Mast cells drive pathologic vascular lesions in Takayasu arteritis.


Journal

The Journal of allergy and clinical immunology
ISSN: 1097-6825
Titre abrégé: J Allergy Clin Immunol
Pays: United States
ID NLM: 1275002

Informations de publication

Date de publication:
01 2022
Historique:
received: 04 12 2020
revised: 30 04 2021
accepted: 04 05 2021
pubmed: 17 5 2021
medline: 4 3 2022
entrez: 16 5 2021
Statut: ppublish

Résumé

Takayasu arteritis (TAK) is a large vessel vasculitis resulting in artery wall remodeling with segmental stenosis and/or aneurysm formation. Mast cells (MCs) are instrumental in bridging cell injury and inflammatory response. This study sought to investigate the contribution of MCs on vessel permeability, angiogenesis, and fibrosis in patients with TAK. MC activation and their tissue expression were assessed in sera and in aorta from patients with TAK and from healthy donors (HDs). In vivo permeability was assessed using a modified Miles assay. Subconfluent cultured human umbilic vein endothelial cells and fibroblasts were used in vitro to investigate the effects of MC mediators on angiogenesis and fibrogenesis. This study found increased levels of MC activation markers (histamine and indoleamine 2,3-dioxygenase) in sera of patients with TAK compared with in sera of HDs. Marked expression of MCs was shown in aortic lesions of patients with TAK compared with in those of noninflammatory aorta controls. Using Miles assay, this study showed that sera of patients with TAK significantly increased vascular permeability in vivo as compared with that of HDs. Vessel permeability was abrogated in MC-deficient mice. MCs stimulated by sera of patients with TAK supported neoangiogenesis (increased human umbilic vein endothelial cell proliferation and branches) and fibrosis by inducing increased production of fibronectin, type 1 collagen, and α-smooth muscle actin by fibroblasts as compared to MCs stimulated by sera of HD. MCs are a key regulator of vascular lesions in patients with TAK and may represent a new therapeutic target in large vessel vasculitis.

Sections du résumé

BACKGROUND
Takayasu arteritis (TAK) is a large vessel vasculitis resulting in artery wall remodeling with segmental stenosis and/or aneurysm formation. Mast cells (MCs) are instrumental in bridging cell injury and inflammatory response.
OBJECTIVES
This study sought to investigate the contribution of MCs on vessel permeability, angiogenesis, and fibrosis in patients with TAK.
METHODS
MC activation and their tissue expression were assessed in sera and in aorta from patients with TAK and from healthy donors (HDs). In vivo permeability was assessed using a modified Miles assay. Subconfluent cultured human umbilic vein endothelial cells and fibroblasts were used in vitro to investigate the effects of MC mediators on angiogenesis and fibrogenesis.
RESULTS
This study found increased levels of MC activation markers (histamine and indoleamine 2,3-dioxygenase) in sera of patients with TAK compared with in sera of HDs. Marked expression of MCs was shown in aortic lesions of patients with TAK compared with in those of noninflammatory aorta controls. Using Miles assay, this study showed that sera of patients with TAK significantly increased vascular permeability in vivo as compared with that of HDs. Vessel permeability was abrogated in MC-deficient mice. MCs stimulated by sera of patients with TAK supported neoangiogenesis (increased human umbilic vein endothelial cell proliferation and branches) and fibrosis by inducing increased production of fibronectin, type 1 collagen, and α-smooth muscle actin by fibroblasts as compared to MCs stimulated by sera of HD.
CONCLUSIONS
MCs are a key regulator of vascular lesions in patients with TAK and may represent a new therapeutic target in large vessel vasculitis.

Identifiants

pubmed: 33992671
pii: S0091-6749(21)00734-X
doi: 10.1016/j.jaci.2021.05.003
pii:
doi:

Substances chimiques

ACTA2 protein, human 0
Actins 0
Collagen Type I 0
Fibronectins 0
Interleukin-33 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

292-301.e3

Informations de copyright

Copyright © 2021 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.

