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Redox signaling

  • Henry Jay Forman
  • Martine Torres
  • Jon Fukuto
Chapter
Part of the Developments in Molecular and Cellular Biochemistry book series (DMCB, volume 37)

Abstract

Reactive oxygen species (ROS) and reactive nitrogen species (RNS) have recently been shown to be involved in a multiplicity of physiological responses through modulation of signaling pathways. Some of the specific signaling components altered by reactive oxygen and nitrogen species (RONS) have begun to be identified. We will discuss RONS signaling by detailing the chemistry of signaling, the roles of antioxidant enzymes as signaling components, thiol chemistry in the specificity of RONS signaling, NO-heme interactions, and some do’s and don’ts of redox signal research. The principal points raised are that: (1) as with classic signaling pathways, signaling by RONS is regulated; (2) antioxidant enzymes are essential ‘turn-off’ components in signaling; (3) spatial relationships are probably more important in RONS signaling than the overall ‘redox state’ of the cell; (4) deprotonation of cysteines to form the thiolate, which can react with RONS, occurs in specific protein sites providing specificity in signaling; (5) although multiple chemical mechanisms exist for producing nitrosothiols, their formation in vivo remains unclear; and (6) caution should be taken in the use of ‘antioxidants’ in signal transduction. (Mol Cell Biochem 234/235: 49–62, 2002)

Key words

reactive oxygen species reactive nitrogen species redox signaling 

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References

  1. 1.
    Sutherland EW, Rall TW, Menon T: Adenyl cyclase I. Distribution, preparation and properties. J Biol Chem 237: 1220–1227, 1962PubMedGoogle Scholar
  2. 2.
    Rodbell M, Birnbaumer L, Pohl SL, Krans HM: The glucagon-sensitive adenyl cyclase system in plasma membranes of rat liver. V. An obligatory role of guanylnucleotides in glucagon action. J Biol Chem 246: 1877–1882, 1971PubMedGoogle Scholar
  3. 3.
    Northup JK, Sternweis PC, Smigel MD, Schleifer LS, Ross EM, Gilman AG: Purification of the regulatory component of adenylate cyclase. Proc Natl Acad Sci USA 77: 6516–6520, 1980PubMedCrossRefGoogle Scholar
  4. 4.
    Takai Y, Kishimoto A, Kikkawa U, Mori T, Nishizuka Y: Unsaturated diacylglycerol as a possible messenger for the activation of calcium-activated, phospholipid-dependent protein kinase system. Biochem Biophys Res Commun 91: 1218–1224, 1979PubMedCrossRefGoogle Scholar
  5. 5.
    Streb H, Irvine RF, Berridge MJ, Schulz I: Release of Cat2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate. Nature 306: 67–69, 1983PubMedCrossRefGoogle Scholar
  6. 6.
    Arnold WP, Mittal CK, Katsuki S, Murad F: Nitric oxide activates guanylate cyclase and increases guanosine 3’:5’-cyclic monophosphate levels in various tissue preparations. Proc NatlAcad Sci USA 74: 3203–3207, 1977CrossRefGoogle Scholar
  7. 7.
    Gruetter CA, Barry BK, McNamara DB, Gruetter DY, Kadowitz PJ, Ignarro L: Relaxation of bovine coronary artery and activation of coronary arterial guanylate cyclase by nitric oxide, nitroprusside and a carcinogenic nitrosoamine. J Cyclic Nucleotide Res 5: 211–224, 1979PubMedGoogle Scholar
  8. 8.
    Rhee SG: Redox signaling: Hydrogen peroxide as intracellular messenger. Exp Mol Med 31: 53–59, 1999PubMedGoogle Scholar
  9. 9.
    Claiborne A, Yeh JI, Mallett, TC, Luba J, Crane EJ, Charrier V: Parsonage, D: Protein-sulfenic acids: Diverse roles for an unlikely player in enzyme catalysis and redox regulation. Biochemistry 38: 15407–15416, 1999PubMedCrossRefGoogle Scholar
  10. 10.
