Tempol ameliorates murine viral encephalomyelitis by preserving the blood-brain barrier, reducing viral load, and lessening inflammation

Free Radical Biology and Medicine

Volumn 48, Issue 5, 2010, Pages 704-712

  Tsuhako, Maria Heloisa ^a   Augusto, Ohara ^b   Linares, Edlaine ^b   Chadi, Gerson ^c   Giorgio, Selma ^d   Pereira, Carlos A ^a  

^a INSTITUTO BUTANTAN   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c Department of Neurology   (Brazil)

^d UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

Anti inflammatory; Antioxidant; Encephalomyelitis; Free radicals; Inflammation; Mouse hepatitis virus; Multiple sclerosis; Nitric oxide derived oxidants; Redox status; Tempol

Indexed keywords

GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; TEMPOL; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG SCREENING; ENCEPHALOMYELITIS; FEMALE; IMMUNE STATUS; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MORNING DOSAGE; MOUSE; MURINE HEPATITIS CORONAVIRUS; NITRATION; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD; SURVIVAL RATE; T LYMPHOCYTE; VIRUS LOAD;

ANIMALS; ANTIOXIDANTS; BLOOD-BRAIN BARRIER; CORONAVIRUS INFECTIONS; CYCLIC N-OXIDES; ENCEPHALOMYELITIS; FEMALE; HUMANS; INFLAMMATION; INTERFERON-GAMMA; MACROPHAGES; MICE; MICE, INBRED C57BL; MULTIPLE SCLEROSIS; MURINE HEPATITIS VIRUS; NITRIC OXIDE SYNTHASE TYPE II; OXIDATION-REDUCTION; SPIN LABELS; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA; VIRAL LOAD;

ANIMALIA; MURINAE; MURINE HEPATITIS VIRUS; MUS;

EID: 75449096560     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.12.013     Document Type: Article

References (55)

