COQ4 is required for the oxidative decarboxylation of the C1 carbon of coenzyme Q in eukaryotic cells

Coenzyme Q (CoQ) is a redox lipid that fulfills critical functions in cellular bioenergetics and homeostasis. CoQ is synthesized by a multi-step pathway that involves several COQ proteins. Two steps of the eukaryotic pathway, the decarboxylation and hydroxylation of position C1, have remained unchar...

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Autores: Pelosi, Ludovic, Morbiato, Laura, Burgardt, Arthur, Tonello, Fiorella, Bartlett, Abigail K., Guerra, Rachel M., Ferizhendi, Katayoun Kazemzadeh, Desbats, María Andrea, Rascalou, Bérengère, Marchi, Marco, Vázquez-Fonseca, Luis, Agosto, Caterina, Zanotti, Giuseppe, Roger-Margueritat, Morgane, Alcázar-Fabra, María, García-Corzo, Laura, Sánchez-Cuesta, Ana, Navas, Plácido, Brea-Calvo, Gloria, Trevisson, Eva, Wendisch, Volker F., Pagliarini, David J., Salviati, Leonardo, Pierrel, Fabien
Tipo de recurso: artículo
Estado:Versión aceptada para publicación
Fecha de publicación:2024
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/365193
Acceso en línea:http://hdl.handle.net/10261/365193
Access Level:acceso abierto
Palabra clave:Coenzyme Q
Coenzyme Q biosynthesis
COQ4
Oxidative decarboxylation
Mitochondria
Respiratory chain
Coenzyme Q deficiency
Corynebacterium
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spelling COQ4 is required for the oxidative decarboxylation of the C1 carbon of coenzyme Q in eukaryotic cellsPelosi, LudovicMorbiato, LauraBurgardt, ArthurTonello, FiorellaBartlett, Abigail K.Guerra, Rachel M.Ferizhendi, Katayoun KazemzadehDesbats, María AndreaRascalou, BérengèreMarchi, MarcoVázquez-Fonseca, LuisAgosto, CaterinaZanotti, GiuseppeRoger-Margueritat, MorganeAlcázar-Fabra, MaríaGarcía-Corzo, LauraSánchez-Cuesta, AnaNavas, PlácidoBrea-Calvo, GloriaTrevisson, EvaWendisch, Volker F.Pagliarini, David J.Salviati, LeonardoPierrel, FabienCoenzyme QCoenzyme Q biosynthesisCOQ4Oxidative decarboxylationMitochondriaRespiratory chainCoenzyme Q deficiencyCorynebacteriumCoenzyme Q (CoQ) is a redox lipid that fulfills critical functions in cellular bioenergetics and homeostasis. CoQ is synthesized by a multi-step pathway that involves several COQ proteins. Two steps of the eukaryotic pathway, the decarboxylation and hydroxylation of position C1, have remained uncharacterized. Here, we provide evidence that these two reactions occur in a single oxidative decarboxylation step catalyzed by COQ4. We demonstrate that COQ4 complements an Escherichia coli strain deficient for C1 decarboxylation and hydroxylation and that COQ4 displays oxidative decarboxylation activity in the non-CoQ producer Corynebacterium glutamicum. Overall, our results substantiate that COQ4 contributes to CoQ biosynthesis, not only via its previously proposed structural role but also via the oxidative decarboxylation of CoQ precursors. These findings fill a major gap in the knowledge of eukaryotic CoQ biosynthesis and shed light on the pathophysiology of human primary CoQ deficiency due to COQ4 mutations.This work was supported by grants from the ANR to F.P. (ANR-19-CE44-0014O2-TABOO), from the NIH to D.J.P. (R35GM131795), from Telethon Italy (GGP13222 and 14187c), from Fondazione IRP Città della Speranza (to L.S.), from Fondazione CARIPARO (2019 FCR) to E.T., and from European Regional Development Fund (FEDER)/Andalusian Regional Government, Spain (FEDER operational program 2014–2020; P18-RT-4572) to G.B.-C. and P.N.Peer reviewedCell PressAgence Nationale de la Recherche (France)National Institutes of Health (US)Telethon ItaliaFondazione CariparoEuropean CommissionJunta de AndalucíaConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Postprintinfo:eu-repo/semantics/acceptedVersionapplication/pdfhttp://hdl.handle.net/10261/365193reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)InglésThe underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1016/j.molcel.2024.01.003https://doi.org/10.1016/j.molcel.2024.01.003Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3651932026-05-22T06:33:51Z
dc.title.none.fl_str_mv COQ4 is required for the oxidative decarboxylation of the C1 carbon of coenzyme Q in eukaryotic cells
title COQ4 is required for the oxidative decarboxylation of the C1 carbon of coenzyme Q in eukaryotic cells
spellingShingle COQ4 is required for the oxidative decarboxylation of the C1 carbon of coenzyme Q in eukaryotic cells
