Nitric Oxide Regulation of Membrane and Lipoprotein Oxidation in the Vasculature

A Radical Hypothesis
  • Bruce A. Freeman
  • Jason Eiserich
  • Valerie O’Donnell
Chapter
Part of the NATO ASI Series book series (NSSA, volume 296)

Abstract

Nitric oxide (·NO, nitrogen monoxide) exerts potent actions in the regulation of cell function and tissue viability that extend far beyond the recognized ability of ·NO to mediate signal transduction via activation of guanylate cyclase. Chemical reactions, cell culture systems, animal models and clinical studies have all revealed an ability of ·NO to modulate oxygen radical reactions and pathologic processes associated with inflammation. The focus of this article is to reveal the reactions of ·NO with reactive oxygen species and lipid radicals (LO· and LOO·) formed during membrane and lipoprotein oxidation. The products of these reactions, LONO/LNO2 and LOONO/LONO2 adducts, are potentially reactive and can serve as mediators of inflammation and tissue injury. Because of the high reactivity of ·NO with lipophilic radicals and the interactions that ·NO can have with lipophilic antioxidants, the reactions of ·NO with membrane and lipoprotein oxidant defense mechanisms will be explored as well.

Keywords

Nitric Oxide NADPH Oxidase Xanthine Oxidase Guanylate Cyclase Lipoprotein Oxidation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abrahamsson, T., Brandt, U., Marklund, S. L., and Sjoqvist, P. O., 1992, Vascular bound recombinant extracellular superoxide dismutase type C protects against the detrimental effects of superoxide radicals on endothelium-dependent arterial relaxation. Circ. Res. 70: 264–271.CrossRefGoogle Scholar
  2. Albina, J. E., and Reichner, J. S.,1995, Nitric oxide in inflammation and immunity. New Horizons 3: 46–64.Google Scholar
  3. Alvarez, B., Rubbo, H., Kirk, M., Barnes, S., Freeman, B. A., and Radi, R., 1996, Peroxynitrite-dependent tryptophan nitration. Chem. Res. Toxicol. 9: 390–396.CrossRefGoogle Scholar
  4. Amelle, D. R., and Stamler, J. S., 1995, NO’, NO. and NO- donation by S-Nitrosothiols: Implications for regulation of physiological functions by S-nitrosylation and acceleration of disulfide formation. Arch. Biochem. Biophys. 318: 279–285.CrossRefGoogle Scholar
  5. Beckman, J. S., Beckman, T. W., Chen, J., Marshall, P. A., and Freeman, B. A., 1990, Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. 87: 1620–1624.CrossRefGoogle Scholar
  6. Beckman, J. S., Ischiropoulos, H., Zhu, L., van der Woerd, M., Smith, C. D., Chen, J D., Harrison, J., Martin, J. C., and Tsai, M., 1992, Kinetics of SOD and iron catalyzed nitration of phenolics by peroxynitrite. Arch. Biochem. Biophys. 298: 438–445.CrossRefGoogle Scholar
  7. Beckman, J. S., Minor, R. L., White, C. W., Rosen, G. M., Repine, J. R., and Freeman, B. A., 1988, Superoxide dismutase and catalase conjugated to polyethylene glycol increases endothelial enzyme activity and oxidant resistance. J. Biol. Chem. 263: 6884–6892.Google Scholar
  8. Beckman, J. S., Ye, Y., Anderson, P. G., Chen, J., Accavitti, M. A., Tarpey, M. M., and White, R., 1994, Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistry. Biol. Chem. Hoppe-Seyler. 375: 81–88.CrossRefGoogle Scholar
  9. Bredt, D. S., Hwang, P. M., Glass, C. E., Lowenstein, C., Reed, R. R., and Snyder, S. H., 1991, Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 351: 714–718.CrossRefGoogle Scholar
  10. Brieland, J. K., Clarke, S. J., Karmil, S., Phan, S. H., and Fantone, J. C., 1992, Transferrin: A potential source of iron for oxygen free radical-mediated endothelial cell injury. Arch. Biochem. Biophys. 294: 265–270.CrossRefGoogle Scholar
