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This work was funded by the Catalan Government (2021SGR01214), MICIU/AEI PID2019-106332GB-I00 and PID2022-141252NB-I00 under "ERDF A way of making Europe", and MCIN/AEI PID2021-122636OB-I00 under ERDF "A way of making Europe". M. B.-S. has been supported by the Research Grant [FI, 2021-FI-B00755 Agencia de Gestio d'Ajuts Universitat i Recerca (AGAUR)], A. P. by the Spanish Ministerio de Ciencia Innovacion y Universidades (grant no. PRE2020-092084, project no. PID2019-106332GB-I00), M. J.-E. by Universitat Rovira i Virgili (grand no. 2023PMF-PIPF-15) and V. C. M. by a research contract from the project PID2019-106332GB-I00 under the collaboration framework agreement between the Diputacio de Tarragona and the Universitat Rovira i Virgili for the period 2020-2023 with the reference number 2022/07: "Els antioxidants derivats de les llavors del raim com molecules preventives en l'envelliment del sistema neuromuscular". We would like to express our heartfelt gratitude to Dr Neus Garcia, whose contribution played a vital role in developing our research. She will always be remembered and missed. This work is dedicated to her memory. We thank Dr Carme Grau-Bove for animal care and technical support.

Analysis of institutional authors

Balanyà-Segura, MartaAuthorPolishchuk, AleksandraAuthorJust-Borras, LaiaAuthorCilleros-Mane, VictorAuthorJami-Elhirchi, MeryemAuthorPinent, MontserratAuthorArdevol, AnnaAuthorTomas, MartaAuthorLanuza, Maria ACorresponding AuthorTomas, JosepAuthor

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April 28, 2025
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Early Access
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Protective effects of grape seed procyanidin extract on neurotrophic and muscarinic signaling pathways in the aging neuromuscular junction

Publicated to:Food & Function. 16 (9): 3575-3590 - 2025-04-15 16(9), DOI: 10.1039/d5fo00286a

Authors: Balanyà-Segura M; Polishchuk A; Just-Borràs L; Cilleros-Mañé V; Silvera C; Jami-ElHirchi M; Pinent M; Ardévol A; Tomàs M; Lanuza MA; Hurtado E; Tomàs J

Affiliations

Univ Rovira & Virgili, MoBioFood Res Grp, Campus Sescelades,Marcel Li Domingo 1, Tarragona 43007, Spain - Author
Univ Rovira & Virgili, Unitat Histol & Neurobiol UHNeurob, Fac Med & Ciencies Salut, St Llorenc 21, Reus 43201, Spain - Author

Abstract

At the neuromuscular junction (NMJ), which coordinates movement, postsynaptic-derived neurotrophic factors have neuroprotective functions and retrogradely regulate the exocytotic machinery involved in neurotransmitter release. In parallel, presynaptic autocrine muscarinic signaling plays a fundamental modulatory role in this synapse. We previously found that these signaling pathways are impaired in the aged neuromuscular system. In this follow-up study, we investigated an anti-aging strategy using grape seed procyanidin extract (GSPE), a common dietary antioxidant known for its neuroprotective properties in various pathologies, but its effects on the aged neuromuscular system remain unexplored. This study analyses whether GSPE can mitigate age-associated impairments in neurotrophic and muscarinic signaling within the neuromuscular system. We assessed the expression (protein levels) and activation (phosphorylation) of the key proteins in the brain-derived-neurotrophic-factor (BDNF)/neurotrophin 4 (NT-4) and muscarinic pathways in the extensor digitorum longus (EDL) muscles of aged rats, with comparisons to GSPE-treated aged rats and young controls. The results demonstrate that GSPE treatment prevents the most relevant aging-induced changes in neurotrophic and muscarinic receptor isoforms, downstream protein kinases, and their targets in the neurotransmitter exocytotic machinery. Nevertheless, GSPE was less effective at preventing alterations in some other proteins within these pathways, such as calcium channels, and did not modify several other molecules involved in these pathways, which remain unchanged during aging. Overall, this study highlights the neuroprotective potential of GSPE in preventing fundamental age-related molecular changes at the NMJ, which helps improve functionality and may increase the quality of life and lifespan in aged individuals.

Keywords

Caloric restrictionCognitive functionKinase-b receptorsMemory impairmentMitochondrial-dnaOxidative stressPhysical-activityProanthocyanidin extractTransmitter releaseTrkb expressio

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Food & Function due to its progression and the good impact it has achieved in recent years, according to the agency WoS (JCR), it has become a reference in its field. In the year of publication of the work, 2025, it was in position 63/313, thus managing to position itself as a Q1 (Primer Cuartil), in the category Biochemistry & Molecular Biology.

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-07-06:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 3.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 3 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 1.

Leadership analysis of institutional authors

There is a significant leadership presence as some of the institution’s authors appear as the first or last signer, detailed as follows: First Author (Balanya Segura, Marta) and Last Author (Tomás Ferré, José Maria).

the authors responsible for correspondence tasks have been Lanuza Escolano, María Angel and Hurtado, Erica.