Peroxynitrite-induced cytotoxicity: Mechanism and opportunities for intervention

Toxicology Letters

Volumn 140-141, Issue , 2003, Pages 113-124

  Virág, László ^a   Szabó, Éva ^a   Gergely, Pál ^a   Szabó, Csaba ^b,c  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b INOTEK CORPORATION   (United States)

^c SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Apoptosis; Cytotoxicity; Necrosis; Peroxynitrite; Poly(ADP ribose) glycohydrolase; Poly(ADP ribose) polymerase

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; ACIDIC FIBROBLAST GROWTH FACTOR; ADENOSINE DIPHOSPHATE RIBOSE; ANTIOXIDANT; CASPASE INHIBITOR; EPIDERMAL GROWTH FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MORPHINE; NERVE GROWTH FACTOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PEROXYNITRITE; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN BCL 2; SOMATOMEDIN; WORTMANNIN;

APOPTOSIS; ARTICLE; CALCIUM SIGNALING; CYTOTOXICITY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; DRUG EFFECT; ENZYME ACTIVATION; HUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

EID: 0344643456     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0378-4274(02)00508-8     Document Type: Article

References (87)

1. Adrie C., Richter C., Bachelet M., Banzet N., Francois D., Dinh-Xuan A.T., Dhainaut J.F., Polla B.S., Richard M.J. Contrasting effects of NO and peroxynitrites on HSP70 expression and apoptosis in human monocytes. Am. J. Physiol. Cell Physiol. 279:2000;C452-C460.
2. Aggarwal B.B. Apoptosis and nuclear factor-kappa B: a tale of association and dissociation. Biochem. Pharmacol. 60:2000;1033-1039.
3. Arnold W.P., Mittal C.K., Katsuki S., Murad F. Nitric oxide activates guanylate cyclase and increases guanosine 3′:5′-cyclic monophosphate levels in various tissue preparations. Proc. Natl. Acad. Sci. USA. 74:1977;3203-3207.
4. Arstall M.A., Sawyer D.B., Fukazawa R., Kelly R.A. Cytokine-mediated apoptosis in cardiac myocytes: the role of inducible nitric oxide synthase induction and peroxynitrite generation. Circ. Res. 85:1999;829-840.
5. Beckman J.S. Oxidative damage and tyrosine nitration from peroxynitrite. Chem. Res. Toxicol. 9:1996;836-844.
6. Beckman J.S., Koppenol W.H. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am. J. Physiol. 271:1996;C1424-C1437.
7. Berger N.A., Sims J.L., Catino D.M., Berger S.J. Poly(ADP-ribose) polymerase mediates the suicide response to massive DNA damage: studies in normal and DNA-repair defective cells. Princess Takamatsu Symp. 13:1983;219-226.
8. Berger S.J., Sudar D.C., Berger N.A. Metabolic consequences of DNA damage: DNA damage induces alterations in glucose metabolism by activation of poly (ADP-Ribose) polymerase. Biochem. Biophys. Res. Commun. 134:1986;227-232.
9. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., Lipton S.A. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA. 92:1995;7162-7166.
10. Bours V., Bentires-Alj M., Hellin A.C., Viatour P., Robe P., Delhalle S., Benoit V., Merville M.P. Nuclear factor-kappa B, cancer, and apoptosis. Biochem. Pharmacol. 60:2000;1085-1089.
11. Choi H.R., Choi J.S., Han Y.N., Bae S.J., Chung H.Y. Peroxynitrite scavenging activity of herb extracts. Phytother. Res. 16:2002;364-367.
12. Choi J.J., Oh Y.K., Kim H.S., Kim H.C., Ko K.H., Kim W.K. Mimosine prevents the death of glucose-deprived immunostimulated astrocytes by scavenging peroxynitrite. Glia. 39:2002;37-46.
13. Cross T.G., Scheel-Toellner D., Henriquez N.V., Deacon E., Salmon M., Lord J.M. Serine/threonine protein kinases and apoptosis. Exp. Cell Res. 256:2000;34-41.