  11. Buckley, B. J., Tanswell, A. K., and Freeman, B. A., 1987, Liposome mediated augmentation of catalase in type II alveolar epithelial cells protects against hydrogen peroxide injury. J. Appl. Physiol. 63: 359–367.Google Scholar
  12. Castro, L., Rodriguez, M., and Radi, R., 1994, Aconitase is readily inactivated by peroxynitrite, but not by its pre-Google Scholar
  13. cursor, nitric oxide. J. Biol. Chem. 269: 29409–29415.Google Scholar
  14. Christen, S., Woodall, A. A., Shigenaga, M. K., Southwell-Keely, P. T., Duncan, M. W., and Ames, B. N., g-Tocopherol traps mutagenic electrophiles such as NOx and complements a-tocopherol: physiological implications. Proc. Natl. Acad. Sci. USA (In Press).Google Scholar
  15. Clancy, R. M., Leszczynska-Piziak, J., and Abramson, S. B., 1992, 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.CrossRefGoogle Scholar
  16. Cooke, J. P., Singer, A. H., Tsao, P., Zera, P., Rowan, R., and Billingham, M. E., 1992, Antiatherogenic effects of L-arginine in the hypercholesterolemic rabbit. J. Clin. Invest. 90: 1168–1172.CrossRefGoogle Scholar
  17. Curran, R. D., Ferrari, F. K., Kispert, P. H., Stadler, J., Stuehr, D. H., Simmons, R. L., and Billiar, T. R., 1991, Nitric oxide and nitric oxide-generating compounds inhibit hepatocyte protein synthesis. FASEB J. 5: 2085–2092.Google Scholar
  18. Daugherty, A., Dunn, J. L., Rateri, D. L., and Heinecke, J., 1994, Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions. J. Clin. Invest. 94: 437–444.CrossRefGoogle Scholar
  19. Day, B. J., and Crapo, J. D., 1996, A metalloporphyrin superoxide dismutase mimetic protects against paraquat-induced lung injury in vivo. Toxicol. Appl. Pharmacol. 140: 94–100.CrossRefGoogle Scholar
  20. De Caterina, R., Libby, P., Peng, H., Thannickal, V., Rajavashisth, T., Gimbrone, M. A., Shin, W., and Liao, J. K., 1995, Nitric oxide decreases cytokine-induced endothelial activation: Nitric oxide selectively reduces endothelial expression of adhesion molecules and proinflammatory cytokines. J. Clin. Invest. 96: 60–68.CrossRefGoogle Scholar
  21. Denicola, A., Freeman, B. A., Trujillo, M., and Radi, R., 1996, Peroxynitrite reaction with carbon dixide/bicarbonate: kinetics and influence on peroxynitrite-mediated oxidations. Arch. Biochem. Biophys. 333: 49–58. Appendix JGoogle Scholar
  22. Eiserich, J. P., Cross, C. E., Jones, A. D., Halliwell, B., and Van der Vliet, A., 1996, Formation of nitrating and chlorinating species by reaction of nitrite with hypochlorous acid: a novel mechanism for nitric oxide-mediated protein modification. J. Biol. Chem. 271: 19199–19208. Appendix GGoogle Scholar
  23. Eiserich, J. P., Hristova, M., Cross, C. E., Jones, A. D., Halliwell, B., and van der Vliet, A., Neutrophil-mediated conversion of nitrite into the nitrating and chlorinating inflammatory oxidant NO2CI. Nature (Submitted, 1997 ).Google Scholar
  24. Faulkner, K. M., Liochev, S.I., and Fridovich, I., 1994, Stable Mn(III) porphyrins mimic superoxide dismutase in vitro and substitute for it in vivo. J. Biol. Chem. 269: 23471–23476.Google Scholar
  25. Flavahan, N. A., 1992, Atherosclerosis or lipoprotein-induced endothelial dysfunction. Potential mechanisms underlying reduction in EDRF/nitric oxide activity. Circulation 85: 1927–1938.CrossRefGoogle Scholar
  26. Forstermann, U., Pollock, J. S., Schmidt, H. H. H. W., Heller, M., and Murad, F., 1991, Calmodulin-dependent endothelium-derived relaxing factor/nitric oxide synthase activity is present in the particulate and cytosolic fractions of bovine aortic endothelial cells. Proc. Natl. Acad. Sci. USA 88: 1788–1792.CrossRefGoogle Scholar
