Endothelial NOS-derived nitric oxide prevents injury resulting from reoxygenation in the hypoxic lung

Free Radical Research

Volumn 44, Issue 9, 2010, Pages 1027-1035

  Rus, Alma ^a   Molina, Francisco ^a   Peinado, M Ángeles ^a   Del Moral, M Luisa ^a  

^a UNIVERSITY OF JAÉN   (Spain)

Author keywords

apoptosis; endothelial nitric oxide synthase; Hypoxia; L NIO; lipid peroxidation; nitric oxide; reoxygenation

Indexed keywords

3 NITROTYROSINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; N5 (1 IMINOETHYL)ORNITHINE; NITRIC OXIDE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; DOWN REGULATION; HYPOXIA; IMMUNOHISTOCHEMISTRY; LIPID PEROXIDATION; LUNG INJURY; NITRATION; NONHUMAN; RAT; REOXYGENATION;

ANIMALS; ANOXIA; CYTOPROTECTION; ENZYME INHIBITORS; IN SITU NICK-END LABELING; LUNG; MALE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; ORNITHINE; OXYGEN; RATS; RATS, WISTAR; REPERFUSION INJURY; THIOBARBITURIC ACID REACTIVE SUBSTANCES; TYROSINE;

RATTUS NORVEGICUS;

EID: 77956372808     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2010.498479     Document Type: Article

References (47)

