Traffic through the trans-golgi Network and the endosomal system requires collaboration between exomer and clathrin adaptors in fission yeast

Despite its biological and medical relevance, traffic from the Golgi to the plasma membrane (PM) is one of the least understood steps of secretion. Exomer is a protein complex that mediates the trafficking of certain cargoes from the trans-Golgi network/early endosomes to the PM in budding yeast. He...

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Authors: Hoya, Marta, Yanguas, Francisco, Moro, Sandra, Prescianotto-Baschong, Cristina, Doncel, Cristina, León, Nagore de, Curto, María Ángeles, Spang, Anne, Valdivieso, María Henar
Format: article
Status:Versión enviada para evaluación y publicación
Publication Date:2017
Country:España
Institution:Consejo Superior de Investigaciones Científicas (CSIC)
Repository:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/157129
Online Access:http://hdl.handle.net/10261/157129
Access Level:Open access
Keyword:Clathrin adaptors
Golgi
Endosomes
Exomer
Yeast
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spelling Traffic through the trans-golgi Network and the endosomal system requires collaboration between exomer and clathrin adaptors in fission yeastHoya, MartaYanguas, FranciscoMoro, SandraPrescianotto-Baschong, CristinaDoncel, CristinaLeón, Nagore deCurto, María ÁngelesSpang, AnneValdivieso, María HenarClathrin adaptorsGolgiEndosomesExomerYeastDespite its biological and medical relevance, traffic from the Golgi to the plasma membrane (PM) is one of the least understood steps of secretion. Exomer is a protein complex that mediates the trafficking of certain cargoes from the trans-Golgi network/early endosomes to the PM in budding yeast. Here, we show that in Schizosaccharomyces pombe the Cfr1 and Bch1 proteins constitute the simplest form of an exomer. Cfr1 co-immunoprecipitates with Assembly Polypeptide adaptor 1 (AP-1), AP-2, and Golgi-localized, gamma-adaptin ear domain homology, ARF-binding (GGA) subunits, and cfr1+ interacts genetically with AP-1 and GGA genes. Exomer-defective cells exhibit multiple mild defects, including alterations in the morphology of Golgi stacks and the distribution of the synaptobrevin-like Syb1 protein, carboxypeptidase missorting, and stress sensitivity. S. pombe apm1Δ cells exhibit a defect in trafficking through the early endosomes that is severely aggravated in the absence of exomer. apm1Δ cfr1Δ cells exhibit a dramatic disorganization of intracellular compartments, including massive accumulation of electron-dense tubulovesicular structures. While the trans-Golgi network/early endosomes are severely disorganized in the apm1Δ cfr1Δ strain, gga21Δ gga22Δ cfr1Δ cells exhibit a significant disturbance of the prevacuolar/vacuolar compartments. Our findings show that exomer collaborates with clathrin adaptors in trafficking through diverse cellular compartments, and that this collaboration is important to maintain their integrity. These results indicate that the effect of eliminating exomer is more pervasive than that described to date, and suggest that exomer complexes might participate in diverse steps of vesicle transport in other organisms.Financial support from the Ministerio de Economía y Competitividad (Spain)/European Union FEDER program (BFU2013-48582-C2-2-P) and from Junta de Castilla y León (SA073U14) to M.-H.V., and from the Swiss National Science Foundation (310030B_163480) to A.S., made this work possible. M.-H.V. was supported by a Junta de Ampliación de Estudios (JAE)-PREDOC Consejo Superior de Investigaciones Científicas (CSIC) fellowship, and F.Y., S.M., N.d.L., and M.-A.C. were supported by Formación de Personal Universitario (FPU) fellowships from the Ministry of Education (Spain).Peer reviewedGenetics Society of AmericaMinisterio de Economía y Competitividad (España)European CommissionJunta de Castilla y LeónSwiss National Science FoundationConsejo Superior de Investigaciones Científicas (España)Ministerio de Educación (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]201720172017info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Preprintinfo:eu-repo/semantics/submittedVersionhttp://hdl.handle.net/10261/157129reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BFU2013-48582-C2-2-Phttps://doi.org/10.1534/genetics.116.193458Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/1571292026-05-22T06:33:51Z
dc.title.none.fl_str_mv Traffic through the trans-golgi Network and the endosomal system requires collaboration between exomer and clathrin adaptors in fission yeast