    Sawyer DT: In: Oxygen Chemistry. Oxford University Press, New York, 1991Google Scholar
  11. 11.
    Boveris A, Cadenas E: Cellular sources and steady-state levels of reactive oxygen species. In: L.B. Clerch, D.J. Massaro (eds). Oxygen, Gene Expression, and Cellular Function. Marcel Dekker, New York, 1997, pp 1–25Google Scholar
  12. 12.
    Babior BM: NADPH oxidase: An update. Blood 93: 1464–1476, 1999PubMedGoogle Scholar
  13. 13.
    Ambruso DR, Knall C, Abell AN, Panepinto J, Kurkchubasche A, Thurman, G, Gonzalez-Aller C, Hiester A, deBoer M, Harbeck RJ, Oyer R, Johnson GL, Roos D: Human neutrophil immunodeficiency syndrome is associated with an inhibitory Rac2 mutation. Proc Natl Acad Sci USA 97: 4654–4659, 2000PubMedCrossRefGoogle Scholar
  14. 14.
    Babior BM: The NADPH oxidase of endothelial cells. IUBMB Life 50, 267–269, 2000PubMedCrossRefGoogle Scholar
  15. 15.
    Dinauer MC, Deck MB, Unanue ER: Mice lacking reduced nicotina-mide adenine dinucleotide phosphate oxidase activity show increased susceptibility to early infection with Listeria monocytogenes. J Immunol 158: 5581–5583, 1997PubMedGoogle Scholar
  16. 16.
    Wang HD, Xu S, Johns DG, Du Y, Quinn MT, Cayatte AJ, Cohen RA: Role of NADPH oxidase in the vascular hypertrophie and oxidative stress response to angiotensin II in mice. Circ Res 88: 947–953, 2001PubMedCrossRefGoogle Scholar
  17. 17.
    Souza HP, Laurindo FR, Ziegelstein RC, Berlowitz CO, Zweier JL: Vascular NAD(P)H oxidase is distinct from the phagocytic enzyme and modulates vascular reactivity control. Am J Physiol Heart Circ Physiol 280: H658–H667, 2001PubMedGoogle Scholar
  18. 18.
    Suh YA, Arnold RS, Lassegue B, Shi J, Xu X, Sorescu D, Chung AB, Griendling KK, Lambeth JD: Cell transformation by the superoxide-generating oxidase Moxl. Nature 401: 79–82, 1999PubMedCrossRefGoogle Scholar
  19. 19.
    Lassegue B, Sorescu D, Szocs K, Yin Q, Akers M, Zhang Y, Grant SL, Lambeth JD, Griendling KK: Novel gp9lph0x homologues in vascular smooth muscle cells: Nox 1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Cire Res 88: 888–894, 2001CrossRefGoogle Scholar
  20. 20.
    Arnold RS, Shi J, Murad E, Whalen AM, Sun CQ, Polavarapu R, Parthasarathy S, Petros JA, Lambeth JD: Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Noxl. Proc Natl Acad Sci USA 98: 5550–5555, 2001PubMedCrossRefGoogle Scholar
  21. 21.
    Stuehr DJ: Structure-function aspects in the nitric oxide synthases. Annu Rev Pharmacol Toxicol 37: 339–359, 1997PubMedCrossRefGoogle Scholar
  22. 22.
    Stuehr DJ, Cho HJ, Kwon NS, Weise MF, Nathan CF: Purification and characterization of the cytokine-induced macrophage nitric oxide synthase: An FAD- and FMN-containing flavoprotein. Proc Natl Acad Sci USA 88: 7773–7777, 1991.PubMedCrossRefGoogle Scholar
  23. 23.
    Forstermann U, Gath I, Schwarz P, Closs EI, Kleinert H: Isoforms of nitric oxide synthase. Properties, cellular distribution and expressional control. Biochem Pharmacol 50: 1321–1332, 1995PubMedCrossRefGoogle Scholar
  24. 24.