  27. Freeman, B. A., and Crapo, J. D., 1981, Hyperoxia increases oxygen radical production in rat lungs and lung mitochondria. J. Biol. Chem. 256: 10986–10992.Google Scholar
  28. Freeman, B. A., and Crapo, J. D., 1982, Biology of disease: Free radicals and tissue injury. Lab. Invest. 47: 412–426.Google Scholar
  29. Freeman, B. A., Young, S. L., and Crapo, J. D., 1983, Liposome-mediated augmentation of superoxide dismutase in endothelial cells prevents oxygen injury. J. Biol. Chem. 258: 12534–12542.Google Scholar
  30. Fujita, H., Morita, I., and Murota, S., 1994, A possible mechanism for vascular endothelial cell injury elicited by activated leukocytes: A significant involvement of adhesion molecules, CD11/CDI8 and ICAM-1. Arch. Biochem. Biophys. 309: 62–69.CrossRefGoogle Scholar
  31. Fukuto, J. M., Chiang, K., Hszieh, R., Wong, P., and Chaudhur, G., 1992, The pharmacological activity of nitroxyl: A potent vasodilator with activity similar to nitric oxide and/or endothelium-derived relaxing factor. J. Pharmacol. Exp. Ther. 263: 546–551.Google Scholar
  32. Furchgott, R. F. and Zawadski, J.B., 1980, The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288: 373–376.CrossRefGoogle Scholar
  33. Gergel, D., Misik, V., Ondrias, K., and Cederbaum, A., 1995, Increased cytotoxicity of 3-morpholinosydnonimine to HepG2 cells in the presence of superoxide dismutase. J. Biol. Chem. 270: 20922–20929.CrossRefGoogle Scholar
  34. Gow, A. J., Duran, D., Malcolm, S., and Ischiropoulos, H., 1996, Effects of peroxynitrite-induced protein modifications on tyrosine phosphorylation and degradation.-FEBS Lett. 385: 63–66.CrossRefGoogle Scholar
  35. Green, S. J., Mellouk, S., Hoffman, S. L., Meltzer, M. S., and Nacy, C. A., 1990, Cellular mechanisms of nonspecific immunity to intracellular infection: cytokine-induced synthesis of toxic nitrogen oxides from L-arginine by macrophages and hepatocytes. Immunol. Lett. 25: 15–20.CrossRefGoogle Scholar
  36. Groves, J. T., and Marla, S. S., 1995, Peroxynitrite-induced DNA strand scission mediated by a manganese porphyrin. J. Am. Chem. Soc. 117: 9578–9579.CrossRefGoogle Scholar
  37. Gutierrez, H. H., Chumley, P., Rivera, A.,and Freeman, B. A., 1996, Nitric oxide regulation of superoxide-dependent lung cell injury: oxidant-protective actions of endogenously produced and exogenously administered nitric oxide. Free. Rad. Biol. Med. 21: 43–52.Google Scholar
  38. Hausladen, A. and Fridovich, I., 1994, Superoxide and peroxynitrite inactivate aconitases, but nitric oxide does not. J. Biol. Chem. 269: 29405–29408.Google Scholar
  39. Hazell, L. J., Arnold, L., Flowers, D., Waeg, G., Malle, E., and Stocker, R., 1996, Presence of hypochlorite-modifled proteins in human atherosclerotic lesions. J. Clin. Invest. 97: 1535–1544.CrossRefGoogle Scholar
  40. Hibbs, Jr. J. B.,Taintor, R. R., Vavrin, Z., and Rachlin, E. M., 1988, Nitric oxide: A cytotoxic activated macrophage effector molecule. Biochem. Biophys. Res. Commun. 157: 87–94.CrossRefGoogle Scholar
  41. Hori, H., Masuya, F., Tsubaki, M., Yoshikawa, S., and Ichikawa, Y., 1992, Electronic and stereochemical characterizations of intermediates in the photolysis of ferric cytochrome P450 nitrosyl complexes. J. Biol. Chem. 267: 18377–18381.Google Scholar
  42. Huie, R. E., and Padmaja, S., 1993, Reaction of NO with OZ-. Free Rad. Res. Comm. 18: 195–199.CrossRefGoogle Scholar
  43. Ignarro, L.J., 1992, Haem-dependent activation of cytosolic guanylate cyclase by nitric oxide: a widespread signal transduction mechanism. Biochem. Soc. Transactions. 20: 465–469.Google Scholar
  44. Inoue, M., Watanabe, N., Morino, Y, Tanaka, Y., Amachi, T., and Sasaki, J., 1990, Inhibition of oxygen toxicity by targeting superoxide dismutase to endothelial cell surface. FEBS Lett. 269: 89–92.CrossRefGoogle Scholar