1. 't Hart B.A., Hintzen R.Q., and Laman J.D. Multiple sclerosis-a response-to-damage model. Trends Mol. Med. 15 (2009) 235-244
2. Ebers G.C., Sadovnick A.D., and Risch N.J. Canadian Collaborative Study Group. A genetic basis for familial aggregation in multiple sclerosis. Nature 377 (1995) 150-151
3. International Multiple Sclerosis Genetics Consortium. Risk alleles for multiple sclerosis identified by a genomewide study. N. Engl. J. Med. 357 (2007) 851-862
4. Risch N., and Merikangas K. The future of genetic studies of complex human diseases. Science 273 (1996) 1516-1517
5. Fazakerley J.K., and Walker R. Virus demyelination. J. Neurovirol. 9 (2003) 148-164
6. Lane T.E., and Buchmeier M.J. Murine coronavirus infection: a paradigm for virus-induced demyelinating disease. Trends Microbiol. 5 (1997) 9-14
7. Glass W.G., Chen B.P., Liu M.T., and Lane T.E. Mouse hepatitis virus infection of the central nervous system: chemokine-mediated regulation of host defense and disease. Viral Immunol. 15 (2002) 261-272
8. Gonsette R.E. Neurodegeneration in multiple sclerosis: the role of oxidative stress and excitotoxicity. J. Neurol. Sci. 274 (2008) 48-53
9. Augusto O., Bonini M.G., Amanso A.M., Linares E., Santos C.C., and de Menezes S.L. Nitrogen dioxide and carbonate radical anion: two emerging radicals in biology. Free Radic. Biol. Med. 32 (2002) 841-859
10. Radi R. Nitric oxide, oxidants, and protein tyrosine nitration. Proc. Natl. Acad. Sci. USA 101 (2004) 4003-4008
11. Szabó C., Ischiropoulos H., and Radi R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discovery 6 (2007) 662-680
12. Scott G.S., Spitsin S.V., Kean R.B., Mikheeva T., Koprowski H., and Hooper D.C. Therapeutic intervention in experimental allergic encephalomyelitis by administration of uric acid precursors. Proc. Natl. Acad. Sci. USA 99 (2002) 16303-16308
13. Teixeira S.A., Castro G.M., Papes F., Rogério F., Langone F., Santos L.M., Arruda P., de Nucci G., and Muscará M.N. Expression and activity of nitric oxide synthase isoforms in rat brain during the development of experimental allergic encephalomyelitis. Brain Res. Mol. Brain Res. 99 (2002) 17-25
14. Zeis T., Probst A., Steck A.J., Stadelmann C., Brück W., and Schaeren-Wiemers N. Molecular changes in white matter adjacent to an active demyelinating lesion in early multiple sclerosis. Brain Pathol. 19 (2008) 459-466
15. Augusto O., Trindade D.F., Linares E., and Vaz S.M. Cyclic nitroxides inhibit the toxicity of nitric oxide-derived oxidants: mechanisms and implications. An. Acad. Bras. Cienc. 80 (2008) 179-189
16. Soule B.P., Hyodo F., Matsumoto K., Simone N.L., Cook J.A., Krishna M.C., and Mitchell J.B. The chemistry and biology of nitroxide compounds. Free Radic. Biol. Med. 42 (2007) 1632-1650
17. Goldstein S., Samuni A., Hideg K., and Merenyi G. Structure-activity relationship of cyclic nitroxides as SOD mimics and scavengers of nitrogen dioxide and carbonate radicals. J. Phys. Chem. A 110 (2006) 3679-3685
18. Goldstein S., Samuni A., and Merenyi G. Reactions of nitric oxide, peroxynitrite and carbonate radical with nitroxides and their corresponding oxammonium cations. Chem. Res. Toxicol. 17 (2004) 250-257
19. Vaz S.M., and Augusto O. Inhibition of myeloperoxidase-mediated protein nitration by tempol: kinetics, mechanism, and implications. Proc. Natl. Acad. Sci. USA 105 (2008) 8191-8196
20. Rees M.D., Bottle S.E., Fairfull-Smith K.E., Malle E., Whitelock M., and Davies M.J. Inhibition of myeloperoxidase-mediated hypochlorous acid production by nitroxides. Biochem. J. 421 (2009) 79-85
21. Goldstein S., Samuni A., and Merenyi G. Kinetics of the reaction between nitroxide and thiyl radicals: nitroxides as antioxidants in the presence of thiols. J. Phys. Chem. 112 (2008) 8600-8605
22. Lam M.A., Pattison D.I., Bottle S.E., Keddie D.J., and Davies M.J. Nitric oxide and nitroxides can act as efficient scavengers of protein-derived free radicals. Chem. Res. Toxicol. 21 (2008) 2111-2119
23. Borisenko G.G., Martin I., Zhao Q., Amoscato A.A., and Kagan V.E. Nitroxides scavenge myeloperoxidase-catalyzed thiyl radicals in model systems and in cells. J. Am. Chem. Soc. 126 (2004) 9221-9232
24. Thiemermann C. Membrane-permeable radical scavengers (tempol) for shock, ischemia-reperfusion injury, and inflammation. Crit. Care Med. 31 (2003) S76-S84
25. Gilmore W., Correale J., and Weiner L.P. Coronavirus induction of class I major histocompatibility complex expression in murine astrocytes is virus strain specific. J. Exp. Med. 180 (1995) 1013-1023
26. Lavi E., Gilden D.H., Wrobleska Z., Rorke L.B., and Whitelock M. Experimental demyelination produced by the A59 strain of mouse hepatitis virus. Neurology 34 (1984) 597-603
27. Tsuhako M.H., Augusto O., Linares E., Dagli M.L.Z., and Pereira C.A. Association between nitric oxide synthesis and vaccination-acquired resistance to murine hepatitis virus by SPF mice. Free Radic. Biol. Med. 41 (2006) 1534-1541
28. Coley S.E., Lavi E., Sawicki S.G., Fu L., Schelle B., Karl N., Siddell S.G., and Thiel V. Recombinant mouse hepatitis virus strain A59 from cloned, full-length cDNA replicates to high titers in vitro and is fully pathogenic in vivo. J. Virol. 79 (2005) 3097-3106
29. Linares E., Giorgio S., and Augusto O. Inhibition of in vivo leishmanicidal mechanisms by tempol: nitric oxide down-regulation and oxidant scavenging. Free Radic. Biol. Med. 44 (2008) 1668-1676
