How abundant are superoxide and hydrogen peroxide in the vasculature lumen, how far can they reach?

Paracrine superoxide (O2•−) and hydrogen peroxide (H2O2) signaling critically depends on these substances' concentrations, half-lives and transport ranges in extracellular media. Here we estimated these parameters for the lumen of human capillaries, arterioles and arteries using reaction-diffus...

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Main Authors: Tânia Sousa, Marcos Gouveia, Rui D.M. Travasso, Armindo Salvador
Format: Article
Language:English
Published: Elsevier 2022-12-01
Series:Redox Biology
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213231722002993
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author Tânia Sousa
Marcos Gouveia
Rui D.M. Travasso
Armindo Salvador
author_facet Tânia Sousa
Marcos Gouveia
Rui D.M. Travasso
Armindo Salvador
author_sort Tânia Sousa
collection DOAJ
description Paracrine superoxide (O2•−) and hydrogen peroxide (H2O2) signaling critically depends on these substances' concentrations, half-lives and transport ranges in extracellular media. Here we estimated these parameters for the lumen of human capillaries, arterioles and arteries using reaction-diffusion-advection models. These models considered O2•− and H2O2 production by endothelial cells and uptake by erythrocytes and endothelial cells, O2•− dismutation, O2•− and H2O2 diffusion and advection by the blood flow. Results show that in this environment O2•− and H2O2 have half-lives <60. ms and <40. ms, respectively, the former determined by the plasma SOD3 activity, the latter by clearance by endothelial cells and erythrocytes. H2O2 concentrations do not exceed the 10 nM scale. Maximal O2•− concentrations near vessel walls exceed H2O2's several-fold when the latter results solely from O2•− dismutation. Cytosolic dismutation of inflowing O2•− may thus significantly contribute to H2O2 delivery to cells. O2•− concentrations near vessel walls decay to 50% of maximum 12 μm downstream from O2•− production sites. H2O2 concentrations in capillaries decay to 50% of maximum 22 μm (6.0 μm) downstream from O2•− (H2O2) production sites. Near arterioles' (arteries') walls, they decay by 50% within 6.0 μm (4. μm) of H2O2 production sites. However, they reach maximal values 50 μm (24 μm) downstream from O2•− production sites and decrease by 50% over 650 μm (500 μm). Arterial/olar endothelial cells might thus signal over a mm downstream through O2•−-derived H2O2, though this requires nM-sensitive H2O2 transduction mechanisms.
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spelling doaj.art-57779d36b7fe413687e49d49db5d8db72022-12-22T04:21:52ZengElsevierRedox Biology2213-23172022-12-0158102527How abundant are superoxide and hydrogen peroxide in the vasculature lumen, how far can they reach?Tânia Sousa0Marcos Gouveia1Rui D.M. Travasso2Armindo Salvador3CNC – Centre for Neuroscience Cell Biology, University of Coimbra, UC-Biotech, Parque Tecnológico de Cantanhede, Núcleo 4, Lote 8, 3060-197, Cantanhede, Portugal; Faculty of Science and Technology, Rua Sílvio Lima, Universidade de Coimbra – Polo II, 3030-790, Coimbra, Portugal; CFisUC, Department of Physics, University of Coimbra, Rua Larga, 3004-516, Coimbra, PortugalCFisUC, Department of Physics, University of Coimbra, Rua Larga, 3004-516, Coimbra, PortugalCFisUC, Department of Physics, University of Coimbra, Rua Larga, 3004-516, Coimbra, Portugal; Corresponding author. CFisUC, Departamento de Física, Rua Larga, 3004-516, Coimbra, Portugal.CNC – Centre for Neuroscience Cell Biology, University of Coimbra, UC-Biotech, Parque Tecnológico de Cantanhede, Núcleo 4, Lote 8, 3060-197, Cantanhede, Portugal; Coimbra Chemistry Center ‐ Institute of Molecular Sciences (CQC‐IMS), University of Coimbra, Rua Larga, 3004-535, Coimbra, Portugal; Institute for Interdisciplinary Research, University of Coimbra, Casa Costa Alemão, Rua Dom Francisco de Lemos, 3030-789, Coimbra, Portugal; Corresponding author. Center for Neuroscience and Cell Biology, University of Coimbra, UC-Biotech, Parque Tecnológico de Cantanhede, Núcleo 4, Lote 8, 3060-197, Cantanhede, Portugal.Paracrine superoxide (O2•−) and hydrogen peroxide (H2O2) signaling critically depends on these substances' concentrations, half-lives and transport ranges in extracellular media. Here we estimated these parameters for the lumen of human capillaries, arterioles and arteries using reaction-diffusion-advection models. These models considered O2•− and H2O2 production by endothelial cells and uptake by erythrocytes and endothelial cells, O2•− dismutation, O2•− and H2O2 diffusion and advection by the blood flow. Results show that in this environment O2•− and H2O2 have half-lives <60. ms and <40. ms, respectively, the former determined by the plasma SOD3 activity, the latter by clearance by endothelial cells and erythrocytes. H2O2 concentrations do not exceed the 10 nM scale. Maximal O2•− concentrations near vessel walls exceed H2O2's several-fold when the latter results solely from O2•− dismutation. Cytosolic dismutation of inflowing O2•− may thus significantly contribute to H2O2 delivery to cells. O2•− concentrations near vessel walls decay to 50% of maximum 12 μm downstream from O2•− production sites. H2O2 concentrations in capillaries decay to 50% of maximum 22 μm (6.0 μm) downstream from O2•− (H2O2) production sites. Near arterioles' (arteries') walls, they decay by 50% within 6.0 μm (4. μm) of H2O2 production sites. However, they reach maximal values 50 μm (24 μm) downstream from O2•− production sites and decrease by 50% over 650 μm (500 μm). Arterial/olar endothelial cells might thus signal over a mm downstream through O2•−-derived H2O2, though this requires nM-sensitive H2O2 transduction mechanisms.http://www.sciencedirect.com/science/article/pii/S2213231722002993Hydrogen peroxideSuperoxideRedox signalingVascular regulationMathematical modelReaction-diffusion-advection model
spellingShingle Tânia Sousa
Marcos Gouveia
Rui D.M. Travasso
Armindo Salvador
How abundant are superoxide and hydrogen peroxide in the vasculature lumen, how far can they reach?
Redox Biology
Hydrogen peroxide
Superoxide
Redox signaling
Vascular regulation
Mathematical model
Reaction-diffusion-advection model
title How abundant are superoxide and hydrogen peroxide in the vasculature lumen, how far can they reach?
title_full How abundant are superoxide and hydrogen peroxide in the vasculature lumen, how far can they reach?
title_fullStr How abundant are superoxide and hydrogen peroxide in the vasculature lumen, how far can they reach?
title_full_unstemmed How abundant are superoxide and hydrogen peroxide in the vasculature lumen, how far can they reach?
title_short How abundant are superoxide and hydrogen peroxide in the vasculature lumen, how far can they reach?
title_sort how abundant are superoxide and hydrogen peroxide in the vasculature lumen how far can they reach
topic Hydrogen peroxide
Superoxide
Redox signaling
Vascular regulation
Mathematical model
Reaction-diffusion-advection model
url http://www.sciencedirect.com/science/article/pii/S2213231722002993
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AT ruidmtravasso howabundantaresuperoxideandhydrogenperoxideinthevasculaturelumenhowfarcantheyreach
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