  45. Ischiropoulos, H., Zhu, L., Chen, J., Tsai, M., Martin, J., Smith, C., and Beckman, J. S., 1992, Peroxynitrite-mediated nitration of tyrosine catalyzed by superoxide dismutase. Arch. Biochem. Biophys. 298: 431–437.CrossRefGoogle Scholar
  46. Kanner, J., Harel, S., and Granit, R., 1991, Nitric oxide as an antioxidant. Arch. Biochem. Biophys. 289: 130–136.CrossRefGoogle Scholar
  47. Karoui, H., Hogg, N., Frejaville, C., Tordo, P., and Kalyanaraman, B., 1996, Characterization of sulfur-centered radical intermediates formed during the oxidation of thiols and sulfite by peroxynitrite. J. Biol. Chem. 271: 6000–6009.CrossRefGoogle Scholar
  48. Khan, B. V., Harrison, D. G., Olbrych, M. T., Alexander, R. W., and Medford, R. M., 1996, Nitric oxide regulates vascular cell adhesion molecule 1 gene expression and redox-sensitive transcriptional events in human vascular endothelial cells. Proc. Natl. Acad. Sci. USA 93: 9114–9119.CrossRefGoogle Scholar
  49. Knudsen, M. A., Svane, D., and Tottrup, A., 1992, Action profiles of nitric oxide, S-nitroso-L-cysteine, SNP, and NANC responses in opossum lower esophageal sphincter. Am. J. Physiol. 262: G840–846.Google Scholar
  50. Kubes, P., Suzuki, M.,and Granger, D. N., 1991, Nitric oxide: An endogenous modulator of leukocyte adhesion.Google Scholar
  51. Proc. Natl. Acad. Sci. USA 88: 4651–4655.Google Scholar
  52. Kurose, I., Wolf, R., Grisham, M. B., and Granger, D. N., 1994, Modulation of ischemialreperfusion-induced microvascular dysfunction by nitric oxide. Circ. Res. 74: 376–382.CrossRefGoogle Scholar
  53. Kwon, N. S., Stuehr, D. H., and Nathan, C. F., 1991, Inhibition of tumor cell ribonucleotide reductase by macrophage-derived nitric oxide. J. Exp. Med. 174: 761–767.CrossRefGoogle Scholar
  54. Lampert, M. B., and Weiss. S. J., 1983, The chlorinating potential of the human monocyte. Blood 62: 645–651.Google Scholar
  55. Lancaster, J. R., 1992, Nitric oxide in cells: This simple molecule plays Janus-faced roles in the body, acting as both messenger and destroyer. Am. Sci. 80: 248–259.Google Scholar
  56. Lancaster, J. R., and Hibbs, J. B. Jr., 1990, EPR demonstration of iron-nitrosyl complex formation by cytotoxic activated macrophages. Proc. Natl. Acad. Sci. USA 87: 1223–1227.CrossRefGoogle Scholar
  57. Laskey, R. E., and Mathews, W. R., 1996, Nitric oxide inhibits peroxynitrite-induced production of hydroxyeicosatetraenoic acids and F2-isoprostanes in phosphatidylcholine liposomes. Arch. Biochem. Biophys. 330: 193–198.CrossRefGoogle Scholar
  58. Laursen, J. B., Rajagopalan, S.,Tarpey, M., Freeman, B. A., and Harrison, D. G., 1997, A role of superoxide in angiotension II-but not catecholamine-induced hypertension. Circulation 95: 588–593.Google Scholar
  59. Leeuwenburgh, C., Hardy, M. M., Hazen, S. L., Wagner, P., Oh-ishi, S., Steinbrecher, U. P., and Heinecke, J. W., 1997, Reactive nitrogen intermediates promote low density lipoprotein oxidation in human atherosclerotic intima. J. Biol. Chem. 272: 1433–1436.CrossRefGoogle Scholar
  60. Lefer, D. J., Nakanishi, K., and Vinten-Johansen, J., 1993, Endothelial and myocardial cell protection by a cysteine-containing nitric oxide donor after myocardial ischemia and reperfusion. J. Cardiovasc. Pharmacol. 22 (Suppl. 7): S34 S43.Google Scholar
  61. Lefer, D. J., Scalia, R., Campbell, B., Nossuli, T., Hayward, R., Salamon, M., Grayson, J., and Lefer, A. M., 1997, Peroxynitrite inhibits leukocyte-endothelial cell interactions and protects against ischemia-reperfusion injury in rats. J. Clin. Invest. 99: 684–691.CrossRefGoogle Scholar