    Sessa WC, Barber CM, Lynch KR: Mutation of N-myristoylation site converts endothelial cell nitric oxide synthase from a membrane to a cytosolic protein. Circ Res 72: 921–924, 1993PubMedCrossRefGoogle Scholar
  25. 25.
    Robinson LJ, Michel T: Mutagenesis of palmitoylation sites in endothelial nitric oxide synthase identifies a novel motif for dual acylation and subcellular targeting. Proc Natl Acad Sci USA 92: 11776–11780,1995PubMedCrossRefGoogle Scholar
  26. 26.
    Feron O, Belhassen L, Kobzik L, Smith TW, Kelly RA, Michel T: Endothelial nitric oxide synthase targeting to caveolae. Specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J Biol Chem 271: 22810–22814, 1996PubMedCrossRefGoogle Scholar
  27. 27.
    Bredt DS, Snyder SH: Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc Natl Acad Sci USA 86: 9030–9033,1989PubMedCrossRefGoogle Scholar
  28. 28.
    Pollock JS, Forstermann U, Mitchell JA, Warner TD, Schmidt HH, Nakane M, Murad F: Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells. Proc Natl Acad Sci USA 88: 10480–10484, 1991PubMedCrossRefGoogle Scholar
  29. 29.
    Cho HJ, Xie Q-W, Calaycay J, Mumford RA, Swiderek KM, Lee TD, Nathan C: Calmodulin is a subunit of nitric oxide synthase from macrophages. J Exp Med 176: 599–604, 1992PubMedCrossRefGoogle Scholar
  30. 30.
    Singh R, Pervin S, Rogers NE, Ignarro LJ, Chaudhuri G: Evidence for the presence of an unusual nitric oxide-and citrulline-producing enzyme in rat kidney. Biochem Biophys Res Commun 232: 672–677, 1997PubMedCrossRefGoogle Scholar
  31. 31.
    Bates TE, Loesch A, Burnstock G, Clark JB: Immunocytochemical evidence for a mitochondrially located nitric oxide synthase in brain and liver. Biochem Biophys Res Commun 213: 896–900, 1995PubMedCrossRefGoogle Scholar
  32. 32.
    Bates TE, Loesch A, Burnstock G, Clark JB: Mitochondrial nitric oxide synthase: A ubiquitous regulator of oxidative phosphorylation? Biochem Biophys Res Commun 218: 40–44, 1996PubMedCrossRefGoogle Scholar
  33. 33.
    Kobzik L, Stringer B, Balligand JL, Reid MB, Stamler JS: Endothelial type nitric oxide synthase in skeletal muscle fibers: Mitochondria] relationships. Biochem Biophys Res Commun 211: 375–381, 1995PubMedCrossRefGoogle Scholar
  34. 34.
    Giulivi C, Poderoso JJ, Boveris A: Production of nitric oxide by mitochondria. J Biol Chem 273: 11038–11043, 1998PubMedCrossRefGoogle Scholar
  35. 35.
    Ghafourifar P, Richter C: Nitric oxide synthase activity in mitochondria. FEBS Lett 418: 291–296, 1997PubMedCrossRefGoogle Scholar
  36. 36.
    Sarkela TM, Berthiaume J, Elfering S, Gybina AA, Giulivi C: The modulation of oxygen radical production by nitric oxide in mitochondria. J Biol Chem 276: 6945–6949, 2001PubMedCrossRefGoogle Scholar
  37. 37.
    Sies H, Arteel GE: Interaction of peroxynitrite with selenoproteins and glutathione peroxidase mimics. Free Radic Biol Med 28: 1451–1455, 2000PubMedCrossRefGoogle Scholar
  38. 38.
    Schafer FQ, Buettner GR: Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30: 1191–1212, 2001PubMedCrossRefGoogle Scholar
  39. 39.