Auteurs

Alexandre Le Joncour (A)

Department of Immunology-Immunopathology-Immunotherapy, Université Pierre-et-Marie-Curie Université de Paris 06, Unite Mixte de Recherche (UMR)S959, Institut National de la Santé et de la Recherche Médicale (INSERM), Sorbonne Universités, Paris, France; Department of Biotherapy, Hôpital Pitié-Salpêtrière, Paris, France; Department of Internal Medicine and Clinical Immunology, Centre National de Références Maladies Autoimmunes et Systémiques Rares, Centre National de Références Maladies Autoinflammatoires Rares et Amylose Inflammatoire, Paris, France.

Anne-Claire Desbois (AC)

Department of Immunology-Immunopathology-Immunotherapy, Université Pierre-et-Marie-Curie Université de Paris 06, Unite Mixte de Recherche (UMR)S959, Institut National de la Santé et de la Recherche Médicale (INSERM), Sorbonne Universités, Paris, France; Department of Biotherapy, Hôpital Pitié-Salpêtrière, Paris, France; Department of Internal Medicine and Clinical Immunology, Centre National de Références Maladies Autoimmunes et Systémiques Rares, Centre National de Références Maladies Autoinflammatoires Rares et Amylose Inflammatoire, Paris, France.

Aurélie S Leroyer (AS)

Centre de Recherche en CardioVasculaire et Nutrition, INSERM U1263, Inrae 1260, Aix-Marseille Université, Marseille, France.

Edwige Tellier (E)

Centre de Recherche en CardioVasculaire et Nutrition, INSERM U1263, Inrae 1260, Aix-Marseille Université, Marseille, France.

Paul Régnier (P)

Department of Immunology-Immunopathology-Immunotherapy, Université Pierre-et-Marie-Curie Université de Paris 06, Unite Mixte de Recherche (UMR)S959, Institut National de la Santé et de la Recherche Médicale (INSERM), Sorbonne Universités, Paris, France; Department of Biotherapy, Hôpital Pitié-Salpêtrière, Paris, France.

Anna Maciejewski-Duval (A)

Department of Immunology-Immunopathology-Immunotherapy, Université Pierre-et-Marie-Curie Université de Paris 06, Unite Mixte de Recherche (UMR)S959, Institut National de la Santé et de la Recherche Médicale (INSERM), Sorbonne Universités, Paris, France; Department of Biotherapy, Hôpital Pitié-Salpêtrière, Paris, France.

Cloé Comarmond (C)

Department of Immunology-Immunopathology-Immunotherapy, Université Pierre-et-Marie-Curie Université de Paris 06, Unite Mixte de Recherche (UMR)S959, Institut National de la Santé et de la Recherche Médicale (INSERM), Sorbonne Universités, Paris, France; Department of Biotherapy, Hôpital Pitié-Salpêtrière, Paris, France; Department of Internal Medicine and Clinical Immunology, Centre National de Références Maladies Autoimmunes et Systémiques Rares, Centre National de Références Maladies Autoinflammatoires Rares et Amylose Inflammatoire, Paris, France.

Stéphane Barete (S)

Department of Internal Medicine and Clinical Immunology, Centre National de Références Maladies Autoimmunes et Systémiques Rares, Centre National de Références Maladies Autoinflammatoires Rares et Amylose Inflammatoire, Paris, France; Department of Dermatology DMU3ID, Unité Fonctionnelle de Dermatologie, Groupe Hospitalier Pitié-Salpêtrière-C. Foix, Paris, France.

Michel Arock (M)

Cell Death and Drug Resistance in Lymphoproliferative Disorders Team, INSERM UMRS1138, Centre de Recherche des Cordeliers, Paris, France; Laboratoire d'Hématologie Biologique, Hôpital Pitié-Salpêtrière, Paris, France.

Patrick Bruneval (P)

Laboratoire d'anatomopathologie, Hôpital Européen Georges Pompidou, Paris, France.

