LPS-enriched small extracellular vesicles from metabolic syndrome patients trigger endothelial dysfunction by activation of TLR4.


Journal

Metabolism: clinical and experimental
ISSN: 1532-8600
Titre abrégé: Metabolism
Pays: United States
ID NLM: 0375267

Informations de publication

Date de publication:
05 2021
Historique:
received: 09 11 2020
revised: 01 02 2021
accepted: 08 02 2021
pubmed: 14 2 2021
medline: 28 5 2021
entrez: 13 2 2021
Statut: ppublish

Résumé

Metabolic syndrome (MetS) is characterized by a cluster of interconnected risk factors -hyperglycemia, dyslipidemia, hypertension and obesity- leading to an increased risk of cardiovascular events. Small extracellular vesicles (sEVs) can be considered as new biomarkers of different pathologies, and they are involved in intercellular communication. Here, we hypothesize that sEVs are implicated in MetS-associated endothelial dysfunction. Circulating sEVs of non-MetS (nMetS) subjects and MetS patients were isolated from plasma and characterized. Thereafter, sEV effects on endothelial function were analyzed by measuring nitric oxide (NO) and reactive oxygen species (ROS) production, and mitochondrial dynamic proteins on human endothelial aortic cells (HAoECs). Circulating levels of sEVs positively correlated with anthropometric and biochemical parameters including visceral obesity, glycaemia, insulinemia, and dyslipidemia. Treatment of HAoECs with sEVs from MetS patients decreased NO production through the inhibition of the endothelial NO-synthase activity. Injection of MetS-sEVs into mice impaired endothelium-dependent relaxation induced by acetylcholine. Furthermore, MetS-sEVs increased DHE and MitoSox-associated fluorescence in HAoECs, reflecting enhanced cytosolic and mitochondrial ROS production which was not associated with mitochondrial biogenesis or dynamic changes. MetS patients displayed elevated circulating levels of LPS in plasma, and, at least in part, it was associated to circulating sEVs. Pharmacological inhibition and down-regulation of TLR4, as well as sEV-carried LPS neutralization, results in a substantial decrease of ROS production induced by MetS-sEVs. These results evidence sEVs from MetS patients as potential new biomarkers for this syndrome, and TLR4 pathway activation by sEVs provides a link between the endothelial dysfunction and metabolic disturbances described in MetS.

Sections du résumé

BACKGROUND
Metabolic syndrome (MetS) is characterized by a cluster of interconnected risk factors -hyperglycemia, dyslipidemia, hypertension and obesity- leading to an increased risk of cardiovascular events. Small extracellular vesicles (sEVs) can be considered as new biomarkers of different pathologies, and they are involved in intercellular communication. Here, we hypothesize that sEVs are implicated in MetS-associated endothelial dysfunction.
METHODS
Circulating sEVs of non-MetS (nMetS) subjects and MetS patients were isolated from plasma and characterized. Thereafter, sEV effects on endothelial function were analyzed by measuring nitric oxide (NO) and reactive oxygen species (ROS) production, and mitochondrial dynamic proteins on human endothelial aortic cells (HAoECs).
RESULTS
Circulating levels of sEVs positively correlated with anthropometric and biochemical parameters including visceral obesity, glycaemia, insulinemia, and dyslipidemia. Treatment of HAoECs with sEVs from MetS patients decreased NO production through the inhibition of the endothelial NO-synthase activity. Injection of MetS-sEVs into mice impaired endothelium-dependent relaxation induced by acetylcholine. Furthermore, MetS-sEVs increased DHE and MitoSox-associated fluorescence in HAoECs, reflecting enhanced cytosolic and mitochondrial ROS production which was not associated with mitochondrial biogenesis or dynamic changes. MetS patients displayed elevated circulating levels of LPS in plasma, and, at least in part, it was associated to circulating sEVs. Pharmacological inhibition and down-regulation of TLR4, as well as sEV-carried LPS neutralization, results in a substantial decrease of ROS production induced by MetS-sEVs.
CONCLUSION
These results evidence sEVs from MetS patients as potential new biomarkers for this syndrome, and TLR4 pathway activation by sEVs provides a link between the endothelial dysfunction and metabolic disturbances described in MetS.

Identifiants

pubmed: 33581132
pii: S0026-0495(21)00027-5
doi: 10.1016/j.metabol.2021.154727
pii:
doi:

Substances chimiques

Lipopolysaccharides 0
Reactive Oxygen Species 0
TLR4 protein, human 0
Toll-Like Receptor 4 0
Nitric Oxide 31C4KY9ESH

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

154727

Informations de copyright

Copyright © 2021 Elsevier Inc. All rights reserved.

Auteurs

Sakina Ali (S)

SOPAM, U1063, INSERM, UNIV Angers, SFR ICAT, Angers, France.

Marine Malloci (M)

SOPAM, U1063, INSERM, UNIV Angers, SFR ICAT, Angers, France.

Zainab Safiedeen (Z)

SOPAM, U1063, INSERM, UNIV Angers, SFR ICAT, Angers, France.

Raffaella Soleti (R)

SOPAM, U1063, INSERM, UNIV Angers, SFR ICAT, Angers, France.

Luisa Vergori (L)

SOPAM, U1063, INSERM, UNIV Angers, SFR ICAT, Angers, France.

Xavier Vidal-Gómez (X)

SOPAM, U1063, INSERM, UNIV Angers, SFR ICAT, Angers, France.

Charlène Besnard (C)

SOPAM, U1063, INSERM, UNIV Angers, SFR ICAT, Angers, France.

Séverine Dubois (S)

SOPAM, U1063, INSERM, UNIV Angers, SFR ICAT, Angers, France; Centre Hospitalo-Universitaire d'Angers, France.

Soazig Le Lay (S)

SOPAM, U1063, INSERM, UNIV Angers, SFR ICAT, Angers, France.

Jérôme Boursier (J)

Centre Hospitalo-Universitaire d'Angers, France.

Arnaud Chevrollier (A)

Centre Hospitalo-Universitaire d'Angers, France; Institut MITOVASC, CNRS 6015, INSERM U1083, UNIV Angers, SFR ICAT, Angers, France.

Frédéric Gagnadoux (F)

SOPAM, U1063, INSERM, UNIV Angers, SFR ICAT, Angers, France; Centre Hospitalo-Universitaire d'Angers, France.

Gilles Simard (G)

SOPAM, U1063, INSERM, UNIV Angers, SFR ICAT, Angers, France; Centre Hospitalo-Universitaire d'Angers, France.

Ramaroson Andriantsitohaina (R)

SOPAM, U1063, INSERM, UNIV Angers, SFR ICAT, Angers, France; Centre Hospitalo-Universitaire d'Angers, France.

M Carmen Martinez (MC)

SOPAM, U1063, INSERM, UNIV Angers, SFR ICAT, Angers, France; Centre Hospitalo-Universitaire d'Angers, France. Electronic address: carmen.martinez@univ-angers.fr.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH