Interplay of endothelial and inducible nitric oxide synthases modulates the vascular response to ischaemia-reperfusion in the rabbit lung

Acta Physiologica

Volumn 204, Issue 3, 2012, Pages 331-343

  Sedoris, K C ^a   Gozal, E ^a   Ovechkin, A V ^a   Theile, A R ^a   Roberts, A M ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

Acute lung injury; Nitric oxide synthase; Oxidative stress; Pulmonary ischaemia reperfusion; Reactive nitrogen species

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRATE; NITRITE; REACTIVE NITROGEN SPECIES; SERINE; THREONINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL REACTIVITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ISCHEMIA; LUNG BLOOD FLOW; LUNG PARENCHYMA; LUNG PERFUSION; LUNG VASCULAR RESISTANCE; LUNG VENTILATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PULMONARY ARTERY; REPERFUSION;

ANIMALS; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; LUNG; NADPH OXIDASE; NITRATES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; NITRITES; PHOSPHORYLATION; PULMONARY ARTERY; PULMONARY CIRCULATION; RABBITS; REACTIVE NITROGEN SPECIES; REPERFUSION INJURY; RESPIRATION, ARTIFICIAL; TIME FACTORS; TYROSINE; VASCULAR RESISTANCE; VASOCONSTRICTION;

EID: 84856536329     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2011.02348.x     Document Type: Article

References (45)

1. Adnot, S., Raffestin, B. & Eddahibi, S. 1995. NO in the lung. Respir Physiol101, 109-20.
2. Afshar, S., Gibson, L.L., Yuhanna, I.S., Sherman, T.S., Kerecman, J.D., Grubb, P.H., Yoder, B.A., McCurnin, D.C. & Shaul, P.W. 2003. Pulmonary NO synthase expression is attenuated in a fetal baboon model of chronic lung disease. Am J Physiol Lung Cell Mol Physiol284, L749-58.
3. Anselmi, A., Abbate, A., Girola, F., Nasso, G., Biondi-Zoccai, G.G., Possati, G. & Gaudino, M. 2004. Myocardial ischemia, stunning, inflammation, and apoptosis during cardiac surgery: a review of evidence. Eur J Cardiothorac Surg25, 304-11.
4. Armengou, A., Hurtado, O., Leira, R., Obon, M., Pascual, C., Moro, M.A., Lizasoain, I., Castillo, J. & Davalos, A. 2003. L-arginine levels in blood as a marker of nitric-oxide-mediated brain damage in acute stroke: a clinical and experimental study. J Cereb Blood Flow Metab23, 978-84.
5. Beckman, J.S. & Koppenol, W.H. 1996. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and the ugly. Am J Physiol271, C1424-7.
6. Cook, S., Vollenweider, P., Menard, B., Egli, M., Nicod, P. & Scherrer, U. 2003. Increased eNO and pulmonary iNOS expression in eNO null mice. Eur Respir J21, 770-3.
7. Dimmeler, S., Fleming, I., Fisslthaler, B., Hermann, C., Busse, R. & Zeiher, A.M. 1999. Activation of NO synthase in endothelial cells by Akt-dependent phosphorylation. Nature399, 601-5.
8. Droge, W. 2002. Free radicals in the physiological control of cell function. Physiol Rev82, 47-95.
9. 2+/calmodulin dependent endothelial nitric oxide synthase activity. Circ Res88, E68-75.
10. Garvey, E.P. 1997. 1400W is a slow, tight binding, and highly selective inhibitor of inducible nitric oxide synthase in vitro and in vivo. J Biol Chem272, 4959-63.
11. Gilroy, R.J. Jr, Bhatte, M.J., Wickersham, N.E., Pou, N.A., Loyd, J.E. & Overholser, K.A. 1993. Postischemic hypoperfusion during unilateral lung reperfusion in vivo. Am Rev Respir Dis147, 276-82.
12. Hampl, V. & Herget, J. 2000. Role of nitric oxide in the pathogenesis of chronic pulmonary hypertension. Physiol Rev80, 1337-72.
13. Hermle, G., Schutte, H., Walmrath, D., Geiger, K., Seeger, W. & Grimminger, F. 1999. Ventilation-perfusion mismatch after lung ischemia-reperfusion: protective effect of nitric oxide. Am J Respir Crit Care Med160, 1179-87.
14. Hunt, J. 2002. Exhaled breath condensate: an evolving tool for noninvasive evaluation of lung disease. J Allergy Clin Immunol110, 28-34.
15. Ischiropoulos, H. 1998. Biological tyrosine nitration: a pathophysiological function of nitric oxide and reactive oxygen species. Arch Biochem Biophys356, 1-11.
16. Ischiropoulous, H., Al-Mehdi, A.B. & Fisher, A.B. 1995. Reactive species in ischemic rat lung injury: contribution of peroxynitrite. Am J Physiol Lung Cell Mol Physiol269(2 Pt1), L158-64.
17. Isobe, M., Katsuramaki, T., Hirata, K., Kimura, H., Nagayama, M. & Matsuno, T. 1999. Beneficial effects of inducible nitric oxide synthase inhibitor on reperfusion injury in the pig liver. Transplantation68, 803-13.
18. Kanwar, S. & Kubes, P. 1995. Nitric oxide is an anti-adhesive molecule for leukocytes. New Horiz3, 93-104.
19. Konduri, G.G., Bakhutashvili, I., Eis, A. & Pritchard, K. Jr 2007. Oxidant stress from uncoupled nitric oxide synthase impairs vasodilation in fetal lambs with persistent pulmonary hypertension. Am J Physiol Heart Circ Physiol292, H1812-20.
20. Kozak, A.J., Liu, F., Funovics, P., Jacoby, A., Kubant, R. & Malinski, T. 2005. Role of peroxynitrite in the process of vascular tone regulation by nitric oxide and prostanoids - a nanotechnological approach. Prostaglandins Leukot Essent Fatty Acids72, 105-13.
21. Kurose, I., Wolf, R., Grisham, M.B. & Granger, D.N. 1994. Modulation of ischemia/reperfusion-induced microvascular dysfunction by nitric oxide. Circ Res74, 376-82.
22. Li, J., Li, W., Liu, W., Altura, B.T. & Altura, B.M. 2004a. Mechanisms of hydroxyl radical-induced contraction of rat aorta. Eur J Pharmacol499, 171-8.
23. Li, Z., Carter, J.D., Dailey, L.A. & Huang, Y.C. 2004b. Vanadyl sulfate inhibits NO production via threonine phosphorylation of eNOS. Environ Health Perspect112, 201-6.
