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Citations to this article

Inhaled NO as a viable antiadhesive therapy for ischemia/reperfusion injury of distal microvascular beds.
A Fox-Robichaud, … , P Reinhardt, P Kubes
A Fox-Robichaud, … , P Reinhardt, P Kubes
Published June 1, 1998
Citation Information: J Clin Invest. 1998;101(11):2497-2505. https://doi.org/10.1172/JCI2736.
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Inhaled NO as a viable antiadhesive therapy for ischemia/reperfusion injury of distal microvascular beds.

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Abstract

Inhaled nitric oxide (NO) is being used more and more in intensive care units as a modality to improve the outcome of patients with pulmonary complications. Our objective was to demonstrate that inhaled NO could impact upon a distally inflamed microvasculature-improving perfusion, leukocyte adhesive interactions, and endothelial dysfunction. Using intravital microscopy to visualize ischemia/reperfusion of postcapillary venules, we were able to demonstrate that the reduction in perfusion, the dramatic increase in leukocyte rolling, adhesion, and emigration, and the endothelial dysfunction could all be significantly abrogated with 80 ppm, but not 20 ppm inhaled NO. Perfusing whole blood directly over an inert P-selectin and CD18 ligand substratum incorporated in a flow chamber recruited the same number of rolling and adhering leukocytes from NO-ventilated and non-NO-ventilated animals, suggesting that inhaled NO was not directly affecting leukocytes. To demonstrate that inhaled NO was actually reaching the peripheral microvasculature in vivo, we applied a NO synthase inhibitor locally to the feline mesentery and demonstrated that the vasoconstriction, as well as leukocyte recruitment, were essentially abolished by inhaled NO, suggesting that a NO-depleted peripheral microvasculature could be replenished with inhaled NO in vivo. Finally, inhaled NO at the same concentration that was effective in ischemia/reperfusion did not affect vascular alterations, leukocyte recruitment, and endothelial dysfunction associated with endotoxemia in the feline mesentery. In conclusion, our data for the first time demonstrate a role for inhaled NO as a therapeutic delivery system to the peripheral microvasculature, showing tremendous efficacy as an antiadhesive, antivasoconstrictive, and antipermeabilizing molecule in NO-depleted tissues, but not normal microvessels or vessels that have an abundance of NO (LPS-treated). The notion that blood borne molecules have NO carrying capacity is conceptually consistent with our observations.

Authors

A Fox-Robichaud, D Payne, S U Hasan, L Ostrovsky, T Fairhead, P Reinhardt, P Kubes

