Nitric oxide inhibition of coxsackievirus replication in vitro

Journal of Clinical Investigation

Volumn 100, Issue 7, 1997, Pages 1760-1767

  Zaragoza, Carlos ^a   Ocampo, Christopher J ^a   Saura, Marta ^a   McMillan, Audrey ^a   Lowenstein, Charles J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autoimmune; Enterovirus; Myocarditis; Nitric oxide synthase; Nuclear factor kappa B

Indexed keywords

COMPLEMENTARY DNA; N ACETYL S NITROSOPENICILLAMINE; NITRIC OXIDE; NITRIC OXIDE DONOR;

ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; COXSACKIE VIRUS B3; DRUG MECHANISM; HUMAN; HUMAN CELL; MYOCARDITIS; PRIORITY JOURNAL; RNA SYNTHESIS; VIRUS GENE; VIRUS REPLICATION;

EID: 0030931643     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119702     Document Type: Article

References (81)

1. Nathan, C., and Q.W. Xie. 1994. Regulation of biosynthesis of nitric oxide. J. Biol. Chem. 269:13725-13728.
2. Nathan, C. 1995. Natural Resistance and Nitric Oxide. Cell. 82:873-876s.
3. Moncada, S., R.M. Palmer, and E.A. Higgs. 1991. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43:109-142.
4. Lowenstein, C.J., and S.H. Snyder. 1992. Nitric oxide, a novel biologic messenger. Cell. 70:705-707.
5. Billiar, T.R. 1995. Nitric oxide. Novel biology with clinical relevance. Ann. Surg. 221:339-349.
6. Marletta, M.A. 1994. Nitric oxide synthase: aspects concerning structure and catalysis. Cell. 78:926-930.
7. Stamler, J.S. 1994. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell. 78:931-936.
8. Bredt, D.S., P.M. Hwang, C.E. Glatt, C. Lowenstein, R.R. Reed, and S.H. Snyder. 1991. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature (Lond.). 351:714-718.
9. Sessa, W.C., J.K. Harrison, C.M. Barber, D. Zeng, M.E. Durieux, D.D. D'Angelo, K.R. Lynch, and M.J. Peach. 1992. Molecular cloning and expression of a cDNA encoding endothelial cell nitric oxide synthase. J. Biol. Chem. 267: 15274-15276.
10. Lamas, S., P.A. Marsden, G.K. Li, P. Tempst, and T. Michel. 1992. Endothelial nitric oxide synthase: molecular cloning and characterization of a distinct constitutive enzyme isoform. Proc. Natl. Acad. Sci. USA. 89:6348-6352.
11. Janssens, S.P., A. Simouchi, T. Quertermous, D.B. Bloch, and K.D. Bloch. 1992. Cloning and expression of a cDNA encoding human endothelium-derived relating factor/nitric oxide synthase. J. Biol. Chem. 267:22694.
12. Lowenstein, C.J., C.S. Glatt, D.S. Bredt, and S.H. Snyder. 1992. Cloned and expressed macrophage nitric oxide synthase contrasts with the brain enzyme. Proc. Natl. Acad. Sci. USA. 89:6711-6715.
13. Xie, Q.W., H.J. Cho, J. Calaycay, R.A. Mumford, K.M. Swiderek, T.D. Lee, A. Ding, T. Troso, and C. Nathan. 1992. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science (Wash. DC). 256:225-228.
14. Lyons, C.R., G.J. Orloff, and J.M. Cunningham. 1992. Molecular cloning and functional expression of an inducible nitric oxide synthase from a murine macrophage cell line. J. Biol. Chem. 267:6370-6374.
15. De Groote, M.A., and F.C. Fang. 1995. NO inhibitions: antimicrobial properties of nitric oxide. Clin. Infect. Dis. 21:S162-S165.
16. Mannick, J.B. 1995. The antiviral role of nitric oxide. Res. Immunol. 146:693-697.
