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: Schiffer, Jodie A., Servello, Francesco A., Heath, William R., Amrit, Francis Raj Ghandi, Stumbur, Stephanie V, Eder, Matthias, Martin, Olivier M. F., Johnsen, Sean B., Stanley, Julia A., Tam, Hannah, Brennan, Sara J., McGowan, Natalie G., Vogelaar, Abigail L., Xu, Yuyan, Serkin, William T., Ghazi, Arjumand, Stroustrup, Nicholas, Apfeld, Javier
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2020
País:España
Institución:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/45487
Acceso en línea:http://hdl.handle.net/10230/45487
http://dx.doi.org/10.7554/eLife.56186
Access Level:acceso abierto
Palabra clave:Caenorhabditis elegans
Genètica
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spelling Caenorhabditis elegans processes sensory information to choose between freeloading and self-defense strategiesSchiffer, Jodie A.Servello, Francesco A.Heath, William R.Amrit, Francis Raj GhandiStumbur, Stephanie VEder, MatthiasMartin, Olivier M. F.Johnsen, Sean B.Stanley, Julia A.Tam, HannahBrennan, Sara J.McGowan, Natalie G.Vogelaar, Abigail L.Xu, YuyanSerkin, William T.Ghazi, ArjumandStroustrup, NicholasApfeld, JavierCaenorhabditis elegansGenèticaHydrogen 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.Supported by NIH Office of Research Infrastructure Programs (P40 OD010440), and the National BioResources Project, Japan. The research was supported by National Science Foundation CAREER grant 1750065 to JA, a Northeastern University Tier one award to JA, a National Institutes of Health grant R01AG051659 to AG, the MEIC Excelencia award BFU2017-88615-P to NS, the Spanish Ministry of Economy, Industry and Competitiveness (MEIC) to the EMBL partnership to NS, the Centro de Excelencia Severo Ochoa to NS, and the CERCA Programme/Generalitat de Catalunya, and European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (Grant agreement No. 852201) to NSeLife202020202020info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/45487http://dx.doi.org/10.7554/eLife.56186reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésElife. 2020 May 5;9:e56186info:eu-repo/grantAgreement/EC/H2020/852201info:eu-repo/grantAgreement/ES/2PE/BFU2017-88615-Pinfo:eu-repo/grantAgreement/ES/2PE/BES-2017-081169© 2020 Jodie A. Schiffer et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are creditedhttps://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/454872026-06-12T07:21:37Z
dc.title.none.fl_str_mv 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
spellingShingle Caenorhabditis elegans processes sensory information to choose between freeloading and self-defense strategies
Schiffer, Jodie A.
Caenorhabditis elegans
Genètica
title_short 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_sort Caenorhabditis elegans processes sensory information to choose between freeloading and self-defense strategies
dc.creator.none.fl_str_mv Schiffer, Jodie A.
Servello, Francesco A.
Heath, William R.
Amrit, Francis Raj Ghandi
Stumbur, Stephanie V
Eder, Matthias
Martin, Olivier M. F.
Johnsen, Sean B.
Stanley, Julia A.
Tam, Hannah
Brennan, Sara J.
McGowan, Natalie G.
Vogelaar, Abigail L.
Xu, Yuyan
Serkin, William T.
Ghazi, Arjumand
Stroustrup, Nicholas
Apfeld, Javier
author Schiffer, Jodie A.
author_facet Schiffer, Jodie A.
Servello, Francesco A.
Heath, William R.
Amrit, Francis Raj Ghandi
Stumbur, Stephanie V
Eder, Matthias
Martin, Olivier M. F.
Johnsen, Sean B.
Stanley, Julia A.
Tam, Hannah
Brennan, Sara J.
McGowan, Natalie G.
Vogelaar, Abigail L.
Xu, Yuyan
Serkin, William T.
Ghazi, Arjumand
Stroustrup, Nicholas
Apfeld, Javier
author_role author
author2 Servello, Francesco A.
Heath, William R.
Amrit, Francis Raj Ghandi
Stumbur, Stephanie V
Eder, Matthias
Martin, Olivier M. F.
Johnsen, Sean B.
Stanley, Julia A.
Tam, Hannah
Brennan, Sara J.
McGowan, Natalie G.
Vogelaar, Abigail L.
Xu, Yuyan
Serkin, William T.
Ghazi, Arjumand
Stroustrup, Nicholas
Apfeld, Javier
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Caenorhabditis elegans
Genètica
topic Caenorhabditis elegans
Genètica
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.
publishDate 2020
dc.date.none.fl_str_mv 2020
2020
2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/45487
http://dx.doi.org/10.7554/eLife.56186
url http://hdl.handle.net/10230/45487
http://dx.doi.org/10.7554/eLife.56186
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Elife. 2020 May 5;9:e56186
info:eu-repo/grantAgreement/EC/H2020/852201
info:eu-repo/grantAgreement/ES/2PE/BFU2017-88615-P
info:eu-repo/grantAgreement/ES/2PE/BES-2017-081169
dc.rights.none.fl_str_mv https://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv eLife
publisher.none.fl_str_mv eLife
dc.source.none.fl_str_mv reponame:Repositorio Digital de la UPF
instname:Universitat Pompeu Fabra
instname_str Universitat Pompeu Fabra
reponame_str Repositorio Digital de la UPF
collection Repositorio Digital de la UPF
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,812455

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