Unraveling Inclusion Body Myositis Using a Patient-derived Fibroblast Model

Background: Inclusion body myositis (IBM) is an inflammatory myopathy clinically characterized by proximal and distal muscle weakness, with inflammatory infiltrates, rimmed vacuoles and mitochondrial changes in muscle histopathology. There is scarce knowledge on IBM aetiology, and non-established bi...

Descripción completa

Detalles Bibliográficos
Autores: Cantó Santos, Judith, Valls Roca, Laura, Tobías, Ester, García-García, Francesc Josep, Guitart Mampel, Mariona, Esteve Codina, Anna, Martín Mur, Beatriz, Casado, Mercedes, Artuch Iriberri, Rafael, Solsona Vilarrasa, Estel, Fernández Checa Torres, José Carlos, García Ruiz, Carmen, Rentero Alfonso, Carles, Enrich Bastús, Carles, Moreno Lozano, Pedro Juan, Milisenda, José, Cardellach, Francesc, Grau Junyent, Josep M. (Josep Maria), Garrabou Tornos, Glòria
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
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:2445/208271
Acceso en línea:https://hdl.handle.net/2445/208271
Access Level:acceso abierto
Palabra clave:Autofàgia
Músculs
Fibroblasts
Miositis
Inflamació
Mitocondris
Autophagy
Muscles
Myositis
Inflammation
Mitochondria
id ES_c7012b2d1d4e7a1bc5b494f90d5a04d3
oai_identifier_str oai:recercat.cat:2445/208271
network_acronym_str ES
network_name_str España
repository_id_str
spelling Unraveling Inclusion Body Myositis Using a Patient-derived Fibroblast ModelCantó Santos, JudithValls Roca, LauraTobías, EsterGarcía-García, Francesc JosepGuitart Mampel, MarionaEsteve Codina, AnnaMartín Mur, BeatrizCasado, MercedesArtuch Iriberri, RafaelSolsona Vilarrasa, EstelFernández Checa Torres, José CarlosGarcía Ruiz, CarmenRentero Alfonso, CarlesEnrich Bastús, CarlesMoreno Lozano, Pedro JuanMilisenda, JoséCardellach, FrancescGrau Junyent, Josep M. (Josep Maria)Garrabou Tornos, GlòriaAutofàgiaMúsculsFibroblastsMiositisInflamacióMitocondrisAutophagyMusclesFibroblastsMyositisInflammationMitochondriaBackground: Inclusion body myositis (IBM) is an inflammatory myopathy clinically characterized by proximal and distal muscle weakness, with inflammatory infiltrates, rimmed vacuoles and mitochondrial changes in muscle histopathology. There is scarce knowledge on IBM aetiology, and non-established biomarkers or effective treatments are available, partly due to the lack of validated disease models. Methods: We have performed transcriptomics and functional validation of IBM muscle pathological hallmarks in fibroblasts from IBM patients (n = 14) and healthy controls (n = 12), paired by age and sex. The results comprise an mRNA-seq, together with functional inflammatory, autophagy, mitochondrial and metabolic changes between patients and controls. Results: Gene expression profile of IBM vs control fibroblasts revealed 778 differentially expressed genes (P-value adj < 0.05) related to inflammation, mitochondria, cell cycle regulation and metabolism. Functionally, an increased inflammatory profile was observed in IBM fibroblasts with higher supernatant cytokine secretion (three-fold increase). Autophagy was reduced considering basal protein mediators (18.4% reduced), time-course autophagosome formation (LC3BII 39% reduced, P-value < 0.05), and autophagosome microscopic evaluation. Mitochondria displayed reduced genetic content (by 33.9%, P-value < 0.05) and function (30.2%-decrease in respiration, 45.6%-decline in enzymatic activity (P-value < 0.001), 14.3%-higher oxidative stress, 135.2%-increased antioxidant defence (P-value < 0.05), 11.6%-reduced mitochondrial membrane potential (P-value < 0.05) and 42.8%-reduced mitochondrial elongation (P-value < 0.05)). In accordance, at