17. Kreil, T.R., and M.M. Eibl. 1996. Nitric oxide and viral infection: NO antiviral activity against a flavivirus in vitro, and evidence for contribution to pathogenesis in experimental infection in vivo. Virology. 219:304-306.
18. Melkova, Z., and M. Esteban. 1995. Inhibition of vaccinia virus DNA replication by inducible expression of nitric oxide synthase. J. Immunol. 155: 5711-5718.
19. Bukrinsky, M.I., H.S. Nottet, H. Schmidtmayerova, L. Dubrovsky, C.R. Flanagan, M.E. Mullins, S.A. Lipton, and H.E. Gendelman. 1995. Regulation of nitric oxide synthase activity in human immunodeficiency virus type 1 (HIV-1)-infected monocytes: implications for HIV-associated neurological disease. J. Exp. Med. 181:735-745.
20. Mannick, J.B., K. Asano, K. Izumi, E. Kieff, and J.S. Stamler. 1994. Nitric oxide produced by human B lymphocytes inhibits apoptosis and Epstein-Barr virus reactivation. Cell. 79:1137-1146.
21. Liu, R.H., J.R. Jacob, B.C. Tennant, and J.H. Hotchkiss. 1992. Nitrite and nitrosamine synthesis by hepatocytes isolated from normal woodchucks (Marmota monax) and woodchucks chronically infected with woodchuck hepatitis virus. Cancer Res. 52:4139-4143.
22. Pietraforte, D., E. Tritarelli, U. Testa, and M. Minetti. 1994. gp120 HIV envelope glycoprotein increases the production of nitric oxide in human monocyte-derived macrophages. J. Leukocyte Biol. 55:175-182.
23. Van Dam, A.M., J. Bauer, W.K. Man-A-Hing, C. Marquette, F.J. Tilders, and F. Berkenbosch. 1995. Appearance of inducible nitric oxide synthase in the rat central nervous system after rabies virus infection and during experimental allergic encephalomyelitis but not after peripheral administration of endotoxin. J. Neurosci. Res. 40:251-260.
24. Butz, E.A., B.S. Hostager, and P.J. Southern. 1994. Macrophages in mice acutely infected with lymphocytic choriomeningitis virus are primed for nitric oxide synthesis. Microb. Pathog. 16:283-295.
25. Tucker, P.C., D.E. Griffin, S. Choi, N. Bui, and S. Wesselingh. 1996. Inhibition of nitric oxide synthesis increases mortality in Sindbis virus encephalitis. J. Virol. 70:3972-3977.
26. Akaike, T., Y. Noguchi, S. Ijiri, K. Setoguchi, M. Suga, Y.M. Zheng, B. Dietzschold, and H. Maeda. 1996. Pathogenesis of influenza virus-induced pneumonia: involvement of both nitric oxide and oxygen radicals. Proc. Natl. Acad. Sci. USA. 93:2448-2453.
27. Rolph, M.S., I.A. Ramshaw, K.A. Rockett, J. Ruby, and W.B. Cowden. 1996. Nitric oxide production is increased during murine vaccinia virus infection, but may not be essential for virus clearance. Virology. 217:470-477.
28. Akarid, K., M. Sinet, B. Desforges, and M.A. Gougerot-Pocidalo. 1995. Inhibitory effect of nitric oxide on the replication of a murine retrovirus in vitro and in vivo. J. Virol. 69:7001-7005.
29. Hooper, D.C., S.T. Ohnishi, R. Kean, Y. Numagami, B. Dietzschold, and H. Koprowski. 1995. Local nitric oxide production in viral and autoimmune diseases of the central nervous system. Proc. Natl. Acad. Sci. USA. 92:5312-5316.
30. Groeneveld, P.H., P. Colson, K.M. Kwappenberg, and J. Clement. 1995. Increased production of nitric oxide in patients infected with the European variant of hantavirus. Scand. J. Infect. Dis. 27:453-456.
