The transsulfuration pathway suppresses the embryonic lethal phenotype of glutathione reductase mutants in Caenorhabditis elegans

[Data availability] C. elegans strains, E. coli strains and plasmids are available upon request. The authors affirm that all data necessary for confirming the conclusions of the article are present within the article, figures and tables with the exception of Supplementary Table 1 which contains C. e...

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Autores: Valenzuela-Villatoro, Marina, Gomez-Orte, Eva, Guerrero-Gómez, David, Cheng, Qing, Zheleva, Angelina, Mora-Lorca, José Antonio, Petrovic, Dunja, O'Neil, Nigel J., Cerón, Julián, Hatakeyama, Akiko, Onami, Shuichi, Ordóñez-Luque, Alexandra, Ayuso, Cristina, Askjaer, Peter, Filipovic, Milos R., Arnér, Elias S. J., Cabello, Juan, Miranda-Vizuete, Antonio
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2025
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/402528
Acceso en línea:http://hdl.handle.net/10261/402528
https://api.elsevier.com/content/abstract/scopus_id/105013530808
Access Level:acceso abierto
Palabra clave:Smg genes
NMD pathway
Cysteine
Cystine
Glutathione
Transsulfuration
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dc.title.none.fl_str_mv The transsulfuration pathway suppresses the embryonic lethal phenotype of glutathione reductase mutants in Caenorhabditis elegans
title The transsulfuration pathway suppresses the embryonic lethal phenotype of glutathione reductase mutants in Caenorhabditis elegans
spellingShingle The transsulfuration pathway suppresses the embryonic lethal phenotype of glutathione reductase mutants in Caenorhabditis elegans
Valenzuela-Villatoro, Marina
Smg genes
NMD pathway
Cysteine
Cystine
Glutathione
Transsulfuration
title_short The transsulfuration pathway suppresses the embryonic lethal phenotype of glutathione reductase mutants in Caenorhabditis elegans
title_full The transsulfuration pathway suppresses the embryonic lethal phenotype of glutathione reductase mutants in Caenorhabditis elegans
title_fullStr The transsulfuration pathway suppresses the embryonic lethal phenotype of glutathione reductase mutants in Caenorhabditis elegans
title_full_unstemmed The transsulfuration pathway suppresses the embryonic lethal phenotype of glutathione reductase mutants in Caenorhabditis elegans
title_sort The transsulfuration pathway suppresses the embryonic lethal phenotype of glutathione reductase mutants in Caenorhabditis elegans
dc.creator.none.fl_str_mv Valenzuela-Villatoro, Marina
Gomez-Orte, Eva
Guerrero-Gómez, David
Cheng, Qing
Zheleva, Angelina
Mora-Lorca, José Antonio
Petrovic, Dunja
O'Neil, Nigel J.
Cerón, Julián
Hatakeyama, Akiko
Onami, Shuichi
Ordóñez-Luque, Alexandra
Ayuso, Cristina
Askjaer, Peter
Filipovic, Milos R.
Arnér, Elias S. J.
Cabello, Juan
Miranda-Vizuete, Antonio
author Valenzuela-Villatoro, Marina
author_facet Valenzuela-Villatoro, Marina
Gomez-Orte, Eva
Guerrero-Gómez, David
Cheng, Qing
Zheleva, Angelina
Mora-Lorca, José Antonio
Petrovic, Dunja
O'Neil, Nigel J.
Cerón, Julián
Hatakeyama, Akiko
Onami, Shuichi
Ordóñez-Luque, Alexandra
Ayuso, Cristina
Askjaer, Peter
Filipovic, Milos R.
Arnér, Elias S. J.
Cabello, Juan
Miranda-Vizuete, Antonio
author_role author
author2 Gomez-Orte, Eva
Guerrero-Gómez, David
Cheng, Qing
Zheleva, Angelina
Mora-Lorca, José Antonio
Petrovic, Dunja
O'Neil, Nigel J.
Cerón, Julián
Hatakeyama, Akiko
Onami, Shuichi
Ordóñez-Luque, Alexandra
Ayuso, Cristina
Askjaer, Peter
Filipovic, Milos R.
Arnér, Elias S. J.
Cabello, Juan
Miranda-Vizuete, Antonio
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Agencia Estatal de Investigación (España)
Ministerio de Ciencia, Innovación y Universidades (España)
European Commission
Junta de Andalucía
Valenzuela-Villatoro, Marina [0000-0001-5601-9462]
Gomez-Orte, Eva [0000-0001-6802-1746]
Guerrero-Gómez, David [0000-0001-9403-6431]
Cheng, Qing [0000-0002-3170-9333]
Zheleva, Angelina [0000-0002-6898-6289]
Mora-Lorca, José Antonio [0000-0003-0389-8744]
Petrovic, Dunja [0009-0003-9013-778X]
O'Neil, Nigel J. [0000-0002-1992-6976]
Cerón, Julián [0000-0003-4739-2243]
Hatakeyama, Akiko [0009-0001-4652-3179]
Onami, Shuichi [0000-0002-8255-1724]
Ordóñez-Luque, Alexandra [0009-0002-9684-949X]
Ayuso, Cristina [0000-0002-7179-4309]
Askjaer, Peter [0000-0003-3192-4428]
Filipovic, Milos R. [0000-0003-0060-0041]
Arnér, Elias S. J. [0000-0002-4807-6114]
Cabello, Juan [0000-0002-3835-0116]
Miranda-Vizuete, Antonio [0000-0002-6856-5396]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Smg genes
NMD pathway
Cysteine
Cystine
Glutathione
Transsulfuration
topic Smg genes
NMD pathway
Cysteine
Cystine
Glutathione
Transsulfuration
description [Data availability] C. elegans strains, E. coli strains and plasmids are available upon request. The authors affirm that all data necessary for confirming the conclusions of the article are present within the article, figures and tables with the exception of Supplementary Table 1 which contains C. elegans strains and genotypes used in this study. WGS data are deposited at the Sequence Read Archive of NCBI with the ID: PRJNA1179913. Supplemental material available at G3 online.
publishDate 2025
dc.date.none.fl_str_mv 2025
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/402528
https://api.elsevier.com/content/abstract/scopus_id/105013530808
url http://hdl.handle.net/10261/402528
https://api.elsevier.com/content/abstract/scopus_id/105013530808
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
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info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/CEX2020-001088-M
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PGC2018-094276-B-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-122311NB-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-127388NB-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2022-137162NB-I00
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1093/g3journal/jkaf102
https://doi.org/10.1093/g3journal/jkaf102

dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Genetics Society of America
Oxford University Press
publisher.none.fl_str_mv Genetics Society of America
Oxford University Press
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
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spelling The transsulfuration pathway suppresses the embryonic lethal phenotype of glutathione reductase mutants in Caenorhabditis elegansValenzuela-Villatoro, MarinaGomez-Orte, EvaGuerrero-Gómez, DavidCheng, QingZheleva, AngelinaMora-Lorca, José AntonioPetrovic, DunjaO'Neil, Nigel J.Cerón, JuliánHatakeyama, AkikoOnami, ShuichiOrdóñez-Luque, AlexandraAyuso, CristinaAskjaer, PeterFilipovic, Milos R.Arnér, Elias S. J.Cabello, JuanMiranda-Vizuete, AntonioSmg genesNMD pathwayCysteineCystineGlutathioneTranssulfuration[Data availability] C. elegans strains, E. coli strains and plasmids are available upon request. The authors affirm that all data necessary for confirming the conclusions of the article are present within the article, figures and tables with the exception of Supplementary Table 1 which contains C. elegans strains and genotypes used in this study. WGS data are deposited at the Sequence Read Archive of NCBI with the ID: PRJNA1179913. Supplemental material available at G3 online.The gsr-1 gene encodes the only glutathione reductase in Caenorhabditis elegans and gsr-1 loss-of-function alleles have a fully penetrant embryonic lethal phenotype. Therefore, maintenance of glutathione redox homeostasis is essential for nematode survival. We report here that impairment of the nonsense-mediated mRNA decay (NMD) pathway suppresses the embryonic lethality of gsr-1 mutants, allowing their normal development and growth. This NMD pathway dependent suppression requires cth-1 and cth-2 that encode 2 isoforms of cystathionine-γ-lyase that catalyze the conversion of cystathionine to cysteine through the transsulfuration pathway. In contrast, the thioredoxin system that can also provide cysteine through the cystine reduction pathway appears to be dispensable for the suppression of the lethal phenotype of gsr-1 embryos when the NMD pathway is inactivated. Together, our data indicate that increasing the activity of the reverse transsulfuration pathway can compensate the detrimental effect of the gsr-1 mutation, raising the interesting question of why C. elegans has not preserved such compensatory mechanism to avoid the embryonic lethality of these mutants.MV-V, DG-G, EG-O, JC, and AM-V were supported by Projects PGC2018-094276-B-I00, PID2021-122311NB-I00, and PID2021-127388NB-I00, financed by MICIU/AEI/10.13039/501100011033 and from FEDER, UE as well as by Projects P20_00229 and DOC_01674 Ayudas a proyectos I + D + I (PAIDI 2020) CTEICU—Junta de Andalucía. Co-financed with FEDER at 80%. Andalucía se mueve con Europa. CA and PA were supported by Projects PID2022-137162NB-I00 and CEX2020-001088-M, financed by MICIU/AEI/10.13039/501100011033 and from FEDER, UE.With funding form the Spanish government through the “María de Maeztu Unit of Excellence” accreditation (CEX2020-001088-M).Peer reviewedGenetics Society of AmericaOxford University PressAgencia Estatal de Investigación (España)Ministerio de Ciencia, Innovación y Universidades (España)European CommissionJunta de AndalucíaValenzuela-Villatoro, Marina [0000-0001-5601-9462]Gomez-Orte, Eva [0000-0001-6802-1746]Guerrero-Gómez, David [0000-0001-9403-6431]Cheng, Qing [0000-0002-3170-9333]Zheleva, Angelina [0000-0002-6898-6289]Mora-Lorca, José Antonio [0000-0003-0389-8744]Petrovic, Dunja [0009-0003-9013-778X]O'Neil, Nigel J. [0000-0002-1992-6976]Cerón, Julián [0000-0003-4739-2243]Hatakeyama, Akiko [0009-0001-4652-3179]Onami, Shuichi [0000-0002-8255-1724]Ordóñez-Luque, Alexandra [0009-0002-9684-949X]Ayuso, Cristina [0000-0002-7179-4309]Askjaer, Peter [0000-0003-3192-4428]Filipovic, Milos R. [0000-0003-0060-0041]Arnér, Elias S. J. [0000-0002-4807-6114]Cabello, Juan [0000-0002-3835-0116]Miranda-Vizuete, Antonio [0000-0002-6856-5396]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252025info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/402528https://api.elsevier.com/content/abstract/scopus_id/105013530808reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/CEX2020-001088-Minfo:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PGC2018-094276-B-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-122311NB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-127388NB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2022-137162NB-I00The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1093/g3journal/jkaf102https://doi.org/10.1093/g3journal/jkaf102Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/4025282026-05-22T06:33:51Z
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