Abstract
Nitric oxide is a radical molecule with antibacterial, -parasitic, and -viral properties. We investigated the mechanism of NO inhibition of Coxsackievirus B3 (CVB3) replication in vitro by determining the effect of NO upon a single replicative cycle of CVB3 grown in HeLa cells. Transfection of inducible NO synthase cDNA into HeLa cells reduces the number of viral particles produced during a single cycle of growth. Similarly, a noncytotoxic concentration of the NO donor S-nitroso-amino-penicillamine reduces the number of viral particles in a dose-dependent manner. To explore the mechanisms by which NO exerts its antiviral effect, we assayed the attachment, replication, and translation steps of the CVB3 life cycle. NO does not affect the attachment of CVB3 to HeLa cells. However, NO inhibits CVB3 RNA synthesis, as shown by a [3H]uridine incorporation assay, reverse transcription-PCR, and Northern analysis. In addition, NO inhibits CVB3 protein synthesis, as shown by [35S]methionine protein labeling and Western blot analysis of infected cells. Thus, NO inhibits CVB3 replication in part by inhibiting viral RNA synthesis by an unknown mechanism.
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- Akaike T., Noguchi Y., Ijiri S., Setoguchi K., Suga M., Zheng Y. M., Dietzschold B., Maeda H. Pathogenesis of influenza virus-induced pneumonia: involvement of both nitric oxide and oxygen radicals. Proc Natl Acad Sci U S A. 1996 Mar 19;93(6):2448–2453. doi: 10.1073/pnas.93.6.2448. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Akarid K., Sinet M., Desforges B., Gougerot-Pocidalo M. A. Inhibitory effect of nitric oxide on the replication of a murine retrovirus in vitro and in vivo. J Virol. 1995 Nov;69(11):7001–7005. doi: 10.1128/jvi.69.11.7001-7005.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barton D. J., Black E. P., Flanegan J. B. Complete replication of poliovirus in vitro: preinitiation RNA replication complexes require soluble cellular factors for the synthesis of VPg-linked RNA. J Virol. 1995 Sep;69(9):5516–5527. doi: 10.1128/jvi.69.9.5516-5527.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bi Z., Reiss C. S. Inhibition of vesicular stomatitis virus infection by nitric oxide. J Virol. 1995 Apr;69(4):2208–2213. doi: 10.1128/jvi.69.4.2208-2213.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bi Z., Reiss C. S. Inhibition of vesicular stomatitis virus infection by nitric oxide. J Virol. 1995 Apr;69(4):2208–2213. doi: 10.1128/jvi.69.4.2208-2213.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Billiar T. R. Nitric oxide. Novel biology with clinical relevance. Ann Surg. 1995 Apr;221(4):339–349. doi: 10.1097/00000658-199504000-00003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Borman A. M., Bailly J. L., Girard M., Kean K. M. Picornavirus internal ribosome entry segments: comparison of translation efficiency and the requirements for optimal internal initiation of translation in vitro. Nucleic Acids Res. 1995 Sep 25;23(18):3656–3663. doi: 10.1093/nar/23.18.3656. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bredt D. S., Hwang P. M., Glatt C. E., Lowenstein C., Reed R. R., Snyder S. H. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature. 1991 Jun 27;351(6329):714–718. doi: 10.1038/351714a0. [DOI] [PubMed] [Google Scholar]