31. Croen, K.D. 1993. Evidence for antiviral effect of nitric oxide. Inhibition of herpes simplex virus type 1 replication. J. Clin. Invest. 91:2446-2452.
32. Karupiah, G., Q.W. Xie, R.M. Buller, C. Nathan, C. Duarte, and J.D. MacMicking. 1993. Inhibition of viral replication by interferon-gamma-induced nitric oxide synthase. Science (Wash. DC). 261:1445-1448.
33. Bi, Z., and C.S. Reiss. 1995. Inhibition of vesicular stomatitis virus infection by nitric oxide. J. Virol. 69:2208-2213.
34. Karupiah, G., and N. Harris. 1995. Inhibition of viral replication by nitric oxide and its reversal by ferrous sulfate and tricarboxylic acid cycle metabolites. J. Exp. Med. 181:2171-2179.
35. Harris, N., R.M. Buller, and G. Karupiah. 1995. Gamma interferon-induced, nitric oxide-mediated inhibition of vaccinia virus replication. J. Virol. 69:910-915.
36. Melnick, J.L. 1985. Enteroviruses: polioviruses, Coxsackieviruses, echoviruses, and newer enteroviruses. In Virology. B.N. Fields, editor. Raven Press, New York. 739-794.
37. Kandolf, R., and P.H. Hofschneider. 1985. Molecular cloning the genome of a cardiotropic coxsackie B3 virus: full length reverse transcribed recombinant cDNA generates infectious virus in mammalian cells. Proc. Natl. Acad. Sci. USA. 82:4818-4822.
38. Okada, I., A. Matsumori, C. Kawai, J. Yodoi, and S. Tracy. 1990. The viral genome in experimental murine Coxsackievirus B3 myocarditis: a Northern blotting analysis. J. Mol. Cell Cardiol. 22:999-1008.
39. Rueckert, R.R. 1985. Picornaviruses and their replication. In Virology. B.N. Fields, editor. Raven Press, New York. 705-738.
40. Herskowitz, A., L.J. Wolfgram, N.R. Rose, and K.W. Beisel. 1987. Coxsackievirus B3 murine myocarditis: a pathologic spectrum of myocarditis in genetically defined inbred strains. J. Am. Coll. Cardiol. 9:1311-1319.
41. Rose, N.R., D.A. Neumann, and A. Herskowitz. 1992. Coxsackievirus myocarditis. Adv. Intern. Med. 37:411-429.
42. Hubert, S.A., and L.P. Job. 1983. Differences in cytolytic T cell response of BALB/c mice: evidence for autoimmunity to myocyte antigens. Infect. Immun. 39:1419-1427.
43. Gauntt, C.J., P.T. Gomez, and P.S. Duffey. 1984. Characterization and myocarditic capabilities of coxsackie virus B3 variants in selected mouse strains. J. Virol. 52:598-605.
44. Godeny, E.K., and C.J. Gauntt. 1986. Invovlement of natural killer cells in Coxsackievirus B3 induced murine myocarditis. J. Immunol. 137:1695-1670.
45. Leslie, K., R. Blay, C. Haisch, A. Lodge, A. Weller, and S. Huber. 1989. Clinical and experimental aspects of viral myocarditis. Clin. Microbiol. Rev. 2: 196-203.
46. Wolfgram, L.J., K.W. Beisel, and N.R. Rose. 1985. Heart-specific autoantibodies following murine Coxsackievirus B3 myocarditis. J. Exp. Med. 161:1112-1121.
47. Woodruff, J.F. 1980. Viral myocarditis: a review. Am. J. Pathol. 101: 425-484.
48. Gauntt, C.J., and M.A. Pallansch. 1996. Coxsackievirus B3 clinical isolates and murine myocarditis. Virus Res. 41:89-99.
49. Tracy, S., N.M. Chapman, J. Romero, and A.I. Ramsingh. 1996. Genetics of Coxsackievirus B cardiovirulence and inflammatory heart muscle disease. Trends Microbiol. 4:175-179.
