Nitric oxide regulation of superoxide-dependent lung injury: Oxidant- protective actions of endogenously produced and exogenously administered nitric oxide

Free Radical Biology and Medicine

Volumn 21, Issue 1, 1996, Pages 43-52

  Gutierrez, Hector H ^a   Nieves, Bedford ^a   Chumley, Phillip ^b   Rivera, Arnold ^b   Freeman, Bruce A ^a,b,c  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Alveolar epithelium; Antioxidant; Free radical; Hydrogen peroxide; Long injury; Nitric oxide; Peroxynitrite; Superoxide

Indexed keywords

ANTIOXIDANT; FREE RADICAL; NITRIC OXIDE; SUPEROXIDE;

ANIMAL CELL; ARTICLE; BASOLATERAL MEMBRANE; CELL DAMAGE; CELL MEMBRANE PERMEABILITY; DNA SYNTHESIS INHIBITION; LUNG ALVEOLUS EPITHELIUM; LUNG INJURY; LUNG PARENCHYMA; MICROCIRCULATION; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; RAT;

EID: 0029957727     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/0891-5849(95)02226-0     Document Type: Article

References (76)

1. 1. Nathan, C.; Xie, Q.-W. Nitric oxide synthases: Roles, tolls, and controls. Cell 78:915-918; 1994.
2. 2. Dawson, V. L.; Dawson, T. M.; London, E. D.; Bredt, D. S.; Snyder, S. H. Nitric oxide mediates neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. USA 88:6368-6371; 1991.
3. 3. Snyder, S. H. Nitric oxide: First in a new class of neurotransmitters? Science 257:494-496; 1993.
4. 4. Matheis, G.; Sherman, M. P.; Buckberg, G. D.; Haybron, D. M.; Young, H. H.; Ignarro, L. J. Role of L-arginine-nitric oxide pathway in myocardial reoxygenation injury. Am. J. Physiol. 262:H616-H620; 1992.
5. 5. Lopez-Belmonte, J.; Whittle, B. J. R.; Moncada, S. The actions of nitric oxide donors in the prevention or induction of injury to the rat gastric mucosa. Br. J. Pharmacol. 108:73; 1993.
6. 6. Mulligan, M. S.; Hevel, J. M.; Marletta, M. A.; Ward, P. A. Tissue injury caused by deposition of immune complexes is L-arginine-dependent. Proc. Natl. Acad. Sci. USA 88:6338-6342; 1991.
7. 7. Mulligan, M. S.; Warren, J. S.; Smith, C. W.; Anderson, D. C.; Yeh, C. G.; Rudolph, A. R.; Ward, P. A. Lung injury after deposition of IgA immune complexes: Requirement for CD18 and L-arginine. J. Immunol. 148:3086-3092; 1992.
8. 8. Hibbs, J. B., Jr.; Taintor, R. R.; Vavrin, Z.; Granger, D. L.; Drapier, J. C.; Amber, I. J.; Lancaster, J. R., Jr. Synthesis of nitric oxide from terminal guanidino nitrogen atom of L-arginine: A molecular mechanism regulating cellular proliferation that targets intracellular iron. In: S. Moncada, S.; Higgs, E. A., eds. Nitric oxide from L-arginine: A bioregulatory system. Amsterdam: Elsevier; 1990:189-223.
9. 9. Cleeter, M. W. J.; Cooper, J. M.; Darley-Usmar, V. M.; Moncada, S.; Schapira, A. H. V. Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett. 345:50-54; 1994.
10. 10. Lepoivre, M.; Flaman, J-M.; Bobé, P.; Lemaire, G.; Henry, Y. Quenching of the tyrosyl free radical of ribonucleotide reductase by nitric oxide: Relationship to cytostasis induced in tumor cells by macrophages. J. Biol. Chem. 269:21891-21897; 1994.