- Bukrinsky M. I., Nottet H. S., Schmidtmayerova H., Dubrovsky L., Flanagan C. R., Mullins M. E., Lipton S. A., Gendelman H. E. 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. 1995 Feb 1;181(2):735–745. doi: 10.1084/jem.181.2.735. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Butz E. A., Hostager B. S., Southern P. J. Macrophages in mice acutely infected with lymphocytic choriomeningitis virus are primed for nitric oxide synthesis. Microb Pathog. 1994 Apr;16(4):283–295. doi: 10.1006/mpat.1994.1029. [DOI] [PubMed] [Google Scholar]
- Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
- Craighead J. E., Huber S. A., Sriram S. Animal models of picornavirus-induced autoimmune disease: their possible relevance to human disease. Lab Invest. 1990 Oct;63(4):432–446. [PubMed] [Google Scholar]
- Croen K. D. Evidence for antiviral effect of nitric oxide. Inhibition of herpes simplex virus type 1 replication. J Clin Invest. 1993 Jun;91(6):2446–2452. doi: 10.1172/JCI116479. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Curran R. D., Ferrari F. K., Kispert P. H., Stadler J., Stuehr D. J., Simmons R. L., Billiar T. R. Nitric oxide and nitric oxide-generating compounds inhibit hepatocyte protein synthesis. FASEB J. 1991 Apr;5(7):2085–2092. doi: 10.1096/fasebj.5.7.1707021. [DOI] [PubMed] [Google Scholar]
- Dasmahapatra B., Rozhon E. J., Hart A. M., Cox S., Tracy S., Schwartz J. Cell-free expression of the coxsackievirus 3C protease using the translational initiation signal of an insect virus RNA and its characterization. Virus Res. 1991 Aug;20(3):237–249. doi: 10.1016/0168-1702(91)90078-a. [DOI] [PubMed] [Google Scholar]
- Davisson R. L., Travis M. D., Bates J. N., Lewis S. J. Hemodynamic effects of L- and D-S-nitrosocysteine in the rat. Stereoselective S-nitrosothiol recognition sites. Circ Res. 1996 Aug;79(2):256–262. doi: 10.1161/01.res.79.2.256. [DOI] [PubMed] [Google Scholar]
- De Groote M. A., Fang F. C. NO inhibitions: antimicrobial properties of nitric oxide. Clin Infect Dis. 1995 Oct;21 (Suppl 2):S162–S165. doi: 10.1093/clinids/21.supplement_2.s162. [DOI] [PubMed] [Google Scholar]
- De Groote M. A., Granger D., Xu Y., Campbell G., Prince R., Fang F. C. Genetic and redox determinants of nitric oxide cytotoxicity in a Salmonella typhimurium model. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6399–6403. doi: 10.1073/pnas.92.14.6399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- De Groote M. A., Testerman T., Xu Y., Stauffer G., Fang F. C. Homocysteine antagonism of nitric oxide-related cytostasis in Salmonella typhimurium. Science. 1996 Apr 19;272(5260):414–417. doi: 10.1126/science.272.5260.414. [DOI] [PubMed] [Google Scholar]
- Gauntt C. J., Gomez P. T., Duffey P. S., Grant J. A., Trent D. W., Witherspoon S. M., Paque R. E. Characterization and myocarditic capabilities of coxsackievirus B3 variants in selected mouse strains. J Virol. 1984 Nov;52(2):598–605. doi: 10.1128/jvi.52.2.598-605.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gauntt C. J., Pallansch M. A. Coxsackievirus B3 clinical isolates and murine myocarditis. Virus Res. 1996 Mar;41(1):89–99. doi: 10.1016/0168-1702(95)01250-8. [DOI] [PubMed] [Google Scholar]
- Gauntt C. J., Tracy S. M., Chapman N., Wood H. J., Kolbeck P. C., Karaganis A. G., Winfrey C. L., Cunningham M. W. Coxsackievirus-induced chronic myocarditis in murine models. Eur Heart J. 1995 Dec;16 (Suppl O):56–58. doi: 10.1093/eurheartj/16.suppl_o.56. [DOI] [PubMed] [Google Scholar]
- Godeny E. K., Gauntt C. J. Involvement of natural killer cells in coxsackievirus B3-induced murine myocarditis. J Immunol. 1986 Sep 1;137(5):1695–1702. [PubMed] [Google Scholar]
