A catalyst of peroxynitrite decomposition inhibits murine experimental autoimmune encephalomyelitis

Journal of Neuroimmunology

Volumn 107, Issue 1, 2000, Pages 21-28

  Cross, Anne H ^a   San, Manuel ^a   Stern, Michael K ^b   Keeling, Richard M ^a   Salvemini, Daniela ^c   Misko, Thomas P ^c  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MONSANTO COMPANY   (United States)

^c PFIZER INC   (United States)

Author keywords

Experimental autoimmune encephalomyelitis; Multiple sclerosis; Nitric oxide; Peroxynitrite; Superoxide

Indexed keywords

3 NITROTYROSINE; MYELIN BASIC PROTEIN; NITRIC OXIDE; PEROXYNITRITE; SUPEROXIDE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATALYST; CONTROLLED STUDY; DECOMPOSITION; FEMALE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL;

ANIMALS; CATALYSIS; CENTRAL NERVOUS SYSTEM; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; FERRIC COMPOUNDS; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE TRANSFUSION; LYMPHOCYTES; METALLOPORPHYRINS; MICE; MICE, INBRED STRAINS; NITRATES; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; TYROSINE;

EID: 0034632225     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-5728(00)00242-3     Document Type: Article

References (41)

1. Alvord E.C., Kies M.W., Suckling A.J. Experimental allergic encephalomyelitis: a useful model for multiple sclerosis. Prog. Clin. Biol. Res. 146:1984;1-554.
2. Ando D.G., Clayton J., Kono D., Urban J.L., Sercarz E.E. Encephalitogenic T cells in the B10.PL model of experimental allergic encephalomyelitis (EAE) are of the Th1 lymphokine subtype. Cell. Immunol. 124:1989;132-143.
3. Bagasra O., Michaels F.H., Zheng Y.M., Bobroski L.E., Spitsin S.V., Fu Z.F., Twadros R., Koprowski H. Activation of the inducible form of nitric oxide synthase in the brains of patients with multiple sclerosis. Proc. Natl. Acad. Sci. USA. 92:1995;12041-12045.
4. Beckman J.S., Crow J.P. Pathological implication of nitric oxide, superoxide and peroxynitrite formation. Biochem. Soc. Trans. 21:1993;330-334.
5. Beckman J.S., Beckman T.W., Chen J., Marshall P.A., Freeman B.A. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA. 87:1990;1620-1624.
6. Beckman J.S., Ye Y.Z., Anderson P.G., Accavitti M.A., Tarpey M.M., White C.R. Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistry. Biol. Chem. Hoppe-Seyler. 375:1994;81-88.
7. Bo L., Dawson T.M., Wesselingh S., Mork S., Choi S., Kong P.H., Hanley D., Trapp B.D. Induction of nitric oxide synthase in demyelinating regions of multiple sclerosis brains. Ann. Neurol. 16:1994;778-786.
8. Brenner T., Brocke S., Szafer F., Sobel R.A., Parkinson J.F., Perez D.H., Steinman L. Inhibition of nitric oxide synthase for treatment of experimental autoimmune encephalomyelitis. J. Immunol. 158:1997;2940-2946.
9. Brosnan C.F., Battistini L., Raine C.S., Dickson D.W., Casadevall A., Lee S.C. Reactive nitrogen intermediates in human neuropathology: an overview. Dev. Neurosci. 16:1994;152-161.
10. Connor J.R., Manning P.T., Settle S.L., Moore W.M., Jerome G.M., Webber R.K., Tjoeng F.S., Currie M.G. Suppression of adjuvant-induced arthritis by selective inhibition of inducible nitric oxide synthase. Eur. J. Pharmacol. 273:1995;15-24.
11. Cowden W.B., Cullen F.A., Staykova M.A., Willenborg D.O. Nitric oxide is a potential down-regulating molecule in autoimmune disease: inhibition of nitric oxide production renders PVG rats highly susceptible to EAE. J. Neuroimmunol. 88:1998;1-8.
12. Cross A.H., Misko T.P., Lin R.F., Hickey W.F., Trotter J.L., Tilton R.G. Aminoguanidine, an inhibitor of inducible nitric oxide synthase, ameliorates experimental autoimmune encephalomyelitis in SJL mice. J. Clin. Invest. 93:1994;2684-2690.
13. Cross A.H., Manning P.T., Stern M.K., Misko T.P. Evidence for the production of peroxynitrite in inflammatory CNS demyelination. J. Neuroimmunol. 80:1997;121-130.
14. Cross A.H., Manning P.T., Keeling R.M., Schmidt R.E., Misko T.P. Peroxynitrite formation within the central nervous system in active multiple sclerosis. J. Neuroimmunol. 88:1998;45-56.
15. DeGroot C.J.A., Ruuls S.R., Theeuwes J.W.M., Dijkstra C.D., Van der Valk P. Immunocytochemical characterization of the expression of inducible and constitutive isoforms of nitric oxide synthase in demyelinating multiple sclerosis lesions. J. Neuropathol. Exp. Neurol. 56:1997;10-20.
16. Ding M., Zhang M., Wong J.L., Rogers N.E., Ignarro L.J., Voskuhl R.R. Antisense knockdown of inducible nitric oxide synthase inhibits induction of experimental autoimmune encephalomyelitis in SJL/J mice. J. Immunol. 160:1998;2560-2564.
