Lack of glycogenin causes glycogen accumulation and muscle function impairment

Glycogenin is considered essential for glycogen synthesis, as it acts as a primer for the initiation of the polysaccharide chain. Against expectations, glycogenin-deficient mice (Gyg KO) accumulate high amounts of glycogen in striated muscle. Furthermore, this glycogen contains no covalently bound p...

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Autores: Testoni, Giorgia, Duran, Jordi, García-Rocha, Mar, Vilaplana, Francisco, Serrano, Antonio L., Sebastián, David, López Soldado, Iliana, Sullivan, Mitchell A., Slebe Concha, Juan Felipe, 1981-, Vilaseca, Marta, Muñoz Cánoves, Pura, 1962-, Guinovart, Joan J. (Joan Josep), 1947-
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2017
País:España
Institución:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10230/36843
Acceso en línea:http://hdl.handle.net/10230/36843
http://dx.doi.org/10.1016/j.cmet.2017.06.008
Access Level:acceso abierto
Palabra clave:Glycogenin
Glycogen
GSD XV
Glycogen storage disease XV
Glycogenosis
Exercise
Muscle performance
Priming protein
Oxidative metabolism
Mitochondrial respiration
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spelling Lack of glycogenin causes glycogen accumulation and muscle function impairmentTestoni, GiorgiaDuran, JordiGarcía-Rocha, MarVilaplana, FranciscoSerrano, Antonio L.Sebastián, DavidLópez Soldado, IlianaSullivan, Mitchell A.Slebe Concha, Juan Felipe, 1981-Vilaseca, MartaMuñoz Cánoves, Pura, 1962-Guinovart, Joan J. (Joan Josep), 1947-GlycogeninGlycogenGSD XVGlycogen storage disease XVGlycogenosisExerciseMuscle performancePriming proteinOxidative metabolismMitochondrial respirationGlycogenin is considered essential for glycogen synthesis, as it acts as a primer for the initiation of the polysaccharide chain. Against expectations, glycogenin-deficient mice (Gyg KO) accumulate high amounts of glycogen in striated muscle. Furthermore, this glycogen contains no covalently bound protein, thereby demonstrating that a protein primer is not strictly necessary for the synthesis of the polysaccharide in vivo. Strikingly, in spite of the higher glycogen content, Gyg KO mice showed lower resting energy expenditure and less resistance than control animals when subjected to endurance exercise. These observations can be attributed to a switch of oxidative myofibers toward glycolytic metabolism. Mice overexpressing glycogen synthase in the muscle showed similar alterations, thus indicating that this switch is caused by the excess of glycogen. These results may explain the muscular defects of GSD XV patients, who lack glycogenin-1 and show high glycogen accumulation in muscle.We wish to thank the following members of IRB Barcelona: Anna Adrover, Emma Veza, Natalia Plana, and Vanessa Hernandez for technical assistance; and Dr. Antonio Zorzano for essential reagents and advice, the histopathology, the mouse mutant, and the biostatistics/bioinformatics core facilities. Thanks also to Dr. Marina Gay for mass spectrometry advice and data analysis and Dr. Mireia Díaz-Lobo for mass spectrometry experiments. Mass spectrometry was performed at the IRB Barcelona Mass Spectrometry and Proteomics Core Facility, which actively participates in the BMBS European COST Action BM 1403 and is a member of Proteored, PRB2-ISCIII, supported by grant PRB2 (IPT13/0001 - ISCIII-SGEFI / FEDER). Thanks also to Dr. Carmen Lopez-Iglesias (University of Barcelona) for assistance with the electron microscope. G.T. is supported by the “La Caixa” PhD Fellowship Program. IRB Barcelona is the recipient of a Severo Ochoa Award of Excellence from MINECO (Government of Spain). This study was supported by grants from the Spanish MINECO (BFU2011-30554-C02-00 and SAF2014-54525-P). M.A.S. was supported by an NHMRC CJ Martin Fellowship (GNT1092451). NIH grants to Velocigene at Regeneron (U01HG004085) and the CSD Consortium (U01HG004080) funded the generation of gene-targeted ES cells in the KOMP Program. None of the supporting agencies had any role in establishing the work or in writing the manuscript.Elsevier201920192017info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/36843http://dx.doi.org/10.1016/j.cmet.2017.06.008reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésCell Metab. 2017 Jul 5;26(1):256-266.e4info:eu-repo/grantAgreement/ES/3PN/BFU2011-30554-C02-00info:eu-repo/grantAgreement/ES/1PE/SAF2014-54525-P© Elsevier This is the published version of an article http://dx.doi.org/10.1016/j.cmet.2017.06.008 that appeared in the journal Cell metabolism. It is published in an Open Archive under an Elsevier user license. Details of this licence are available here: https://www.elsevier.com/about/our-business/policies/open-access-licenses/elsevier-user-licensehttp://www.elsevier.com/open-access/userlicense/1.0/info:eu-repo/semantics/openAccessoai:recercat.cat:10230/368432026-05-29T05:05:01Z