50. Gauntt, C.J., S.M. Tracy, N. Chapman, H.J. Wood, P.C. Kolbeck, A.G. Karaganis, C.L. Winfrey, and M.W. Cunningham. 1995. Coxsackievirus-induced chronic myocarditis in murine models. Eur. Heart J. 16(Suppl.):56-58.
51. Huber, S.A. 1992. Viral myocarditis - a tale of two diseases. Lab. Invest. 66:1-3.
52. Craighead, J.E., S.A. Huber, and S. Sriram. 1990. Animal models of picornavirus-induced autoimmune disease: their possible relevance to human disease. Lab. Invest. 63:432-446.
53. Lowenstein, C.J., S.L. Hill, A. Lafond-Walker, J. Wu, G. Allen, M. Landavere, N.R. Rose, and A. Herskowitz. 1996. Nitric oxide inhibits viral replication in murine myocarditis. J. Clin. Invest. 97:1837-1843.
54. Mikami, S., S. Kawashima, K. Kanazawa, K. Hirata, Y. Katayama, H. Hotta, Y. Hayashi, H. Ito, and M. Yokoyama. 1996. Expression of nitric oxide synthase in a murine model of viral myocarditis induced by Coxsackievirus B3. Biochem. Biophys. Res. Commun. 220:983-989.
55. Curran, R.D., F.K. Ferrari, P.H. Kispert, J. Stadler, D.J. Stuehr, R.L. Simmons, and T.R. Billiar. 1991. Nitric oxide and nitric oxide-generating compounds inhibit hepatocyte protein synthesis. FASEB. J. 5:2085-2092.
56. Klump, W.M., I. Bergmann, B.C. Muller, D. Ameis, and R. Kandolf. 1990. Complete nucleotide sequence of infectious Coxsackievirus B3 cDNA: two initial 5′ uridine residues are regained during plus-strand RNA synthesis. J. Virol. 64:1573-1583.
57. Hohenadl, C., K. Klingel, P. Rieger, P.H. Hofschneider, and R. Kandolf. 1994. Investigation of the Coxsackievirus B3 nonstructural proteins 2B, 2C, and 3AB: generation of specific polyclonal antisera and detection of replicating virus in infected tissue. J. Virol. Methods. 47:279-295.
58. Trousdale, R.E., R.E. Paque, and C.J. Gauntt. 1977. Isolation of Coxsackievirus B3 temperature-sensitive mutants and their assignment to complementation groups. Biochem. Biophys. Res. Commun. 76:368-375.
59. Chomczynski, P., and N. Sacchi. 1987. Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
60. Saiki, R.K., S. Scharf, F. Faloona, K.B. Mullis, G.T. Horn, H.A. Erlich, and N. Arnheim. 1985. Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science (Wash. DC). 230:1350-1354.
61. Schmid, M., and E. Wimmer. 1994. IRES-controlled protein synthesis and genome replication of poliovirus. Arch. Virol. 9(Suppl.):279-289.
62. Stamler, J.S., D.J. Singel, and J. Loscalzo. 1992. Biochemistry of nitric oxide and its redox-activated forms. Science (Wash. DC). 258:1898-1902.
63. De Groote, M.A., T. Testerman, Y. Xu, G. Stauffer, and F.C. Fang. 1996. Homocysteine antagonism of nitric oxide-related cytostasis in Salmonella typhimurium. Science (Wash. DC). 272:414-417.
64. De Groote, M.A., D. Granger, Y. Xu, G. Campbell, R. Prince, and F.C. Fang. 1995. Genetic and redox determinants of nitric oxide cytotoxicity in a Salmonella typhimurium model. Proc. Natl. Acad. Sci. USA. 92:6399-6403.
65. Davisson, R.L., M.D. Travis, J.N. Bates, and S.J. Lewis. 1996. Hemodynamic effects of L-and D-S-nitrosocysteine in the rat. Stereoselective 5-nitrosothiol recognition sites. Circ. Res. 79:256-262.
66. Bi, Z., and C.S. Reiss. 1995. Inhibition of vesicular stomatitis virus infection by nitric oxide. J. Virol. 69:2208-2213.