title Traffic through the trans-golgi Network and the endosomal system requires collaboration between exomer and clathrin adaptors in fission yeast
spellingShingle Traffic through the trans-golgi Network and the endosomal system requires collaboration between exomer and clathrin adaptors in fission yeast
Hoya, Marta
Clathrin adaptors
Golgi
Endosomes
Exomer
Yeast
title_short Traffic through the trans-golgi Network and the endosomal system requires collaboration between exomer and clathrin adaptors in fission yeast
title_full Traffic through the trans-golgi Network and the endosomal system requires collaboration between exomer and clathrin adaptors in fission yeast
title_fullStr Traffic through the trans-golgi Network and the endosomal system requires collaboration between exomer and clathrin adaptors in fission yeast
title_full_unstemmed Traffic through the trans-golgi Network and the endosomal system requires collaboration between exomer and clathrin adaptors in fission yeast
title_sort Traffic through the trans-golgi Network and the endosomal system requires collaboration between exomer and clathrin adaptors in fission yeast
dc.creator.none.fl_str_mv Hoya, Marta
Yanguas, Francisco
Moro, Sandra
Prescianotto-Baschong, Cristina
Doncel, Cristina
León, Nagore de
Curto, María Ángeles
Spang, Anne
Valdivieso, María Henar
author Hoya, Marta
author_facet Hoya, Marta
Yanguas, Francisco
Moro, Sandra
Prescianotto-Baschong, Cristina
Doncel, Cristina
León, Nagore de
Curto, María Ángeles
Spang, Anne
Valdivieso, María Henar
author_role author
author2 Yanguas, Francisco
Moro, Sandra
Prescianotto-Baschong, Cristina
Doncel, Cristina
León, Nagore de
Curto, María Ángeles
Spang, Anne
Valdivieso, María Henar
author2_role author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Economía y Competitividad (España)
European Commission
Junta de Castilla y León
Swiss National Science Foundation
Consejo Superior de Investigaciones Científicas (España)
Ministerio de Educación (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Clathrin adaptors
Golgi
Endosomes
Exomer
Yeast
topic Clathrin adaptors
Golgi
Endosomes
Exomer
Yeast
description Despite its biological and medical relevance, traffic from the Golgi to the plasma membrane (PM) is one of the least understood steps of secretion. Exomer is a protein complex that mediates the trafficking of certain cargoes from the trans-Golgi network/early endosomes to the PM in budding yeast. Here, we show that in Schizosaccharomyces pombe the Cfr1 and Bch1 proteins constitute the simplest form of an exomer. Cfr1 co-immunoprecipitates with Assembly Polypeptide adaptor 1 (AP-1), AP-2, and Golgi-localized, gamma-adaptin ear domain homology, ARF-binding (GGA) subunits, and cfr1+ interacts genetically with AP-1 and GGA genes. Exomer-defective cells exhibit multiple mild defects, including alterations in the morphology of Golgi stacks and the distribution of the synaptobrevin-like Syb1 protein, carboxypeptidase missorting, and stress sensitivity. S. pombe apm1Δ cells exhibit a defect in trafficking through the early endosomes that is severely aggravated in the absence of exomer. apm1Δ cfr1Δ cells exhibit a dramatic disorganization of intracellular compartments, including massive accumulation of electron-dense tubulovesicular structures. While the trans-Golgi network/early endosomes are severely disorganized in the apm1Δ cfr1Δ strain, gga21Δ gga22Δ cfr1Δ cells exhibit a significant disturbance of the prevacuolar/vacuolar compartments. Our findings show that exomer collaborates with clathrin adaptors in trafficking through diverse cellular compartments, and that this collaboration is important to maintain their integrity. These results indicate that the effect of eliminating exomer is more pervasive than that described to date, and suggest that exomer complexes might participate in diverse steps of vesicle transport in other organisms.
publishDate 2017
dc.date.none.fl_str_mv 2017
2017
2017
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Preprint
info:eu-repo/semantics/submittedVersion
format article
status_str submittedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/157129
url http://hdl.handle.net/10261/157129
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BFU2013-48582-C2-2-P
https://doi.org/10.1534/genetics.116.193458
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Genetics Society of America
publisher.none.fl_str_mv Genetics Society of America
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
repository.mail.fl_str_mv
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score 15,81155

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