Experimental allergic encephalomyelitis in the rat is inhibited by aminoguanidine, an inhibitor of nitric oxide synthase

Journal of Neuroimmunology

Volumn 64, Issue 2, 1996, Pages 123-133

  Zhao, Weiguo ^a   Tilton, Ronald G ^b   Corbett, John A ^b   McDaniel, Michael L ^b   Misko, Thomas P ^c   Williamson, Joseph R ^b   Cross, Anne H ^b   Hickey, William F ^a  

^a DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MONSANTO COMPANY   (United States)

Author keywords

Aminoguanidine; Experimental allergic encephalomyelitis; Multiple sclerosis; NADPH diaphorase; Nitric oxide

Indexed keywords

AMINOGUANIDINE; NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; ETIOLOGY; FEMALE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0029871609     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/0165-5728(95)00158-1     Document Type: Article

References (57)

1. Arnon, R. (1981) Experimental allergic encephalomyelitis: susceptibility and suppression. Immunol. Rev. 55, 5-30.
2. Ben-Nun, A., Wekerle, H. and Cohen, I.R. (1981) The rapid isolation of clonable antigen-specific T lymphocyte lines capable of mediating autoimmune encephalomyelitis. Eur. J. Immunol. 11, 195-199.
3. Billau, A., Heremans, H., Vanderkerckhove, F., Dijkmans, R., Sobis, H., Meulepas, E. and Carton, H. (1988) Enhancement of experimental allergic encephalomyelitis in mice by antibodies against IFN-γ. J. Immunol. 140, 1506-1510.
4. Bo, L., Dawson, T.M., Wesselingh, S., Mork, S., Choi, S., Kong, P.A., Hanley, D. and Trapp, B. (1994) Induction of nitric oxide synthase in demyelinating regions of multiple sclerosis brains. Ann. Neurol. 36, 778-786.
5. Bolton, C., Borel, J.F., Cuzner, L.M., Davison, A.N. and Turner, A.M. (1982) Immunosuppression by cyclosporin A of experimental allergic encephalomyelitis. J. Neurol. Sci. 56, 147-153.
6. Bredt, D.S. and Snyder, S.H. (1990) Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. USA 87, 682-685.
7. Brosnan, C.F., Bernstein, M.B. and Bloom, B.R. (1981) The effects of macrophage depletion on the clinical and pathologic expression of experimental allergic encephalomyelitis. J. Immunol. 126, 614-620.
8. Brosnan, C.F., Goldmuntz, E.A., Cammer, W., Factor, S.M., Bloom, B.R. and Norton, W.T. (1985) Prazosin, an α1-adrenergic receptor antagonist, suppresses experimental autoimmune encephalomyelitis in the Lewis rat. Proc. Natl. Acad. Sci. USA 82, 5915-5919.
9. Brostoff, S.W. and Mason, D.W. (1984) Experimental allergic encephalomyelitis: successful treatment in vivo with a monoclonal antibody that recognizes T helper cells. J. Immunol. 133, 1938-1942.
10. Brownlee, M., Vlassara, H., Kooney, A., Ulrich, P. and Cerami, A. (1986) Aminoguanidine prevents diabetes-induced arterial wall protein cross-linking. Science 232, 1629-1632.
11. Brownlee, M., Cerami, A. and Vlassara, H. (1988) Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications. New Engl. J. Med. 318, 1315-1321.
12. Corbett, J.A. and McDaniel, M.L. (1995) Intra-islet release of interleukin 1 inhibits beta cell function by inducing beta cell expression of inducible nitric oxide synthase. J. Exp. Med. 181, 559-568.
13. Corbett, J.A., Tilton, R.G., Chang, K., Hasan, K.S., Ido, Y., Wang, J.L., Sweetland, M.A., Lancaster, J.R. Jr., Williamson, J.R. and McDaniel, M.L. (1992) Aminoguanidine, a novel inhibitor of nitric oxide formation, prevents diabetic vascular dysfunction. Diabetes 41, 552-556.
14. Corbett, J.A., Mikhael, A., Shimizu, J., Frederick, K., Misko, T.P., McDaniel, M.L., Kanagawa, O. and Unanue, E.R. (1993a) Nitric oxide production in islets from nonobese diabetic mice: aminoguanidine-sensitive and -resistant stages in the immunological diabetic process. Proc. Natl. Acad. Sci. USA 90, 8992-8995.
15. Corbett, J.A., Kwon, G., Turk, J. and McDaniel, M.L. (1993b) IL-1 beta induces the coexpression of both nitric oxide synthase and cyclooxygenase by islets of Langerhans: activation of cyclooxygenase by nitric oxide. Biochemistry 32, 13767-13770.
