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Endothelial glycocalyx dimensions are reduced in growing collateral arteries and modulate leucocyte adhesion in arteriogenesis

During collateral artery growth, monocytes adhere to the endothelium and secrete cytokines from the perivascular space promoting arteriogenesis. Recently, the endothelial glycocalyx has been shown to modulate leucocyte infiltration in atherogenic regions. The role of this endothelial surface coating...

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Autores principales: Grundmann, Sebastian, Schirmer, Stephan H, Hekking, Liesbeth H P, Post, Jan Andries, Ionita, Mihaela G, de Groot, Daphne, van Royen, Niels, van den Berg, Bernard, Vink, Hans, Moser, Martin, Bode, Christoph, de Kleijn, Dominique, Pasterkamp, Gerard, Piek, Jan J, Hoefer, Imo E
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Ltd 2009
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4516501/
https://www.ncbi.nlm.nih.gov/pubmed/19438808
http://dx.doi.org/10.1111/j.1582-4934.2009.00735.x
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author Grundmann, Sebastian
Schirmer, Stephan H
Hekking, Liesbeth H P
Post, Jan Andries
Ionita, Mihaela G
de Groot, Daphne
van Royen, Niels
van den Berg, Bernard
Vink, Hans
Moser, Martin
Bode, Christoph
de Kleijn, Dominique
Pasterkamp, Gerard
Piek, Jan J
Hoefer, Imo E
author_facet Grundmann, Sebastian
Schirmer, Stephan H
Hekking, Liesbeth H P
Post, Jan Andries
Ionita, Mihaela G
de Groot, Daphne
van Royen, Niels
van den Berg, Bernard
Vink, Hans
Moser, Martin
Bode, Christoph
de Kleijn, Dominique
Pasterkamp, Gerard
Piek, Jan J
Hoefer, Imo E
author_sort Grundmann, Sebastian
collection PubMed
description During collateral artery growth, monocytes adhere to the endothelium and secrete cytokines from the perivascular space promoting arteriogenesis. Recently, the endothelial glycocalyx has been shown to modulate leucocyte infiltration in atherogenic regions. The role of this endothelial surface coating in arteriogenesis, however, has not been investigated so far. We now report that local plasma levels of hyaluronic acid are specifically increased in collateral arterial blood of coronary artery disease patients and hypothesized that components of the endothelial glycocalyx are shed during arteriogenesis, resulting in decreased glycocalyx dimensions and an increased leucocyte extravasation. In a rabbit model of femoral artery ligation, electron microscopy revealed a decrease in glycocalyx dimensions in collateral arteries compared with quiescent anastomoses (67.5 ± 47.2 nm versus 101.0 ± 11.3 nm; P < 0.001). This decrease was correlated with a higher number of perivascular macrophages around collateral arteries. The additional glycocalyx perturbation by local hyaluronidase infusion almost completely removed the endothelial surface layer and temporarily stimulated leucocyte accumulation in the perivascular space. However, complete perturbation of the glycocalyx by hyaluronidase infusion resulted in a significant attenuation of collateral artery growth assessed by microsphere-based perfusion measurements (ml/min/100 mmHg: hyaluronidase: 27.5 ± 3.5; Controls: 47.1 ± 3.83; P < 0.001) and a lower percentage of actively proliferating vascular smooth muscle cells. A decreased expression of the shear-stress regulated pro-arteriogenic genes eNOS and TGF-β1 suggests an impaired mechanotransduction as the underlying mechanisms. For the first time, we describe the role of the endothelial glycocalyx in collateral artery growth. Although complete abrogation led to attenuated arteriogenesis, shedding of glycocalyx components is observed during collateral artery growth.
