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A small TAT-TrkB peptide prevents BDNF receptor cleavage and restores synaptic physiology in Alzheimer's disease

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dc.contributor.authorFonseca-Gomes, João
dc.contributor.authorCosta-Coelho, Tiago
dc.contributor.authorFerreira-Manso, Mafalda
dc.contributor.authorInteiro-Oliveira, Sara
dc.contributor.authorVaz, Sandra H.
dc.contributor.authorAlemãn-Serrano, Nuno
dc.contributor.authorAtalaia Barbacena, Henrique
dc.contributor.authorRibeiro Rodrigues, Leonor
dc.contributor.authorRamalho, Rita Mira
dc.contributor.authorClimaco Pinto, Rui
dc.contributor.authorVicente Miranda, Hugo
dc.contributor.authorTanqueiro, Sara
dc.contributor.authorde Almeida-Borlido, Carolina
dc.contributor.authorRamalho, Maria João
dc.contributor.authorMiranda-Lourenço, Catarina
dc.contributor.authorBelo, Rita F.
dc.contributor.authorFerreira, Catarina B.
dc.contributor.authorNeves, Vera
dc.contributor.authorRombo, Diogo M.
dc.contributor.authorViais, Ricardo
dc.contributor.authorUmemori, Juzoh
dc.contributor.authorMartins, Ivo C.
dc.contributor.authorJerónimo-Santos, André
dc.contributor.authorCaetano, António
dc.contributor.authorManso, Nuno
dc.contributor.authorMäkinen, Petra
dc.contributor.authorMarttinen, Mikael
dc.contributor.authorTakalo, Mari
dc.contributor.authorBremang, Michael
dc.contributor.authorPike, Ian
dc.contributor.authorHaapasalo, Annakaisa
dc.contributor.authorLoureiro, Joana A.
dc.contributor.authorPereira, Maria Carmo
dc.contributor.authorSantos, Nuno C.
dc.contributor.authorOuteiro, Tiago
dc.contributor.authorCastanho, Miguel A. R. B.
dc.contributor.authorFernandes, Adelaide
dc.contributor.authorHiltunen, Mikko
dc.contributor.authorDuarte, Carlos B.
dc.contributor.authorCastrén, Eero
dc.contributor.authorDe Mendonça, Alexandre
dc.contributor.authorSebastião, Ana M
dc.contributor.authorRodrigues, Tiago M.
dc.contributor.authorDiógenes, Maria José
dc.date.accessioned2025-02-21T14:46:29Z
dc.date.available2025-02-21T14:46:29Z
dc.date.issued2024
dc.description© 2024 The Author(s). Published by Elsevier Inc. on behalf of The American Society of Gene and Cell Therapy. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)pt_PT
dc.description.abstractIn Alzheimer's disease (AD), amyloid β (Aβ)-triggered cleavage of TrkB-FL impairs brain-derived neurotrophic factor (BDNF) signaling, thereby compromising neuronal survival, differentiation, and synaptic transmission and plasticity. Using cerebrospinal fluid and postmortem human brain samples, we show that TrkB-FL cleavage occurs from the early stages of the disease and increases as a function of pathology severity. To explore the therapeutic potential of this disease mechanism, we designed small TAT-fused peptides and screened their ability to prevent TrkB-FL receptor cleavage. Among these, a TAT-TrkB peptide with a lysine-lysine linker prevented TrkB-FL cleavage both in vitro and in vivo and rescued synaptic deficits induced by oligomeric Aβ in hippocampal slices. Furthermore, this TAT-TrkB peptide improved the cognitive performance, ameliorated synaptic plasticity deficits and prevented Tau pathology progression in vivo in the 5XFAD mouse model of AD. No evidence of liver or kidney toxicity was found. We provide proof-of-concept evidence for the efficacy and safety of this therapeutic strategy and anticipate that this TAT-TrkB peptide has the potential to be a disease-modifying drug that can prevent and/or reverse cognitive deficits in patients with AD.pt_PT
dc.description.sponsorshipThis work was supported by Fundação para a Ciência e a Tecnologia – Ministério da Ciência, Tecnologia e Ensino Superior (FCT-MCTES, Portugal) (PTDC/SAU-NMU/110838/2009, PTDC/SAU-ENB/117013/2010, PTDC/NEU-OSD/5644/2014, PTDC/CTM-NAN/3547/2014, PTDC/MED-NEU/27946/2017), Santa Casa da Misericórdia de Lisboa (MB37–2017 and MB35-2021), the Plano de Recuperação e Resiliência (Pacto de Inovação “HfPT – Health from Portugal [Componente 5 do Plano de Recuperação e Resiliência, ao abrigo do concurso no. 02/C05-i01/2022]), the Academy of Finland (grant nos. 297211, 307416, 307866, and 315459), the Sigrid Jusélius Foundation, the Jane and Aatos Erkko Foundation, and the Strategic Neuroscience Funding of the University of Eastern Finland. It was also supported by the projects UID/BIM/50005/2019, UIBD/04539/2020, UIDB/00511/2020, and UIDP/00511/2020, financed by FCT-MCTES, through Fundos do Orçamento de Estado. J.F.