  62. Lepoivre, M., Flaman, J. M., and Henry, Y., 1992, Early loss of the tyrosyl radical in ribonucleotide reductase of adenocarcinoma cells producing nitric oxide. J. Biol. Chem. 267: 22994–23000.Google Scholar
  63. Liu, T. H., Beckman, J. S., Freeman, B. A., Hogan, E. L., and Hsu, C. Y., 1989, Polyethylene glycol-conjugated superoxide dismutase and catalase reduce ischemic brain injury. Am. J. Physiol. 260: H589–593.Google Scholar
  64. Lowenstein, C. J., Glass, C. S., Bredt, D. S., and Snyder, S H., 1992, Cloned and expressed macrophage nitric oxide synthase contrasts with the brain enzyme. Proc. Natl. Acad. Sci. USA 89: 6711–6715.CrossRefGoogle Scholar
  65. Maragos, C. M., 1991, Complexes of nitric oxide with nucleophiles as agents for the controlled biological release of nitric oxide. J. Med. Chem. 34: 3242–3247.CrossRefGoogle Scholar
  66. Marklund, S., 1992, Regulation of cytokines of extracellular superoxide dismutase and other superoxide dismutase isoenzymes in fibroblasts. J. Biol. Chem. 267: 6696–6701.Google Scholar
  67. Marsden, P. A., Schappert, K. T., Chen, H. S., Flowers, M., Sundell, C. L., Wilcox, J. N., Lamas, S.,and Michel, T., 1992, Molecular cloning and characterization of human endothelial nitric oxide synthase. FEBS Lett. 307: 287–293.Google Scholar
  68. Mami, N., Offermann, M., Swerlick, R., Kunsch, C., Ahmad, M., Alexander, R., and Medford, R. M., 1993, VCAM-1 gene transcription and expression are regulated through an antioxidant-sensitive mechanism in human vascular endothelial cells. J. Clin. Invest. 92: 1866–1874.CrossRefGoogle Scholar
  69. Matthews, J. R., Botting, C. H., Panico, M., Morris, H. R., and Hay, R. T., 1996, Inhibition of NF-kB DNA binding by nitric oxide. Nucleic Acids Research 24: 2236–2242.CrossRefGoogle Scholar
  70. McAdams, M., Vickers, S., and Freeman, B. A., A specific receptor for xanthine oxidase on vascular endothelium. FEBS Lett. (submitted).Google Scholar
  71. Miles, A. M., Bohle, D. S., Glassbrenner, P. A., Hansert, B., Wink, D. A., and Grisham, M. B., 1996, Modulation of superoxide-dependent oxidation and hydroxylation reactions by nitric oxide. J. Biol. Chem. 271: 40–47.CrossRefGoogle Scholar
  72. Miller, R. A., and Britigan,.B. E., 1995. The formation and biologic significance of phagocyte-derived oxidants. J. Invest. Med. 43: 39–49.Google Scholar
  73. Mittal, C. K., and Murad, F., 1977, Activation of guanylate cyclase by superoxide dismutase and hydroxyl radical: A physiological regulator of guanosine 3’,5’-monophosphate formation. Proc. Natl. Acad. Sci. USA 74: 4360–4364.CrossRefGoogle Scholar
  74. Moncada, S., and Higgs, E. A., 1991, Endogenous nitric oxide: physiology, pathology and clinical relevance. Eur. J. Clin. Inv. 21: 361–374.CrossRefGoogle Scholar
  75. Mohazzab, K. M., Kaminski, P. M., and Wolin,.M. S., 1995, NADH oxidoreductase is a major source of superoxide anion in bovine coronary artery endothelium. Am. J. Physiol. 266, H2568 - H2572.Google Scholar
  76. Munoz-Fernandez, M. A., Fernandez, M A.,and Fresno,.M, 1992, Synergism between tumor necrosis factor-a and interferon-g on macrophage activation for the killing of intracellular Trypanosoma cruzi through a nitric oxide-dependent mechanism. Eur. J. Immunol. 22: 301–307.Google Scholar
  77. Munzel, T., Sayegh, H., Freeman, B. A., Tarpey, M. M., and Harrison, D. G., 1995, Evidence for enhanced vascular superoxide anion production in nitrate tolerance: a novel mechanism underlying tolerance and cross tolerance. J. Clin. Invest. 95: 187–194.CrossRefGoogle Scholar
  78. Murphy, M. E., and Sies, H., 1991, Reversible conversion of nitroxyl anion to nitric oxide by superoxide dismutase. Proc. Natl. Acad. Sci. USA 88: 10860–10864.CrossRefGoogle Scholar
