Hyperglycemia-induced endothelial dysfunction is alleviated by thioredoxin mimetic peptides through the restoration of VEGFR-2-induced responses and improved cell survival.


Journal

International journal of cardiology
ISSN: 1874-1754
Titre abrégé: Int J Cardiol
Pays: Netherlands
ID NLM: 8200291

Informations de publication

Date de publication:
01 06 2020
Historique:
received: 09 04 2019
revised: 05 12 2019
accepted: 29 12 2019
pubmed: 21 1 2020
medline: 15 5 2021
entrez: 21 1 2020
Statut: ppublish

Résumé

Diabetes mellitus is an important cardiovascular risk factor characterized by elevated plasma glucose levels. High glucose (HG) negatively influences endothelial cell (EC) function, which is characterized by the inability of ECs to respond to vascular endothelial growth factor (VEGF-A) stimulation. We aimed to identify potential strategies to improve EC function in diabetes. Human umbilical cord endothelial cells (HUVECs) were subjected to hyperglycemic milieu by exposing cells to HG together with glucose metabolite, methylglyoxal (MG) in vitro. Hyperglycemic cells showed reduced chemotactic responses towards VEGF-A as revealed by Boyden chamber migration assays, indicating the development of "VEGF resistance" phenotype. Furthermore, HG/MG-exposed cells were defective in their general migratory and proliferative responses and were in a pro-apoptotic state. Mechanistically, the exposure to HG/MG resulted in reactive oxygen species (ROS) accumulation which is secondary to the impairment of thioredoxin (Trx) activity in these cells. Pharmacological and genetic targeting of Trx recapitulated VEGF resistance. Functional supplementation of Trx using thioredoxin mimetic peptides (TMP) reversed the HG/MG-induced ROS generation, improved the migration, proliferation, survival and restored VEGF-A-induced chemotaxis and sprouting angiogenesis of hyperglycemic ECs. Importantly, TMP treatment reduced ROS accumulation and improved VEGF-A responses of placental arterial endothelial cells isolated from gestational diabetes mellitus patients. Our findings suggest a putative role for Trx in modulating EC function and its functional impairment in HG conditions contribute to EC dysfunction. Supplementation of TMP could be used as a novel strategy to improve endothelial cell function in diabetes.

Sections du résumé

BACKGROUND
Diabetes mellitus is an important cardiovascular risk factor characterized by elevated plasma glucose levels. High glucose (HG) negatively influences endothelial cell (EC) function, which is characterized by the inability of ECs to respond to vascular endothelial growth factor (VEGF-A) stimulation. We aimed to identify potential strategies to improve EC function in diabetes.
METHODS AND RESULTS
Human umbilical cord endothelial cells (HUVECs) were subjected to hyperglycemic milieu by exposing cells to HG together with glucose metabolite, methylglyoxal (MG) in vitro. Hyperglycemic cells showed reduced chemotactic responses towards VEGF-A as revealed by Boyden chamber migration assays, indicating the development of "VEGF resistance" phenotype. Furthermore, HG/MG-exposed cells were defective in their general migratory and proliferative responses and were in a pro-apoptotic state. Mechanistically, the exposure to HG/MG resulted in reactive oxygen species (ROS) accumulation which is secondary to the impairment of thioredoxin (Trx) activity in these cells. Pharmacological and genetic targeting of Trx recapitulated VEGF resistance. Functional supplementation of Trx using thioredoxin mimetic peptides (TMP) reversed the HG/MG-induced ROS generation, improved the migration, proliferation, survival and restored VEGF-A-induced chemotaxis and sprouting angiogenesis of hyperglycemic ECs. Importantly, TMP treatment reduced ROS accumulation and improved VEGF-A responses of placental arterial endothelial cells isolated from gestational diabetes mellitus patients.
CONCLUSIONS
Our findings suggest a putative role for Trx in modulating EC function and its functional impairment in HG conditions contribute to EC dysfunction. Supplementation of TMP could be used as a novel strategy to improve endothelial cell function in diabetes.

Identifiants

pubmed: 31955977
pii: S0167-5273(19)31854-6
doi: 10.1016/j.ijcard.2019.12.065
pii:
doi:

Substances chimiques

Vascular Endothelial Growth Factor A 0
Thioredoxins 52500-60-4
Vascular Endothelial Growth Factor Receptor-2 EC 2.7.10.1

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

73-81

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2019. Published by Elsevier B.V.

Déclaration de conflit d'intérêts

Declaration of competing interest None declared.

Auteurs

Pia Hemling (P)

Experimental and Molecular Cardiology, Department of Cardiovascular Medicine, University Hospital Münster, Münster, Germany; Molecular Cardiology, Department of Cardiology I - Coronary and Peripheral Vascular Disease, Heart Failure, University Hospital Münster, Münster, Germany; Cells-in-Motion Cluster of Excellence (EXC 1003-CiM), University of Münster, Münster, Germany.

Darya Zibrova (D)

Institute for Molecular Cell Biology, Center for Molecular Biomedicine, University Hospital Jena, Jena, Germany.

Jasmin Strutz (J)

Department of Obstetrics and Gynecology, Medical University of Graz, Austria.

Yahya Sohrabi (Y)

Molecular Cardiology, Department of Cardiology I - Coronary and Peripheral Vascular Disease, Heart Failure, University Hospital Münster, Münster, Germany.

Gernot Desoye (G)

Department of Obstetrics and Gynecology, Medical University of Graz, Austria.

Henny Schulten (H)

Experimental and Molecular Cardiology, Department of Cardiovascular Medicine, University Hospital Münster, Münster, Germany; Department of Physiology, Cardiovascular Research Institute Maastricht (CARIM), Maastricht, the Netherlands.

Hannes Findeisen (H)

Molecular Cardiology, Department of Cardiology I - Coronary and Peripheral Vascular Disease, Heart Failure, University Hospital Münster, Münster, Germany.

Regine Heller (R)

Institute for Molecular Cell Biology, Center for Molecular Biomedicine, University Hospital Jena, Jena, Germany.

Rinesh Godfrey (R)

Experimental and Molecular Cardiology, Department of Cardiovascular Medicine, University Hospital Münster, Münster, Germany; Molecular Cardiology, Department of Cardiology I - Coronary and Peripheral Vascular Disease, Heart Failure, University Hospital Münster, Münster, Germany; Department of Physiology, Cardiovascular Research Institute Maastricht (CARIM), Maastricht, the Netherlands; Cells-in-Motion Cluster of Excellence (EXC 1003-CiM), University of Münster, Münster, Germany. Electronic address: rine.godfrey@gmail.com.

Johannes Waltenberger (J)

Experimental and Molecular Cardiology, Department of Cardiovascular Medicine, University Hospital Münster, Münster, Germany; Department of Physiology, Cardiovascular Research Institute Maastricht (CARIM), Maastricht, the Netherlands; Cells-in-Motion Cluster of Excellence (EXC 1003-CiM), University of Münster, Münster, Germany; Department of Internal Medicine I, SRH Central Hospial, Suhl, Germany. Electronic address: waltenberger@email.de.

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Classifications MeSH