Therapeutic targeting of adipose tissue macrophages ameliorates liver fibrosis in non-alcoholic fatty liver disease.

Adipose tissue inflammation Dextran dexamethasone conjugates Drug delivery Liver injury Nanomedicine Nanoparticle Non-alcoholic steatohepatitis Targeted therapy

Journal

JHEP reports : innovation in hepatology
ISSN: 2589-5559
Titre abrégé: JHEP Rep
Pays: Netherlands
ID NLM: 101761237

Informations de publication

Date de publication:
Oct 2023
Historique:
received: 11 10 2022
revised: 02 05 2023
accepted: 05 06 2023
medline: 13 9 2023
pubmed: 13 9 2023
entrez: 13 9 2023
Statut: epublish

Résumé

: The accumulation of adipose tissue macrophages (ATMs) in obesity has been associated with hepatic injury. However, the contribution of ATMs to hepatic fibrosis in non-alcoholic fatty liver disease (NAFLD) remains to be elucidated. Herein, we investigate the relationship between ATMs and liver fibrosis in patients with patients with NAFLD and evaluate the impact of modulation of ATMs over hepatic fibrosis in an experimental non-alcoholic steatohepatitis (NASH) model. Adipose tissue and liver biopsies from 42 patients with NAFLD with different fibrosis stages were collected. ATMs were characterised by immunohistochemistry and flow cytometry and the correlation between ATMs and liver fibrosis stages was assessed. Selective modulation of the ATM phenotype was achieved by Patients with NAFLD presented an increased accumulation of pro-inflammatory ATMs that correlated with hepatic fibrosis. Long-term modulation of ATMs significantly reduced pro-inflammatory phenotype and ameliorated adipose tissue inflammation. Moreover, ATMs modulation was associated with an improvement in steatosis and hepatic inflammation and significantly reduced fibrosis progression in an experimental NASH model. Pro-inflammatory ATMs increase in parallel with fibrosis degree in patients with NAFLD and their modulation in an experimental NASH model improves liver fibrosis, uncovering the potential of ATMs as a therapeutic target to mitigate liver fibrosis in NAFLD. We report that human adipose tissue pro-inflammatory macrophages correlate with hepatic fibrosis in non-alcoholic fatty liver disease (NAFLD). Furthermore, the modulation of adipose tissue macrophages (ATMs) by dextran-nanocarrier conjugated with dexamethasone shifts the pro-inflammatory phenotype of ATMs to an anti-inflammatory phenotype in an experimental murine model of non-alcoholic steatohepatitis. This shift ameliorates adipose tissue inflammation, hepatic inflammation, and fibrosis. Our results highlight the relevance of adipose tissue in NAFLD pathophysiology and unveil ATMs as a potential target for NAFLD.

Sections du résumé

Background & Aims UNASSIGNED
: The accumulation of adipose tissue macrophages (ATMs) in obesity has been associated with hepatic injury. However, the contribution of ATMs to hepatic fibrosis in non-alcoholic fatty liver disease (NAFLD) remains to be elucidated. Herein, we investigate the relationship between ATMs and liver fibrosis in patients with patients with NAFLD and evaluate the impact of modulation of ATMs over hepatic fibrosis in an experimental non-alcoholic steatohepatitis (NASH) model.
Methods UNASSIGNED
Adipose tissue and liver biopsies from 42 patients with NAFLD with different fibrosis stages were collected. ATMs were characterised by immunohistochemistry and flow cytometry and the correlation between ATMs and liver fibrosis stages was assessed. Selective modulation of the ATM phenotype was achieved by
Results UNASSIGNED
Patients with NAFLD presented an increased accumulation of pro-inflammatory ATMs that correlated with hepatic fibrosis. Long-term modulation of ATMs significantly reduced pro-inflammatory phenotype and ameliorated adipose tissue inflammation. Moreover, ATMs modulation was associated with an improvement in steatosis and hepatic inflammation and significantly reduced fibrosis progression in an experimental NASH model.
Conclusions UNASSIGNED
Pro-inflammatory ATMs increase in parallel with fibrosis degree in patients with NAFLD and their modulation in an experimental NASH model improves liver fibrosis, uncovering the potential of ATMs as a therapeutic target to mitigate liver fibrosis in NAFLD.
Impact and implications UNASSIGNED
We report that human adipose tissue pro-inflammatory macrophages correlate with hepatic fibrosis in non-alcoholic fatty liver disease (NAFLD). Furthermore, the modulation of adipose tissue macrophages (ATMs) by dextran-nanocarrier conjugated with dexamethasone shifts the pro-inflammatory phenotype of ATMs to an anti-inflammatory phenotype in an experimental murine model of non-alcoholic steatohepatitis. This shift ameliorates adipose tissue inflammation, hepatic inflammation, and fibrosis. Our results highlight the relevance of adipose tissue in NAFLD pathophysiology and unveil ATMs as a potential target for NAFLD.

Identifiants

pubmed: 37701336
doi: 10.1016/j.jhepr.2023.100830
pii: S2589-5559(23)00161-1
pmc: PMC10494470
doi:

Types de publication

Journal Article

Langues

eng

Pagination

100830

Informations de copyright

© 2023 The Authors.

Déclaration de conflit d'intérêts

All authors declare no conflicts of interest related to this manuscript. Please refer to the accompanying ICMJE disclosure forms for further details.

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Auteurs

Celia Martínez-Sánchez (C)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.
Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Madrid, Spain.

Octavi Bassegoda (O)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.
Liver Unit, Hospital Clínic of Barcelona, Faculty of Medicine, University of Barcelona, Barcelona, Spain.