- Groeneveld P. H., Colson P., Kwappenberg K. M., Clement J. Increased production of nitric oxide in patients infected with the European variant of hantavirus. Scand J Infect Dis. 1995;27(5):453–456. doi: 10.3109/00365549509047045. [DOI] [PubMed] [Google Scholar]
- Gromeier M., Alexander L., Wimmer E. Internal ribosomal entry site substitution eliminates neurovirulence in intergeneric poliovirus recombinants. Proc Natl Acad Sci U S A. 1996 Mar 19;93(6):2370–2375. doi: 10.1073/pnas.93.6.2370. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Harris N., Buller R. M., Karupiah G. Gamma interferon-induced, nitric oxide-mediated inhibition of vaccinia virus replication. J Virol. 1995 Feb;69(2):910–915. doi: 10.1128/jvi.69.2.910-915.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herskowitz A., Wolfgram L. J., Rose N. R., Beisel K. W. Coxsackievirus B3 murine myocarditis: a pathologic spectrum of myocarditis in genetically defined inbred strains. J Am Coll Cardiol. 1987 Jun;9(6):1311–1319. doi: 10.1016/s0735-1097(87)80471-0. [DOI] [PubMed] [Google Scholar]
- Hohenadl C., Klingel K., Rieger P., Hofschneider P. H., Kandolf R. 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. 1994 May;47(3):279–295. doi: 10.1016/0166-0934(94)90025-6. [DOI] [PubMed] [Google Scholar]
- Hooper D. C., Ohnishi S. T., Kean R., Numagami Y., Dietzschold B., Koprowski H. Local nitric oxide production in viral and autoimmune diseases of the central nervous system. Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5312–5316. doi: 10.1073/pnas.92.12.5312. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huber S. A., Job L. P. Differences in cytolytic T cell response of BALB/c mice infected with myocarditic and non-myocarditic strains of coxsackievirus group B, type 3. Infect Immun. 1983 Mar;39(3):1419–1427. doi: 10.1128/iai.39.3.1419-1427.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huber S. A. Viral myocarditis--a tale of two diseases. Lab Invest. 1992 Jan;66(1):1–3. [PubMed] [Google Scholar]
- Janssens S. P., Simouchi A., Quertermous T., Bloch D. B., Bloch K. D. Cloning and expression of a cDNA encoding human endothelium-derived relating factor/nitric oxide synthase. J Biol Chem. 1992 Nov 5;267(31):22694–22694. [PubMed] [Google Scholar]
- Kandolf R., Hofschneider P. H. Molecular cloning of the genome of a cardiotropic Coxsackie B3 virus: full-length reverse-transcribed recombinant cDNA generates infectious virus in mammalian cells. Proc Natl Acad Sci U S A. 1985 Jul;82(14):4818–4822. doi: 10.1073/pnas.82.14.4818. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Karupiah G., Harris N. Inhibition of viral replication by nitric oxide and its reversal by ferrous sulfate and tricarboxylic acid cycle metabolites. J Exp Med. 1995 Jun 1;181(6):2171–2179. doi: 10.1084/jem.181.6.2171. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Karupiah G., Xie Q. W., Buller R. M., Nathan C., Duarte C., MacMicking J. D. Inhibition of viral replication by interferon-gamma-induced nitric oxide synthase. Science. 1993 Sep 10;261(5127):1445–1448. doi: 10.1126/science.7690156. [DOI] [PubMed] [Google Scholar]