14. Cuzzocrea S., Zingarelli B., Gilad E., Hake P., Salzman A.L., Szabo C. Protective effect of melatonin in carrageenan-induced models of local inflammation: relationship to its inhibitory effect on nitric oxide production and its peroxynitrite scavenging activity. J. Pineal Res. 23:1997;106-116.
15. Cuzzocrea S., Zingarelli B., O'Connor M., Salzman A.L., Szabo C. Effect of L-buthionine-(S,R)-sulphoximine, an inhibitor of gamma-glutamylcysteine synthetase on peroxynitrite- and endotoxic shock-induced vascular failure. Br. J. Pharmacol. 123:1998;525-537.
16. Drake J., Kanski J., Varadarajan S., Tsoras M., Butterfield D.A. Elevation of brain glutathione by gamma-glutamylcysteine ethyl ester protects against peroxynitrite-induced oxidative stress. J. Neurosci. Res. 68:2002;776-784.
17. Ferrer-Sueta G., Batinic-Haberle I., Spasojevic I., Fridovich I., Radi R. Catalytic scavenging of peroxynitrite by isomeric Mn(III) N-methylpyridylporphyrins in the presence of reductants. Chem. Res. Toxicol. 12:1999;442-449.
18. Foresti R., Sarathchandra P., Clark J.E., Green C.J., Motterlini R. Peroxynitrite induces haem oxygenase-1 in vascular endothelial cells: a link to apoptosis. Biochem. J. 339:(Pt 3):1999;729-736.
19. Gao F., Yao C.L., Gao E., Mo Q.Z., Yan W.L., McLaughlin R., Lopez B.L., Christopher T.A., Ma X.L. Enhancement of glutathione cardioprotection by ascorbic acid in myocardial reperfusion injury. J. Pharmacol. Exp. Ther. 301:2002;543-550.
20. Ghafourifar P., Richter C. Nitric oxide synthase activity in mitochondria. FEBS Lett. 418:1997;291-296.
21. Gilad E., Cuzzocrea S., Zingarelli B., Salzman A.L., Szabo C. Melatonin is a scavenger of peroxynitrite. Life Sci. 60:1997;PL169-PL174.
22. Gow A.J., Duran D., Malcolm S., Ischiropoulos H. Effects of peroxynitrite-induced protein modifications on tyrosine phosphorylation and degradation. FEBS Lett. 385:1996;63-66.
23. Green D., Kroemer G. The central executioners of apoptosis: caspases or mitochondria? Trends Cell Biol. 8:1998;267-271.
24. Guidarelli A., Fiorani M., Cantoni O. Calcium-dependent mitochondrial formation of species promoting strand scission of genomic DNA in U937 cells exposed to tert-butylhydroperoxide: the role of arachidonic acid. Free Radical Res. 33:2000;477-487.
25. Guidarelli A., Palomba L., Cantoni O. Peroxynitrite-mediated release of arachidonic acid from PC12 cells. Br. J. Pharmacol. 129:2000;1539-1541.
26. Guidarelli A., Tommasini I., Fiorani M., Cantoni O. Essential role of the mitochondrial respiratory chain in peroxynitrite-induced strand scission of genomic DNA. IUBMB Life. 50:2000;195-201.
27. Hadjivassiliou V., Green M.H., James R.F., Swift S.M., Clayton H.A., Green I.C. Insulin secretion, DNA damage, and apoptosis in human and rat islets of Langerhans following exposure to nitric oxide, peroxynitrite, and cytokines. Nitric Oxide. 2:1998;429-441.
28. Holmstrom T.H., Eriksson J.E. Phosphorylation-based signaling in Fas receptor-mediated apoptosis. Crit. Rev. Immunol. 20:2000;121-152.
29. Jackson R.M., Parish G., Helton E.S. Peroxynitrite modulates MnSOD gene expression in lung epithelial cells. Free Radical Biol. Med. 25:1998;463-472.
30. Janssen-Heininger Y.M., Poynter M.E., Baeuerle P.A. Recent advances towards understanding redox mechanisms in the activation of nuclear factor kappaB. Free Radical Biol. Med. 28:2000;1317-1327.
31. Kaji T., Kaieda I., Hisatsune T., Kaminogawa S. 3-Morpholinosydnonimine hydrochloride induces p53-dependent apoptosis in murine primary neural cells: a critical role for p21(ras)-MAPK-p19(ARF) pathway. Nitric Oxide. 6:2002;125-134.