11. 11. Kwon, N. S.; Stuehr, D. H.; Nathan, C. F. Inhibition of tumor cell ribonucleotide reductase by macrophage-derived nitric oxide. J. Exp. Med. 174:761-767; 1991.
12. 12. Curran, R. D.; Ferrari, F. K.; Kispert, P. H.; Stadler, J.; Stuehr, D. H.; Simmons, R. L.; Billiar, T. R. Nitric oxide and nitric oxide-generating compounds inhibit hepatocyte protein synthesis. FASEB J. 5:2085-2092; 1991.
13. 13. Kubes, P.; Granger, D. N. Nitric oxide modulates microvascular permeability. Am. J. Physiol. 263:H611-615; 1992.
14. 14. Wink, D. A.; Osawa, Y.; Darbyshire, J.; Jones, C. R.; Eshenaur, S.; Nims, R. W. Inhibition of cytochromes P450 by nitric oxide and a nitric oxide-releasing agent. Arch. Biochem. Biophys. 300:115-123; 1993.
15. 15. Fukahori, M.; Ichimori, K.; Ishida, H.; Nakagawa, H.; Okino, H. Nitric oxide reversibly supresses xanthine oxidase activity. Free Radic. Res. 21:203-212; 1994.
16. 16. Knowles, R. G.; Moncada, S. Nitric oxide as a signal in blood vessels. Trends Biochem. Sci. 17:399-402; 1993.
17. -. Free Radic. Res. Commun. 18:195-199; 1993.
18. 18. Beckman, J. S.; Beckman, T. W.; Chen, J.; Marshall, P. A.; Freeman, B. A. Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury by nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA 87:1620-1624; 1990.
19. 19. Radi, R.; Beckman, J. S.; Bush, K. M.; Freeman, B. A. Peroxynitrite-induced membrane lipid peroxidation: The cytotoxic potential of superoxide and nitric oxide. Arch. Biochem. Biophys. 288:481-487; 1991.
20. 20. Koppenol, W. H.; Moreno, J. J.; Pryor, W. A.; Ischiropoulos, H.; Beckman, J. S. Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. Chem. Res. Toxicol. 5:834-840; 1992.
21. 21. Radi, R.; Beckman, J. S.; Freeman, B. A. Peroxynitrite oxidation of sulhydryls: The cytotoxic potential of endothelial-derived superoxide and nitric oxide. J. Biol. Chem. 266:4244-4250; 1991.
22. 22. Rubbo, H.; Radi, R.; Trujillo, M.; Telleri, R.; Kalyanaraman, B.; Barnes, S.; Kirk, M.; Freeman, B. A. Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation: Formation of novel nitrogen-containing oxidized lipid derivatives. J. Biol. Chem. 269:26066-26075; 1994.
23. 23. Ischiropoulos, H.; Zhu, L.; Chen, J.; Tsai, M.; Martin, J.; Smith, C.; Beckman, J. S. Peroxynitrite-mediated nitration of tyrosine catalized by superoxide dismutase. Arch. Biochem. Biophys. 298:431-437; 1992.
24. 24. Beckman, J. S.; Chen, J.; Ischiropoulos, H.; Crow, J. P. Oxidative chemistry of peroxynitrite. Methods Enzymol. 233:229-240; 1994.
25. 25. White, R.; Brock, T.; Chang, L.; Crapo, J.; Briscoe, P.; Ku, D.; Bradley, W.; Gianturco, S.; Gore, J.; Freeman, B. A.; Tarpey, M. M. Superoxide and peroxynitrite in atherosclerosis. Proc. Natl. Acad. Sci. USA 91:1044-1048; 1994.
26. 26. Beckman, J. S.; Ye, Y. Z.; Anderson, P. G.; Chen, J.; Accavitti, M. A.; Tarpey, M. M.; White, R. Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistry. Biol. Chem. Hoppe-Seyler 375:81-88; 1994.
27. 27. Haddad, I.; Pataki, G.; Hu, P.; Galliani, C.; Beckman, J. S.; Matalon, S. Quantitation of nitrotyrosine levels in lung sections of patients and animals with acute lung injury. J. Clin. Invest. 94:2407-2413; 1994.