  79. Myers, R. R., Minor, R. L., Guerra, R., Bates, J. N., and Harrison, D. G., 1990, Vasorelaxant properties of the endothelial-derived relaxant factor more closely resemble S-nitrosocysteine than nitric oxide. Nature 365: 161–163.CrossRefGoogle Scholar
  80. Nakazono, K., Watanabe, N., Matsuno, K., Sasaki, J., Sato, T., and Inoue, M., 1991, Does superoxide underlie the pathogenesis of hypertension? Proc. Natl. Acad. Sci. USA 88: 10045–10048.CrossRefGoogle Scholar
  81. Nathan, C., 1992, Nitric oxide as a secretory product of mammalian cells. FASEB J. 6: 3051–3064.Google Scholar
  82. Niu, X. F., Ibbotson, G., and Kubes, P., 1996, A balance between nitric oxide and oxidants regulates mast cell-dependent neutrophil-endothelial cell interactions. Circ. Res. 79: 992–999.CrossRefGoogle Scholar
  83. Nussler, A., Drapier, J. C., Renia, L., Pied, S., Miltgen, F., Gentilini, M., and Mazier, D., 1991, L-arginine-dependent destruction of intrahepatic malaria parasites in response to tumor necrosis factor and/or interleukin-6 stimulation. Eur. J. Immunol. 21: 227–230.CrossRefGoogle Scholar
  84. Padgett, E. L., and Pruett, S. B., 1992, Evaluation of nitrite production by human monocyte-derived macrophages. Biochem. Biophys. Res. Commun. 186: 775–781.CrossRefGoogle Scholar
  85. Padmaja, S., and Huie, R. E., 1993, The reaction of nitric oxide with organic peroxyl radicals. Biochem. Biophys. Res.Comm. 195, 539–544.CrossRefGoogle Scholar
  86. Pagano, P., Ito, Y., Tornheim, K., Gallop, P., Tauber, A., and Cohen, R., 1995, An NADPH oxidase superoxide-generating system in the rabbit aorta. Am. J. Physiol. 268, H2274–2280.Google Scholar
  87. Palmer, R. M. J., Ferrige, A. G., and Moncada, S., 1987, Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327: 524–526.CrossRefGoogle Scholar
  88. Peng, H., Libby, P., and Liao, J. K., 1995, Induction and stabilization of IkB by nitric oxide mediates inhibition of NFkB. J. Biol. Chem. 270: 14214–14219.CrossRefGoogle Scholar
  89. Pfeiffer, S., Gorren, A. C. F., Schmidt, K., Werner, E. R., Hansert, B., Bohle, D. S., and Mayer, B., 1997, Metabolic fate of peroxynitrite in aqueous solution: reaction with nitric oxide and pH-dependent decomposition to nitrite and oxygen in a 2:1 stoichiometry. J. Biol. Chem. 272: 3465–3470.CrossRefGoogle Scholar
  90. Radi, R., Beckman, J. S., Bush, K. M., and Freeman, B. A., 1991a, Peroxynitrite oxidation of sulfhydryls: the cytotoxic potential of endothelial-derived superoxide and nitric oxide. J. Biol. Chem. 266: 4244–4250.Google Scholar
  91. Radi, R., Beckman, J. S., Bush, K. M., and Freeman, B. A., 1991b, Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch. Biochem. Biophys. 288: 481–487.CrossRefGoogle Scholar
  92. Radi, R., Cosgrove, T. P., Beckman, J. S., and Freeman, B. A., 1993, Peroxynitrite-induced luminol chemilumines-Google Scholar
  93. cence. Biochem. J. 290: 51–57.Google Scholar
  94. Reif, D. W., and Simmons,.R. D, 1990, Nitric oxide mediates iron release from ferritin. Arch. Biochem. Biophys. 283: 537–541.CrossRefGoogle Scholar
  95. Rubbo, H., Parthasarathy, S., Kalyanaraman, B., Barnes, S., Kirk, M., and Freeman, B. A., 1995, Nitric oxide inhibition of lipoxygenase-dependent liposome and low density lipoprotein oxidation: Termination of radical chain propagation reactions and formation of nitrogen-containing oxidized lipid derivatives. Arch. Biochem. Biophys. 324: 15–25.CrossRefGoogle Scholar
  96. Rubbo, H.; Radi, R., Trujillo, M., Telleri, R., Kalyanaraman, B., Barnes, S., Kirk M.,and Freeman, B. A., 1994, Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation: Formation of novel nitrogen-containing oxidized lipid derivatives. J. Biol. Chem. 269: 26066–26075.Google Scholar
