistance and reduces survival.
format Online
Article
Text
id pubmed-7041677
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Rockefeller University Press
record_format MEDLINE/PubMed
spelling pubmed-70416772020-08-03 The stress-responsive gene GDPGP1/mcp-1 regulates neuronal glycogen metabolism and survival Schulz, Alexander Sekine, Yuichi Oyeyemi, Motunrayo J. Abrams, Alexander J. Basavaraju, Manasa Han, Sung Min Groth, Marco Morrison, Helen Strittmatter, Stephen M. Hammarlund, Marc J Cell Biol Article Maladaptive responses to stress might play a role in the sensitivity of neurons to stress. To identify novel cellular responses to stress, we performed transcriptional analysis in acutely stressed mouse neurons, followed by functional characterization in Caenorhabditis elegans. In both contexts, we found that the gene GDPGP1/mcp-1 is down-regulated by a variety of stresses. Functionally, the enzyme GDPGP1/mcp-1 protects against stress. Knockdown of GDPGP1 in mouse neurons leads to widespread neuronal cell death. Loss of mcp-1, the single homologue of GDPGP1 in C. elegans, leads to increased degeneration of GABA neurons as well as reduced survival of animals following environmental stress. Overexpression of mcp-1 in neurons enhances survival under hypoxia and protects against neurodegeneration in a tauopathy model. GDPGP1/mcp-1 regulates neuronal glycogen levels, indicating a key role for this metabolite in neuronal stress resistance. Together, our data indicate that down-regulation of GDPGP1/mcp-1 and consequent loss of neuronal glycogen is a maladaptive response that limits neuronal stress resistance and reduces survival. Rockefeller University Press 2020-01-22 /pmc/articles/PMC7041677/ /pubmed/31968056 http://dx.doi.org/10.1083/jcb.201807127 Text en © 2019 Schulz et al. http://www.rupress.org/terms/https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
spellingShingle Article
Schulz, Alexander
Sekine, Yuichi
Oyeyemi, Motunrayo J.
Abrams, Alexander J.
Basavaraju, Manasa
Han, Sung Min
Groth, Marco
Morrison, Helen
Strittmatter, Stephen M.
Hammarlund, Marc
The stress-responsive gene GDPGP1/mcp-1 regulates neuronal glycogen metabolism and survival
title The stress-responsive gene GDPGP1/mcp-1 regulates neuronal glycogen metabolism and survival
title_full The stress-responsive gene GDPGP1/mcp-1 regulates neuronal glycogen metabolism and survival
title_fullStr The stress-responsive gene GDPGP1/mcp-1 regulates neuronal glycogen metabolism and survival
title_full_unstemmed The stress-responsive gene GDPGP1/mcp-1 regulates neuronal glycogen metabolism and survival
title_short The stress-responsive gene GDPGP1/mcp-1 regulates neuronal glycogen metabolism and survival
title_sort stress-responsive gene gdpgp1/mcp-1 regulates neuronal glycogen metabolism and survival
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7041677/
https://www.ncbi.nlm.nih.gov/pubmed/31968056
http://dx.doi.org/10.1083/jcb.201807127
work_keys_str_mv AT schulzalexander thestressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT sekineyuichi thestressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT oyeyemimotunrayoj thestressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT abramsalexanderj thestressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT basavarajumanasa thestressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT hansungmin thestressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT grothmarco thestressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT morrisonhelen thestressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT strittmatterstephenm thestressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT hammarlundmarc thestressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT schulzalexander stressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT sekineyuichi stressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT oyeyemimotunrayoj stressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT abramsalexanderj stressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT basavarajumanasa stressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT hansungmin stressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT grothmarco stressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT morrisonhelen stressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT strittmatterstephenm stressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival
AT hammarlundmarc stressresponsivegenegdpgp1mcp1regulatesneuronalglycogenmetabolismandsurvival