28. 28. Kooy, N. W.; Royall, J. A.; Ye, Y. Z.; Beckman, J. S. Peroxynitrite is produced during human adult respiratory distress syndrome. Am. J. Respir. Crit. Care Med. 151:1250-1254; 1995.
29. 29. Yamamoto, S.; Golanov, E. V.; Berger S. B.; Reis, D. J. Inhibition of nitric oxide synthesis increases focal ischemic infarction in rat. J. Cereb. Blood Flow Metab. 12:717-726; 1992.
30. 30. Wink, D. A.; Hanbauer, I.; Krishna, M. C.; DeGraff, W.; Gamson, J.; Mitchell, J. B. Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc. Natl. Acad. Sci. USA 90:9813-9817; 1993.
31. 31. Kuluz, J. W.; Prado, R. J.; Dietrich, D.; Schleien, C. L.; Watson, B. D. The effect of nitric oxide synthase inhibition on infarct volume after reversible focal cerebral ischemia in conscious rats. Stroke 24:2023-2029; 1993.
32. 32. Bautista, A. P.; Spitzer, J. J. Inhibition of nitric oxide formation in vivo enhances superoxide release by the perfused liver. Am. J. Physiol. 266:G783-G788; 1994.
33. 33. Payne, D.; Kubes, P. Nitric oxide donors reduce the rise in reperfusion-induced intestinal mucosa permeability. Am. J. Physiol. 265:G189-G195; 1993.
34. 34. László, F.; Whittle, B. J. R. Constitutive nitric oxide modulates the injurious actions of vasopressin on rat intestinal microcirculation in acute endotoxaemia. Eur. J. Pharmacol. 260:265-268; 1994.
35. 35. Shultz, P. J.; Raij, L. Endogenously synthesized nitric oxide prevents endotoxin-induced glomerular thrombosis. J. Clin. Invest. 90:1718-1725; 1992.
36. 36. Pinsky, D. J.; Naka, Y.; Chowdhury, N. C.; Liao, H.; Oz, M. C.; Michler, R. E.; Kubaszewiski, E.; Malinski, T.; Stern, D. M. The nitric oxide/cyclic GMP pathway in organ transplantation: Critical role in successful lung preservation. Proc. Natl. Acad. Sci. USA 91:12086-12090; 1994.
37. 37. Kavanagh, B. P.; Mouchawar, A.; Goldsmith, J.; Pearl, R. G. Effects of inhaled nitric oxide and inhibition of endogenous nitric oxide synthesis in oxidant-induced acute lung injury. J. Appl. Physiol. 76:1324-1329; 1994.
38. 38. Cooke, J. P.; Tsao, P. S. Cytoprotective effects of nitric oxide. Circulation 88:2451-2454; 1993.
39. 39. Siegfried, M. R.; Carey, C.; Ma, X.; Lefer, A. M. Beneficial effects of SPM-5185, a cysteine-containing nitric oxide donor in myocardial ischemia-reperfusion. Am. J. Physiol. 263:H771-H777; 1992.
40. 40. Clancy, R. M.; Leszcynska-Piziak, J.; Abramson, S. B. Nitric oxide, an endothelial cell relaxation factor, inhibits neutrophil superoxide anion production via a direct action on the NADPH oxidase. J. Clin. Invest. 90:1116-1121; 1992.
41. 41. Asano, K.; Chee, C. B. E.; Gaston, B.; Lilly, C. M.; Gerard, C.; Drazen, J. M.; Stamler, J. S. Constitutive and inducible nitric oxide synthase gene expression, regulation, and activity in human lung epithelial cells. Proc. Natl. Acad. Sci. USA 91:10089-10093; 1994.
42. 42. Robbins, R. A.; Barnes, P. J.; Springall, D. R.; Warren, J. B.; Kwon, O. J.; Buttery, L. D. K.; Wilson, A. J.; Geller, D. A.; Polak, J. M. Expression of inducible nitric oxide in human lung epithelial cells. Biochem. Biophys. Res. Commun. 203:209-218; 1994.