24. Liu, M., Tremblay, L., Cassivi, S.D., Bai, X.H., Mourgeon, E., Pierre, A.F., Slutsky, A.S., Post, M. & Keshavjee, S. 2000. Alterations of nitric oxide synthase expression and activity during rat lung transplantation. Am J Physiol Lung Cell Mol Physiol278, L1071-81.
25. Marczin, N., Bundy, R.E., Hoare, G.S. & Yacoub, M. 2003. Redox regulation following cardiac ischemia and reperfusion. Coron Artery Dis14, 123-33.
26. Michell, B.J., Chen, Z.P., Tiganis, T., Stapleton, D., Katsis, F., Power, D.A., Sim, A.T. & Kemp, B.E. 2001. Coordinated control of endothelial nitric oxide synthase phosphorylation by protein kinase C and the cAMP-dependent protein kinase. J Biol Chem276, 17625-8.
27. Miller, D.L. & Roberts, A.M. 1999. Pulmonary artery occlusion and reperfusion causes microvascular constriction in the rabbit lung. Ann Thorac Surg67, 323-8.
28. Numata, M., Suzuki, S., Miyazawa, N., Miyashita, A., Nagashima, Y., Inoue, S., Kaneko, T. & Okubo, T. 1998. Inhibition of inducible nitric oxide synthase prevents LPS-induced acute lung injury in dogs. J Immunol160, 3031-7.
29. Ovechkin, A.V., Lominadze, D., Sedoris, K.C., Gozal, E., Robinson, T.W. & Roberts, A.M. 2005. Inhibition of inducible nitric oxide synthase attenuates platelet adhesion in subpleural arterioles during lung reperfusion in rabbits. J Appl Physiol99, 2423-32.
30. Parviz, M., Bousamra, M.II, Chammas, J.H., Birks, E.K., Presberg, K.W., Jacobs, E.R. & Nelin, L.D. 1999. Effects of chronic pulmonary over circulation on pulmonary vasomotor tone. Ann Thorac Surg67, 522-7.
31. de Perrot, N., Liu, M., Waddell, T.K. & Keshavjee, S. 2003. Ischemia-reperfusion-induced lung injury. Am J Respir Crit Care Med167, 490-511.
32. Poon, B.Y., Raharjo, E., Patel, K.D., Tavener, S. & Kubes, P. 2003. Complexity of inducible nitric oxide synthase: cellular source determines benefit versus toxicity. Circulation108, 1107-12.
33. Roberts, A.M., Ovechkin, A.V., Mowbray, J.G., Robinson, T.W. & Lominadze, D. 2004. Effects of pulmonary IR on platelet adhesion in subpleural arterioles in rabbits. Microvasc Res67, 29-37.
34. Robertson, B.E., Warren, J.B. & Nye, P.C. 1990. Inhibition of nitric oxide synthesis potentiates hypoxic vasoconstriction in isolated rat lungs. Exp Physiol75, 255-7.
35. Sittipunt, C., Steinberg, K.P., Ruzinski, J.T., Myles, C., Zhu, S., Goodman, R.B., Hudson, L.D., Matalon, S. & Martin, T.R. 2001. Nitric oxide and nitrotyrosine in the lungs of patients with acute respiratory distress syndrome. Am J Respir Crit Care Med163, 503-10.
36. Sumimoto, H. 2008. Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J275, 3249-77.
37. Varadarajan, R., Golden-Mason, L., Young, L., McLoughlin, P., Nolan, N., McEntee, G., Traynor, O., Geoghegan, J., Hegarty, J.E. & O'Farrelly, C. 2004. Nitric oxide in early ischemia reperfusion injury during human orthotopic liver transplantation. Transplantation78, 250-6.
38. Vural, K.M. & Oz, C.M. 2000. Endothelial adhesivity, pulmonary hemodynamics and nitric oxide synthesis in ischemia-reperfusion. Eur J Cardiothorac Surg18, 348-52.
39. Wadsworth, R.M. 1999. Superoxide in the pulmonary circulation. Pharmacol Ther84, 355-65.
40. Wink, D.A. & Mitchell, J.B. 1998. Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic Biol Med25, 434-56.
41. Worral, N.K., Chang, K., Suau, G.M., Allison, W.S., Misko, T.P., Sullivan, P.M., Tilton, R.G., Williamson, J.R. & Ferguson, T.B. Jr 1996. Inhibition of inducible nitric oxide synthase prevents myocardial and systemic vascular barrier dysfunction during early cardiac allograft rejection. Cir Res78, 769-79.
42. Wright, K.L. & Ward, S.G. 2000. Interactions between phospatidylinositol 3-kinase and nitric oxide: explaining the paradox. Mol Cell Biol Res Commun4, 137-43.
43. Zhao, X., Ross, M.E. & Iadecola, C. 2003. L-arginine increases ischemic injury in wild-type mice but not in iNOS-deficient mice. Brain Res966, 308-11.
44. Zou, M.H., Hou, X.Y., Shi, C.M., Nagata, D., Walsh, K. & Cohen, R.A. 2002. Modulation by peroxynitrite of Akt and AMP activated kinase dependent SER 1179 phosphorylation of endothelial nitric oxide synthase. J Biol Chem277, 32552-7.
45. Zou, M.H., Cohen, R. & Ullrich, V. 2004. Peroxynitrite and vascular dysfunction in diabetes mellitus. Endothelium11, 89-97.