the metabolite level, organic acid showed a 1.8-fold change increase, with conserved amino acid profile. Correlating to disease evolution, oxidative stress and inflammation emerge as potential markers of prognosis. Conclusions: These findings confirm the presence of molecular disturbances in peripheral tissues from IBM patients and prompt patients’ derived fibroblasts as a promising disease model, which may eventually be exported to other neuromuscular disorders. We additionally identify new molecular players in IBM associated with disease progression, setting the path to deepen in disease aetiology, in the identification of novel biomarkers or in the standardization of biomimetic platforms to assay new therapeutic strategies for preclinical studies.John Wiley & Sons2024202420232024info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersion14 p.application/pdfhttps://hdl.handle.net/2445/208271Articles publicats en revistes (Medicina)reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésReproducció del document publicat a: https://doi.org/doi: 10.1002/jcsm.13178Journal of Cachexia Sarcopenia and Muscle, 2023, vol. 14, num.2, p. 964-977https://doi.org/doi: 10.1002/jcsm.13178cc-by (c) Judith Cantó-Santos et al., 2023http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:recercat.cat:2445/2082712026-05-29T05:05:01Z
dc.title.none.fl_str_mv Unraveling Inclusion Body Myositis Using a Patient-derived Fibroblast Model
title Unraveling Inclusion Body Myositis Using a Patient-derived Fibroblast Model
spellingShingle Unraveling Inclusion Body Myositis Using a Patient-derived Fibroblast Model
Cantó Santos, Judith
Autofàgia
Músculs
Fibroblasts
Miositis
Inflamació
Mitocondris
Autophagy
Muscles
Fibroblasts
Myositis
Inflammation
Mitochondria
title_short Unraveling Inclusion Body Myositis Using a Patient-derived Fibroblast Model
title_full Unraveling Inclusion Body Myositis Using a Patient-derived Fibroblast Model
title_fullStr Unraveling Inclusion Body Myositis Using a Patient-derived Fibroblast Model
title_full_unstemmed Unraveling Inclusion Body Myositis Using a Patient-derived Fibroblast Model
title_sort Unraveling Inclusion Body Myositis Using a Patient-derived Fibroblast Model
dc.creator.none.fl_str_mv Cantó Santos, Judith
Valls Roca, Laura
Tobías, Ester
García-García, Francesc Josep
Guitart Mampel, Mariona
Esteve Codina, Anna
Martín Mur, Beatriz
Casado, Mercedes
Artuch Iriberri, Rafael
Solsona Vilarrasa, Estel
Fernández Checa Torres, José Carlos
García Ruiz, Carmen
Rentero Alfonso, Carles
Enrich Bastús, Carles
Moreno Lozano, Pedro Juan
Milisenda, José
Cardellach, Francesc
Grau Junyent, Josep M. (Josep Maria)
Garrabou Tornos, Glòria
author Cantó Santos, Judith
author_facet Cantó Santos, Judith
Valls Roca, Laura
Tobías, Ester
García-García, Francesc Josep
Guitart Mampel, Mariona
Esteve Codina, Anna
Martín Mur, Beatriz
Casado, Mercedes
Artuch Iriberri, Rafael
Solsona Vilarrasa, Estel
Fernández Checa Torres, José Carlos
García Ruiz, Carmen
Rentero Alfonso, Carles
Enrich Bastús, Carles
Moreno Lozano, Pedro Juan
Milisenda, José
Cardellach, Francesc
Grau Junyent, Josep M. (Josep Maria)
Garrabou Tornos, Glòria
author_role author
author2 Valls Roca, Laura
Tobías, Ester
García-García, Francesc Josep
Guitart Mampel, Mariona
Esteve Codina, Anna
Martín Mur, Beatriz
Casado, Mercedes
Artuch Iriberri, Rafael
Solsona Vilarrasa, Estel
Fernández Checa Torres, José Carlos
García Ruiz, Carmen
Rentero Alfonso, Carles
Enrich Bastús, Carles
Moreno Lozano, Pedro Juan
Milisenda, José
Cardellach, Francesc
Grau Junyent, Josep M. (Josep Maria)
Garrabou Tornos, Glòria
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Autofàgia
Músculs
Fibroblasts