-G. was supported by FCT (SFRH/PD/BD/114441/2016) and SynaNet – Twinning Action funded by European Union’s H2020 (GA-692340). T.M.R. was supported by Fundação Calouste Gulbenkian and GAPIC/Faculty of Medicine of the University of Lisbon (20130002/PEC/BG and 20150010/BG). FCT supported T.C.-C. (PD/BD/10594/2022), M.F.-M. (PD/BD/10313/2022), S.H.V. (SFRH/BPD/81627/2011), H.A.-B. (PD/BD/05182/2023), L.R.-R. (PD/BD/150344/2019), R.M.R. (SFRH/BPD/94474/2013), H.V.M. (SFRH/BPD/109347/2015), S.R.T. (PD/BD/128091/2016), M.J.R. (CEEC-IND/01741/2021), C.M.-L. (PD/BD/118238/2016), R.F.B. (PD/BD/114337/2016), C.B.F. (PD/BD/128390/2017), A.J.-S. (PD/BD/62828/2009), and I.C.M. (“Investigador FCT” [IF/00772/2013] and “Concurso de Estímulo ao Emprego Científico” [CEECIND/01670/2017]). S.I.-O. was supported by Plano de Recuperação e Resiliência (PRR) (IMM/BII/12-2023). N.A.-S. and N.M. were supported by GAPIC/Faculty of Medicine of the University of Lisbon (project ref. 20210028 and 2018009). M.M. was supported by the Sigrid Jusélius Foundation. M.B. and I.P. were funded by Proteomic Sciences. T.F.O. was supported by Neurofold and the DFG Center for Nanoscale Microscopy and Molecular Physiology of the Brain.pt_PT
dc.description.versioninfo:eu-repo/semantics/publishedVersionpt_PT
dc.identifier.citationMol Ther. 2024 Oct 2;32(10):3372-3401pt_PT
dc.identifier.doi10.1016/j.ymthe.2024.08.022pt_PT
dc.identifier.eissn1525-0024
dc.identifier.issn1525-0016
dc.identifier.urihttp://hdl.handle.net/10400.5/98623
dc.language.isoengpt_PT
dc.peerreviewedyespt_PT
dc.publisherElsevierpt_PT
dc.relationPTDC/SAU-NMU/110838/2009pt_PT
dc.relationAMYLOIDETECTORS: Employing amyloid fibrils as biosensors of the interaction of peptides with phospholipids and/or protein domains.
dc.relationTargeting the glycation defenses as a protective strategy for Parkinson’s disease
dc.relationBaiTS - Biodegradable dendrimers for Targeted neuroprotective therapies in Stroke
dc.relationUIBD/04539/2020pt_PT
dc.relationLaboratory for Process Engineering, Environment, Biotechnology and Energy
dc.relationGA-692340pt_PT
dc.relation20130002/PEC/BGpt_PT
dc.relation20150010/BGpt_PT
dc.relationPD/BD/10594/2022pt_PT
dc.relationPD/BD/10313/2022pt_PT
dc.relationMODULATION OF THE BIDIRECTIONAL COMMUNICATION BETWEEN NEURONS AND ASTROCYTES AT THE SYNAPSE: INFLUENCE OF BDNF AND P2 RECEPTORS
dc.relationA definir
dc.relationTargeting the glycation defenses as a protective strategy for Parkinson’s disease
dc.relationModulation of BDNF effects by adenosine: a new strategy for schizophrenia treatment - Adenosinergic signaling as a new pharmacological target for schizophrenia treatment
dc.relationPD/BD/118238/2016pt_PT
dc.relationPD/BD/114337/2016pt_PT
dc.relationPD/BD/62828/2009pt_PT
dc.relationA nanotechnology approach to Flavivirus-targeted drug development strategies
dc.relationNot Available
dc.relation2018009pt_PT
dc.relation.publisherversionhttps://www.sciencedirect.com/journal/molecular-therapypt_PT
dc.rights.urihttp://creativecommons.org/licenses/by-nc-nd/4.0/pt_PT
dc.subjectAlzheimer’s diseasept_PT
dc.subjectBrain derived neurotrophic factor (BDNF)pt_PT
dc.subjectTAT peptidept_PT
dc.subjectTAT-TrkBpt_PT
dc.subjectTrkB receptorpt_PT
dc.subjectAmyloid βpt_PT
dc.subjectDrug screeningpt_PT
dc.subjectHippocampal plasticitypt_PT
dc.subjectLearningpt_PT
dc.subjectMemorypt_PT
dc.subjectProtein cleavage.pt_PT
dc.titleA small TAT-TrkB peptide prevents BDNF receptor cleavage and restores synaptic physiology in Alzheimer's diseasept_PT
dc.typejournal article
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oaire.awardTitleBaiTS - Biodegradable dendrimers for Targeted neuroprotective therapies in Stroke
oaire.awardTitleLaboratory for Process Engineering, Environment, Biotechnology and Energy
oaire.awardTitleMODULATION OF THE BIDIRECTIONAL COMMUNICATION BETWEEN NEURONS AND ASTROCYTES AT THE SYNAPSE: INFLUENCE OF BDNF AND P2 RECEPTORS
oaire.awardTitleA definir
oaire.awardTitleTargeting the glycation defenses as a protective strategy for Parkinson’s disease
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oaire.citation.endPage3401pt_PT
oaire.citation.issue10pt_PT
oaire.citation.startPage3372pt_PT
oaire.citation.titleMolecular Therapypt_PT
oaire.citation.volume32pt_PT
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IMM - Artigos em Revistas Internacionais
FM-IFN-Artigos em Revistas Internacionais