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Caenorhabditis elegans processes sensory information to choose between freeloading and self-defense strategies

Hydrogen peroxide is the preeminent chemical weapon that organisms use for combat. Individual cells rely on conserved defenses to prevent and repair peroxide-induced damage, but whether similar defenses might be coordinated across cells in animals remains poorly understood. Here, we identify a neuro...

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Autores principales: Schiffer, Jodie A, Servello, Francesco A, Heath, William R, Amrit, Francis Raj Gandhi, Stumbur, Stephanie V, Eder, Matthias, Martin, Olivier MF, Johnsen, Sean B, Stanley, Julian A, Tam, Hannah, Brennan, Sarah J, McGowan, Natalie G, Vogelaar, Abigail L, Xu, Yuyan, Serkin, William T, Ghazi, Arjumand, Stroustrup, Nicholas, Apfeld, Javier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7213980/
https://www.ncbi.nlm.nih.gov/pubmed/32367802
http://dx.doi.org/10.7554/eLife.56186
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author Schiffer, Jodie A
Servello, Francesco A
Heath, William R
Amrit, Francis Raj Gandhi
Stumbur, Stephanie V
Eder, Matthias
Martin, Olivier MF
Johnsen, Sean B
Stanley, Julian A
Tam, Hannah
Brennan, Sarah J
McGowan, Natalie G
Vogelaar, Abigail L
Xu, Yuyan
Serkin, William T
Ghazi, Arjumand
Stroustrup, Nicholas
Apfeld, Javier
author_facet Schiffer, Jodie A
Servello, Francesco A
Heath, William R
Amrit, Francis Raj Gandhi
Stumbur, Stephanie V
Eder, Matthias
Martin, Olivier MF
Johnsen, Sean B
Stanley, Julian A
Tam, Hannah
Brennan, Sarah J
McGowan, Natalie G
Vogelaar, Abigail L
Xu, Yuyan
Serkin, William T
Ghazi, Arjumand
Stroustrup, Nicholas
Apfeld, Javier
author_sort Schiffer, Jodie A
collection PubMed
description Hydrogen peroxide is the preeminent chemical weapon that organisms use for combat. Individual cells rely on conserved defenses to prevent and repair peroxide-induced damage, but whether similar defenses might be coordinated across cells in animals remains poorly understood. Here, we identify a neuronal circuit in the nematode Caenorhabditis elegans that processes information perceived by two sensory neurons to control the induction of hydrogen peroxide defenses in the organism. We found that catalases produced by Escherichia coli, the nematode’s food source, can deplete hydrogen peroxide from the local environment and thereby protect the nematodes. In the presence of E. coli, the nematode’s neurons signal via TGFβ-insulin/IGF1 relay to target tissues to repress expression of catalases and other hydrogen peroxide defenses. This adaptive strategy is the first example of a multicellular organism modulating its defenses when it expects to freeload from the protection provided by molecularly orthologous defenses from another species.
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spelling pubmed-72139802020-05-13 Caenorhabditis elegans processes sensory information to choose between freeloading and self-defense strategies Schiffer, Jodie A Servello, Francesco A Heath, William R Amrit, Francis Raj Gandhi Stumbur, Stephanie V Eder, Matthias Martin, Olivier MF Johnsen, Sean B Stanley, Julian A Tam, Hannah Brennan, Sarah J McGowan, Natalie G Vogelaar, Abigail L Xu, Yuyan Serkin, William T Ghazi, Arjumand Stroustrup, Nicholas Apfeld, Javier eLife Developmental Biology Hydrogen peroxide is the preeminent chemical weapon that organisms use for combat. Individual cells rely on conserved defenses to prevent and repair peroxide-induced damage, but whether similar defenses might be coordinated across cells in animals remains poorly understood. Here, we identify a neuronal circuit in the nematode Caenorhabditis elegans that processes information perceived by two sensory neurons to control the induction of hydrogen peroxide defenses in the organism. We found that catalases produced by Escherichia coli, the nematode’s food source, can deplete hydrogen peroxide from the local environment and thereby protect the nematodes. In the presence of E. coli, the nematode’s neurons signal via TGFβ-insulin/IGF1 relay to target tissues to repress expression of catalases and other hydrogen peroxide defenses. This adaptive strategy is the first example of a multicellular organism modulating its defenses when it expects to freeload from the protection provided by molecularly orthologous defenses from another species. eLife Sciences Publications, Ltd 2020-05-05 /pmc/articles/PMC7213980/ /pubmed/32367802 http://dx.doi.org/10.7554/eLife.56186 Text en © 2020, Schiffer et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology
Schiffer, Jodie A
Servello, Francesco A
Heath, William R
Amrit, Francis Raj Gandhi
Stumbur, Stephanie V
Eder, Matthias
Martin, Olivier MF
Johnsen, Sean B
Stanley, Julian A
Tam, Hannah
Brennan, Sarah J
McGowan, Natalie G
Vogelaar, Abigail L
Xu, Yuyan
Serkin, William T
Ghazi, Arjumand
Stroustrup, Nicholas
Apfeld, Javier
Caenorhabditis elegans processes sensory information to choose between freeloading and self-defense strategies
title Caenorhabditis elegans processes sensory information to choose between freeloading and self-defense strategies
title_full Caenorhabditis elegans processes sensory information to choose between freeloading and self-defense strategies
title_fullStr Caenorhabditis elegans processes sensory information to choose between freeloading and self-defense strategies
title_full_unstemmed Caenorhabditis elegans processes sensory information to choose between freeloading and self-defense strategies
title_short Caenorhabditis elegans processes sensory information to choose between freeloading and self-defense strategies
title_sort caenorhabditis elegans processes sensory information to choose between freeloading and self-defense strategies
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7213980/
https://www.ncbi.nlm.nih.gov/pubmed/32367802
http://dx.doi.org/10.7554/eLife.56186
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