1. Kiang JG, Tsen KT. Biology of hypoxia. Chin J Physiol 2006;49:223-233.
2. Vaughan DJ, Brogan TV, Kerr ME, Deem S, Luchtel DL, Swenson ER. Contributions of nitric oxide synthase isozymes to exhaled nitric oxide and hypoxic pulmonary vasoconstric-tion in rabbit lungs. Am J Physiol Lung Cell Mol Physiol 2003;284:834-843.
3. Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987;327:524-526. (Pubitemid 17085822)
4. Jung F, Palmer LA, Zhou N, Johns RA. Hypoxic regulation of inducible nitric oxide synthase via hypoxia inducible fac-tor-1 in cardiac myocytes. Circ Res 2000;86:319-325.
5. Ricciardolo FL, Sterk PJ, Gaston B, Folkerts G. Nitric oxide in health and disease of the respiratory system. Physiol Rev 2004;84:731-765. Review.
6. Kobzik L, Bredt DS, Lowenstein CJ, Drazen J, Gaston B, Sugarbaker D, Stamler JS. Nitric oxide synthase in human and rat lung: immunocytochemical and histochemical localization. Am J Respir Cell Mol Biol 1993;4:371-377.
7. Sherman TS, Chen Z, Yuhanna IS, Lau KS, Margraf LR, Shaul P W. Nitric oxide synthase isoform expression in the developing lung epithelium. Am J Physiol 1999;276: 383-390.
8. Shaul PW, North AJ, Brannon TS, Ujiie K, Wells LB, Nisen PA, Lowenstein CJ, Snyder SH, Star RA. Prolonged in vivo hypoxia enhances nitric oxide synthase type I and type III gene expression in adult rat lung. Am J Respir Cell Mol Biol 1995;13:167-174.
9. Szabo C. The pathophysiological role of peroxynitrite in shock, inflammation, and in ischemia-reperfusion injury. Shock 1996;6:79-88
10. Hemia. The role of xanthine oxidase. Adv Myocardiol 1985;5:183-189.
11. Venardos KM, Perkins A, Headrick J, Kaye DM. Myocardial ischemia-reperfusion injury, antioxidant enzyme systems, and selenium: a review. Curr Med Chem 2007;14:1539-1549.
12. Haddad IY, Pataki G, Hu P, Galliani C, Beckman JS, Matalon S. Quantitation of nitrotyrosine levels in lung sections of patients and animals with acute lung injury. J Clin Invest 1994;94:2407-2413.
13. Steudel W, Scherrer-Crosbie M, Bloch KD, Weimann J, Huang PL, Jones RC, Picard MH, Zapol WM. Sustained pulmonary hypertension and right ventricular hypertrophy after chronic hypoxia in mice with congenital deficiency of nitric oxide synthase 3. J Clin Invest 1998;101:2468-2477.
14. Fagan KA, Fouty BW, Tyler RC, Morris KG, Hepler LK, Sato K, LeCras TD, Abman SH, Weinberger HD, Huang PL, McMurtry IF, Rodman DM. The pulmonary circulation of homozygous or heterozygous eNOS-null mice is hyperrespon-sive to mild hypoxia. J Clin Invest 1999;103:291-299.
15. Murata T, Kinoshita K, Hori M, Kuwahara M, Tsubone H, Karaki H, Ozaki H. Statin protects endothelial nitric oxide synthase activity in hypoxia-induced pulmonary hypertension. Arterioscler Thromb Vasc Biol 2005;25:2335-2342.
16. Kaminski A, Kasch C, Zhang L, Kumar S, Sponholz C, Choi YH, Ma N, Liebold A, Ladilov Y, Steinhoff G, Stamm C. Endothelial nitric oxide synthase mediates protective effects of hypoxic preconditioning in lungs. Respir Physiol Neurobiol 2007;155:280-285
17. Vaupel DB, Kimes AS, London ED. Nitric oxide synthase inhibitors. Preclinical studies of potential use for treatment of opioid withdrawal. Neuropsychopharmacol 1995;13: 315-322.
18. Benamar K, Yondorf MZ, Kon D, Geller EB, Adler MW. Role of the nitric-oxide synthase isoforms during morphine-induced hyperthermia in rats. J Pharmacol Exp Ther 2003;307:219-222.
19. Xu Y, Krukoff TL. Decrease in arterial pressure induced by adrenomedullin in the hypothalamic paraventricular nucleus is mediated by nitric oxide and GABA. Regul Pept 2004; 119:21-30.
20. Rees DD, Palmer RM, Schulz R, Hodson HF, Moncada S. Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br J Pharmacol 1990;101: 746-752. (Pubitemid 20357206)
21. Wolff DJ, Lubeskie A, Gauld DS, Neulander MJ. Inactivation of nitric oxide synthases and cellular nitric oxide formation by N6-iminoethyl-L-lysine and N5-iminoethyl-L-ornithine. Eur J Pharmacol 1998;350:325-334.
22. López-Ramos JC, Martínez-Romero R, Molina F, Cañuelo A, Martínez-Lara E, Siles E, Peinado MA. Evidence of a decrease in nitric oxide-storage molecules following acute hypoxia and/or hypobaria, by means of chemiluminescence analysis. Nitric Oxide 2005;13:62-67.
23. Martínez-Romero R, Cañuelo A, Martínez-Lara E, Hernández R, Del Moral ML, Pedrosa JA, Peinado MA, Siles E. Aging affects but does not eliminate the enzymatic antioxidative response to hypoxia/reoxygenation in cerebral cortex. Exp Gerontol 2006;41:25-31
