Mast cells participate in smooth muscle cell reprogramming and atherosclerotic plaque calcification.


Journal

Vascular pharmacology
ISSN: 1879-3649
Titre abrégé: Vascul Pharmacol
Pays: United States
ID NLM: 101130615

Informations de publication

Date de publication:
06 2023
Historique:
received: 31 01 2023
revised: 14 03 2023
accepted: 19 03 2023
medline: 7 6 2023
pubmed: 24 3 2023
entrez: 23 3 2023
Statut: ppublish

Résumé

Calcification, a key feature of advanced human atherosclerosis, is positively associated with vascular disease burden and adverse events. We showed that macrocalcification can be a stabilizing factor for carotid plaque molecular biology, due to inverse association with immune processes. Mast cells (MCs) are important contributors to plaque instability, but their relationship with macrocalcification is unexplored. With a hypothesis that MC activation negatively associates with carotid plaque macrocalcification, we aimed to investigate the link between MCs and carotid plaque vulnerability, and study MC role in plaque calcification via smooth muscle cells (SMCs). Pre-operative computed tomography angiographies of patients (n = 40) undergoing surgery for carotid stenosis were used to characterize plaque morphology. Plaque microarrays (n = 40 and n = 126) were used for bioinformatic deconvolution of immune cell populations. Tissue microarrays (n = 103) were used to histologically validate the contribution of activated and resting MCs in plaques. Activated MCs and their typical markers were negatively correlated with macrocalcification. The ratio of activated vs. resting MCs was increased in low-calcified plaques from symptomatic patients. There was no modulating effect of medication on MC ratios. In vitro experiments showed that SMC calcification attenuated MC activation, while both active and resting MCs stimulated SMC calcification and induced dedifferentiation towards a pro-inflammatory-, osteochondrocyte-like phenotype, without modulating their migro-proliferative function. Integrative analyses from human plaques showed that MC activation is inversely associated with macrocalcification and positively with parameters of plaque vulnerability. Mechanistically, MCs induce SMC osteogenic reprograming, while matrix calcification in turn attenuates MC activation, offering new therapeutic avenues for exploration.

Sections du résumé

BACKGROUND
Calcification, a key feature of advanced human atherosclerosis, is positively associated with vascular disease burden and adverse events. We showed that macrocalcification can be a stabilizing factor for carotid plaque molecular biology, due to inverse association with immune processes. Mast cells (MCs) are important contributors to plaque instability, but their relationship with macrocalcification is unexplored. With a hypothesis that MC activation negatively associates with carotid plaque macrocalcification, we aimed to investigate the link between MCs and carotid plaque vulnerability, and study MC role in plaque calcification via smooth muscle cells (SMCs).
METHODS
Pre-operative computed tomography angiographies of patients (n = 40) undergoing surgery for carotid stenosis were used to characterize plaque morphology. Plaque microarrays (n = 40 and n = 126) were used for bioinformatic deconvolution of immune cell populations. Tissue microarrays (n = 103) were used to histologically validate the contribution of activated and resting MCs in plaques.
RESULTS
Activated MCs and their typical markers were negatively correlated with macrocalcification. The ratio of activated vs. resting MCs was increased in low-calcified plaques from symptomatic patients. There was no modulating effect of medication on MC ratios. In vitro experiments showed that SMC calcification attenuated MC activation, while both active and resting MCs stimulated SMC calcification and induced dedifferentiation towards a pro-inflammatory-, osteochondrocyte-like phenotype, without modulating their migro-proliferative function.
CONCLUSIONS
Integrative analyses from human plaques showed that MC activation is inversely associated with macrocalcification and positively with parameters of plaque vulnerability. Mechanistically, MCs induce SMC osteogenic reprograming, while matrix calcification in turn attenuates MC activation, offering new therapeutic avenues for exploration.

Identifiants

pubmed: 36958707
pii: S1537-1891(23)00027-7
doi: 10.1016/j.vph.2023.107167
pii:
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

107167

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The funding bodies and companies were not involved in the study design, manuscript writing or any other involvement in the creation of this manuscript.

Auteurs

Nikolaos T Skenteris (NT)

Cardiovascular Medicine, Department of Medicine, Karolinska Institute, Stockholm, Sweden; Vascular Surgery, Department of Molecular Medicine and Surgery, Karolinska Institute and Karolinska University Hospital, Stockholm, Sweden; Department of Pathology, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University Medical Centre, The Netherlands.

Esmeralda Hemme (E)

Division of BioTherapeutics, Leiden Academic Centre for Drug Research, Leiden University, The Netherlands.

Lucie Delfos (L)

Division of BioTherapeutics, Leiden Academic Centre for Drug Research, Leiden University, The Netherlands.

Glykeria Karadimou (G)

Vascular Surgery, Department of Molecular Medicine and Surgery, Karolinska Institute and Karolinska University Hospital, Stockholm, Sweden.

Eva Karlöf (E)

Vascular Surgery, Department of Molecular Medicine and Surgery, Karolinska Institute and Karolinska University Hospital, Stockholm, Sweden.

Mariette Lengquist (M)

Vascular Surgery, Department of Molecular Medicine and Surgery, Karolinska Institute and Karolinska University Hospital, Stockholm, Sweden.

Malin Kronqvist (M)

Vascular Surgery, Department of Molecular Medicine and Surgery, Karolinska Institute and Karolinska University Hospital, Stockholm, Sweden.

Xiang Zhang (X)

Vascular Surgery, Department of Molecular Medicine and Surgery, Karolinska Institute and Karolinska University Hospital, Stockholm, Sweden.

Lars Maegdefessel (L)

Cardiovascular Medicine, Department of Medicine, Karolinska Institute, Stockholm, Sweden; Technical University Munich, Klinikum rechts der Isar, Department for Vascular and Endovascular Surgery, Germany.

Leon J Schurgers (LJ)

Department of Biochemistry and CARIM, School for Cardiovascular Diseases, Maastricht University, The Netherlands; Institute of Experimental Medicine and Systems Biology, RWTH Aachen University, Aachen, Germany.

Hildur Arnardottir (H)

Cardiovascular Medicine, Department of Medicine, Karolinska Institute, Stockholm, Sweden.

Erik A L Biessen (EAL)

Department of Pathology, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University Medical Centre, The Netherlands.

Ilze Bot (I)

Division of BioTherapeutics, Leiden Academic Centre for Drug Research, Leiden University, The Netherlands.

Ljubica Matic (L)

Vascular Surgery, Department of Molecular Medicine and Surgery, Karolinska Institute and Karolinska University Hospital, Stockholm, Sweden. Electronic address: Ljubica.Matic@ki.se.

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