Miositis
Inflamació
Mitocondris
Autophagy
Muscles
Fibroblasts
Myositis
Inflammation
Mitochondria
topic Autofàgia
Músculs
Fibroblasts
Miositis
Inflamació
Mitocondris
Autophagy
Muscles
Fibroblasts
Myositis
Inflammation
Mitochondria
description Background: Inclusion body myositis (IBM) is an inflammatory myopathy clinically characterized by proximal and distal muscle weakness, with inflammatory infiltrates, rimmed vacuoles and mitochondrial changes in muscle histopathology. There is scarce knowledge on IBM aetiology, and non-established biomarkers or effective treatments are available, partly due to the lack of validated disease models. Methods: We have performed transcriptomics and functional validation of IBM muscle pathological hallmarks in fibroblasts from IBM patients (n = 14) and healthy controls (n = 12), paired by age and sex. The results comprise an mRNA-seq, together with functional inflammatory, autophagy, mitochondrial and metabolic changes between patients and controls. Results: Gene expression profile of IBM vs control fibroblasts revealed 778 differentially expressed genes (P-value adj < 0.05) related to inflammation, mitochondria, cell cycle regulation and metabolism. Functionally, an increased inflammatory profile was observed in IBM fibroblasts with higher supernatant cytokine secretion (three-fold increase). Autophagy was reduced considering basal protein mediators (18.4% reduced), time-course autophagosome formation (LC3BII 39% reduced, P-value < 0.05), and autophagosome microscopic evaluation. Mitochondria displayed reduced genetic content (by 33.9%, P-value < 0.05) and function (30.2%-decrease in respiration, 45.6%-decline in enzymatic activity (P-value < 0.001), 14.3%-higher oxidative stress, 135.2%-increased antioxidant defence (P-value < 0.05), 11.6%-reduced mitochondrial membrane potential (P-value < 0.05) and 42.8%-reduced mitochondrial elongation (P-value < 0.05)). In accordance, at the metabolite level, organic acid showed a 1.8-fold change increase, with conserved amino acid profile. Correlating to disease evolution, oxidative stress and inflammation emerge as potential markers of prognosis. Conclusions: These findings confirm the presence of molecular disturbances in peripheral tissues from IBM patients and prompt patients’ derived fibroblasts as a promising disease model, which may eventually be exported to other neuromuscular disorders. We additionally identify new molecular players in IBM associated with disease progression, setting the path to deepen in disease aetiology, in the identification of novel biomarkers or in the standardization of biomimetic platforms to assay new therapeutic strategies for preclinical studies.
publishDate 2023
dc.date.none.fl_str_mv 2023
2024
2024
2024
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 https://hdl.handle.net/2445/208271
url https://hdl.handle.net/2445/208271
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Reproducció del document publicat a: https://doi.org/doi: 10.1002/jcsm.13178
Journal of Cachexia Sarcopenia and Muscle, 2023, vol. 14, num.2, p. 964-977
https://doi.org/doi: 10.1002/jcsm.13178
dc.rights.none.fl_str_mv cc-by (c) Judith Cantó-Santos et al., 2023
http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv cc-by (c) Judith Cantó-Santos et al., 2023
http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 14 p.
application/pdf
dc.publisher.none.fl_str_mv John Wiley & Sons
publisher.none.fl_str_mv John Wiley & Sons
dc.source.none.fl_str_mv Articles publicats en revistes (Medicina)
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
repository.name.fl_str_mv
repository.mail.fl_str_mv
_version_ 1869419120261332992
score 15,811543