  97. Schmidt, H., 1992, NO’, CO and ‘OH, endogenous guanylyl cyclase-activating factors. FEBS Lett 397: 102–107.CrossRefGoogle Scholar
  98. Schmidt, H. H. H. W., Hofmann, H., Schindler, U., Shutenko, Z. S., Cunningham, D. D., and Feelisch, M., 1996, No NO from NO synthase. Proc. Natl. Acad. Sci. USA 93: 14492–14497.CrossRefGoogle Scholar
  99. Sherman, M. P., Loro, M. L., Wong, V. Z., and Tashkin, D. P., 1991, Cytokine-and Pneumocystis carinii-induced L-arginine oxidation by murine and human pulmonary alveolar macrophages. J. Protozool. 38: 234S - 236S.Google Scholar
  100. Shigenaga, M. K., Lee, H., Blount, B., Christen, S., Shigeno, E. T., Yip, H., and Ames, B. N., Inflammation and NOR-induced nitration: assay for 3-nitrotyrosine by HPLC with electrochemical detection. Proc. Natl. Acad. Sci. USA (In Press).Google Scholar
  101. Siegfried, M. R., Carey, C., Ma, X.,and Lefer, A. M., 1992, Beneficial effects of SPM-5185, a cysteine-containing nitric oxide donor in myocardial ischemia-reperfusion. Am. J. Physiol. 263: H771–777.Google Scholar
  102. Stadler, J., Billiar, T. R., Curran, R. D., Stuehr, D. J., Ochoa, J. B., and Simmons, R. L., 1991, Effect of exogenous and endogenous nitric oxide on mitochondrial respiration of rat hepatocytes. Am. J. Physiol. 260: C910–916.Google Scholar
  103. Stamler, J. S., 1995, S-nitrosothiols and bioregulatory actions of nitrogen oxides through reactions with thiol groups. Cur. Top. Mic. Immunol. 196: 19–36.CrossRefGoogle Scholar
  104. Stamler, J. S., Jaraki, O., Osborne, J., Simon, D. I., Keaney, J., Vita, J., Single, D., Valeri, C. R., and Loscalzo, J., 1992a, Nitric oxide circulates in mammalian plasma primarily as an S-nitroso adduct of serum albumin. Proc. Natl. Acad. Sci. USA 89: 7674–7677.CrossRefGoogle Scholar
  105. Stamler, J. S., Simon, D. I., Osborne, J. A., Mullins, M. E., Jaraki, O., Michel, T., Singel, D. J., and Loscalzo, J., 1992b, S-nitrosylation of proteins with nitric oxide: Synthesis and characterization of biologically active compounds. Proc. Natl. Acad. Sci. USA 89: 444–448.CrossRefGoogle Scholar
  106. Stamler, J. S., Singel, D. J., Loscalzo, J., 1992c, Biochemistry of nitric oxide and its redox-activated forms. Science 258: 1898–1902.CrossRefGoogle Scholar
  107. Stuehr, D. J., and Marietta, M. A., 1985, Mammalian nitrate biosynthesis: Mouse macrophages produce nitrite and nitrate in response to Escherichia coli lipopolysaccharide. Proc. Natl. Acad. Sci. USA 82: 7738–7742.CrossRefGoogle Scholar
  108. Stuehr, D. J., and Nathan, C. F., 1989, Nitric oxide–a macrophage product responsible for cytostasis and respiratory inhibition in tumor target cells. J. Exp. Med. 169: 1543–1555.CrossRefGoogle Scholar
  109. Tamir, S., Lewis, R. S., de Rojas, W. T., Dean, W. M., Wishnok, J. S., and Tannenbaum, S. R., 1993, The influence of delivery rate on the chemistry and biological effects of nitric oxide. Chem. Res. Toxicol. 6: 895–899.CrossRefGoogle Scholar
  110. Tamura, Y., Chi, L., Driscoll, E. M. Jr., Hoff, P. T., Freeman, B. A., Gallagher, K. P., and Lucchesi, B. R., 1988, Superoxide dismutase conjugated to polyethylene glycol provides sustained protection against myocardial ischemia/reperfusion injury in the canine heart. Circ. Res. 63: 944–959.CrossRefGoogle Scholar
  111. Turrens, J. F., Crapo, J. D., and Freeman, B. A., 1984, Protection against oxygen toxicity by intravenous injection of liposome-entrapped catalase and superoxide dismutase. J. Clin. Invest. 73: 87–95.CrossRefGoogle Scholar