43. 43. Gutierrez, H. H.; Pitt, B. R.; Schwarz, M.; Watkins, S. C.; Lowenstein, C.; Caniggia, I.; Chumley, P.; Freeman, B. A. Pulmonary alveolar epithelial inducible nitric oxide synthase gene expression: Regulation by inflammatory mediators. Am. J. Physiol. 268:L501-L508; 1995.
44. 44. Dupuy, P. M.; Shore, S. A.; Drazen, J. M.; Frostell, C.; Hill, W. A.; Zapol, W. M. Bronchodilator action of inhaled nitric oxide in guinea-pigs. J. Clin. Invest. 90:421-428; 1992.
45. 45. Pepke-Zaba, J.; Higenbottan, T. W.; Dinh-Xuan, A. T.; Stone, D.; Wallwork, J. Inhaled nitric oxide as a cause of selective pulmonary vasodilatation in pulmonary hypertension. Lancet 338:1173-1174; 1991.
46. 46. Belvisi, M. G.; Stretton, C. D.; Yacoub, M.; Barnes, P. J. Nitric oxide is the endogenous neurotranmitter of bronchodilator nerves in human airways in guinea-pig airways. Eur. J. Pharmacol. 210:221-222; 1992.
47. 47. Heiss, L. N.; Lancaster, J. R.; Corbett, J. A.; Goldman, W. E. Epithelial autotoxicity of nitric oxide: Role in the respiratory cytopathology of pertussis. Proc. Natl. Acad. Sci. USA 91:267-270; 1994.
48. 48. Punjabi, C. J.; Laskin, J. D.; Pendino, K. J.; Goller, N. L.; Durham, S. K.; Laskin, D. L. Production of nitric oxide by rat type II penumocytes: Increased expression of inducible nitric oxide synthase following inhalation of a pulmonary irritant. Am. J. Respir. Cell Mol. Biol. 11:165-172; 1994.
49. 49. Berisha, H. I.; Pakbaz, H.; Absood, A.; Said, S. I. Nitric oxide as a mediator of oxidant lung injury due to paraquat. Proc. Natl. Acad. Sci. USA 91:7445-7449; 1994.
50. 125Icontaining acylating agents. Biochem. J. 133:529-539; 1973.
51. 51. Stamler, J. S.; Loscalzo, J. Capillary zone electrophoretic detection of biological thiols and their S-nitrosated derivatives. Anal. Chem. 64:779-785; 1992.
52. 14N] nitrite in biological fluids. Anal. Biochem. 126:131-138; 1982.
53. 53. Kooy, N. W.; Royall, J. A.; Ischiropoulos, H.; Beckman, J. S. Peroxynitrite-mediated oxidation of dihydrorhodamine 123. Free Radic. Biol. Med. 16:149-156; 1994.
54. 54. Caniggia, I.; Tseu, I.; Han, R. N.; Smith, B. T.; Tanswell, A. K.; Post, M. Spatial and temporal differences in fibroblast behavior in fetal rat lung. Am. J. Physiol. 261:L424-L433; 1991.
55. 55. Folz, R. J.; Crapo, J. D. Pulmonary oxygen toxicity. Curr. Pulmonol. 15:113-136; 1994.
56. 56. Haddad, I. Y.; Crow, J. P.; Hu, P.; Ye, Y.; Beckman, J. S.; Matalon, S. Concurrent generation of nitric oxide and superoxide damages surfactant protein A. Am. J. Physiol. 267:L242-L249; 1994.
57. 57. Nathan, C.; Xie, Q.-W. Regulation of biosynthesis of nitric oxide. J. Biol. Chem. 269:13725-13728; 1994.
58. 58. Felley-Bosco, E.; Ambs, S.; Lowenstein, C. J.; Keefer, L. K.; Harris, C. C. Constitutive expression of inducible nitric oxide synthase in human bronchial epithelial cells induces c-fos and stimulates the cGMP pathway. Am. J. Respir. Cell Mol. Biol. 11:159-164; 1994.
59. 59. Kobzik, L.; Bredt, D. S.; Lowenstein, C. J.; Drazen, J.; Gaston, B.; Sugarbaker, D.; Stamler, J. S. Nitric oxide synthase in human and rat lung: Immunocytochemical and histochemical localization. Am. J. Respir. Cell Mol. Biol. 9:371-377; 1993.