- Klump W. M., Bergmann I., Müller B. C., Ameis D., Kandolf R. Complete nucleotide sequence of infectious Coxsackievirus B3 cDNA: two initial 5' uridine residues are regained during plus-strand RNA synthesis. J Virol. 1990 Apr;64(4):1573–1583. doi: 10.1128/jvi.64.4.1573-1583.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kreil T. R., Eibl M. M. 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. 1996 May 1;219(1):304–306. doi: 10.1006/viro.1996.0252. [DOI] [PubMed] [Google Scholar]
- Kräusslich H. G., Nicklin M. J., Toyoda H., Etchison D., Wimmer E. Poliovirus proteinase 2A induces cleavage of eucaryotic initiation factor 4F polypeptide p220. J Virol. 1987 Sep;61(9):2711–2718. doi: 10.1128/jvi.61.9.2711-2718.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuhn R. J., Tada H., Ypma-Wong M. F., Semler B. L., Wimmer E. Mutational analysis of the genome-linked protein VPg of poliovirus. J Virol. 1988 Nov;62(11):4207–4215. doi: 10.1128/jvi.62.11.4207-4215.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lamas S., Marsden P. A., Li G. K., Tempst P., Michel T. Endothelial nitric oxide synthase: molecular cloning and characterization of a distinct constitutive enzyme isoform. Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6348–6352. doi: 10.1073/pnas.89.14.6348. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lamphear B. J., Kirchweger R., Skern T., Rhoads R. E. Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases. Implications for cap-dependent and cap-independent translational initiation. J Biol Chem. 1995 Sep 15;270(37):21975–21983. doi: 10.1074/jbc.270.37.21975. [DOI] [PubMed] [Google Scholar]
- Lamphear B. J., Yan R., Yang F., Waters D., Liebig H. D., Klump H., Kuechler E., Skern T., Rhoads R. E. Mapping the cleavage site in protein synthesis initiation factor eIF-4 gamma of the 2A proteases from human Coxsackievirus and rhinovirus. J Biol Chem. 1993 Sep 15;268(26):19200–19203. [PubMed] [Google Scholar]
- Leslie K., Blay R., Haisch C., Lodge A., Weller A., Huber S. Clinical and experimental aspects of viral myocarditis. Clin Microbiol Rev. 1989 Apr;2(2):191–203. doi: 10.1128/cmr.2.2.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu R. H., Jacob J. R., Tennant B. C., Hotchkiss J. H. Nitrite and nitrosamine synthesis by hepatocytes isolated from normal woodchucks (Marmota monax) and woodchucks chronically infected with woodchuck hepatitis virus. Cancer Res. 1992 Aug 1;52(15):4139–4143. [PubMed] [Google Scholar]
- Lowenstein C. J., Glatt C. S., Bredt D. S., Snyder S. H. Cloned and expressed macrophage nitric oxide synthase contrasts with the brain enzyme. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6711–6715. doi: 10.1073/pnas.89.15.6711. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lowenstein C. J., Hill S. L., Lafond-Walker A., Wu J., Allen G., Landavere M., Rose N. R., Herskowitz A. Nitric oxide inhibits viral replication in murine myocarditis. J Clin Invest. 1996 Apr 15;97(8):1837–1843. doi: 10.1172/JCI118613. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lowenstein C. J., Snyder S. H. Nitric oxide, a novel biologic messenger. Cell. 1992 Sep 4;70(5):705–707. doi: 10.1016/0092-8674(92)90301-r. [DOI] [PubMed] [Google Scholar]
- Lyons C. R., Orloff G. J., Cunningham J. M. Molecular cloning and functional expression of an inducible nitric oxide synthase from a murine macrophage cell line. J Biol Chem. 1992 Mar 25;267(9):6370–6374. [PubMed] [Google Scholar]