24. Vi ñ as JL, Sola A, Genesc à M, Alfaro V, P í F, Hotter G. NO and NOS isoforms in the development of apoptosis in renal ischemia/reperfusion. Free Radic Biol Med 2006;40: 992-1003.
25. Fontijn A, Sabadell AJ, Ronco RJ. Homogenous chemilumi-niscent measurement of nitric oxide with ozone. Implications for continuous selective monitoring of gaseous air pollutants. Anal Chem 1997;42:575-579.
26. Laitinen J, Liesivuori J, Linnainmaa M, Kalliokoski P. Evaluation of monitoring methods for nitrogen oxides. Ann Occup Hyg 1993;37:307-314.
27. Braman RS, Hendrix SA. Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium (III) reduction with chemiluminescence detection. Anal Chem 1989;61:2715-2718.
28. Buege JA, Aust SD. Mitochondrial lipid peroxidacion. Methods Enzymol 1978;52:302-310.
29. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem1976;72: 248-254.
30. Shu SY, Ju G, Fan LZ. The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci Lett 1998;85:169-171.
31. Drapper HH, Squires EJ, Manmoodi H, Wu S, Agawal S, Hadley M. A comparative evaluacion of thiobarbituric acid methods for the determination of malondialdehyde in biological materials. Free Radic Biol Med 1993;15:353-363.
32. Rus A, Peinado MA, Castro L, del Moral ML. Lung eNOS and iNOS are reoxygenation time-dependent upregulated after acute hypoxia. Anat Rec 2010;293:1089-1098.
33. Tsai SK, Hung LM, Fu YT, Cheng H, Nien MW, Liu HY, Zhang FB, Huang SS. Resveratrol neuroprotective effects during focal cerebral ischemia injury via nitric oxide mechanism in rats. J Vasc Surg 2007;46:346-353.
34. Chaitoff KA, Patel D, Ally A. Effects of endothelial NOS antagonism within the periaqueductal gray on cardiovascular responses and neurotransmission during mechanical, heat, and cold nociception. Brain Res 2008;1236:93-104.
35. Sosroseno W, Sugiatno E, Samsudin AR, Ibrahim F. The role of nitric oxide on the proliferation of a human osteoblast cell line stimulated with hydroxyapatite. J Oral Implantol 2008; 34:196-202.
36. Mehta VB, Zhou Y, Radulescu A, Besner GE. HB-EGF stimulates eNOS expression and nitric oxide production and promotes eNOS dependent angiogenesis. Growth Factors 2008;26:301-315.
37. Rubbo H, Radi R, Trujillo M, Telleri R, Kalyanaraman B, Barnes S, Kirk M, Freeman B. Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. Formation of novel nitrogen-containing oxidized lipid derivatives. J Biol Chem 1994;269:26066-26075.
38. Yamazaki I, Piette LH. ESR spin-trapping studies on the reaction of Fe2+ ions with H2O2-reactive species in oxygen toxicity in biology. J Biol Chem 1990;265:13589-13594.
39. Kanner J, Harel S, Granit R. Nitric oxide as an antioxidant. Arch Biochem Biophys 1991;289:130-136.
40. Leist M, Single B, Naumann H, Fava E, Simon B, Kühnle S, Nicotera P. Inhibition of mitochondrial ATP generation by nitric oxide switches apoptosis to necrosis. Exp Cell Res 1999;249:396-403.
41. Fierro IM, Barja-Fidalgo C, Canedo RM, Cunha FQ, Fer-reira SH. An increase in nitric oxide produced by rat peritoneal neutrophils is not involved in cell apoptosis. Mediators Inflamm 1995;4:222-228.
42. Yamanaka N, Oda O, Nagao S. Nitric oxide released from zwitterionic polyamine/NO adducts inhibits Cu2+-induced low density lipoprotein oxidation. FEBS Lett 1996;398: 53-56.
43. Utepbergenov DI, Mertsch K, Sporbert A, Tenz K, Paul M, Haseloff RF, Blasig IE. Nitric oxide protects blood-brain barrier in vitro from hypoxia/reoxygenation-mediated injury. FEBS Lett 1998;424:197-201.
44. Van der Vliet A, Smith D, O'Neill CA, Kaur H, Darley-Usmar V, Cross CE, Halliwell B. Interactions of peroxyni-trite with human plasma and its contituents: oxidative damage and antioxidant depletion. Biochem J 1994;303:295-301.
45. Bola ñ os JP, Peuchen S, Heales SJ, Land JM, Clark JB. Nitric oxide-mediated inhibition of the mitochondrial respiratory chain in cultured astrocytes. J Neurochem 1994;63:910-916.
46. Alonso D, Encinas JM, Uttenthal LO, Bosc á L, Serrano J, Fern á ndez AP, Castro-Blanco S, Santacana M, Bentura ML, Richart A, Fern á ndez-Vizarra P, Rodrigo J. Coexistence of translocated cytrochrome c and nitrated protein in neurons of the rat cerebral cortex after oxygen and glucose deprivation. Neuroscience 2002;111:47-56
47. Demiry ü rek AT, Karamsetty MR, McPhaden AR, Wadsworth RM, Kane KA, MacLean MR. Accumulation of nitrotyrosine correlates with endothelial NO synthase in pulmonary resistance arteries during chronic hypoxia in the rat. Pulm Pharmacol Ther 2000;13:157-165.