32. Kim M.S., Cheong Y.P., So H.S., Lee K.M., Kim T.Y., Oh J., Chung Y.T., Son Y., Kim B.R., Park R. Protective effects of morphine in peroxynitrite-induced apoptosis of primary rat neonatal astrocytes: potential involvement of G protein and phosphatidylinositol 3-kinase (PI3 kinase). Biochem. Pharmacol. 61:2001;779-786.
33. Klotz L.O., Schieke S.M., Sies H., Holbrook N.J. Peroxynitrite activates the phosphoinositide 3-kinase/Akt pathway in human skin primary fibroblasts. Biochem. J. 352:(Pt 1):2000;219-225.
34. Kong S.K., Yim M.B., Stadtman E.R., Chock P.B. Peroxynitrite disables the tyrosine phosphorylation regulatory mechanism: lymphocyte-specific tyrosine kinase fails to phosphorylate nitrated cdc2(6-20)NH2 peptide. Proc. Natl. Acad. Sci. USA. 93:1996;3377-3382.
35. Leist M., Single B., Castoldi A.F., Kuhnle S., Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J. Exp. Med. 185:1997;1481-1486.
36. Li C.Q., Trudel L.J., Wogan G.N. Genotoxicity, mitochondrial damage, and apoptosis in human lymphoblastoid cells exposed to peroxynitrite generated from SIN-1. Chem. Res. Toxicol. 15:2002;527-535.
37. Lin K.T., Xue J.Y., Lin M.C., Spokas E.G., Sun F.F., Wong P.Y. Peroxynitrite induces apoptosis of HL-60 cells by activation of a caspase-3 family protease. Am. J. Physiol. 274:1998;C855-C860.
38. Lizasoain I., Moro M.A., Knowles R.G., Darley-Usmar V., Moncada S. Nitric oxide and peroxynitrite exert distinct effects on mitochondrial respiration which are differentially blocked by glutathione or glucose. Biochem. J. 314:1996;877-880.
39. Marletta M.A., Hurshman A.R., Rusche K.M. Catalysis by nitric oxide synthase. Curr. Opin. Chem. Biol. 2:1998;656-663.
40. Marshall H.E., Stamler J.S. Nitrosative stress-induced apoptosis through inhibition of NF-kappa B. J. Biol. Chem. 277:2002;34233-34238.
41. Masumoto H., Sies H. The reaction of ebselen with peroxynitrite. Chem. Res. Toxicol. 9:1996;262-267.
42. Matata B.M., Galinanes M. Peroxynitrite is an essential component of cytokines production mechanism in human monocytes through modulation of nuclear factor-kappa B DNA binding activity. J. Biol. Chem. 277:2002;2330-2335.
43. Mattson M.P., Goodman Y., Luo H., Fu W., Furukawa K. Activation of NF-kappaB protects hippocampal neurons against oxidative stress-induced apoptosis: evidence for induction of manganese superoxide dismutase and suppression of peroxynitrite production and protein tyrosine nitration. J. Neurosci. Res. 49:1997;681-697.
44. Mihm M.J., Coyle C.M., Schanbacher B.L., Weinstein D.M., Bauer J.A. Peroxynitrite induced nitration and inactivation of myofibrillar creatine kinase in experimental heart failure. Cardiovasc. Res. 49:2001;798-807.
45. Mihm M.J., Jing L., Bauer J.A. Nitrotyrosine causes selective vascular endothelial dysfunction and DNA damage. J. Cardiovasc. Pharmacol. 36:2000;182-187.
46. Mihm M.J., Schanbacher B.L., Wallace B.L., Wallace L.J., Uretsky N.J., Bauer J.A. Free 3-nitrotyrosine causes striatal neurodegeneration in vivo. J. Neurosci. 21:2001;RC149.
47. Nathan C. Inducible nitric oxide synthase: what difference does it make? J. Clin. Invest. 100:1997;2417-2423.
48. Nicotera P., Leist M., Ferrando-May E. Intracellular ATP, a switch in the decision between apoptosis and necrosis. Toxicol. Lett. 102-103:1998;139-142.
49. Nicotera P., Leist M., Fava E., Berliocchi L., Volbracht C. Energy requirement for caspase activation and neuronal cell death. Brain Pathol. 10:2000;276-282.
50. Peng H.B., Libby P., Liao J.K. Induction and stabilization of I kappa B alpha by nitric oxide mediates inhibition of NF-kappa B. J. Biol. Chem. 270:1995;14214-14219.
