Effects of a metalloporphyrinic peroxynitrite decomposition catalyst, ww-85, in a mouse model of spinal cord injury

Free Radical Research

Volumn 43, Issue 7, 2009, Pages 631-645

  Genovese, Tiziana ^a   Mazzon, Emanuela ^a   Esposito, Emanuela ^a   Di Paola, Rosanna ^a   Murthy, Kanneganti ^b   Neville, Lewis ^b   Bramanti, Placido ^a   Cuzzocrea, Salvatore ^a,c  

^a IRCCS CENTRO NEUROLESI BONINO PULEJO   (Italy)

^b INOTEK CORPORATION   (United States)

^c UNIVERSITY OF MESSINA   (Italy)

Author keywords

Peroxynitrite; Spinal cord injury; ww 85

Indexed keywords

3 NITROTYROSINE; ANTIINFLAMMATORY AGENT; FAS LIGAND; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; METALLOPORPHYRIN; MYELOPEROXIDASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PEROXYNITRITE; PROTEIN BAX; PROTEIN BCL 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; WW 85;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CATALYST; CONTROLLED STUDY; CYTOKINE PRODUCTION; DECOMPOSITION; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFICACY; DURA MATER; EDEMA; ENZYME ACTIVATION; LAMINECTOMY; LIPID PEROXIDATION; MALE; MOTOR PERFORMANCE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN EXPRESSION; SPINAL CORD INJURY; THORACIC SPINE; TISSUE INJURY;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CYTOKINES; DISEASE MODELS, ANIMAL; IMMUNOENZYME TECHNIQUES; IN SITU NICK-END LABELING; LIPID PEROXIDATION; MALE; MICE; MOTOR ACTIVITY; NEUTROPHIL INFILTRATION; NF-KAPPA B; PEROXIDASE; PEROXYNITROUS ACID; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEINS C-BCL-2; SPINAL CORD INJURIES; THIOBARBITURIC ACID REACTIVE SUBSTANCES; TYROSINE;

MUS;

EID: 67650889078     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.1080/10715760902954126     Document Type: Article

References (74)