- Malcolm B. A. The picornaviral 3C proteinases: cysteine nucleophiles in serine proteinase folds. Protein Sci. 1995 Aug;4(8):1439–1445. doi: 10.1002/pro.5560040801. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mannick J. B., Asano K., Izumi K., Kieff E., Stamler J. S. Nitric oxide produced by human B lymphocytes inhibits apoptosis and Epstein-Barr virus reactivation. Cell. 1994 Dec 30;79(7):1137–1146. doi: 10.1016/0092-8674(94)90005-1. [DOI] [PubMed] [Google Scholar]
- Mannick J. B. The antiviral role of nitric oxide. Res Immunol. 1995 Nov-Dec;146(9):693–697. doi: 10.1016/0923-2494(96)84920-0. [DOI] [PubMed] [Google Scholar]
- Marletta M. A. Nitric oxide synthase: aspects concerning structure and catalysis. Cell. 1994 Sep 23;78(6):927–930. doi: 10.1016/0092-8674(94)90268-2. [DOI] [PubMed] [Google Scholar]
- Melková Z., Esteban M. Inhibition of vaccinia virus DNA replication by inducible expression of nitric oxide synthase. J Immunol. 1995 Dec 15;155(12):5711–5718. [PubMed] [Google Scholar]
- Mikami S., Kawashima S., Kanazawa K., Hirata K., Katayama Y., Hotta H., Hayashi Y., Ito H., Yokoyama M. Expression of nitric oxide synthase in a murine model of viral myocarditis induced by coxsackievirus B3. Biochem Biophys Res Commun. 1996 Mar 27;220(3):983–989. doi: 10.1006/bbrc.1996.0519. [DOI] [PubMed] [Google Scholar]
- Mohr S., Stamler J. S., Brüne B. Posttranslational modification of glyceraldehyde-3-phosphate dehydrogenase by S-nitrosylation and subsequent NADH attachment. J Biol Chem. 1996 Feb 23;271(8):4209–4214. doi: 10.1074/jbc.271.8.4209. [DOI] [PubMed] [Google Scholar]
- Molla A., Harris K. S., Paul A. V., Shin S. H., Mugavero J., Wimmer E. Stimulation of poliovirus proteinase 3Cpro-related proteolysis by the genome-linked protein VPg and its precursor 3AB. J Biol Chem. 1994 Oct 28;269(43):27015–27020. [PubMed] [Google Scholar]
- Moncada S., Palmer R. M., Higgs E. A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 1991 Jun;43(2):109–142. [PubMed] [Google Scholar]
- Nathan C. Natural resistance and nitric oxide. Cell. 1995 Sep 22;82(6):873–876. doi: 10.1016/0092-8674(95)90019-5. [DOI] [PubMed] [Google Scholar]
- Nathan C., Xie Q. W. Regulation of biosynthesis of nitric oxide. J Biol Chem. 1994 May 13;269(19):13725–13728. [PubMed] [Google Scholar]
- Okada I., Matsumori A., Kawai C., Yodoi J., Tracy S. The viral genome in experimental murine Coxsackievirus B3 myocarditis: a Northern blotting analysis. J Mol Cell Cardiol. 1990 Sep;22(9):999–1008. doi: 10.1016/0022-2828(90)91039-a. [DOI] [PubMed] [Google Scholar]
- Pietraforte D., Tritarelli E., Testa U., Minetti M. gp120 HIV envelope glycoprotein increases the production of nitric oxide in human monocyte-derived macrophages. J Leukoc Biol. 1994 Feb;55(2):175–182. doi: 10.1002/jlb.55.2.175. [DOI] [PubMed] [Google Scholar]
- Rodriguez P. L., Carrasco L. Gliotoxin: inhibitor of poliovirus RNA synthesis that blocks the viral RNA polymerase 3Dpol. J Virol. 1992 Apr;66(4):1971–1976. doi: 10.1128/jvi.66.4.1971-1976.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rolph M. S., Ramshaw I. A., Rockett K. A., Ruby J., Cowden W. B. Nitric oxide production is increased during murine vaccinia virus infection, but may not be essential for virus clearance. Virology. 1996 Mar 15;217(2):470–477. doi: 10.1006/viro.1996.0141. [DOI] [PubMed] [Google Scholar]
- Rose N. R., Neumann D. A., Herskowitz A. Coxsackievirus myocarditis. Adv Intern Med. 1992;37:411–429. [PubMed] [Google Scholar]
- Saiki R. K., Scharf S., Faloona F., Mullis K. B., Horn G. T., Erlich H. A., Arnheim N. Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science. 1985 Dec 20;230(4732):1350–1354. doi: 10.1126/science.2999980. [DOI] [PubMed] [Google Scholar]