    Gilbert HF: Biological disulfides: the third messenger? Modulation of phosphofructokinase activity by thiol/disulfide exchange. J Biol Chem 257: 12086–12091, 1982PubMedGoogle Scholar
  40. 40.
    Winterbourn CC, Metodiewa D: Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radic Biol Med 27: 322–328, 1999PubMedCrossRefGoogle Scholar
  41. 41.
    Chen JW, Dodia C, Feinstein SI, Jain MK, Fisher AB: 1-Cys peroxiredoxin, a bifunctional enzyme with glutathione peroxidase and phospholipase A2 activities. J Biol Chem 275: 28421–28427, 2000PubMedCrossRefGoogle Scholar
  42. 42.
    Akerboom TPM, Sies H: Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples. Meth Enzymol 77: 373–382, 1981PubMedCrossRefGoogle Scholar
  43. 43.
    Loeb GA, Skelton DC, Forman HJ: Dependence of mixed disulfide formation in alveolar macrophages upon production of oxidized glutathione: Effect of selenium depletion. Biochem Pharmacol 38: 31193121, 1989PubMedCrossRefGoogle Scholar
  44. 44.
    Tu BP, Ho-Schleyer SC, Travers KJ, Weissman JS: Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science 290: 1571–1574, 2000PubMedCrossRefGoogle Scholar
  45. 45.
    Rietsch A, Beckwith J: The genetics of disulfide bond metabolism. Annu Rev Genet 32: 163–184, 1998PubMedCrossRefGoogle Scholar
  46. 46.
    Loeb GA, Skelton DC, Coates TD, Forman HJ: Role of the selenium dependent glutathione peroxidase in antioxidant defenses in rat alveolar macrophages. Exp Lung Res 14: 921–936, 1988PubMedCrossRefGoogle Scholar
  47. 47.
    Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, Kawabata M, Miyazono K, Ichijo H: Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 17: 2596–2606, 1998PubMedCrossRefGoogle Scholar
  48. 48.
    Gopalakrishna R, Jaken S: Protein kinase C signaling and oxidative stress. Free Radic Biol Med 28: 1349–1361, 2000PubMedCrossRefGoogle Scholar
  49. 49.
    Gopalakrishna R, Chen Z-H, Gundimeda U: Protein kinase C as a sensor for oxidative stress in tumor promotion and chemoprevention. In: H.J. Forman, E. Cadenas (eds). Oxidative Stress and Signal Transduction. Chapman and Hall, New York, 1997, pp 157–180CrossRefGoogle Scholar
  50. 50.
    Kaul N, Gopalakrishna R, Gundimeda U, Choi J, Forman HJ: Role of protein kinase C in basal and hydrogen peroxide-stimulated NF-03 activation in the murine macrophage J774A.1 cell line. Arch Biochem Biophys 350: 79–86, 1998PubMedCrossRefGoogle Scholar
  51. 51.
    Gordon JA: Use of vanadate as protein-phosphotyrosine phosphatase inhibitor. Meth Enzymol 201: 477–482, 1991PubMedCrossRefGoogle Scholar
  52. 52.
    Denu JM, Tanner KG: Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: Evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry 37: 5633–5642, 1998PubMedCrossRefGoogle Scholar
  53. 53.
    Lee SR, Kwon KS, Kim SR, Rhee SG: Reversible inactivation of protein-tyrosine phosphatase IB in A431 cells stimulated with epidermal growth factor. J Biol Chem 273: 15366–15372, 1998PubMedCrossRefGoogle Scholar
  54. 54.
    Fauman EB, Saper MA: Structure and function of the protein tyrosine phosphatases. Trends Biochem Sci 21: 413–417, 1996PubMedCrossRefGoogle Scholar
  55. 55.
    Kim JR, Yoon HW, Kwon KS, Lee SR, Rhee SG: Identification of proteins containing cysteine residues that are sensitive to oxidation by hydrogen peroxide at neutral pH. Anal Biochem 283: 214–221, 2000PubMedCrossRefGoogle Scholar
  56. 56.