1. Pineau I, Lacroix S. Proinflammatory cytokine synthesis in the injured mouse spinal cord: Multiphasic expression pattern and identification of the cell types involved. J Comp Neurol 2007;500:267-285.
2. Amar AP, Levy ML. Pathogenesis and pharmacological strategies for mitigating secondary damage in acute spinal cord injury. Neurosurgery 1999;44:1027-1040.
3. Bao F, DeWitt DS, Prough DS, Liu D. Peroxynitrite generated in the rat spinal cord induces oxidation and nitration of proteins: Reduction by mn (iii) tetrakis (4-benzoic acid) porphyrin. J Neurosci Res 2003;71:220-227.
4. Bao F, Liu D. Peroxynitrite generated in the rat spinal cord induces neuron death and neurological deficits. Neuroscience 2002;115:839-849.
5. Bao F, Liu D. Peroxynitrite generated in the rat spinal cord induces apoptotic cell death and activates caspase-3. Neuroscience 2003;116:59-70.
6. Liu D, Bao F, Prough DS, Dewitt DS. Peroxynitrite generated at the level produced by spinal cord injury induces peroxidation of membrane phospholipids in normal rat cord: Reduction by a metalloporphyrin. J Neurotrauma 2005;22:1123-1133.
7. Liu D, Ling X, Wen J, Liu J. The role of reactive nitrogen species in secondary spinal cord injury: Formation of nitric oxide, peroxynitrite, and nitrated protein. J Neurochem 2000;75:2144-2154.
8. Scott GS, Jakeman LB, Stokes BT, Szabo C. Peroxynitrite production and activation of poly (adenosine diphosphateribose) synthetase in spinal cord injury. Ann Neurol 1999;45:120-124.
9. Scott GS, Szabo C, Hooper DC. Poly(adp-ribose) polymerase activity contributes to peroxynitrite-induced spinal cord neuronal cell death in vitro. J Neurotrauma 2004;21: 1255-1263.
10. Xiong Y, Rabchevsky AG, Hall ED. Role of peroxynitrite in secondary oxidative damage after spinal cord injury. J Neurochem 2007;100:639-649.
11. Xu J, Kim GM, Chen S, Yan P, Ahmed SH, Ku G, Beckman JS, Xu XM, Hsu CY. Inos and nitrotyrosine expression after spinal cord injury. J Neurotrauma 2001;18:523-532.
12. Bolanos JP, Heales SJ, Land JM, Clark JB. Effect of peroxynitrite on the mitochondrial respiratory chain: Differential susceptibility of neurones and astrocytes in primary culture. J Neurochem 1995;64:1965-1972.
13. Blanchard-Fillion B, Souza JM, Friel T, Jiang GC, Vrana K, Sharov V, Barron L, Schoneich C, Quijano C, Alvarez B, Radi R, Przedborski S, Fernando GS, Horwitz J, Ischiropoulos H. Nitration and inactivation of tyrosine hydroxylase by peroxynitrite. J Biol Chem 2001;276:46017-46023.
14. Alvarez B, Radi R. Peroxynitrite reactivity with amino acids and proteins. Amino Acids 2003;25:295-311.
15. Genovese T, Mazzon E, Muia C, Bramanti P, De Sarro A, Cuzzocrea S. Attenuation in the evolution of experimental spinal cord trauma by treatment with melatonin. J Pineal Res 2005;38:198-208.
16. Salvemini D, Wang ZQ, Stern MK, Currie MG, Misko TP. Peroxynitrite decomposition catalysts: Therapeutics for peroxynitrite- mediated pathology. Proc Natl Acad Sci USA 1998;95:2659-2663.
17. Groves JT. Peroxynitrite: Reactive, invasive and enigmatic. Curr Opin Chem Biol 1999;3:226-235.
18. Misko TP, Highkin MK, Veenhuizen AW,Manning PT, Stern MK, Currie MG, Salvemini D. Characterization of the cytoprotective action of peroxynitrite decomposition catalysts. J Biol Chem 1998;273:15646-15653.
19. Salvemini D, Jensen MP, Riley DP, Misko TP. Therapeutic manipulations of peroxynitrite. Drug News Perspect 1998; 11:204-214.
20. Shimanovich R, Groves JT. Mechanisms of peroxynitrite decomposition catalyzed by fetmps, a bioactive sulfonated iron porphyrin. Arch Biochem Biophys 2001;387:307-317.