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A Roman, R LeGallo, ED McGahren
Journal of Pediatric Surgery 2004
Circulating no pool: assessment of nitrite and nitroso species in blood and tissues
T Rassaf, M Feelisch, M Kelm
Free radical biology & medicine 2004
Chimeric SOD2/3 inhibits at the endothelial-neutrophil interface to limit vascular dysfunction in ischemia-reperfusion
CS Bonder, D Knight, D Hernandez-Saavedra, JM McCord, P Kubes
AJP Gastrointestinal and Liver Physiology 2004
The Role of Nitric Oxide in Heart Failure
BI Jugdutt
2004
Heart Disease and Erectile Dysfunction
RA Kloner
2004
REVIEW: Ischemia–Reperfusion Injury of the Intestine and Protective Strategies Against Injury
IH Mallick, W Yang, MC Winslet, AM Seifalian
Digestive Diseases and Sciences 2004
Nitric oxide's reactions with hemoglobin: a view through the SNO-storm
MT Gladwin, JR Lancaster, BA Freeman, AN Schechter
Nature Medicine 2003
The role of hydroxyurea in the management of sickle cell disease
SC Davies, A Gilmore
Blood Reviews 2003
The physiology ofS-nitrosothiols: carrier molecules for nitric oxide
ES Ng, P Kubes
Canadian Journal of Physiology and Pharmacology 2003
An emerging role for nitric oxide in sickle cell disease vascular homeostasis and therapy
CD Reiter, MT Gladwin
Current Opinion in Hematology 2003
Inhaled nitric oxide inhibits platelet-leukocyte interactions in patients with acute respiratory distress syndrome
A Gries, A Herr, S Kirsch, C Günther, S Weber, G Szabo, A Holzmann, BW Böttiger, E Martin
Critical Care Medicine 2003
Beneficial effects of intraluminal nitroglycerin in intestinal ischemia-reperfusion injury in rats
A Khanna, J Rossman, MG Caty, HL Fung
Journal of Surgical Research 2003
Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation
K Cosby, KS Partovi, JH Crawford, RP Patel, CD Reiter, S Martyr, BK Yang, MA Waclawiw, G Zalos, X Xu, KT Huang, H Shields, DB Kim-Shapiro, AN Schechter, RO Cannon, MT Gladwin
Nature Medicine 2003
NO Solutions
Alan Schechter, Mark Gladwin, Richard O. Cannon
Journal of Clinical Investigation 2002
Nitric oxide and cardioprotection during ischemia-reperfusion
Bodh I Jugdutt
Heart Failure Reviews 2002
Nitric oxide in respiratory diseases
BJ Nevin, KJ Broadley
Pharmacology & Therapeutics 2002
Oxidative stress promotes blood cell-endothelial cell interactions in the microcirculation
D Cooper, KY Stokes, A Tailor, DN Granger
Cardiovascular Toxicology 2002
Inhaled nitric oxide: Is systemic host defense at risk? *
X Cui, ZM Quezado, PQ Eichacker
Critical Care Medicine 2002
Nitric oxide donor properties of hydroxyurea in patients with sickle cell disease
MT Gladwin, JH Shelhamer, FP Ognibene, ME Pease-Fye, JS Nichols, B Link, DB Patel, MA Jankowski, LK Pannell, AN Schechter, GP Rodgers
British Journal of Haematology 2002
Ischemia/Reperfusion Injury
R Anaya-Prado, LH Toledo-Pereyra, AB Lentsch, PA Ward
Journal of Surgical Research 2002
Protective effects of cyclosporin A from endotoxin-induced myocardial dysfunction and apoptosis in rats
H Fauvel, P Marchetti, G Obert, O Joulain, C Chopin, P Formstecher, R Nevière
American journal of respiratory and critical care medicine 2002
Is There a Place for Inhaled Nitric Oxide in the Therapy of Acute Pulmonary Embolism?
JE Tanus-Santos, MJ Theodorakis
American Journal of Respiratory Medicine 2002
Plasma Nitrosothiols Contribute to the Systemic Vasodilator Effects of Intravenously Applied NO: Experimental and Clinical Study on the Fate of NO in Human Blood
T Rassaf, P Kleinbongard, M Preik, A Dejam, P Gharini, T Lauer, J Erckenbrecht, A Duschin, R Schulz, G Heusch, M Feelisch, M Kelm
Circulation research 2002
Nitric oxide inhalation effects on regional blood flow: Evidence for intravascular transport of bioactive nitric oxide