- Schmid M., Wimmer E. IRES-controlled protein synthesis and genome replication of poliovirus. Arch Virol Suppl. 1994;9:279–289. doi: 10.1007/978-3-7091-9326-6_28. [DOI] [PubMed] [Google Scholar]
- Sessa W. C., Harrison J. K., Barber C. M., Zeng D., Durieux M. E., D'Angelo D. D., Lynch K. R., Peach M. J. Molecular cloning and expression of a cDNA encoding endothelial cell nitric oxide synthase. J Biol Chem. 1992 Aug 5;267(22):15274–15276. [PubMed] [Google Scholar]
- Stadler J., Billiar T. R., Curran R. D., Stuehr D. J., Ochoa J. B., Simmons R. L. Effect of exogenous and endogenous nitric oxide on mitochondrial respiration of rat hepatocytes. Am J Physiol. 1991 May;260(5 Pt 1):C910–C916. doi: 10.1152/ajpcell.1991.260.5.C910. [DOI] [PubMed] [Google Scholar]
- Stamler J. S. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell. 1994 Sep 23;78(6):931–936. doi: 10.1016/0092-8674(94)90269-0. [DOI] [PubMed] [Google Scholar]
- Stamler J. S., Singel D. J., Loscalzo J. Biochemistry of nitric oxide and its redox-activated forms. Science. 1992 Dec 18;258(5090):1898–1902. doi: 10.1126/science.1281928. [DOI] [PubMed] [Google Scholar]
- Tracy S., Chapman N. M., Romero J., Ramsingh A. I. Genetics of coxsackievirus B cardiovirulence and inflammatory heart muscle disease. Trends Microbiol. 1996 May;4(5):175–179. doi: 10.1016/0966-842x(96)10026-3. [DOI] [PubMed] [Google Scholar]
- Trousdale M. D., Paque R. E., Gauntt C. J. Isolation of Coxsackievirus B3 temperture-sensitive mutants and their assignment to complementation groups. Biochem Biophys Res Commun. 1976 May 23;76(2):368–375. doi: 10.1016/0006-291x(77)90734-3. [DOI] [PubMed] [Google Scholar]
- Tucker P. C., Griffin D. E., Choi S., Bui N., Wesselingh S. Inhibition of nitric oxide synthesis increases mortality in Sindbis virus encephalitis. J Virol. 1996 Jun;70(6):3972–3977. doi: 10.1128/jvi.70.6.3972-3977.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Van Dam A. M., Bauer J., Man-A-Hing W. K., Marquette C., Tilders F. J., Berkenbosch F. 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. 1995 Feb 1;40(2):251–260. doi: 10.1002/jnr.490400214. [DOI] [PubMed] [Google Scholar]
- Ventoso I., Carrasco L. A poliovirus 2A(pro) mutant unable to cleave 3CD shows inefficient viral protein synthesis and transactivation defects. J Virol. 1995 Oct;69(10):6280–6288. doi: 10.1128/jvi.69.10.6280-6288.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weiss G., Goossen B., Doppler W., Fuchs D., Pantopoulos K., Werner-Felmayer G., Grünewald K., Wachter H., Hentze M. W. Stimulation of IRE-BP activity of IRF by tetrahydrobiopterin and cytokine dependent induction of nitric oxide synthase. Adv Exp Med Biol. 1994;356:133–139. doi: 10.1007/978-1-4615-2554-7_15. [DOI] [PubMed] [Google Scholar]
- Wolfgram L. J., Beisel K. W., Rose N. R. Heart-specific autoantibodies following murine coxsackievirus B3 myocarditis. J Exp Med. 1985 May 1;161(5):1112–1121. doi: 10.1084/jem.161.5.1112. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Woodruff J. F. Viral myocarditis. A review. Am J Pathol. 1980 Nov;101(2):425–484. [PMC free article] [PubMed] [Google Scholar]
- Xie Q. W., Cho H. J., Calaycay J., Mumford R. A., Swiderek K. M., Lee T. D., Ding A., Troso T., Nathan C. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science. 1992 Apr 10;256(5054):225–228. doi: 10.1126/science.1373522. [DOI] [PubMed] [Google Scholar]