Basic Study
Copyright ©The Author(s) 2020. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Diabetes. Dec 15, 2020; 11(12): 622-643
Published online Dec 15, 2020. doi: 10.4239/wjd.v11.i12.622
Vanadium-dependent activation of glucose transport in adipocytes by catecholamines is not mediated via adrenoceptor stimulation or monoamine oxidase activity
Jessica Fontaine, Geneviève Tavernier, Nathalie Morin, Christian Carpéné
Jessica Fontaine, Geneviève Tavernier, Nathalie Morin, Christian Carpéné, Institut des Maladies Métaboliques et Cardiovasculaires, Institut National de la Santé et de la Recherche Médicale, INSERM UMR1048, Université Paul Sabatier Toulouse III, Toulouse 31432, France
Nathalie Morin, INSERM UMR 1139 Faculté de Pharmacie, Université de Paris, Paris 75006, France
Author contributions: Carpéné C designed the studies, performed the rat experiments, reviewed the literature, and wrote the manuscript; Tavernier G performed the mouse experiments, contributed to the literature review and revised the manuscript; Fontaine J isolated the cells for in vitro studies; Morin N was involved in the generation and analysis of the data.
Institutional review board statement: The study was approved by the I2MC Institutional Review Board: Institut des maladies métaboliques et cadiovasculaires.
Institutional animal care and use committee statement: Mice were housed and manipulated according to the INSERM guidelines and European Directive 2010/63/UE by competent and expert technicians or researchers in animal care facilities with agreement number A 31 555 04 and C 31 555 07. The experimental protocol was approved by the local ethical committee CEEA nb122.
Conflict-of-interest statement: The authors declare no competing financial interests.
Data sharing statement: No additional data are available.
ARRIVE guidelines statement: The authors have read the ARRIVE guidelines, and the manuscript was prepared and revised according to the ARRIVE guideline.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Corresponding author: Christian Carpéné, PhD, Senior Researcher, Institut des Maladies Métaboliques et Cardiovasculaires, Institut National de la Santé et de la Recherche Médicale, INSERM UMR1048, Université Paul Sabatier Toulouse III, CHU Rangueil, Toulouse 31432, France. christian.carpene@inserm.fr
Received: August 31, 2020
Peer-review started: August 31, 2020
First decision: October 5, 2020
Revised: October 12, 2020
Accepted: October 26, 2020
Article in press: October 26, 2020
Published online: December 15, 2020
Processing time: 103 Days and 18 Hours
ARTICLE HIGHLIGHTS
Research background

Catecholamines have been demonstrated to induce oxidative stress by generating excessive reactive oxygen species (ROS) via amine oxidase-catalyzed oxidative deamination and via autoxidation. Like other metals, vanadium has been speculated to contribute to catecholamine oxidation. While catecholamines are recognized to mobilize lipids, vanadium is known to facilitate glucose consumption in fat cells. However, the effects of the combination of catecholamines plus vanadium on glucose utilization by adipose cells require clarification.

Research motivation

Vanadium is a potential antidiabetic agent, the use of which is limited by toxicological issues, since several vanadate salts tend to unselectively replace phosphate in many biological reactions. The search for other forms of biological vanadium complexes with either natural compounds or with designed molecules aims at developing novel less toxic and more potent antihyperglycemic agents.

Research objectives

To evaluate the impact of various biogenic amines, including the catecholamines, dopamine, adrenaline and noradrenaline, without and with vanadium, on glucose transport in adipose cells. To decipher the mode of action of the synergism between amines and vanadate regarding glucose transport activation.

Research methods

Research methods included animal husbandry, especially rats and mice deficient in all the β-adrenoceptor subtypes, preparations of freshly isolated adipocytes, quantitative exploration of glucose transport using uptake assays of its non-metabolizable analogue 2-deoxyglucose, together with appropriate use of pharmacological agents.

Research results

In adipose cells, we confirmed the strong stimulatory action of insulin on glucose transport, leading to a tenfold increase over baseline. This was not altered by the addition of 100 µmol/L sodium orthovanadate or clearly reproduced by any of the 25 biogenic amines tested. However, when some amines were added at millimolar doses together with vanadium, they strongly increased glucose uptake up to 70% of the maximal response to insulin. This was the case for methylamine, benzylamine and tyramine, already demonstrated elsewhere to produce hydrogen peroxide when oxidized by monoamine oxidase (MAO) or semicarbazide-sensitive amine oxidase (SSAO) highly expressed in adipocytes. In addition to these amines of reference, known to exert insulin-like effects when combined with vanadate, the catecholamines dopamine, adrenaline and noradrenaline also stimulated glucose transport in a vanadium-dependent manner. Contrarily to reference amines, the stimulation by catecholamines was resistant to MAO and SSAO inhibition. Not all the tested α- and β-adrenergic agonists displayed a clear-cut stimulation of glucose uptake, and the effects of catecholamines were not inhibited by dopaminergic or adrenergic antagonists. These latter effects were even detected in mice genetically invalidated for β-adrenergic receptors. Only antioxidants, such as ascorbate, impaired the stimulation of glucose uptake by the combination of catecholamines plus vanadate.

Research conclusions

It is likely an interaction between vanadium and catecholamine autoxidation that generates intermediates activating in a ROS-dependent manner glucose transport in adipose cells.

Research perspectives

The observed synergism provides the basis for possible future research of novel vanadium/amine complexes with antidiabetic properties.