Richard O. Cannon III, Alan N. Schechter, Julio A. Panza, Frederick P. Ognibene, Margaret E. Pease-Fye, Myron A. Waclawiw, James H. Shelhamer, Mark T. Gladwin
Journal of Clinical Investigation 2001
Simvastatin Has Anti-Inflammatory and Antiatherosclerotic Activities Independent of Plasma Cholesterol Lowering
CP Sparrow, CA Burton, M Hernandez, S Mundt, H Hassing, S Patel, R Rosa, A Hermanowski-Vosatka, PR Wang, D Zhang, L Peterson, PA Detmers, YS Chao, SD Wright
Arteriosclerosis, thrombosis, and vascular biology 2001
Is nitric oxide overproduction the target of choice for the management of septic shock?
F Feihl, B Waeber, L Liaudet
Pharmacology & Therapeutics 2001
Inhaled nitric oxide in cardiology
CS Hayward, AM Keogh, PS Macdonald
Expert Opinion on Investigational Drugs 2001
Vascular Manifestations of Systemic Autoimmune Diseases
C Kallenberg, JC Tervaert
Vascular Manifestations of Systemic Autoimmune Diseases 2001
Pro: Inhaled nitric oxide should be used routinely in patients undergoing lung transplantation
JD Lang, W Lell
Journal of Cardiothoracic and Vascular Anesthesia 2001
Nitric oxide therapy in sickle cell disease
M T Gladwin, A N Schechter
Seminars in Hematology 2001
Nitric oxide transport on sickle cell hemoglobin: Where does it bind?
MT Gladwin, FP Ognibene, JH Shelhamer, ME Pease-Fye, CT Noguchi, GP Rodgers, AN Schechter
Free Radical Research 2001
Liposome-Mediated Gene Transfection of Endothelial Nitric Oxide Synthase Reduces Endothelial Activation and Leukocyte Infiltration in Transplanted Hearts
A Iwata, S Sai, Y Nitta, M Chen, R de Fries-Hallstrand, J Dalesandro, R Thomas, MD Allen
Circulation 2001
Physiology of Inflammation
K Ley
2001
Nitric Oxide and Inflammation
D Salvemini, TR Billiar, Y Vodovotz
2001
Reperfusion Injury of Cardiac Myocytes: Mechanisms, Treatment, and Implications for Advanced Practice Nursing
J Brennan
AACN Clinical Issues: Advanced Practice in Acute & Critical Care 2000
Biochemical aspects of the reaction of hemoglobin and NO: implications for Hb-based blood substitutes
RP Patel
Free radical biology & medicine 2000
Inhaled nitric oxide for hypoxemic respiratory failure: passing bad gas?
ND Ferguson, JT Granton
CMAJ : Canadian Medical Association journal = journal de l'Association medicale canadienne 2000
Relative role of heme nitrosylation and beta-cysteine 93 nitrosation in the transport and metabolism of nitric oxide by hemoglobin in the human circulation
MT Gladwin, FP Ognibene, LK Pannell, JS Nichols, ME Pease-Fye, JH Shelhamer, AN Schechter
Proceedings of the National Academy of Sciences 2000
Effects of Short-Term Nitrogen Monoxide Inhalation on Leukocyte Adhesion Molecules, Generation of Reactive Oxygen Species, and Cytokine Release in Human Blood
H Opdahl, T Haugen, IA Hagberg, T Aspelin, T Lyberg
Nitric Oxide 2000
INHALED NITRIC OXIDE AND ACUTE LUNG INJURY
DM Payen
Clinics in Chest Medicine 2000
S-Nitrosothiol Formation in Blood of Lipopolysaccharide-Treated Rats
D Jourd'heuil, L Gray, MB Grisham
Biochemical and Biophysical Research Communications 2000
Inhaled nitric oxide: More than a selective pulmonary vasodilator
ZM Quezado, PQ Eichacker
Critical Care Medicine 2000
Relative role of heme nitrosylation and beta -cysteine 93 nitrosation in the transport and metabolism of nitric oxide by hemoglobin in the human circulation
MT Gladwin, FP Ognibene, LK Pannell, JS Nichols, ME Pease-Fye, JH Shelhamer, AN Schechter
Proceedings of the National Academy of Sciences 2000
Inhaled nitric oxide modulates leukocyte kinetics in the mesenteric venules of endotoxemic rats:
R Nevière, S Mordon, X Maréchal, B Buys, B Guery, D Mathieu, F Wattel, C Chopin
Critical Care Medicine 2000
Effect of inhaled nitric oxide on key mediators of the inflammatory response in patients with acute lung injury:
BH Cuthbertson, HF Galley, NR Webster
Critical Care Medicine 2000