Hongping Deng (H)

Micro and Nanotechnology Laboratory, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA.
Shanghai Frontiers Science Center for Chinese Medicine Chemical Biology, Institute of Interdisciplinary Integrative Medicine Research, Shanghai University of Traditional Chinese Medicine, Shanghai, China.
Division of Nutritional Sciences, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA.

Xènia Almodóvar (X)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.

Ainitze Ibarzabal (A)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.
Obesity Unit, Endocrinology and Nutrition Department, Hospital Clínic de Barcelona, Barcelona, Spain.
Gastrointestinal Surgery Department, Hospital Clínic de Barcelona, Barcelona, Spain.
Centro de Investigación Biomédica en Red de la Fisiopatología de la Obesidad y Nutrición (CIBEROBN), Instituto de Salud Carlos III (ISCIII), Madrid, Spain.

Ana de Hollanda (A)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.
Obesity Unit, Endocrinology and Nutrition Department, Hospital Clínic de Barcelona, Barcelona, Spain.
Centro de Investigación Biomédica en Red de la Fisiopatología de la Obesidad y Nutrición (CIBEROBN), Instituto de Salud Carlos III (ISCIII), Madrid, Spain.

Raquel-Adela Martínez García de la Torre (RA)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.

Delia Blaya (D)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.

Silvia Ariño (S)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.
Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Madrid, Spain.

Natalia Jiménez-Esquivel (N)

Liver Unit, Hospital Clínic of Barcelona, Faculty of Medicine, University of Barcelona, Barcelona, Spain.

Beatriz Aguilar-Bravo (B)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.

Julia Vallverdú (J)

Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Madrid, Spain.

Carla Montironi (C)

Molecular Biology Core & Pathology Department, Hospital Clínic of Barcelona, Spain.

Oscar Osorio-Conles (O)

Centro de Investigación Biomédica en Red de Diabetes y Enfermedades Metabólicas Asociadas (CIBERDEM), Instituto de Salud Carlos III (ISCIII), Madrid, Spain.

Yiliam Fundora (Y)

Department of General and Digestive Surgery, Hospital Clinic de Barcelona, Barcelona, Spain.

Francisco Javier Sánchez Moreno (FJ)

Department of General and Digestive Surgery, Hospital Clinic de Barcelona, Barcelona, Spain.

Alicia G Gómez-Valadés (AG)

Neuronal Control of Metabolism (NeuCoMe) Laboratory, Fundació de Recerca Clínic Barcelona-Institut d'Investigacions Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.

Laia Aguilar-Corominas (L)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.

Anna Soria (A)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.
Liver Unit, Hospital Clínic of Barcelona, Faculty of Medicine, University of Barcelona, Barcelona, Spain.

Elisa Pose (E)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.
Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Madrid, Spain.
Liver Unit, Hospital Clínic of Barcelona, Faculty of Medicine, University of Barcelona, Barcelona, Spain.

Adrià Juanola (A)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.
Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Madrid, Spain.
Liver Unit, Hospital Clínic of Barcelona, Faculty of Medicine, University of Barcelona, Barcelona, Spain.

Marta Cervera (M)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.

Martina Perez (M)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.
Liver Unit, Hospital Clínic of Barcelona, Faculty of Medicine, University of Barcelona, Barcelona, Spain.

Virginia Hernández-Gea (V)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.
Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Madrid, Spain.
Liver Unit, Hospital Clínic of Barcelona, Faculty of Medicine, University of Barcelona, Barcelona, Spain.

Silvia Affò (S)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.

Kelly S Swanson (KS)

Division of Nutritional Sciences, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA.
Department of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA.

Joana Ferrer-Fàbrega (J)

Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Madrid, Spain.
Barcelona Clínic Liver Cancer Group (BCLC), IDIBAPS, Barcelona, Spain.
Hepatic Oncology Unit, Hospital Clínic, Barcelona, Spain.
Hepatobiliopancreatic Surgery and Liver and Pancreatic Transplantation Unit, Department of Surgery, Institute Clínic of Digestive and Metabolic Diseases (ICMDiM), Hospital Clínic, Barcelona, Spain.
Department of Medicine, University of Barcelona, Barcelona, Spain.

Jose Maria Balibrea (JM)

Endocrine, Metabolic & Bariatric Surgery Unit, Germans Trias i Pujol Hospital, Autonomous University of Barcelona, Barcelona, Spain.

Pau Sancho-Bru (P)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.
Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Madrid, Spain.

Josep Vidal (J)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.
Obesity Unit, Endocrinology and Nutrition Department, Hospital Clínic de Barcelona, Barcelona, Spain.
Centro de Investigación Biomédica en Red de Diabetes y Enfermedades Metabólicas Asociadas (CIBERDEM), Instituto de Salud Carlos III (ISCIII), Madrid, Spain.

Pere Ginès (P)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.
Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Madrid, Spain.
Liver Unit, Hospital Clínic of Barcelona, Faculty of Medicine, University of Barcelona, Barcelona, Spain.
Department of General and Digestive Surgery, Hospital Clinic de Barcelona, Barcelona, Spain.

Andrew M Smith (AM)

Micro and Nanotechnology Laboratory, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA.
Department of Bioengineering, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
Cancer Center at Illinois, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
Carle Illinois College of Medicine, Urbana, IL, USA.
Department of Materials Science and Engineering, University of Illinois at Urbana-Champaign, Urbana, IL, USA.

Isabel Graupera (I)

Fundació de Recerca Clínic Barcelona-Institut d'Investigacións Biomèdiques August Pi i Sunyer (FCRB-IDIABPS), Barcelona, Spain.
Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Madrid, Spain.
Liver Unit, Hospital Clínic of Barcelona, Faculty of Medicine, University of Barcelona, Barcelona, Spain.

Mar Coll (M)

Department of Medicine, University of Barcelona, Barcelona, Spain.

Classifications MeSH