Jean-Marie Launay (JM)

INSERM, UMR-S 942, F-75010, Paris, France.

Pierre Fouret (P)

Laboratoire d'Anatomopathologie, Groupe Hospitalier Pitié-Salpêtrière, Paris, France.

Ulrich Blank (U)

Center of Research on Inflammation, INSERM UMR S1149 and Centre National de la Recherche Scientifique Experimental Research Laboratory 8252, Universite de Paris, Sorbonne Paris Cite, Laboratoire d'Excellence INFLAMEX, Paris, France.

Michelle Rosenzwajg (M)

Department of Immunology-Immunopathology-Immunotherapy, Université Pierre-et-Marie-Curie Université de Paris 06, Unite Mixte de Recherche (UMR)S959, Institut National de la Santé et de la Recherche Médicale (INSERM), Sorbonne Universités, Paris, France; Department of Biotherapy, Hôpital Pitié-Salpêtrière, Paris, France; Department of Internal Medicine and Clinical Immunology, Centre National de Références Maladies Autoimmunes et Systémiques Rares, Centre National de Références Maladies Autoinflammatoires Rares et Amylose Inflammatoire, Paris, France.

David Klatzmann (D)

Department of Immunology-Immunopathology-Immunotherapy, Université Pierre-et-Marie-Curie Université de Paris 06, Unite Mixte de Recherche (UMR)S959, Institut National de la Santé et de la Recherche Médicale (INSERM), Sorbonne Universités, Paris, France; Department of Biotherapy, Hôpital Pitié-Salpêtrière, Paris, France; Department of Internal Medicine and Clinical Immunology, Centre National de Références Maladies Autoimmunes et Systémiques Rares, Centre National de Références Maladies Autoinflammatoires Rares et Amylose Inflammatoire, Paris, France.

Mohamed Jarraya (M)

Banque des Tissus Humains, Hôpital Saint Louis, Paris, France.

Laurent Chiche (L)

Service de Chirurgie Vasculaire, Groupe Hospitalier Pitié-Salpêtrière, Assistance Publique-Hôpitaux de Paris, Paris, France.

Fabien Koskas (F)

Service de Chirurgie Vasculaire, Groupe Hospitalier Pitié-Salpêtrière, Assistance Publique-Hôpitaux de Paris, Paris, France.

Patrice Cacoub (P)

Department of Immunology-Immunopathology-Immunotherapy, Université Pierre-et-Marie-Curie Université de Paris 06, Unite Mixte de Recherche (UMR)S959, Institut National de la Santé et de la Recherche Médicale (INSERM), Sorbonne Universités, Paris, France; Department of Biotherapy, Hôpital Pitié-Salpêtrière, Paris, France; Department of Internal Medicine and Clinical Immunology, Centre National de Références Maladies Autoimmunes et Systémiques Rares, Centre National de Références Maladies Autoinflammatoires Rares et Amylose Inflammatoire, Paris, France.

Gilles Kaplanski (G)

Centre de Recherche en CardioVasculaire et Nutrition, INSERM U1263, Inrae 1260, Aix-Marseille Université, Marseille, France; Service de Médecine Interne, Centre Hospitalier Universitaire Conception, Assistance Publique Hôpitaux de Marseille, Marseille, France.

David Saadoun (D)

Department of Immunology-Immunopathology-Immunotherapy, Université Pierre-et-Marie-Curie Université de Paris 06, Unite Mixte de Recherche (UMR)S959, Institut National de la Santé et de la Recherche Médicale (INSERM), Sorbonne Universités, Paris, France; Department of Biotherapy, Hôpital Pitié-Salpêtrière, Paris, France; Department of Internal Medicine and Clinical Immunology, Centre National de Références Maladies Autoimmunes et Systémiques Rares, Centre National de Références Maladies Autoinflammatoires Rares et Amylose Inflammatoire, Paris, France. Electronic address: david.saadoun@aphp.fr.

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