51. Potoka D.A., Upperman J.S., Nadler E.P., Wong C.T., Zhou X., Zhang X.R., Ford H.R. NF-kappaB inhibition enhances peroxynitrite-induced enterocyte apoptosis. J. Surg. Res. 106:2002;7-14.
52. Radi R., Beckman J.S., Bush K.M., Freeman B.A. Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J. Biol. Chem. 266:1991;4244-4250.
53. 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. 288:1991;481-487.
54. Radi R., Peluffo G., Alvarez M.N., Naviliat M., Cayota A. Unraveling peroxynitrite formation in biological systems. Free Radical Biol. Med. 30:2001;463-488.
55. Reiff D.A., Kelpke S., Rue L. III, Thompson J.A. Acidic fibroblast growth factor attenuates the cytotoxic effects of peroxynitrite in primary human osteoblast precursors. J. Trauma. 50:2001;433-438.
56. Roussyn I., Briviba K., Masumoto H., Sies H. Selenium-containing compounds protect DNA from single-strand breaks caused by peroxynitrite. Arch. Biochem. Biophys. 330:1996;216-218.
57. Saeki M., Kamisaki Y., Maeda S. Involvement of mitogen-activated protein kinase in peroxynitrite-induced cell death of human neuroblastoma SH-SY5Y cells. Neurosci. Res. 38:2000;213-216.
58. Saeki M., Maeda S., Wada K., Kamisaki Y. Insulin-like growth factor-1 protects peroxynitrite-induced cell death by preventing cytochrome c-induced caspase-3 activation. J. Cell Biochem. 84:2002;708-716.
59. Salgo M.G., Squadrito G.L., Pryor W.A. Peroxynitrite causes apoptosis in rat thymocytes. Biochem. Biophys. Res. Commun. 215:1995;1111-1118.
60. Salvemini D., Wang Z.Q., Stern M.K., Currie M.G., Misko T.P. Peroxynitrite decomposition catalysts: therapeutics for peroxynitrite-mediated pathology. Proc. Natl. Acad. Sci. USA. 95:1998;2659-2663.
61. Sarmay G. Phosphatidylinositol 3-kinase, phosphoinositides and apoptosis. Polyphosphoinositol phosphatase and apoptosis. Subcell. Biochem. 36:2002;309-333.
62. Sata N., Klonowski-Stumpe H., Han B., Haussinger D., Niederau C. Cytotoxicity of peroxynitrite in rat pancreatic acinar AR4-2J cells. Pancreas. 15:1997;278-284.
63. Schmidt K.N., Amstad P., Cerutti P., Baeuerle P.A. The roles of hydrogen peroxide and superoxide as messengers in the activation of transcription factor NF-kappa B. Chem. Biol. 2:1995;13-22.
64. Shimanovich R., Groves J.T. Mechanisms of peroxynitrite decomposition catalyzed by FeTMPS, a bioactive sulfonated iron porphyrin. Arch. Biochem. Biophys. 387:2001;307-317.
65. Spear N., Estevez A.G., Barbeito L., Beckman J.S., Johnson G.V. Nerve growth factor protects PC12 cells against peroxynitrite-induced apoptosis via a mechanism dependent on phosphatidylinositol 3-kinase. J. Neurochem. 69:1997;53-59.
66. Spear N., Estevez A.G., Johnson G.V., Bredesen D.E., Thompson J.A., Beckman J.S. Enhancement of peroxynitrite-induced apoptosis in PC12 cells by fibroblast growth factor-1 and nerve growth factor requires p21Ras activation and is suppressed by Bcl-2. Arch. Biochem. Biophys. 356:1998;41-45.
67. Szabo C., Day B.J., Salzman A.L. Evaluation of the relative contribution of nitric oxide and peroxynitrite to the suppression of mitochondrial respiration in immunostimulated macrophages using a manganese mesoporphyrin superoxide dismutase mimetic and peroxynitrite scavenger. FEBS Lett. 381:1996;82-86.
68. Szabo C., Wong H.R., Salzman A.L. Pre-exposure to heat shock inhibits peroxynitrite-induced activation of poly(ADP) ribosyltransferase and protects against peroxynitrite cytotoxicity in J774 macrophages. Eur. J. Pharmacol. 315:1996;221-226.