30. Berube G.R., Powers M.M., and Clarck G. Iron hematoxylin chelates. I. The Weil staining bath. Stain. Technol. 40 (1965) 53-62
31. Fabis M.J., Scott G.S., Kean R.B., Koprowski H., and Hooper D.C. Loss of blood-brain barrier integrity in the spinal cord is common to experimental allergic encephalomyelitis in knockout mouse models. Proc. Natl. Acad. Sci. USA 104 (2009) 5656-5661
32. Chadi G., Rosen L., Cintra A., Tinner B., Zoli M., Pettersson R.F., and Fuxe K. Corticosterone increases FGF-2 (bFGF) immunoreactivity in the substantia nigra of the rat. NeuroReport 4 (1993) 783-786
33. Salinovich O., and Montelano R.C. Reversible staining and peptide mapping of proteins transferred to nitrocellulose after separation by sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Anal. Biochem. 156 (1986) 341-347
34. Moreira C., Tsuhako M.H., de Franco M.T., Modolell M., and Pereira C.A. Arginine metabolism during macrophage autocrine activation and infection with mouse hepatitis virus 3. Immunobiology 209 (2004) 585-598
35. Frei K., Eugster H.P., Bopst M., Constantinescu C.S., Lavi E., and Fontana A. Tumor necrosis factor alpha and lymphotoxin alpha are not required for induction of acute experimental autoimmune encephalomyelitis. J. Exp. Med. 185 (1997) 2177-2182
36. Tanaka Y., Koido S., Xia J., Ohana M., Liu C., Cote G.M., Sawyer D.B., Calderwood S., and Gong J. Development of antigen-specific CD8+ CTL in MHC class I-deficient mice through CD4 to CD8 conversion. J. Immunol 172 (2004) 7848-7858
37. Munder M., Eichmann K., Moran J.M., Centeno F., Soler G., and Modolell M. Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells. J. Immunol. 163 (1999) 3771-3777
38. Wilcox C.S., and Pearlman A. Chemistry and antihypertensive effects of tempol and other nitroxides. Pharmacol. Rev. 60 (2008) 418-469
39. Hawkins B.T., and Davis T.P. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol. Rev. 57 (2005) 173-185
40. Victor V.M., Rocha M., and De la Fuente M. Immune cells: free radicals and antioxidants in sepsis. Int. Immunopharmacol. 4 (2004) 327-347
41. Nencioni L., Luvara A., Aquilano K., Ciriolo M.R., Cozzolino F., Rotilio G., Garaci E., and Palamara A.T. Influenza A virus replication is dependent on an antioxidant pathway that involves GSH and Bcl-2. FASEB J. 17 (2003) 758-760
42. Sahaf B., Heydari K., Herzenberg L.A., and Herzenberg L.A. The extracellular microenvironment plays a key role in regulating the redox status of cell surface proteins in HIV-infected subjects. Arch. Biochem. Biophys. 434 (2005) 26-32
43. Carta S., Catellani P., Delfino L., Tassi S., Vené R., and Rubatlelli A. DAMPS and inflammatory processes: the role of redox in the different outcomes. J. Leukocyte Biol. 86 (2009) 549-555
44. Cuzzocrea S., Pisano B., Dugo L., Ianaro A., Patel N.S., Caputi A.P., and Thiemermann C. Tempol reduces the activation of nuclear factor-kappaB in acute inflammation. Free Radic. Res. 38 (2004) 813-819
45. Akaike T., and Maeda H. Nitric oxide and virus infection. Immunology 101 (2000) 300-308
46. Akaike T., Fujii S., Kato A., Yoshitake J., Miyamoto Y., Sawa T., Okamoto S., Suga M., Asakawa M., Nagai Y., and Maeda H. Viral mutation accelerated by nitric oxide production during infection in vivo. FASEB J. 14 (2000) 1447-1454
47. Linares E., Giorgio S., Mortara R.A., Santos C.X., Yamada A.T., and Augusto O. Role of peroxynitrite in macrophage microbicidal mechanisms in vivo revealed by protein nitration and hydroxylation. Free Radic. Biol. Med. 30 (2001) 1234-1242
48. Bonini M., Mason R.P., and Augusto O. The mechanism by which 4-hydroxy-2,2,6,6-tetramethylpiperidene-1-oxyl (tempol) diverts peroxynitrite decomposition from nitrating to nitrosating species. Chem. Res. Toxicol. 15 (2002) 506-511
49. Fernandes D.C., Medinas D.B., Alves M.J., and Augusto O. Tempol diverts peroxynitrite/carbon dioxide reactivity toward albumin and cells from protein-tyrosine nitration to protein-cysteine nitrosation. Free Radic. Biol. Med. 38 (2005) 189-200
50. Chen B.P., and Lane T.E. Lack of nitric oxide synthase type 2 (NOS2) results in reduced neuronal apoptosis and mortality following mouse hepatitis virus infection of the central nervous system. J. Neurovirol. 8 (2002) 58-63
51. Hooper D.C., Spitsin S., Kean R.B., Champion J.M., Dickson G.M., Chaudhry I., and 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
52. Hooper D.C., Scott G.S., Zborek A., Mikheeva T., Kean R.B., Koprowski H., and Spitsin S.V. Uric acid, a peroxynitrite scavenger, inhibits CNS inflammation, blood-CNS barrier permeability changes, and tissue damage in a mouse model of multiple sclerosis. FASEB J. 14 (2000) 691-698
53. Augusto O., Queiroz R.F., Vaz S.M., Malvezzi A., T-do Amaral A., Jordão A.K., Cunha A.C., and Ferreira V.F. Inhibition of the chlorinating activity of myeloperoxidase by nitroxides. 6th International Human Peroxidase Meeting, Chapel Hill, North Caroline, April 19-22 (2009)
54. Nagra R.M., Becher B., Tourtellotte W.W., Antel J.P., Gold D., Paladino T., Smith R.A., Nelson J.R., and Reynolds W.F. Immunohistochemical and genetic evidence of myeloperoxidase involvement in multiple sclerosis. J. Neuroimmunol. 78 (1997) 97-107
55. Chen J.W., Breckwoldt M.O., Aikawa E., Chiang G., and Weissleder R. Myeloperoxidase-targeted imaging of active inflammatory lesions in murine experimental autoimmune encephalomyelitis. Brain 131 (2008) 1123-1133