16. Cross, A.H., Misko, T.P., Lin, R.F., Hickey, W.F., Trotter, J.L. and Tilton, R.G. (1994) Aminoguanidine, an inhibitor of inducible nitric oxide synthase, ameliorates experimental autoimmune encephalomyelitis in SJL mice. J. Clin. Invest. 93, 2684-2690.
17. Dawson, T.M., Bredt, D.S., Fotuhi, M., Hwang, P.M. and Snyder, S.H. (1991) Nitric oxide synthase and neuronal NADPH-d are identical in brain and peripheral tissues. Proc. Natl. Acad. Sci. USA 88, 7797-7801.
18. De Groot, C.J., Sminia, T. and Dijkstra, C.D. (1989) Isolation and characterization of brain macrophages from the newborn and adult rats with EAE. Immunobiology 179, 314-327.
19. Engelhardt, B.T., Diamantstein, T. and Wekerle, H. (1989) Immunotherapy of experimental autoimmune encephalomyelitis (EAE): differential effect of anti-IL-2 receptor antibody therapy on actively induced and T-line mediated EAE of the Lewis rat. J. Autoimmun. 2, 61-73.
20. Galea, E., Feinstein, D.L. and Reis, D.J. (1992) Induction of calcium-independent nitric oxide synthase activity in primary rat glial cultures. Proc. Natl. Acad. Sci. USA 89, 10945-10949.
21. Hashim, G.A., Vandenbark, A.A., Galang, A.B., Diamanduros, T., Carvalho, E., Srinivasan, J., Jones, R., Vainiene, M., Morrison, W.J. and Offner, H. (1990) Antibodies specific for Vβ8 receptor peptide suppress experimental autoimmune encephalomyelitis. J. Immunol. 144, 4621-4627.
22. Hibbs, J.B. (1990) In: S. Moncada and E.A. Higgs (Eds.), Nitric Oxide from L-Arginine: A Bioregulatory System. Elsevier, New York, NY, pp. 189-223.
23. Hibbs, 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.
24. Hickey, W.F., Gonatas, N.K., Kimura, H. and Wilson, D.B. (1983) Identification and quantitation of T lymphocyte subsets found in the spinal cord of the Lewis rat during acute experimental allergic encephalomyelitis. J. Immunol. 131, 2805-2809.
25. Hickey, W.F., Cohen, J.A, and Burns, J.B. (1987) A quantitative immunohistochemical comparison of actively versus adoptively induced experimental allergic encephalomyelitis in the Lewis rat. Cell. Immunol. 109, 272-282.
26. Hope, B.T., Michael, G.J., Knigge, K.M. and Vincent, S.R. (1991) Neuronal NADPH diaphorase is a nitric oxide synthase. Proc. Natl. Acad. Sci. USA 88, 2811-2814.
27. Hui, J.Y. and Taylor, S.L. (1985) Inhibition of in vivo histamine metabolism in rats by foodborne and pharmacologic inhibitors of diamine oxidase, histamine N-methyltransferase, and monoamine oxidase. Toxicol. Appl. Pharmacol. 81, 241-249.
28. Ialenti, A., Ianaro, A., Moncada, S. and DiRosa, M. (1992) Modulation of acute inflammation by endogenous nitric oxide. Eur. J. Pharmacol. 211, 177-182.
29. Ignarro, L.J. (1991) Signal transduction mechanisms involving nitric oxide. Biochem. Pharmacol. 41, 485-490.
30. Iyengar, R., Stuehr, D.J. and Marletta, M.A. (1987) Macrophage synthesis of nitrite, nitrate and N-nitrosamines: precursors and role of the respiratory burst. Proc. Natl. Acad. Sci. USA 84, 6369-6373.
31. Jefferies, W.A., Green, J.R. and Williams, A.F. (1985) Authentic T helper CD4 (W3/25) antigen on rat peritoneal macrophages. J. Exp. Med. 162, 117-127.
32. + suppressor cells inhibit the function of effector cells of experimental autoimmune encephalomyelitis through a mechanism involving transforming growth factor-beta. J. Immunol. 146, 1163-1168.
33. Kolb, H. and Kolb-Bachofen, V. (1992) Nitric oxide: a pathogenic factor in autoimmunity. Immunol. Today 13, 157-160.
34. Lassmann, H., Zimprich, F., Rossler, K. and Vass, K. (1991) Inflammation in the nervous system. Basic mechanisms and immunological concepts. Revue Neurol. 147, 763-781.
35. Lemire, J.M. and Archer, D.C. (1991) 1,25-Dihydroxyvitamin D3 prevents the in vivo induction of murine experimental autoimmune encephalomyelitis. J. Clin. Invest. 87, 1103-1107.
36. Liew, F.Y. and Cox, F.E.G. (1991) Immunoparasitol. Today, A17-A21.
37. Loewenstein, C.J., Dinerman, J.L. and Snyder, S.H. (1994) Nitric oxide: a physiologic messenger. Ann. Int. Med. 120, 227-237.