dc.title.none.fl_str_mv Lack of glycogenin causes glycogen accumulation and muscle function impairment
title Lack of glycogenin causes glycogen accumulation and muscle function impairment
spellingShingle Lack of glycogenin causes glycogen accumulation and muscle function impairment
Testoni, Giorgia
Glycogenin
Glycogen
GSD XV
Glycogen storage disease XV
Glycogenosis
Exercise
Muscle performance
Priming protein
Oxidative metabolism
Mitochondrial respiration
title_short Lack of glycogenin causes glycogen accumulation and muscle function impairment
title_full Lack of glycogenin causes glycogen accumulation and muscle function impairment
title_fullStr Lack of glycogenin causes glycogen accumulation and muscle function impairment
title_full_unstemmed Lack of glycogenin causes glycogen accumulation and muscle function impairment
title_sort Lack of glycogenin causes glycogen accumulation and muscle function impairment
dc.creator.none.fl_str_mv Testoni, Giorgia
Duran, Jordi
García-Rocha, Mar
Vilaplana, Francisco
Serrano, Antonio L.
Sebastián, David
López Soldado, Iliana
Sullivan, Mitchell A.
Slebe Concha, Juan Felipe, 1981-
Vilaseca, Marta
Muñoz Cánoves, Pura, 1962-
Guinovart, Joan J. (Joan Josep), 1947-
author Testoni, Giorgia
author_facet Testoni, Giorgia
Duran, Jordi
García-Rocha, Mar
Vilaplana, Francisco
Serrano, Antonio L.
Sebastián, David
López Soldado, Iliana
Sullivan, Mitchell A.
Slebe Concha, Juan Felipe, 1981-
Vilaseca, Marta
Muñoz Cánoves, Pura, 1962-
Guinovart, Joan J. (Joan Josep), 1947-
author_role author
author2 Duran, Jordi
García-Rocha, Mar
Vilaplana, Francisco
Serrano, Antonio L.
Sebastián, David
López Soldado, Iliana
Sullivan, Mitchell A.
Slebe Concha, Juan Felipe, 1981-
Vilaseca, Marta
Muñoz Cánoves, Pura, 1962-
Guinovart, Joan J. (Joan Josep), 1947-
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Glycogenin
Glycogen
GSD XV
Glycogen storage disease XV
Glycogenosis
Exercise
Muscle performance
Priming protein
Oxidative metabolism
Mitochondrial respiration
topic Glycogenin
Glycogen
GSD XV
Glycogen storage disease XV
Glycogenosis
Exercise
Muscle performance
Priming protein
Oxidative metabolism
Mitochondrial respiration
description Glycogenin is considered essential for glycogen synthesis, as it acts as a primer for the initiation of the polysaccharide chain. Against expectations, glycogenin-deficient mice (Gyg KO) accumulate high amounts of glycogen in striated muscle. Furthermore, this glycogen contains no covalently bound protein, thereby demonstrating that a protein primer is not strictly necessary for the synthesis of the polysaccharide in vivo. Strikingly, in spite of the higher glycogen content, Gyg KO mice showed lower resting energy expenditure and less resistance than control animals when subjected to endurance exercise. These observations can be attributed to a switch of oxidative myofibers toward glycolytic metabolism. Mice overexpressing glycogen synthase in the muscle showed similar alterations, thus indicating that this switch is caused by the excess of glycogen. These results may explain the muscular defects of GSD XV patients, who lack glycogenin-1 and show high glycogen accumulation in muscle.
publishDate 2017
dc.date.none.fl_str_mv 2017
2019
2019
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/10230/36843
http://dx.doi.org/10.1016/j.cmet.2017.06.008
url http://hdl.handle.net/10230/36843
http://dx.doi.org/10.1016/j.cmet.2017.06.008
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Cell Metab. 2017 Jul 5;26(1):256-266.e4
info:eu-repo/grantAgreement/ES/3PN/BFU2011-30554-C02-00
info:eu-repo/grantAgreement/ES/1PE/SAF2014-54525-P
dc.rights.none.fl_str_mv http://www.elsevier.com/open-access/userlicense/1.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://www.elsevier.com/open-access/userlicense/1.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
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