Pelosi, Ludovic
Coenzyme Q
Coenzyme Q biosynthesis
COQ4
Oxidative decarboxylation
Mitochondria
Respiratory chain
Coenzyme Q deficiency
Corynebacterium
title_short COQ4 is required for the oxidative decarboxylation of the C1 carbon of coenzyme Q in eukaryotic cells
title_full COQ4 is required for the oxidative decarboxylation of the C1 carbon of coenzyme Q in eukaryotic cells
title_fullStr COQ4 is required for the oxidative decarboxylation of the C1 carbon of coenzyme Q in eukaryotic cells
title_full_unstemmed COQ4 is required for the oxidative decarboxylation of the C1 carbon of coenzyme Q in eukaryotic cells
title_sort COQ4 is required for the oxidative decarboxylation of the C1 carbon of coenzyme Q in eukaryotic cells
dc.creator.none.fl_str_mv Pelosi, Ludovic
Morbiato, Laura
Burgardt, Arthur
Tonello, Fiorella
Bartlett, Abigail K.
Guerra, Rachel M.
Ferizhendi, Katayoun Kazemzadeh
Desbats, María Andrea
Rascalou, Bérengère
Marchi, Marco
Vázquez-Fonseca, Luis
Agosto, Caterina
Zanotti, Giuseppe
Roger-Margueritat, Morgane
Alcázar-Fabra, María
García-Corzo, Laura
Sánchez-Cuesta, Ana
Navas, Plácido
Brea-Calvo, Gloria
Trevisson, Eva
Wendisch, Volker F.
Pagliarini, David J.
Salviati, Leonardo
Pierrel, Fabien
author Pelosi, Ludovic
author_facet Pelosi, Ludovic
Morbiato, Laura
Burgardt, Arthur
Tonello, Fiorella
Bartlett, Abigail K.
Guerra, Rachel M.
Ferizhendi, Katayoun Kazemzadeh
Desbats, María Andrea
Rascalou, Bérengère
Marchi, Marco
Vázquez-Fonseca, Luis
Agosto, Caterina
Zanotti, Giuseppe
Roger-Margueritat, Morgane
Alcázar-Fabra, María
García-Corzo, Laura
Sánchez-Cuesta, Ana
Navas, Plácido
Brea-Calvo, Gloria
Trevisson, Eva
Wendisch, Volker F.
Pagliarini, David J.
Salviati, Leonardo
Pierrel, Fabien
author_role author
author2 Morbiato, Laura
Burgardt, Arthur
Tonello, Fiorella
Bartlett, Abigail K.
Guerra, Rachel M.
Ferizhendi, Katayoun Kazemzadeh
Desbats, María Andrea
Rascalou, Bérengère
Marchi, Marco
Vázquez-Fonseca, Luis
Agosto, Caterina
Zanotti, Giuseppe
Roger-Margueritat, Morgane
Alcázar-Fabra, María
García-Corzo, Laura
Sánchez-Cuesta, Ana
Navas, Plácido
Brea-Calvo, Gloria
Trevisson, Eva
Wendisch, Volker F.
Pagliarini, David J.
Salviati, Leonardo
Pierrel, Fabien
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Agence Nationale de la Recherche (France)
National Institutes of Health (US)
Telethon Italia
Fondazione Cariparo
European Commission
Junta de Andalucía
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Coenzyme Q
Coenzyme Q biosynthesis
COQ4
Oxidative decarboxylation
Mitochondria
Respiratory chain
Coenzyme Q deficiency
Corynebacterium
topic Coenzyme Q
Coenzyme Q biosynthesis
COQ4
Oxidative decarboxylation
Mitochondria
Respiratory chain
Coenzyme Q deficiency
Corynebacterium
description Coenzyme Q (CoQ) is a redox lipid that fulfills critical functions in cellular bioenergetics and homeostasis. CoQ is synthesized by a multi-step pathway that involves several COQ proteins. Two steps of the eukaryotic pathway, the decarboxylation and hydroxylation of position C1, have remained uncharacterized. Here, we provide evidence that these two reactions occur in a single oxidative decarboxylation step catalyzed by COQ4. We demonstrate that COQ4 complements an Escherichia coli strain deficient for C1 decarboxylation and hydroxylation and that COQ4 displays oxidative decarboxylation activity in the non-CoQ producer Corynebacterium glutamicum. Overall, our results substantiate that COQ4 contributes to CoQ biosynthesis, not only via its previously proposed structural role but also via the oxidative decarboxylation of CoQ precursors. These findings fill a major gap in the knowledge of eukaryotic CoQ biosynthesis and shed light on the pathophysiology of human primary CoQ deficiency due to COQ4 mutations.
publishDate 2024
dc.date.none.fl_str_mv 2024
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Postprint
info:eu-repo/semantics/acceptedVersion
format article
status_str acceptedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/365193
url http://hdl.handle.net/10261/365193
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1016/j.molcel.2024.01.003
https://doi.org/10.1016/j.molcel.2024.01.003

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 Cell Press
publisher.none.fl_str_mv Cell 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
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repository.mail.fl_str_mv
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