  112. Van der Vliet, A., Eiserich, J. P., O’Neill, C. A., Halliwell, B., and Cross, C. E., 1995, Tyrosine modification by reactive nitrogen species: a closer look. Arch. Biochem. Biophys. 319: 341–349.CrossRefGoogle Scholar
  113. Van der Vliet, A., JP Eiserich, J. P., B Halliwell, B., and CE Cross, C. E., 1997, Formation of reactive nitrogen species during peroxidase-catalyzed oxidation of nitrite: a potential additional mechanism of nitric oxide-dependent toxicity. J. Biol. Chem. 272: 7617–7625.CrossRefGoogle Scholar
  114. Vanin, A. F., 1991, Endothelium-derived relaxing factor is a nitrosyl iron complex with thiol ligands. FEBS Lett. 289: 1–3.CrossRefGoogle Scholar
  115. White, R., Darley-Usmar, V., McAdams, M., Berrington, W. R., Gore, J., Thomson, J. A., Parks, D. A., Tarpey, M. M., and Freeman, B. A., 1996, Circulating plasma xanthine oxidase contributes to vascular dysfunction in hypercholesterolemic rabbits. Proc. Natl. Acad. Sci. USA 93: 8745–8749.CrossRefGoogle Scholar
  116. White, K. A., and Marietta, M. A., 1992, Nitric oxide synthase is a P-450 type hemoprotein. Biochemistry 31: 6627–6631.CrossRefGoogle Scholar
  117. Wink, D. A., Cook, J., Krishna, M. C., Hanbauer, I., DeGraff, W., Gamson, J., and Mitchell, J. B., 1995, Nitric oxide protects against alkyl peroxide-mediated cytotoxicity: Further insight into the role nitric oxide plays in oxidative stress. Arch. Biochem. Biophys. 319: 402–407.CrossRefGoogle Scholar
  118. Wink, D. A, Cook, J. A., Pacelli, R., DeGraff, W., Gamson, J., Liebmann, J., Krishna, M. C., and Mitchell, J. B., 1996, The effect of various nitric oxide-donor agents on hydrogen peroxide-mediated toxicity: a direct correlation between nitric oxide formation and protection. Arch. Biochem. Biophys. 331: 241–248.CrossRefGoogle Scholar
  119. Wink, D. A., Hanbauer, I., Krishna, M. C., DeGraff, W., Gamson, J., and Mitchell, J. B., 1993, Nitric oxide protects against cellular damage and cytotoxicity from reactive species. Proc. Natl. Acad. Sci. USA 90: 9813–9817.CrossRefGoogle Scholar
  120. Witztum, J. L., and Steinberg, D., 1991, Role of oxidized low density lipoprotein in atherogenesis. J. Clin. Invest. 84: 1086–1095.Google Scholar
  121. Wu, X. B., Brune, B., von Appen, F., and Ullrich, V., 1992, Reversible activation of soluble guanylate cyclase by oxidizing agents. Arch. Biochem. Biophys. 294: 75–82.CrossRefGoogle Scholar
  122. Wu, M., Pritchard, Jr. K. A.,, Kaminski, P. M., Fayngersh, R. P., Hintze, T. H., and Wolin, M. S., 1995, Involvement of nitric oxide and nitrosothiols in relaxation of pulmonary arteries to peroxynitrite. Am. J. Physiol. 266: H2108 - H2113.Google Scholar
  123. Xia, Y., Dawson, V. L., Dawson, T. M., Snyder, S. H., and Zweier, J. L., 1996, Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellular injury. Proc. Natl. Acad. Sci. USA 93: 6770–6774.CrossRefGoogle Scholar
  124. Yagoob, M., Edelstein, C. L., and Schrier, R. W., 1996, Role of nitric oxide and superoxide balance in hypoxia-reoxygenation proximal tubular injury. Nephrol. Dial. Transplant. 11: 1743–1746.CrossRefGoogle Scholar
  125. Yermilov, V., Yoshie, Y., Rubio, J., and Ohshima, H., 1996, Effects of carbon dioxide/bicarbonate on induction of DNA single-strand breaks and formation of 8-nitroguanine, 8-oxoguanine and base-propenal mediated by peroxynitrite. FEBS Lett. 399: 67–70.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1998

Authors and Affiliations

  • Bruce A. Freeman
    • 1
    • 2
  • Jason Eiserich
    • 1
  • Valerie O’Donnell
    • 1
  1. 1.Departments of AnesthesiologyUniversity of Alabama at BirminghamBirminghamUSA
  2. 2.Biochemistry and Molecular GeneticsUniversity of Alabama at BirminghamBirminghamUSA

Personalised recommendations