38. MacPhee, I.A., Antoni, F.A. and Mason, D.W. (1989) Spontaneous recovery of rats from experimental allergic encephalomyelitis is dependent on regulation of the immune system by endogenous adrenal corticosteroids. J. Exp. Med. 169, 431-445.
39. Matsumoto, Y., Hara, N., Tanaka, R. and Fujiwara, M. (1986) Immunohistochemical analysis of the rat central nervous system during experimental allergic encephalomyelitis, with special reference to Ia-positive cells with dendritic morphology. J. Immunol. 136, 3668-3676.
40. Mason, D.W., Arthur, R.P., Dallman, D.J., Green, J.R., Spickett, G.P. and Thomas, M.L. (1983) Functions of rat T-lymphocyte subsets isolated by means of monoclonal antibodies. Immunol. Rev. 74, 57-82.
41. McCartney-Francis, N., Allen, J.B. and Mizel, D.E. (1993) Suppression of arthritis by an inhibitor of nitric oxide synthase. J. Exp. Med. 178, 749-754.
42. McMaster, W.R. and Williams, A.F. (1979) Identification of Ia glycoproteins in the rat thymus and purification from rat spleen. Eur. J. Immunol. 9, 426-433.
43. Merrill, J.E., Ignarro, L.J., Sherman, M.P., Melinek, J. and Lane, T.E. (1993) Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J. Immunol. 151, 2132-2141.
44. Moncada, S., Palmer, R.M. and Higgs, E.A. (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43, 109-141.
45. Oswald, I.P., Eltoum, I., Wynn, T.A., Schwartz, B., Caspar, P., Paulin, D., Sher, A. and James, S.L. (1994) Endothelial cells are activated by cytokine treatment to kill an intravascular parasite, Schistosoma mansoni, through the production of nitric oxide. Proc. Natl. Acad. Sci. USA 91, 999-1003.
46. Radomski, M.W., Palmer, R.M., Moncada, S. (1990) Glucocorticoids inhibit the expression of an inducible, but not the constitutive nitric oxide synthase in vascular endothelial cells. Proc. Natl. Acad. Sci. USA 87, 10043-10047.
47. Rosenberg, S.A., Spiess, P.L. and Schwarz, S. (1978) In vitro growth of murine T cells. I. Production of factors necessary for T cell growth. J. Immunol. 121, 1946-1950.
48. Ruddle, N.H., Bergman, C.M., McGrath, K.M., Lingenheld, E.G., Grunnet, M.L., Padula, S.J. and Clark, R.B. (1990) An antibody to lymphotoxin and tumor necrosis factor prevents transfer of experimental allergic encephalomyelitis. J. Exp. Med. 172, 1193-1200.
49. Schluesener, H.J. and Lider, O. (1989) Transforming growth factors beta 1 and beta 2: cytokines with identical immunosuppressive effects and a potential role in the regulation of autoimmune T cell function. J. Neuroimmunol. 24, 249-58.
50. Simmons, M.L. and Murphy, S. (1992) Induction of nitric oxide synthase in glial cells. J. Neurochem. 59, 897-905.
51. Stuehr, D.J., Cho, H.J., Kwon, N.S., Weise, M.F. and Nathan, C.F. (1991) 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.
52. Vandenbark, A.A., Gill, T. and Offner, H. (1985) Myelin basic protein-specific T lymphocyte line that mediates experimental allergic encephalomyelitis. J. Immunol. 135, 223-228.
53. Vincent, S.R. (1986) In: P. Panula, H. Paivarinta and S. Soinila (Eds.), Neurohistochemistry: Modern Methods and Applications. Alan R. Liss, New York, NY, pp. 375-396.
54. Xie, Q. and Nathan, C. (1994) The high-output nitric oxide pathway: role and regulation. J. Leuk. Biol. 56, 576-582.
55. Zhang, J., Dawson, V.L., Dawson, T.M. and Snyder, S.H. (1994) Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science 263, 687-689.
56. Zheng, Y.M., Schafer, M.K.-H., Weihe, E., Sheng, H., Corisdeo, S., Fu, Z.F., Koprowski, H. and Dietzschold, B. (1993) Severity of neurological signs and degree of inflammatory lesions in the brains of rats with Borna diseases correlate with the induction of nitric oxide synthase. J. Virol. 67, 5786-5791.
57. Zielasek, J., Jung, S., Gold, R., Liew, F.Y., Tokka, K.V. and Hartung, H.P. (1995) Administration of nitric oxide synthase inhibitors in experimental autoimmune neuritis and experimental autoimmune encephalitis. J. Neuroimmunol. 58, 81-88.