21. Bianchi C, Wakiyama H, Faro R, Khan T, McCully JD, Levitsky S, Szabo C, Sellke FW. A novel peroxynitrite decomposer catalyst (fp-15) reduces myocardial infarct size in an in vivo peroxynitrite decomposer and acute ischemia-reperfusion in pigs. Ann Thorac Surg 2002;74: 1201-1207.
22. Ferdinandy P, Danial H, Ambrus I, Rothery RA, Schulz R. Peroxynitrite is a major contributor to cytokine-induced myocardial contractile failure. Circ Res 2000;87:241-247.
23. Pacher P, Liaudet L, Bai P, Mabley JG, Kaminski PM, Virag L, Deb A, Szabo E, Ungvari Z, Wolin MS, Groves JT, Szabo C. Potent metalloporphyrin peroxynitrite decomposition catalyst protects against the development of doxorubicininduced cardiac dysfunction. Circulation 2003;107:896-904.
24. Lancel S, Tissier S, Mordon S, Marechal X, Depontieu F, Scherpereel A, Chopin C, Neviere R. Peroxynitrite decomposition catalysts prevent myocardial dysfunction and inflammation in endotoxemic rats. J Am Coll Cardiol 2004;43:2348-2358.
25. Genovese T, Mazzon E, Esposito E, Muia C, Di Paola R, Bramanti P, Cuzzocrea S. Beneficial effects of fetspp, a peroxynitrite decomposition catalyst, in a mouse model of spinal cord injury. Free Radic Biol Med 2007;43:763-780.
26. Pieper GM, Nilakantan V, Chen M, Zhou J, Khanna AK, Henderson JD Jr, Johnson CP, Roza AM, Szabo C. Protective mechanisms of a metalloporphyrinic peroxynitrite decomposition catalyst, ww85, in rat cardiac transplants. J Pharmacol Exp Ther 2005;314:53-60.
27. Mullane K. Neutrophil-platelet interactions and post-ischemic myocardial injury. Prog Clin Biol Res 1989;301: 39-51.
28. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979;95:351-358.
29. Sirin BH, Ortac R, Cerrahoglu M, Saribulbul O, Baltalarli A, Celebisoy N, Iskesen I, Rendeci O. Ischaemic preconditioning reduces spinal cord injury in transient ischaemia. Acta Cardiol 2002;57:279-285.
30. Bethea JR, Castro M, Keane RW, Lee TT, Dietrich WD, Yezierski RP. Traumatic spinal cord injury induces nuclear factor-kappab activation. J Neurosci 1998;18:3251-3260.
31. Basso DM, Beattie MS, Bresnahan JC. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 1995;12:1-21.
32. Joshi M, Fehlings MG. Development and characterization of a novel, graded model of clip compressive spinal cord injury in the mouse: Part 2. Quantitative neuroanatomical assessment and analysis of the relationships between axonal tracts, residual tissue, and locomotor recovery. J Neurotrauma 2002;19:191-203.
33. Joshi M, Fehlings MG. Development and characterization of a novel, graded model of clip compressive spinal cord injury in the mouse: Part 1. Clip design, behavioral outcomes, and histopathology. J Neurotrauma 2002;19:175-90.
34. Cuzzocrea S, Genovese T, Mazzon E, Crisafulli C, MinW, Di Paola R, Muia C, Li JH, Esposito E, Bramanti P, Xu W, Massuda E, Zhang J, Wang ZQ. Poly(adp-ribose) glycohydrolase activity mediates post-traumatic inflammatory reaction after experimental spinal cord trauma. J Pharmacol Exp Ther 2006;319:127-138.
35. Genovese T, Mazzon E, Mariotto S, Menegazzi M, Cardali S, Conti A, Suzuki H, Bramanti P, Cuzzocrea S. Modulation of nitric oxide homeostasis in a mouse model of spinal cord injury. J Neurosurg Spine 2006;4:145-153.
36. Glaser J, Gonzalez R, Sadr E, Keirstead HS. Neutralization of the chemokine cxcl10 reduces apoptosis and increases axon sprouting after spinal cord injury. J Neurosci Res 2006;84:724-734.
37. Tator CH. Review of experimental spinal cord injury with emphasis on the local and systemic circulatory effects. Neurochirurgie 1991;37:291-302.
38. Anderson DK, Hall ED. Pathophysiology of spinal cord trauma. Ann Emerg Med 1993;22:987-992.