    Caselli A, Marzocchini R, Camici G, Manao G, Moneti G, Pieraccini G, Ramponi G: The inactivation mechanism of low molecular weight phosphotyrosine-protein phosphatase by H202. J Biol Chem 273: 32554–32560,1998PubMedCrossRefGoogle Scholar
  57. 57.
    Barrett WC, DeGnore JP, Konig S, Fales HM, Keng YF, Zhang ZY, Yim MB, Chock PB: Regulation of PTP1B via glutathionylation of the active site cysteine 215. Biochemistry 38: 6699–6705, 1999PubMedCrossRefGoogle Scholar
  58. 58.
    Barrett WC, DeGnore JP, Keng YF, Zhang ZY, Yim MB, Chock PB: Roles of superoxide radical anion in signal transduction mediated by reversible regulation of protein-tyrosine phosphatase 1B. J Biol Chem 274: 3454334546,1999Google Scholar
  59. 59.
    Richter-Addo GB, Legzdins P: In: Metal Nitrosyls. Oxford University Press, New York, 1992Google Scholar
  60. 60.
    Williams DLH: The chemistry of S-nitrosothiols. Acc Chem Res 32: 869–876, 1999CrossRefGoogle Scholar
  61. 61.
    Goldstein S, Czapski G: Mechanism of the nitrosation of thiols and amines by oxygenated NO solutions: The nature of the nitrosating intermediates. J Am Chem Soc 118: 3419–3425, 1996CrossRefGoogle Scholar
  62. 62.
    Liu X, Miller MJ, Joshi MS, Thomas DD, Lancaster JR Jr: Accelerated reaction of nitric oxide with 02 within the hydrophobic interior of biological membranes. Proc Natl Acad Sci USA 95: 2175–2179, 1998PubMedCrossRefGoogle Scholar
  63. 63.
    Wade RS, Castro CE: Redox reactivity of iron([II) porphyrins and heme proteins with nitric oxide. Nitrosyl transfer to carbon, oxygen, nitrogen, and sulfur. Chem Res Toxicol 3: 289–291, 1990PubMedCrossRefGoogle Scholar
  64. 64.
    Boese M, Mordvintcev PI, Vanin AF, Busse R, Mulsch A: S-nitrosation of serum albumin by dinitrosyl-iron complex. J Biol Chem 270: 29244–29449, 1995PubMedCrossRefGoogle Scholar
  65. 65.
    Gow AJ, Buerk DG, Ischiropoulos H: A novel reaction mechanism for the formation of S-nitrosothiol in vivo. J Biol Chem 272: 2841–2845, 1997PubMedCrossRefGoogle Scholar
  66. 66.
    Pryor WA, Church DF, Govindan CK, Crank G: Oxidation of thiols by nitric oxide nitrogen dioxide: Synthetic utility toxicological implications. J Org Chem 47, 1982Google Scholar
  67. 67.
    Prutz WA, Monig H, Butler J, Land EJ: Reactions of nitrogen dioxide in aqueous model systems: Oxidation of tyrosine units in peptides and proteins. Arch Biochem Biophys 243: 125–134, 1985PubMedCrossRefGoogle Scholar
  68. 68.
    Oae S, Kim YH, Fukushima D, Shinhama K: New syntheses of thionitrites their chemical reactivities. J Chem Soc, Perkin Trans 1, 1978Google Scholar
  69. 69.
    van der Vliet A, Hoen PA, Wong PS, Bast A, Cross CE: Formation of S-nitrosothiols via direct nucleophilic nitrosation of thiols by peroxynitrite with elimination of hydrogen peroxide. J Biol Chem 273: 3025530262, 1998Google Scholar
  70. 70.
    Fukuto JM, Ignarro LJ: In Vivo aspects of nitric oxide (NO) chemistry: Does peroxynitrite (-OONO) play a major role in cytotoxicity? Acc Chem Res 30: 149–152, 1997CrossRefGoogle Scholar
  71. 71.
