Equine endothelial cell; Anoxia/Reoxygenation; High-Resolution oxygraphy; Gas Chromatography; Electron spine resonance; Reactive Oxygen Species; Free Radicals
Abstract :
[en] The endothelium plays an active role in ischemia/reperfusion injuries. Herein, we report the effect of a single or successive cycles of anoxia/reoxygenation (A/R) on the mitochondrial respiratory function of equine endothelial cells (cultured from carotids) monitored by high resolution oxymetry, and on their production of reactive oxygen species (ROS). ROS were measured by electron paramagnetic resonance (ESR) using POBN and DMPO spin traps, and by gas chromatography (GC) of ethylene released by ROS-induced alpha-keto-gamma-(methylthio)butyric acid (KMB) oxidation. The oxygen consumption significantly decreased with the number of A/R cycles, and POBN-ESR spectra were specific of adducts formed in the cells from superoxide anion. After a one-hour A/R cycle, high intensity DMPO-ESR spectra were observed and assigned to superoxide anion trapping; the GC results confirmed an important production of ROS compared to normoxic cells. These results show that A/R induces mitochondrial alterations in endothelial cells, and strongly stimulates their oxidative activity as demonstrated by ESR and GC methods.
Research Center/Unit :
CORD - Centre de l'Oxygène, Recherche et Développement - ULiège
Disciplines :
Biochemistry, biophysics & molecular biology Veterinary medicine & animal health
Author, co-author :
de la Rebière de Pouyade, Geoffroy ; Université de Liège - ULiège > Département clinique des animaux de compagnie et des équidés > Anesthésiologie gén. et pathologie chirurg. des grds animaux
Salciccia, Alexandra ; Université de Liège - ULiège > Département clinique des animaux de compagnie et des équidés > Département clinique des animaux de compagnie et des équidés
Ceusters, Justine ; Université de Liège - ULiège > Centre de l'oxygène : Recherche et développement (C.O.R.D.)
Deby-Dupont, Ginette
Serteyn, Didier ; Université de Liège - ULiège > Département clinique des animaux de compagnie et des équidés > Anesthésiologie gén. et pathologie chirurg. des grds animaux
Mouithys-Mickalad, Ange ; Université de Liège - ULiège > Centre de l'oxygène : Recherche et développement (C.O.R.D.)
Language :
English
Title :
Production of free radicals and oxygen consumption by primary equine endothelial cells during anoxia-reoxygenation.
Publication date :
2011
Journal title :
Open Biochemistry Journal
eISSN :
1874-091X
Publisher :
Bentham Science Publishers, Netherlands
Volume :
5
Pages :
52-9
Peer reviewed :
Peer reviewed
Funders :
FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture
Rubanyi, G.M. The role of endothelium in cardiovascular homeostasis and diseases. J. Cardiovasc. Pharm., 1993, 22, S1-14.
Nomura, M.; Yamagishi, S.; Harada, S.; Hayashi, Y.; Yamashima, T.; Yamashita, J.; Yamamoto, H. Possible participation of autocrine and paracrine vascular endothelial growth factors in hypoxia-induced proliferation of endothelial cells and pericytes. J. Biol. Chem., 1995, 270, 28316-28324.
Duffy, T.C.; Kirby, R.; Rudloff, E. Critical role of the vascular endothelial cell in health and disease: a review article. J. Vet. Emerg. Crit. Car., 2004, 14, 84-99.
Matsuda, N.; Hattori, I. Vascular biology in sepsis: pathophysiological and therapeutic significance of vascular dysfunction. J. Smooth Muscle Res., 2007, 43, 117-137.
Arndt, H.; Kubes, P.; Granger, D.N. Involvement of neutrophils in ischemia-reperfusion injury in the small intestine. Klin. Wochenschr. 1991, 69, 1056-1060.
Bzeizi, K.I.; Jalan, R.; MacGregor, I.; Drummond, O.; Lee, A.; Hayes, P.C. Neutrophil elastase: a determinant of endothelial damage and reperfusion injury after liver transplantation? Transplantation, 1996, 62, 916-920.
Deby-Dupont, G.; Deby, C.; Lamy, M. Neutrophil myeloperoxidase revisited: it's role in health and disease. Intensivmed, 1999, 36, 500-513.
Benbarek, H.; Grulke, S.; Deby-Dupont, G.; Deby, C.; Mathy-Hartert, M.; Caudron, I.; Dessy-Doize, C.; Lamy, M.; Serteyn, D. Cytotoxicity of stimulated equine neutrophils on equine endothelial cells in culture. Equine Vet. J., 2000, 32, 327-333.
Harada, N.; Okajima, K.; Isobe, H. Role of neutrophil elastase in development of pulmonary vascular injury and septic shock in rats. Shock, 2008, 30, 379-387.
Duilio, C.; Ambrosio, G.; Kuppusamy, P.; DiPaula, A.; Becker, L.C.; Zweier, J.L. Neutrophils are primary source of O2 radicals during reperfusion after prolonged myocardial ischemia. Am. J. Physiol. Heart Circ. Physiol., 2001, 280, H2649-H2657.
Zweier, J.L.; Duke, S.S.; Kuppusamy, P.; Sylvester, J.T.; Gabrielson, E.W. Electron paramagnetic resonance evidence that cellular oxygen toxicity is caused by the generation of superoxide and hydroxyl free radicals. FEBS Lett., 1989, 252, 12-26.
Zweier, J.L.; Broderick, R.; Kuppusamy, P.; Thompson-Gorman, S.; Lutty, G.A. Determination of the mechanism of free radical generation in human aortic endothelial cells exposed to anoxia and reoxygenation. J. Biol. Chem., 1994, 269, 24156-24162.