39. Radi R, Beckman JS, Bush KM, Freeman BA. Peroxynitriteinduced membrane lipid peroxidation: The cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys 1991;288:481-487.
40. Klebanoff SJ. Reactive nitrogen intermediates and antimicrobial activity: Role of nitrite. Free Radic Biol Med 1993;14:351-360.
41. Bohle DS. Pathophysiological chemistry of nitric oxide and its oxygenation by-products. Curr Opin Chem Biol 1998;2:194- 200.
42. Greenacre SA, Ischiropoulos H. Tyrosine nitration: Localisation, quantification, consequences for protein function and signal transduction. Free Radic Res 2001;34:541-581.
43. Cuzzocrea S, Riley DP, Caputi AP, Salvemini D. Antioxidant therapy: A new pharmacological approach in shock, inflammation, and ischemia/ reperfusion injury. Pharmacol Rev 2001;53:135-159.
44. Pasternack RF, Gillies BS, Stromsted JP. Substitution reactions of a water-soluble metalloporphyrin with azide and 1,1,3,3-tetramethyl-2-thiourea. Bioinorg Chem 1978;8: 33-44.
45. Balavoine GG, Geletti YV, Bejan D. Catalysis of peroxynitrite reactions by manganese and iron porphyrins. Nitric Oxide 1997;1:507-521.
46. Szabo C, Mabley JG, Moeller SM, Shimanovich R, Pacher P, Virag L, Soriano FG, Van Duzer JH, Williams W, Salzman AL, Groves JT. Part i: Pathogenetic role of peroxynitrite in the development of diabetes and diabetic vascular complications: Studies with fp15, a novel potent peroxynitrite decomposition catalyst. Mol Med 2002;8:571-580.
47. Digerness SB, Harris KD, Kirklin JW, Urthaler F, Viera L, Beckman JS, Darley-Usmar V. Peroxynitrite irreversibly decreases diastolic and systolic function in cardiac muscle. Free Radic Biol Med 1999;27:1386-1392.
48. Mabley JG, Suarez-Pinzon WL, Hasko G, Salzman AL, Rabinovitch A, Kun E, Szabo C. Inhibition of poly (adpribose) synthetase by gene disruption or inhibition with 5-iodo-6-amino-1,2-benzopyrone protects mice from multiple- low-dose-streptozotocin-induced diabetes. Br J Pharmacol 2001;133:909-919.
49. Maybauer DM, Maybauer MO, Szabo C, Westphal M, Traber LD, Enkhbaatar P, Murthy KG, Nakano Y, Salzman AL, Herndon DN, Traber DL. Lung-protective effects of the metalloporphyrinic peroxynitrite decomposition catalyst ww- 85 in interleukin-2 induced toxicity. Biochem Biophys Res Commun 2008;377:786-791.
50. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 1996;271:C1424-C1437.
51. Eiserich JP, Hristova M, Cross CE, Jones AD, Freeman BA, Halliwell B, van der Vliet A. Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature 1998;391:393-397.
52. Sampson JB, Ye Y, Rosen H, Beckman JS. Myeloperoxidase and horseradish peroxidase catalyze tyrosine nitration in proteins from nitrite and hydrogen peroxide. Arch Biochem Biophys 1998;356:207-213.
53. Naidu BV, Fraga C, Salzman AL, Szabo C, Verrier ED, Mulligan MS. Critical role of reactive nitrogen species in lung ischemia-reperfusion injury. J Heart Lung Transplant 2003;22:784-793.
54. Bowie A, O'Neill LA. Oxidative stress and nuclear factorkappab activation: A reassessment of the evidence in the light of recent discoveries. Biochem Pharmacol 2000;59:13-23.
55. Haddad JJ. Antioxidant and prooxidant mechanisms in the regulation of redox(y)-sensitive transcription factors. Cell Signal 2002;14:879-897.
56. Verma IM. Nuclear factor (nf)-kappab proteins: Therapeutic targets. Ann Rheum Dis 2004;63(Suppl 2):iI57-ii61.
57. Genovese T, Mazzon E, Crisafulli C, Di Paola R, Muia C, Bramanti P, Cuzzocrea S. Immunomodulatory effects of etanercept in an experimental model of spinal cord injury. J Pharmacol Exp Ther 2006;316:1006-1016.