    Barnett DJ, McAninly J, Williams DLH: Transnitrosation between nitrosothiols and thiols. J Chem Soc, Perkin Trans 2: 1131–1133, 1994Google Scholar
  72. 72.
    Barnett DJ, Rios A, Williams DLH: NO-group transfer (transnitrosation) between S-nitrosothiols and thiols. Part 2. J Chem Soc, Perkin Trans 2: 1279–1282, 1994Google Scholar
  73. 73.
    Williams DLH: Nitric oxide release from S-nitrosothiols (RSNO)-the role of copper ions. Trans Metal Chem 21: 189–191, 1996CrossRefGoogle Scholar
  74. 74.
    Dicks AP, Swift HR, Williams DLH, Butler AR, Al-Sa’doni HH, Cox BG: Identification of Cu+ as the effective reagent in nitric oxide formation from S-nitrosothiols (RSNO). J Chem Soc, Perkin Trans 2: 48 1487, 1996Google Scholar
  75. 75.
    Arnelle DR, Stamler JS: NO+, NO, and NO- donation by S-nitroso thiols: implications for regulation of physiological functions by Snitrosylation and acceleration of disulfide formation. Arch Biochem Biophys 318: 279–285, 1995PubMedCrossRefGoogle Scholar
  76. 76.
    Wong PS, Hyun J, Fukuto JM, Shirota FN, DeMaster EG, Shoeman DW, Nagasawa HT, Reaction between S-nitrosothiols and thiols: generation of nitroxyl (HNO) and subsequent chemistry. Biochemistry 37: 5362–5371, 1998PubMedCrossRefGoogle Scholar
  77. 77.
    Liu L, Hausladen A, Zeng M, Que L, Heitman J, Stamler JS: A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410: 490–494, 2001PubMedCrossRefGoogle Scholar
  78. 78.
    Stamler JS, Toone EJ, Lipton SA, Sucher NJ: (S)NO signals: Translocation, regulation, and a consensus motif. Neuron 18: 691–696, 1997PubMedCrossRefGoogle Scholar
  79. 79.
    Perez-Mato I, Castro C, Ruiz FA, Corrales FJ, Mato JM: Methionine adenosyltransferase 5-nitrosylation is regulated by the basic and acidic amino acids surrounding the target thiol. J Biol Chem 274: 1707517079, 1999PubMedCrossRefGoogle Scholar
  80. 80.
    Whitmarsh AJ, Davis RJ: Structural organization of MAP-kinase signaling modules by scaffold proteins in yeast and mammals. Trends Biochem Sci 23: 481–485, 1998PubMedCrossRefGoogle Scholar
  81. 81.
    Klauck TM, Faux MC, Labudda K, Langeberg LK, Jaken S, Scott JD: Coordination of three signaling enzymes by AKAP79, a mammalian scaffold protein. Science 271: 1589–1592, 1996PubMedCrossRefGoogle Scholar
  82. 82.
    Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH: Protein S-nitrosylation: A physiological signal for neuronal nitric oxide. Nat Cell Biol 3: 193–197, 2001PubMedCrossRefGoogle Scholar
  83. 83.
    Lander HM: An essential role for free radicals and derived species in signal transduction. FASEB J 11: 118–124, 1997PubMedGoogle Scholar
  84. 84.
    Govers R, Rabelink TJ: Cellular regulation of endothelial nitric oxide synthase. Am J Physiol Renal Physiol 280: F193—F206, 2001Google Scholar
  85. 85.
    Pfeilschifter J, Eberhardt W, Beck KF: Regulation of gene expression by nitric oxide. Pflügers Arch 442: 479–486, 2001PubMedCrossRefGoogle Scholar
  86. 86.
    Park HS, Huh SH, Kim MS, Lee SH, Choi EJ: Nitric oxide negatively regulates c-Jun N-terminal kinase/stress-activated protein kinase by means of S-nitrosylation. Proc Natl Acad Sci USA 97: 14382–14387, 2000PubMedCrossRefGoogle Scholar
  87. 87.