60. 60. Repine, J. E. Scientific perspectives on adult respiratory distress syndrome. Lancet 339:466-469; 1992.
61. 61. Freeman, B. A.; Crapo, J. D. Hyperoxia increases oxygen radical production in rat lungs and lung mitochondria. J. Biol. Chem. 256:10986-10992; 1981.
62. 62. Turrens, J. F.; Freeman, B. A.; Crapo, J. D. Hyperoxia increases H2O2 release by lung mitochondria and microsomes. Arch. Biochem. Biophys. 217:411-421; 1982.
63. 63. Kennedy, T. P.; Rao, N. V.; Hopkins, C.; Pennington, L.; Tolley, E.; Hoidal, J. R. Role of reactive oxygen species in reperfusion injury of the rabbit lung. J. Clin. Invest. 83:1326-1335; 1989.
64. 64. Ignarro, L. J. Biosynthesis and metabolism of endothelium-derived nitric oxide. Annu. Rev. Pharmacol. Toxicol. 30:335-360; 1990.
65. 65. Reddy, D.; Lancaster, J.; Comforth, D. P. Nitrite inhibition of Clostridium botulinum: Electron spin resonance detection of iron-nitric complexes. Science 221:769-770; 1983.
66. 66. Kanner, J.; Harel, S.; Granit, R. Nitric oxide as an antioxidant. Arch. Biochem. Biophys. 289:130-136; 1991.
67. 67. Rubbo, H.; Parthasarathy, S.; Kalyanaraman, B.; Barnes, S.; Kirk, M.; Freeman, B. A. Nitric oxide inhibition of lipoxygenase-dependent liposome and low density lipoprotein oxidation: Formation of novel nitrogen-containing oxidized lipid derivatives. Arch. Biochem. Biophys. 3(24):15-25; 1995.
68. 68. Reif, D. W.; Simmons, R. D. Nitric oxide mediates iron release from ferritin. Arch. Biochem. Biophys. 283:537-541; 1990.
69. 69. Radomski, M. W.; Palmer, R. M. J.; Moncada, S. Endogenous nitric oxide inhibits human platelet adhesion to vascular endothelium. Lancet 2:1057-1058; 1987.
70. 70. Kubes, P.; Suzuki, M.; Granger, D. M. Nitric oxide: An endogenous modulator of leukocyte adhesion. Proc. Natl. Acad. Sci. USA 88:4651-4655; 1991.
71. 71. Kurose, I.; Wolf, R.; Grisham, M. B.; Granger, D. N. Modulation of ischemia-reperfusion-induced microvascular dysfunction by nitric oxide. Circ. Res. 74:376-382; 1994.
72. 72. Lefer, D. J.; Nakanishi, K.; Johnston, W. E.; Vinten-Johansen, J. Anti-neutrophil and myocardial protecting actions of a novel nitric oxide donor following acute myocardial ischemia and reperfusion. Circulation 88:2337-2350; 1993.
73. 73. Gaston, B.; Drazen, J. M.; Loscalzo, J.; Stamler, J. S. The biology of nitrogen oxides in the airways. Am. J. Respir. Crit. Care Med. 149:538-551; 1994.
74. 74. Rubbo, H.; Denicola, A.; Radi, R. Peroxynitrite inactivates thiolcontaining enzymes of T. cruzi oxidative metabolism and inhibits cell respiration. Arch. Biochem. Biophys. 308:96-102; 1994.
75. 75. Chumley, P.; Rubbo, H.; Gutierrez, H. H.; Freeman, B. A. Nitric oxide regulation of superoxide, hydrogen peroxide and peroxynitrite-dependent injury to vascular endothelium. Free Radic. Biol. Med. (submitted).
76. 76. Klug, D.; Rabani, J.; Fridovich, I. A direct demonstration of the catalytic action of superoxide dismutase through the use of pulse radiolysis. J. Biol. Chem. 247:4839-4842; 1972.