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spelling pubmed-45165012015-08-03 Endothelial glycocalyx dimensions are reduced in growing collateral arteries and modulate leucocyte adhesion in arteriogenesis Grundmann, Sebastian Schirmer, Stephan H Hekking, Liesbeth H P Post, Jan Andries Ionita, Mihaela G de Groot, Daphne van Royen, Niels van den Berg, Bernard Vink, Hans Moser, Martin Bode, Christoph de Kleijn, Dominique Pasterkamp, Gerard Piek, Jan J Hoefer, Imo E J Cell Mol Med Tissue Remodeling/Regeneration During collateral artery growth, monocytes adhere to the endothelium and secrete cytokines from the perivascular space promoting arteriogenesis. Recently, the endothelial glycocalyx has been shown to modulate leucocyte infiltration in atherogenic regions. The role of this endothelial surface coating in arteriogenesis, however, has not been investigated so far. We now report that local plasma levels of hyaluronic acid are specifically increased in collateral arterial blood of coronary artery disease patients and hypothesized that components of the endothelial glycocalyx are shed during arteriogenesis, resulting in decreased glycocalyx dimensions and an increased leucocyte extravasation. In a rabbit model of femoral artery ligation, electron microscopy revealed a decrease in glycocalyx dimensions in collateral arteries compared with quiescent anastomoses (67.5 ± 47.2 nm versus 101.0 ± 11.3 nm; P < 0.001). This decrease was correlated with a higher number of perivascular macrophages around collateral arteries. The additional glycocalyx perturbation by local hyaluronidase infusion almost completely removed the endothelial surface layer and temporarily stimulated leucocyte accumulation in the perivascular space. However, complete perturbation of the glycocalyx by hyaluronidase infusion resulted in a significant attenuation of collateral artery growth assessed by microsphere-based perfusion measurements (ml/min/100 mmHg: hyaluronidase: 27.5 ± 3.5; Controls: 47.1 ± 3.83; P < 0.001) and a lower percentage of actively proliferating vascular smooth muscle cells. A decreased expression of the shear-stress regulated pro-arteriogenic genes eNOS and TGF-β1 suggests an impaired mechanotransduction as the underlying mechanisms. For the first time, we describe the role of the endothelial glycocalyx in collateral artery growth. Although complete abrogation led to attenuated arteriogenesis, shedding of glycocalyx components is observed during collateral artery growth. John Wiley & Sons, Ltd 2009-09 2009-03-06 /pmc/articles/PMC4516501/ /pubmed/19438808 http://dx.doi.org/10.1111/j.1582-4934.2009.00735.x Text en © 2009 The Authors Journal compilation © 2009 Foundation for Cellular and Molecular Medicine/Blackwell Publishing Ltd
spellingShingle Tissue Remodeling/Regeneration
Grundmann, Sebastian
Schirmer, Stephan H
Hekking, Liesbeth H P
Post, Jan Andries
Ionita, Mihaela G
de Groot, Daphne
van Royen, Niels
van den Berg, Bernard
Vink, Hans
Moser, Martin
Bode, Christoph
de Kleijn, Dominique
Pasterkamp, Gerard
Piek, Jan J
Hoefer, Imo E
Endothelial glycocalyx dimensions are reduced in growing collateral arteries and modulate leucocyte adhesion in arteriogenesis
title Endothelial glycocalyx dimensions are reduced in growing collateral arteries and modulate leucocyte adhesion in arteriogenesis
title_full Endothelial glycocalyx dimensions are reduced in growing collateral arteries and modulate leucocyte adhesion in arteriogenesis
title_fullStr Endothelial glycocalyx dimensions are reduced in growing collateral arteries and modulate leucocyte adhesion in arteriogenesis
title_full_unstemmed Endothelial glycocalyx dimensions are reduced in growing collateral arteries and modulate leucocyte adhesion in arteriogenesis
title_short Endothelial glycocalyx dimensions are reduced in growing collateral arteries and modulate leucocyte adhesion in arteriogenesis
title_sort endothelial glycocalyx dimensions are reduced in growing collateral arteries and modulate leucocyte adhesion in arteriogenesis
topic Tissue Remodeling/Regeneration
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4516501/
https://www.ncbi.nlm.nih.gov/pubmed/19438808
http://dx.doi.org/10.1111/j.1582-4934.2009.00735.x
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