    Takakura K, Beckman JS, MacMillan-Crow LA, Crow JP: Rapid and irreversible inactivation of protein tyrosine phosphatases PTP1B, CD45, and LAR by peroxynitrite. Arch Biochem Biophys 369: 197207, 1999PubMedCrossRefGoogle Scholar
  88. 88.
    Ignarro LJ: Biological actions and properties of endothelium-derived nitric oxide formed and released from artery and vein. Cire Res 65: 121, 1989.CrossRefGoogle Scholar
  89. 89.
    Traylor TG, Sharma VS: Why NO? Biochemistry 31: 2847–2849, 1992PubMedCrossRefGoogle Scholar
  90. 90.
    Traylor TG, Duprat AF, Sharma VS: Nitric oxide-triggered heme-mediated hydrolysis: A possible model for biological reactions of NO. J Am Chem Soc 115: 811–813, 1993CrossRefGoogle Scholar
  91. 91.
    Cooper CE: Nitric oxide and iron proteins. Biochim Biophys Acta 1411: 290–309, 1999PubMedCrossRefGoogle Scholar
  92. 92.
    Brown GC: Nitric oxide regulates mitochondrial respiration and cell functions by inhibiting cytochrome oxidase. FEBS Lett 369: 136–139, 1995PubMedCrossRefGoogle Scholar
  93. 93.
    Hoshino M, Ozawa K, Seki H, Ford PC: Photochemistry of nitric oxide adducts of water-soluble iron(III) porphyrin ferrihemoproteins studied by nanosecond laser photolysis. J Am Chem Soc 115: 95689575, 1993CrossRefGoogle Scholar
  94. 94.
    Das KC, Lewis-Molock Y, White CW: Activation ofNF-KB and elevation of MnSOD gene expression by thiol reducing agents in lung adenocarcinoma (A549) cells. Am J Physiol 269: L588–L602, 1995.PubMedGoogle Scholar
  95. 95.
    Chan ED, Riches DW, White CW: Redox paradox: effect ofN-acetylcysteine and serum on oxidation reduction-sensitive mitogen-activated protein kinase signaling pathways. Am J Respir Cell Mol Biol 24: 627632, 2001PubMedGoogle Scholar
  96. 96.
    Brennan P, O’Neill LA: 2-Mercaptoethanol restores the ability of nuclear factor-kB (NF-KB) to bind DNA in nuclear extracts from interleukin 1-treated cells incubated with pyrollidine dithiocarbamate 98. (PDTC). Evidence for oxidation of glutathione in the mechanism of inhibition of NF-KB by PDTC. Biochem J 320: 975–981, 1996PubMedGoogle Scholar
  97. 97.
    Azzi A, Aratri E, Boscoboinik D, Clement S, Ozer NK, Ricciarelli R, 99.Spycher, S: Molecular basis of alpha-tocopherol control of smooth muscle cell proliferation. Biofactors 7: 3–14, 1998PubMedCrossRefGoogle Scholar
  98. 98.
    Tarpey MM, Fridovich I: Methods of detection of vascular reactive species: Nitric oxide, superoxide, hydrogen peroxide, and peroxynitrite. Circ Res 89: 224–236, 2001CrossRefGoogle Scholar
  99. 99.
    Torres M, Forman HJ: Activation of several MAP kinases upon stimulation of rat alveolar macrophages: Role of the NADPH oxidase. Arch Biochem Biophys 366: 231–239, 1999PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Henry Jay Forman
    • 1
  • Martine Torres
    • 2
  • Jon Fukuto
    • 3
  1. 1.Department of Environmental Health Sciences, School of Public HealthUniversity of Alabama at BirminghamBirmingham
  2. 2.Childrens Hospital Los Angeles Research Institute, Department of Pediatrics, School of MedicineUniversity of Southern CaliforniaLos Angeles
  3. 3.Department of PharmacologyUniversity of California at Los AngelesLos AngelesUSA

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