Differential regulation of insulin signalling by monomeric and oligomeric amyloid beta-peptide

Alzheimer's disease and Type 2 diabetes are pathological processes associated to ageing. Moreover, there are evidences supporting a mechanistic link between Alzheimer's disease and insulin resistance (one of the first hallmarks of Type 2 diabetes). Regarding Alzheimer's di...

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Autores: Molina Fernández, Rubén, Picón-Pagès, Pol, Barranco Almohalla, Alejandro, Crepin, Giulia, Herrera-Fernández, Víctor, Garcia-Elias Heras, Anna, Fanlo-Ucar, Hugo, Fernàndez Busquets, Xavier, García Ojalvo, Jordi, Oliva Miguel, Baldomero, Muñoz López, Francisco José, 1964-
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2022
País:España
Institución:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/54779
Acceso en línea:http://hdl.handle.net/10230/54779
http://dx.doi.org/10.1093/braincomms/fcac243
Access Level:acceso abierto
Palabra clave:Akt
Alzheimer’s disease
Amyloid β-peptide
Insulin
Insulin resistance
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oai_identifier_str oai:repositori.upf.edu:10230/54779
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network_name_str España
repository_id_str
dc.title.none.fl_str_mv Differential regulation of insulin signalling by monomeric and oligomeric amyloid beta-peptide
title Differential regulation of insulin signalling by monomeric and oligomeric amyloid beta-peptide
spellingShingle Differential regulation of insulin signalling by monomeric and oligomeric amyloid beta-peptide
Molina Fernández, Rubén
Akt
Alzheimer’s disease
Amyloid β-peptide
Insulin
Insulin resistance
title_short Differential regulation of insulin signalling by monomeric and oligomeric amyloid beta-peptide
title_full Differential regulation of insulin signalling by monomeric and oligomeric amyloid beta-peptide
title_fullStr Differential regulation of insulin signalling by monomeric and oligomeric amyloid beta-peptide
title_full_unstemmed Differential regulation of insulin signalling by monomeric and oligomeric amyloid beta-peptide
title_sort Differential regulation of insulin signalling by monomeric and oligomeric amyloid beta-peptide
dc.creator.none.fl_str_mv Molina Fernández, Rubén
Picón-Pagès, Pol
Barranco Almohalla, Alejandro
Crepin, Giulia
Herrera-Fernández, Víctor
Garcia-Elias Heras, Anna
Fanlo-Ucar, Hugo
Fernàndez Busquets, Xavier
García Ojalvo, Jordi
Oliva Miguel, Baldomero
Muñoz López, Francisco José, 1964-
author Molina Fernández, Rubén
author_facet Molina Fernández, Rubén
Picón-Pagès, Pol
Barranco Almohalla, Alejandro
Crepin, Giulia
Herrera-Fernández, Víctor
Garcia-Elias Heras, Anna
Fanlo-Ucar, Hugo
Fernàndez Busquets, Xavier
García Ojalvo, Jordi
Oliva Miguel, Baldomero
Muñoz López, Francisco José, 1964-
author_role author
author2 Picón-Pagès, Pol
Barranco Almohalla, Alejandro
Crepin, Giulia
Herrera-Fernández, Víctor
Garcia-Elias Heras, Anna
Fanlo-Ucar, Hugo
Fernàndez Busquets, Xavier
García Ojalvo, Jordi
Oliva Miguel, Baldomero
Muñoz López, Francisco José, 1964-
author2_role author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Akt
Alzheimer’s disease
Amyloid β-peptide
Insulin
Insulin resistance
topic Akt
Alzheimer’s disease
Amyloid β-peptide
Insulin
Insulin resistance
description Alzheimer's disease and Type 2 diabetes are pathological processes associated to ageing. Moreover, there are evidences supporting a mechanistic link between Alzheimer's disease and insulin resistance (one of the first hallmarks of Type 2 diabetes). Regarding Alzheimer's disease, amyloid β-peptide aggregation into β-sheets is the main hallmark of Alzheimer's disease. At monomeric state, amyloid β-peptide is not toxic but its function in brain, if any, is unknown. Here we show, by in silico study, that monomeric amyloid β-peptide 1-40 shares the tertiary structure with insulin and is thereby able to bind and activate insulin receptor. We validated this prediction experimentally by treating human neuroblastoma cells with increasing concentrations of monomeric amyloid β-peptide 1-40. Our results confirm that monomeric amyloid β-peptide 1-40 activates insulin receptor autophosphorylation, triggering downstream enzyme phosphorylations and the glucose Transporter 4 translocation to the membrane. On the other hand, neuronal insulin resistance is known to be associated to Alzheimer's disease since early stages. We thus modelled the docking of oligomeric amyloid β-peptide 1-40 to insulin receptor. We found that oligomeric amyloid β-peptide 1-40 blocks insulin receptor, impairing its activation. It was confirmed in vitro by observing the lack of insulin receptor autophosphorylation, and also the impairment of insulin-induced intracellular enzyme activations and the glucose Transporter 4 translocation to the membrane. By biological system analysis, we have carried out a mathematical model recapitulating the process that turns amyloid β-peptide binding to insulin receptor from the physiological to the pathophysiological regime. Our results suggest that monomeric amyloid β-peptide 1-40 contributes to mimic insulin effects in the brain, which could be good when neurons have an extra requirement of energy beside the well-known protective effects on insulin intracellular signalling, while its accumulation and subsequent oligomerization blocks the insulin receptor producing insulin resistance and compromising neuronal metabolism and protective pathways.