Functional Coupling of Oxygen Binding and Vasoactivity in S -Nitrosohemoglobin
TJ McMahon, AE Stone, J Bonaventura, DJ Singel, JS Stamler
The Journal of biological chemistry 2000
A Redox Site Involved in Integrin Activation
B Yan, JW Smith
The Journal of biological chemistry 2000
Inhaled NO reduces leukocyte-endothelial cell interactions and myocardial dysfunction in endotoxemic rats
R Nevière, B Guery, S Mordon, F Zerimech, S Charré, F Wattel, C Chopin
American journal of physiology. Heart and circulatory physiology 2000
C-peptide inhibits leukocyte–endothelium interaction in the microcirculation during acute endothelial dysfunction
R Scalia, KM Coyle, BJ LEVINE, G Booth, AM Lefer
The FASEB Journal 2000
Inhaled nitric oxide augments nitric oxide transport on sickle cell hemoglobin without affecting oxygen affinity
MT Gladwin, AN Schechter, JH Shelhamer, LK Pannell, DA Conway, BW Hrinczenko, JS Nichols, ME Pease-Fye, CT Noguchi, GP Rodgers, FP Ognibene
Journal of Clinical Investigation 1999
Autoimmunity and Vascular Involvement in Systemic Sclerosis (SSc)
MB Kahalefp, EC Leroy
Autoimmunity 1999
Inhaled Nitric Oxide
W Steudel, WE Hurford, WM Zapol
Anesthesiology 1999
Physiological reactions of nitric oxide and hemoglobin: a radical rethink
SS Gross, P Lane
Proceedings of the National Academy of Sciences 1999
The oxyhemoglobin reaction of nitric oxide
AJ Gow, BP Luchsinger, JR Pawloski, DJ Singel, JS Stamler
Proceedings of the National Academy of Sciences 1999
The Perioperative Management of Portopulmonary Hypertension with Nitric Oxide and Epoprostenol
MA Ramsay, C Spikes, CA East, K Lynch, TH Hein, KJ Ramsay, GB Klintmalm
Anesthesiology 1999
Physiological reactions of nitric oxide and hemoglobin: A radical rethink
SS Gross, P Lane
Proceedings of the National Academy of Sciences 1999
Nitric Oxide Inhibits Microvascular Protein Leakage Induced by Leukocyte Adhesion-Independent and Adhesion-Dependent Inflammatory Mediators
B Johnston, JP Gaboury, M Suematsu, P Kubes
Microcirculation 1999
Nitric oxide and the gastrointestinal tract:
MR Losser, D Payen
Current Opinion in Critical Care 1999
Molecular mechanisms of cytoadherence in malaria
M Ho, NJ White
American journal of physiology. Cell physiology 1999
Inhaled NO impacts vascular but not extravascular compartments in postischemic peripheral organs
P Kubes, D Payne, MB Grisham, D Jourd-Heuil, A Fox-Robichaud
American journal of physiology. Heart and circulatory physiology 1999
II. Nitric oxide protects in intestinal inflammation
AM Lefer, DJ Lefer
AJP Gastrointestinal and Liver Physiology 1999
Inhaled NO preadministration modulates local and remote ischemia-reperfusion organ injury in a rat model
B Guery, R Neviere, N Viget, C Foucher, P Fialdes, F Wattel, G Beaucaire
Journal of applied physiology 1999
Inhaled NO reaches distal vasculatures to inhibit endothelium- but not leukocyte-dependent cell adhesion
A Fox-Robichaud, D Payne, P Kubes
American journal of physiology. Lung cellular and molecular physiology 1999
Myocardial ischemia-reperfusion injury is exacerbated in absence of endothelial cell nitric oxide synthase
SP Jones, WG Girod, AJ Palazzo, DN Granger, MB Grisham, D JourdHeuil, PL Huang, DJ Lefer
American journal of physiology. Heart and circulatory physiology 1999
Yearbook of Intensive Care and Emergency Medicine 1999
JL Vincent
1999
Modulation of inflammation and immunity by arginine supplements
DT Efron, A Barbul
Current Opinion in Clinical Nutrition and Metabolic Care 1998
Molecular mechanisms underlying the role of nitric oxide in the cardiovascular system
JC Stoclet, E Troncy, B Muller, C Brua, AL Kleschyov
Expert Opinion on Investigational Drugs 1998
Nitric Oxide
RA Schroeder, PC Kuo
Anesthesia & Analgesia 1995

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