17. Fenyk-Meoldy J.E., Garrison A.E., Brunnert S.R., Weidner J.R., Shen F., Shelton B.A., Mudgett J.S. Experimental autoimmune encephalomyelitis is exacerbated in mice lacking the NOS2 gene. J. Immunol. 160:1998;2940-2946.
18. Haddad I.Y., 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. 94:1994;2407-2413.
19. 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. 267:1994;L242-L249.
20. Hooper D.C., Bagasra O., Marini J.C., Zborek A., Ohnishi S.T., Kean R., Champion J.M., Sarker A.B., Bobroski L., Farber J., Akaike T., Maeda H., Koprowski H. Prevention of experimental allergic encephalomyelitis by targeting nitric oxide and peroxynitrite: implications for the treatment of multiple sclerosis. Proc. Natl. Acad. Sci. USA. 94:1997;2528-2533.
21. Hooper D.C., Spitsin S., Khan R.B., Champion J.M., Dickson G.M., Chaudhry I., Koprowski H. Uric acid, a natural scavenger of peroxynitrite, in experimental allergic encephalomyelitis and multiple sclerosis. Proc. Natl. Acad. Sci. USA. 95:1998;675-680.
22. Ischiropoulos H., Zhu L., Beckman J.S. Peroxynitrite formation from macrophage-derived nitric oxide. Arch. Biochem. Biophys. 198:1992;446-451.
23. Johnson A.W., Land J.M., Thompson E.J., Bolanos J.P., Clark J.B., Heales S.J.R. Evidence for increased nitric oxide production in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry. 58:1995;107.
24. Koprowski H., Zheng Y.M., Heber-Katz E., Fraser N., Rorke L., Fu Z.F., Hanlon C., Dietzschold B. In vivo expression of inducible nitric oxide synthase in experimentally induced neurologic disease. Proc. Natl. Acad. Sci. USA. 90:1993;3024-3027.
25. Lin R.F., Lin T.W., Tilton R.G., Cross A.H. Nitric oxide localized to spinal cords of mice with experimental allergic encephalomyelitis: an electron paramagnetic resonance study. J. Exp. Med. 178:1993;643-648.
26. Martin B.B.L., Wu D., Jakes S., Graves D.J. Chemical influences on the specificity of tyrosine phosphorylation. J. Biol. Chem. 265:1990;7108-7111.
27. Misko T.P., Highkin M.K., Veenhuizen A.W., Manning P.T., Stern M.K., Currie M.G., Salvemini D. Characterization of the cytoprotective action of peroxynitrite decomposition catalysts. J. Biol. Chem. 273:1998;15646-15653.
28. Mitrovic B., Ignarro L.J., Montestruque S., Smoll A., Merrill J.E. Nitric oxide as a potential pathological mechanism in demyelination: its differential effects on primary glial cells in vitro. Neuroscience. 61:1994;575-585.
29. Moncada S., Palmer R.M.J., Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43:1991;109-142.
30. Nathan C.F., Hibbs J.B. Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol. 3:1991;65-70.
31. Okuda Y., Sakoda S., Fujimara H., Yanagihara T. Nitric oxide via an inducible isoform of nitric oxide synthase is a possible factor to eliminate inflammatory cells from the central nervous system of mice with experimental autoimmune encephalomyelitis. J. Neuroimmunol. 73:1997;107-116.
32. Pryor W.A., Squadrito G.L. The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am. J. Physiol. 268:1995;L699-L721.
33. Rachmilewitz D., Stamler J.S., Karmeli F., Mullins M.E., Singel D.J., Loscalzo J., Xavier R.J., Podolsky D.K. Peroxynitrite-induced rat colitis - a new model of colonic inflammation. Gastroenterology. 105:1993;1681-1688.
34. Ruuls S.R., Vanderlinden S., Sontrop K., Huitinga I., Dijkstra C.D. Aggravation of experimental allergic encephalomyelitis by administration of nitric oxide synthase inhibitors. Clin. Exp. Immunol. 103:1996;467-474.
35. 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.
36. Stern M.K., Jensen M.P., Kramer K. Peroxynitrite decomposition catalysts. J. Am. Chem. Soc. 18:1996;8735-8736.
37. Van der Veen R.C., Hinton D.R., Incardonna F., Hofman F.M. Extensive peroxynitrite activity during progressive stages of central nervous system inflammation. J. Neuroimmunol. 77:1997;1-7.
38. Xie Q.-W., Nathan C. The high-output nitric oxide pathway: role and regulation. J. Leukoc. Biol. 56:1994;576-582.
39. Zamvil S., Nelson P., Trotter J., Mitchell D., Knobler R., Fritz R., Steinman L. T cell clones specific for myelin basic protein induce chronic relapsing paralyses and demyelination. Nature (London). 317:1985;355-358.
40. Zhao W., Tilton R.G., Corbett J.A., McDaniel M.L., Misko T.P., Williamson J.R., Cross A.H., Hickey W.F. Experimental allergic encephalomyelitis in the rat is inhibited by aminoguanidine, an inhibitor of inducible nitric oxide synthase. J. Neuroimmunol. 64:1996;123-133.
41. Zielasek J., Jung S., Gold R., Liew F.Y., Toyka K.V., Hartung H.P. Administration of nitric oxide synthase inhibitors in experimental autoimmune neuritis and experimental autoimmune encephalomyelitis. J. Neuroimmunol. 58:1995;81-88.