67. Rodriguez, P.L., and L. Carrasco. 1992. Gliotoxin: inhibitor of poliovirus RNA synthesis that blocks the viral RNA polymerase 3Dpol. J. Virol. 66: 1971-1976.
68. Nicklin, M.J., H.G. Krausslich, H. Toyoda, J.J. Dunn, and E. Wimmer. 1996. Poliovirus polypeptide precursors: expression in vitro and processing by exogenous 3C and 2A proteinases. Proc. Nat. Acad. Sci. USA. 93:2370-2375.
69. Ventoso, I., and L. Carrasco. 1995. A poliovirus 2A(pro) mutant unable to cleave 3CD shows inefficient viral protein synthesis and transactivation defects. J. Virol. 69:6280-6288.
70. Malcolm, B.A. 1995. The picornaviral 3C proteinases: cysteine nucleophiles in serine proteinase folds. Prot. Sci. 4:1439-1445.
71. Barton, D.J., E.P. Black, and J.B. Flanegan. 1995. Complete replication of poliovirus in vitro: preinitiation RNA replication complexes require soluble cellular factors for the synthesis of VPg-linked RNA. J. Virol. 69:5516-5527.
72. Molla, A., K.S. Harris, A.V. Paul, S.H. Shin, J. Mugavero, and E. Wimmer. 1994. Stimulation of poliovirus protemase 3Cpro-related proteolysis by the genome-linked protein VPg and its precursor 3AB. J. Biol. Chem. 269: 27015-27020.
73. Kuhn, R.J., H. Tada, M.F. Ypma-Wong, B.L. Semler, and E. Wimmer. 1988. Mutational analysis of the genome-linked protein VPg of poliovirus. J. Virol. 62:4207-4215.
74. Krausslich, H.G., M.J. Nicklin, H. Toyoda, D. Etchison, and E. Wimmer. 1987. Poliovirus proteinase 2A induces cleavage of eucaryotic initiation factor 4F polypeptide p220. J. Virol. 61:2711-2718.
75. Lamphear, B.J., R. Yan, F. Yang, D. Waters, H.D. Liebig, H. Klump, E. Kuechler, T. Skern, and R.E. Rhoads. 1993. Mapping the cleavage site in protein synthesis initiation factor eIF-4 gamma of the 2A proteases from human Coxsackievirus and rhinovirus. J. Biol. Chem. 268:19200-19203.
76. Dasmahapatra, B., E.J. Rozhon, A.M. Hart, S. Cox, S. Tracy, and J. Schwartz. 1991. Cell-free expression of the Coxsackievirus 3C protease using the translational initiation signal of an insect virus RNA and its characterization. Virus Res. 20:237-249.
77. Borman, A.M., J.L. Bailly, M. Girard, and K.M. Kean. 1995. Picornavirus internal ribosome entry segments: comparison of translation efficiency and the requirements for optimal internal initiation of translation in vitro. Nucleic Acids Res. 23:3656-3663.
78. Lamphear, B.J., R. Kirchweger, T. Skern, and R.E. Rhoads. 1995. Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases. Implications for cap-dependent and capindependent translational initiation. J. Biol. Chem. 270:21975-21983.
79. Mohr, S., J.S. Stamler, and B. Brune. 1996. Posttranslational modification of glyceraldehyde-3-phosphate dehydrogenase by S-nitrosylation and subsequent NADH attachment. J. Biol. Chem. 271:4209-4214.
80. Weiss, G., B. Goossen, W. Doppler, D. Fuchs, K. Pantopoulos, G. Werner-Felmayer, K. Grunewald, H. Wachter, and M.W. Hentze. 1994. Stimulation of IRE-BP activity of IRF by tetrahydrobiopterin and cytokine dependent induction of nitric oxide synthase. Adv. Exp. Med. Biol. 356:133-139.
81. Stadler, J., T.R. Billiar, R.D. Curran, D.J. Stuehr, J.B. Ochoa, and R.L. Simmons. 1991. Effect of exogenous and endogenous nitric oxide on mitochondrial respiration of rat hepatocytes. Am. J. Physiol. 260:C910-C916.