publishDate 2022
dc.date.none.fl_str_mv 2022
2022
2022
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/10230/54779
http://dx.doi.org/10.1093/braincomms/fcac243
url http://hdl.handle.net/10230/54779
http://dx.doi.org/10.1093/braincomms/fcac243
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Brain Commun. 2022 Sep 24;4(5):fcac243
info:eu-repo/grantAgreement/ES/2PE/PID2020-117691RB-I00
info:eu-repo/grantAgreement/ES/2PE/SAF2017-83372-R
info:eu-repo/grantAgreement/ES/2PE/BIO2017-85329-R
info:eu-repo/grantAgreement/ES/2PE/PGC2018-101251-B-I00
info:eu-repo/grantAgreement/ES/2PE/RTI2018-094579-B-I00
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 Oxford University Press
publisher.none.fl_str_mv Oxford University Press
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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spelling Differential regulation of insulin signalling by monomeric and oligomeric amyloid beta-peptideMolina Fernández, RubénPicón-Pagès, PolBarranco Almohalla, AlejandroCrepin, GiuliaHerrera-Fernández, VíctorGarcia-Elias Heras, AnnaFanlo-Ucar, HugoFernàndez Busquets, XavierGarcía Ojalvo, JordiOliva Miguel, BaldomeroMuñoz López, Francisco José, 1964-AktAlzheimer’s diseaseAmyloid β-peptideInsulinInsulin resistanceAlzheimer's disease and Type 2 diabetes are pathological processes associated to ageing. Moreover, there are evidences supporting a mechanistic link between Alzheimer's disease and insulin resistance (one of the first hallmarks of Type 2 diabetes). Regarding Alzheimer's disease, amyloid β-peptide aggregation into β-sheets is the main hallmark of Alzheimer's disease. At monomeric state, amyloid β-peptide is not toxic but its function in brain, if any, is unknown. Here we show, by in silico study, that monomeric amyloid β-peptide 1-40 shares the tertiary structure with insulin and is thereby able to bind and activate insulin receptor. We validated this prediction experimentally by treating human neuroblastoma cells with increasing concentrations of monomeric amyloid β-peptide 1-40. Our results confirm that monomeric amyloid β-peptide 1-40 activates insulin receptor autophosphorylation, triggering downstream enzyme phosphorylations and the glucose Transporter 4 translocation to the membrane. On the other hand, neuronal insulin resistance is known to be associated to Alzheimer's disease since early stages. We thus modelled the docking of oligomeric amyloid β-peptide 1-40 to insulin receptor. We found that oligomeric amyloid β-peptide 1-40 blocks insulin receptor, impairing its activation. It was confirmed in vitro by observing the lack of insulin receptor autophosphorylation, and also the impairment of insulin-induced intracellular enzyme activations and the glucose Transporter 4 translocation to the membrane. By biological system analysis, we have carried out a mathematical model recapitulating the process that turns amyloid β-peptide binding to insulin receptor from the physiological to the pathophysiological regime. Our results suggest that monomeric amyloid β-peptide 1-40 contributes to mimic insulin effects in the brain, which could be good when neurons have an extra requirement of energy beside the well-known protective effects on insulin intracellular signalling, while its accumulation and subsequent oligomerization blocks the insulin receptor producing insulin resistance and compromising neuronal metabolism and protective pathways.This work was supported by the Spanish Ministry of Science and Innovation and Agencia Estatal de Investigación plus European Regional Development Fund (FEDER Funds) through grants PID2020-117691RB-I00/AEI/10.13039/501100011033 (F.J.M.), SAF2017-83372-R (F.J.M.), BIO2017-85329-R (B.O.), PGC2018-101251-B-I00 (J.G.-O.) and RTI2018-094579-B-I00 (X.F.-B.). This work was also funded by the Spanish Institute of Health Carlos III by project reference AC20/00009 -FEDER/UE and European Research Era Net (ERANET) ERA-CVD_JTC2020-015 (J.G.-O.), by the ‘María de Maeztu Programme’ for Units of Excellence in Research and Development (R&D; award CEX2018-000792-M), Generalitat de Catalunya (Spain) through the grant 2017-SGR-908 (X.F.-B.) and Fundación QUAES through Cátedra QUAES-UPF de Biomedicina e Ingeniería Biomédica. The Instituto de Salud Global de Barcelona (ISGlobal) and Institute for Bioengineering of Catalonia (IBEC) are members of the Centres de Recerca de Catalunya (CERCA) Programme, Generalitat de Catalunya (Spain). We acknowledge support from the Spanish Ministry of Science, Innovation and Universities through the ‘Centro de Excelencia Severo Ochoa 2019–2023’ Programme (CEX2018-000806-S). This research is part of ISGlobal's Programme on the Molecular Mechanisms of Malaria, which is partially supported by the Fundación Ramón Areces. J.G.-O. also acknowledges support from the Institució Catalana de Recerca i Estudis Avançats (ICREA) Academia programme.Oxford University Press202220222022info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/54779http://dx.doi.org/10.1093/braincomms/fcac243reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésBrain Commun. 2022 Sep 24;4(5):fcac243info:eu-repo/grantAgreement/ES/2PE/PID2020-117691RB-I00info:eu-repo/grantAgreement/ES/2PE/SAF2017-83372-Rinfo:eu-repo/grantAgreement/ES/2PE/BIO2017-85329-Rinfo:eu-repo/grantAgreement/ES/2PE/PGC2018-101251-B-I00info:eu-repo/grantAgreement/ES/2PE/RTI2018-094579-B-I00© The Author(s) 2022. Published by Oxford University Press on behalf of the Guarantors of Brain. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.https://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/547792026-06-12T07:21:37Z
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