Duchen, M.R. Mitochondria in health and disease: perspectives on a new mitochondrial biology. Mol. Aspects Med., 2004, 25, 365-451.
De Vriese, A.S.; Verbeuren, T.J.; Van de Voorde, J.; Lameire, N.H.; Vanhoutte, P.M. Endothelial dysfunction in diabetes. Brit. J. Pharmacol., 2000, 130, 963-974.
Simonini, G.; Pignone, A.; Generini, S.; Falcini, F.; Cerinic, M.M. Emerging potentials for an antioxidant therapy as a new approach to the treatment of systemic sclerosis. Toxicology, 2000, 155, 1-15.
Settergren, M.; Bohm, F.; Malmstrom, R.E.; Channon, K.M.; Pernow, J. l-Arginine and tetrahydrobiopterin protects against ischemia/reperfusion-induced endothelial dysfunction in patients with type 2 diabetes mellitus and coronary artery disease. Atherosclerosis, 2009, 204, 73-78.
Hood, D.M.; Grosenbaugh, D.A.; Mostafa, M.B.; Morgan, S.J.; Thomas, B.C. The Role of vascular mechanisms in the development of acute equine laminitis. J. Vet. Intern. Med., 1993, 7, 228-234.
Moore, R.M.; Muir, W.W.; Granger, D.N. Mechanisms of gastrointestinal ischemia-reperfusion injury and potential therapeutic interventions: a review and its implications in the horse. J. Vet. Intern. Med., 1995, 9, 115-132.
de la Rebiere, G.; Franck, T.; Deby-Dupont, G.; Salciccia, A.; Grulke, S.; Peters, F.; Serteyn, D. Effects of unfractionated and fractionated heparins on myeloperoxidase activity and interactions with endothelial cells: possible effects on the pathophysiology of equine laminitis. Vet. J., 2008, 178, 62-69.
Deby-Dupont, G.; Mouithys-Mickalad, A.; Serteyn, D.; Lamy, M.; Deby, C. Resveratrol and curcumin reduce the respiratory burst of Chlamydia-primed THP-1 cells. Biochem. Biophys. Res. Commun., 2005, 333, 21-27.
Saikumar, P.; Dong, Z.; Weinberg, J.M.; Venkatachalam, M.A. Mechanisms of cell death in hypoxia/reoxygenation injury. Oncogene, 1998, 17, 3341-3349.
Simon, H.U.; Haj-Yehia, A.; Levi-Schaffer, F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis, 2000, 5, 415-418.
Mouithys-Mickalad, A.; Mathy-Hartert, M.; Du, G.; Sluse, F.; Deby, C.; Lamy, M.; Deby-Dupont, G. Oxygen consumption and electron spin resonance studies of free radical production by alveolar cells exposed to anoxia: inhibiting effects of the antibiotic ceftazidime. Redox Rep., 2002, 7, 85-94.
Gueler, F.; Gwinner, W.; Schwarz, A.; Haller, H. Long-term effects of acute ischemia and reperfusion injury. Kidney Int., 2004, 66, 523-527.
Schneider, N.; Mouithys-Mickalad, A.L.; Lejeune, J.P.; Deby-Dupont, G.P.; Hoebeke, M.; Serteyn, D.A. Synoviocytes, not chondrocytes, release free radicals after cycles of anoxia/re- oxygenation. Biochem. Biophys. Res. Commun., 2005, 334, 669-673.
Du, G.; Mouithys-Mickalad, A.; Sluse, F.E. Generation of superoxide anion by mitochondria and impairment of their functions during anoxia and reoxygenation in vitro. Free Radic. Biol. Med., 1998, 25, 1066-1074.
Arroyo, C.M.; Carmichael, A.J.; Bouscarel, B.; Liang, J.H.; Weglicki, W.B. Endothelial cells as a source of oxygen-free radicals. An ESR study. Free Radic. Res. Commun., 1990, 9, 287-296.
Berliner, L.J.; Khramtsov, V.; Fujii, H.; Clanton, T.L. Unique in vivo applications of spin traps. Free Radic. Biol. Med., 2001, 30, 489-499.
Vasquez-Vivar, J.; Kalyanaraman, B.; Kennedy, M.C. Mitochondrial aconitase is a source of hydroxyl radical. An electron spin resonance investigation. J. Biol. Chem., 2000, 275, 14064-14069.
Fariss, M.W.; Chan, C.B.; Patel, M.; Van Houten, B.; Orrenius, S. Role of mitochondria in toxic oxidative stress. Mol. Interv., 2005, 5, 94-111.
Hurley, D.J.; Parks, R.J.; Reber, A.J.; Donovan, D.C.; Okinaga, T.; Vandenplas, M.L.; Peroni, J.F.; Moore, J.N. Dynamic changes in circulating leukocytes during the induction of equine laminitis with black walnut extract. Vet. Immunol. Immunopathol., 2006, 110, 195-206.
Fraticelli, A.; Serrano, C.V.; Bochner, Jr B.S.; Capogrossi, M.C.; Zweier, J.L. Hydrogen peroxide and superoxide modulate leukocyte adhesion molecule expression and leukocyte endothelial adhesion. Biochim. Biophys. Acta, 1996, 1310, 251-259.
Ichikawa, H.; Kokura, S.; Aw, T.Y. Role of endothelial mitochondria in oxidant production and modulation of neutrophil adherence. J. Vasc. Res., 2004, 41, 432-444.
Rudolph, T.K.; Rudolph, V.; Witte, A.; Klinke, A.; Szoecs, K.; Lau, D.; Heitzer, T.; Meinertz, T.; Baldus, S. Liberation of vessel adherent myeloperoxidase by enoxaparin improves endothelial function. Int. J. Cardiol., 2010, 140, 42-47.