58. Streit WJ, Semple-Rowland SL, Hurley SD, Miller RC, Popovich PG, Stokes BT. Cytokine mrna profiles in contused spinal cord and axotomized facial nucleus suggest a beneficial role for inflammation and gliosis. Exp Neurol 1998;152:74- 87.
59. Liu J, MarinoMW,Wong G, Grail D, Dunn A, Bettadapura J, Slavin AJ, Old L, Bernard CC. Tnf is a potent antiinflammatory cytokine in autoimmune-mediated demyelination. Nat Med 1998;4:78-83.
60. Ousman SS, David S. Mip-1alpha, mcp-1, gm-csf, and tnfalpha control the immune cell response that mediates rapid phagocytosis of myelin from the adult mouse spinal cord. J Neurosci 2001;21:4649-4656.
61. Shafit-Zagardo B, Sharma N, Berman JW, Bornstein MB, Brosnan CF. Csf-1 expression is upregulated in astrocyte cultures by il-1 and tnf and affects microglial proliferation and morphology in organotypic cultures. Int J Dev Neurosci 1993;11:189-198.
62. Sharma HS, Winkler T, Stalberg E, Gordh T, Alm P, Westman J. Topical application of tnf-alpha antiserum attenuates spinal cord trauma induced edema formation, microvascular permeability disturbances and cell injury in the rat. Acta Neurochir Suppl 2003;86:407-413.
63. Genovese T, Mazzon E, Rossi A, Di Paola R, Cannavo G, Muia C, Crisafulli C, Bramanti P, Sautebin L, Cuzzocrea S. Involvement of 5-lipoxygenase in spinal cord injury. J Neuroimmunol 2005;166:55-64.
64. Crocker SJ, Whitmire JK, Frausto RF, Chertboonmuang P, Soloway PD, Whitton JL, Campbell IL. Persistent macrophage/microglial activation and myelin disruption after experimental autoimmune encephalomyelitis in tissue inhibitor of metalloproteinase-1-deficient mice. Am J Pathol 2006;169:2104-2116.
65. Holtz A, Nystrom B, Gerdin B. Spinal cord injury in rats: Inability of nimodipine or anti-neutrophil serum to improve spinal cord blood flow or neurologic status. Acta Neurol Scand 1989;79:460-467.
66. Fan LH, Wang KZ, Cheng B, Wang CS, Dang XQ. Antiapoptotic and neuroprotective effects of tetramethylpyrazine following spinal cord ischemia in rabbits. BMC Neurosci 2006;7:48.
67. Scholz J, Broom DC, Youn DH, Mills CD, Kohno T, Suter MR, Moore KA, Decosterd I, Coggeshall RE, Woolf CJ. Blocking caspase activity prevents transsynaptic neuronal apoptosis and the loss of inhibition in lamina ii of the dorsal horn after peripheral nerve injury. J Neurosci 2005;25: 7317-7323.
68. Woodhouse A, Vincent AJ, Kozel MA, Chung RS, Waite PM, Vickers JC, West AK, Chuah MI. Spinal cord tissue affects ensheathing cell proliferation and apoptosis. Neuroreport 2005;16:737-740.
69. Merrill JE, Ignarro LJ, Sherman MP, Melinek J, Lane TE. Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J Immunol 1993;151:2132-2141.
70. Wang JY, Shum AY, Ho YJ, Wang JY. Oxidative neurotoxicity in rat cerebral cortex neurons: Synergistic effects of h2o2 and no on apoptosis involving activation of p38 mitogen-activated protein kinase and caspase-3. J Neurosci Res 2003;72:508- 519.
71. Chittenden T, Harrington EA, O'Connor R, Flemington C, Lutz RJ, Evan GI, Guild BC. Induction of apoptosis by the bcl-2 homologue bak. Nature 1995;374:733-736.
72. Bar-Peled O, Knudson M, Korsmeyer SJ, Rothstein JD. Motor neuron degeneration is attenuated in bax-deficient neurons in vitro. J Neurosci Res 1999;55:542-556.
73. Pieper AA, Verma A, Zhang J, Snyder SH. Poly (adp-ribose) polymerase, nitric oxide and cell death. Trends Pharmacol Sci 1999;20:171-181.
74. LaPlaca MC, Raghupathi R, Verma A, Pieper AA, Saatman KE, Snyder SH, McIntosh TK. Temporal patterns of poly(adp-ribose) polymerase activation in the cortex following experimental brain injury in the rat. J Neurochem 1999;73:205-213.