69. Szabó É., Virág L., Bakondi E., Gyüre L., Haskó G., Bai P., Hunyadi J., Gergely P., Szabó C. Peroxynitrite production, DNA breakage and poly(ADP-ribose) polymerase activation in a mouse model of oxazolone-induced contact hypersensitivity. J. Invest. Dermatol. 117:2001;74-80.
70. Valdez L.B., Actis-Goretta L., Boveris A. Polyphenols in red wines prevent NADH oxidation induced by peroxynitrite. Ann. NY Acad. Sci. 957:2002;274-278.
71. Vieira H.L., Belzacq A.S., Haouzi D., Bernassola F., Cohen I., Jacotot E., Ferri K.F., El Hamel C., Bartle L.M., Melino G., Brenner C., Goldmacher V., Kroemer G. The adenine nucleotide translocator: a target of nitric oxide, peroxynitrite, and 4-hydroxynonenal. Oncogene. 20:2001;4305-4316.
72. Virag L., Salzman A.L., Szabo C. Poly(ADP-ribose) synthetase activation mediates mitochondrial injury during oxidant-induced cell death. J. Immunol. 161:1998;3753-3759.
73. Virag L., Scott G.S., Cuzzocrea S., Marmer D., Salzman A.L., Szabo C. Peroxynitrite-induced thymocyte apoptosis: the role of caspases and poly (ADP-ribose) synthetase (PARS) activation. Immunology. 94:1998;345-355.
74. Virág L., Szabó C. The crucial role of apopain in the peroxynitrite-induced apoptotic DNA fragmentation. Free Radical Biol. Med. 25:1998;1075-1082.
75. Virág L., Salzman A.L., Szabó C. Inhibition of poly(ADP-ribose) synthetase (PARS) and protection against peroxynitrite-induced cytotoxicity by zinc chelation. Br. J. Pharmacol. 126:1999;769-777.
76. Virag L., Scott G.S., Antal-Szalmas P., O'Connor M., Ohshima H., Szabo C. Requirement of intracellular calcium mobilization for peroxynitrite-induced poly(ADP-ribose) synthetase activation and cytotoxicity. Mol. Pharmacol. 56:1999;824-833.
77. Virág L., Szabó C. Bcl-2 protects peroxynitrite-treated thymocytes from poly(ADP-ribose) synthase (PARS) independent apoptotic but not from PARS-mediated necrotic cell death. Free Radical Biol. Med. 29:2000;704-713.
78. Virag L., Szabo C. Purines inhibit poly(ADP-ribose) polymerase activation and modulate oxidant-induced cell death. FASEB J. 15:2001;99-107.
79. Virag L., Szabo C. The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharm. Rev. 54:2002;375-429.
80. Volbracht C., Leist M., Nicotera P. ATP controls neuronal apoptosis triggered by microtubule breakdown or potassium deprivation. Mol. Med. 5:1999;477-489.
81. von Knethen A., Callsen D., Brune B. Superoxide attenuates macrophage apoptosis by NF-kappa B and AP-1 activation that promotes cyclooxygenase-2 expression. J. Immunol. 163:1999;2858-2866.
82. Weller R., Pattullo S., Smith L., Golden M., Ormerod A., Benjamin N. Nitric oxide is generated on the skin surface by reduction of sweat nitrate. J. Invest. Dermatol. 107:1996;327-331.
83. Yamamoto T., Maruyama W., Kato Y., Yi H., Shamoto-Nagai M., Tanaka M., Sato Y., Naoi M. Selective nitration of mitochondrial complex I by peroxynitrite: involvement in mitochondria dysfunction and cell death of dopaminergic SH-SY5Y cells. J. Neural Transm. 109:2002;1-13.
84. Ying W., Swanson R.A. The poly(ADP-ribose) glycohydrolase inhibitor gallotannin blocks oxidative astrocyte death. Neuroreport. 11:2000;1385-1388.
85. Ying W., Sevigny M.B., Chen Y., Swanson R.A. Poly(ADP-ribose) glycohydrolase mediates oxidative and excitotoxic neuronal death. Proc. Natl. Acad. Sci. USA. 98:2001;12227-12232.
86. Ying W., Chen Y., Alano C.C., Swanson R.A. Tricarboxylic acid cycle substrates prevent PARP-mediated death of neurons and astrocytes. J. Cereb. Blood Flow Metab. 22:2002;774-779.
87. Zhuang S., Simon G. Peroxynitrite-induced apoptosis involves activation of multiple caspases in HL-60 cells. Am. J. Physiol. Cell Physiol. 279:2000;C341-C351.