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PMID: 9032354 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Disassociation between the in vitro and in vivo effects of nitric oxide on a neurotropic murine coronavirus.

Journal of virology ·Vol. 71 ·No. 3 ·1997-03-00 ·Pages 2202-10

Lane TE, Paoletti AD, Buchmeier MJ

Abstract

Intranasal inoculation of the neuroattenuated OBLV60 strain of mouse hepatitis virus results in infection of mitral neurons in the olfactory bulb, followed by spread along olfactory and limbic pathways to the brain. Immunocompetent BALB/c mice were able to clear virus by 11 days postinfection (p.i.). Gamma interferon (IFN-gamma) may play a role in clearance of OBLV60 from infected immunocompetent BALB/c mice through a nonlytic mechanism. Among the variety of immunomodulatory activities of IFN-gamma is the induction of expression of inducible nitric oxide synthase (iNOS), an enzyme responsible for the production of nitric oxide (NO). Studies were undertaken to investigate the role of IFN-gamma and NO in host defense and clearance of OBLV60 from the central nervous system (CNS). Exposure of OBLV60-infected OBL21a cells, a mouse neuronal cell line, to the NO-generating compound S-nitroso-L-acetyl penicillamine resulted in a significant decrease in viral replication, indicating that NO interfered with viral replication. Furthermore, infection of IFN-gamma knockout (GKO) mice and athymic nude mice with OBLV60 resulted in low-level expression of iNOS mRNA and protein in the brains compared to that of OBLV60-infected BALB/c mice. Nude mice were unable to clear virus and eventually died between days 11 and 14 p.i. (B. D. Pearce, M. V. Hobbs, T. S. McGraw, and M. J. Buchmeier, J. Virol. 68:5483-5495, 1994); however, GKO mice survived infection and cleared virus by day 18 p.i. These data suggest that IFN-gamma production in the olfactory bulb contributed to but may not be essential for clearance of OBLV60 from the brain. In addition, treatment of OBLV60-infected BALB/c mice with aminoguanidine, a selective inhibitor of iNOS activity, did not result in any increase in mortality, and the mice cleared the virus by 11 days p.i. These data suggest that although NO was able to block replication of virus in vitro, expression of iNOS with NO release in vivo did not appear to be the determinant factor in clearance of OBLV60 from CNS neurons.

MeSH Terms
Animals Cell Line Coronavirus Infections/immunology,metabolism,virology Enzyme Inhibitors/pharmacology In Situ Hybridization Interferon-gamma/genetics,immunology Mice Mice, Inbred BALB C Mice, Knockout Mice, Nude Murine hepatitis virus/drug effects,genetics,growth & development,immunology Nitric Oxide/immunology Nitric Oxide Synthase/genetics,metabolism Penicillamine/analogs & derivatives,pharmacology RNA, Messenger RNA, Viral/analysis S-Nitroso-N-Acetylpenicillamine Time Factors Tumor Cells, Cultured Virus Replication/drug effects
Chemicals
Enzyme Inhibitors RNA, Messenger RNA, Viral Nitric Oxide N-acetylpenicillamine S-Nitroso-N-Acetylpenicillamine Interferon-gamma Nitric Oxide Synthase Penicillamine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Lane T E
Department of Neuropharmacology, The Scripps Research Institute, La Jolla, California 92037, USA.
Paoletti A D
Buchmeier M J
References (48)
48 references, click to expand
  1. The role of gamma interferon in infection of susceptible mice with murine coronavirus, MHV-JHM.
    Arch Virol. 1991;121(1-4):89-100 PMID: 1662041
  2. Inhibition of nitric oxide synthesis increases mortality in Sindbis virus encephalitis.
    J Virol. 1996 Jun;70(6):3972-7 PMID: 8648734
  3. Aminoguanidine, a novel inhibitor of nitric oxide formation, prevents diabetic vascular dysfunction.
    Diabetes. 1992 Apr;41(4):552-6 PMID: 1376704
  4. Induction of nitric oxide synthase in glial cells.
    J Neurochem. 1992 Sep;59(3):897-905 PMID: 1379633
  5. Cloned and expressed macrophage nitric oxide synthase contrasts with the brain enzyme.
    Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6711-5 PMID: 1379716
  6. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes.
    Science. 1993 Mar 19;259(5102):1739-42 PMID: 8456300
  7. In vivo expression of inducible nitric oxide synthase in experimentally induced neurologic diseases.
    Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):3024-7 PMID: 7681993
  8. Selective inhibition of the inducible nitric oxide synthase by aminoguanidine.
    Eur J Pharmacol. 1993 Mar 16;233(1):119-25 PMID: 7682510
  9. A case for cytokines as effector molecules in the resolution of virus infection.
    Immunol Today. 1993 Apr;14(4):155-7 PMID: 8499074
  10. Evidence for antiviral effect of nitric oxide. Inhibition of herpes simplex virus type 1 replication.
    J Clin Invest. 1993 Jun;91(6):2446-52 PMID: 8390481
  11. Nitric oxide localized to spinal cords of mice with experimental allergic encephalomyelitis: an electron paramagnetic resonance study.
    J Exp Med. 1993 Aug 1;178(2):643-8 PMID: 8393479
  12. Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide.
    J Immunol. 1993 Aug 15;151(4):2132-41 PMID: 8102159
  13. Inhibition of viral replication by interferon-gamma-induced nitric oxide synthase.
    Science. 1993 Sep 10;261(5127):1445-8 PMID: 7690156
  14. Severity of neurological signs and degree of inflammatory lesions in the brains of rats with Borna disease correlate with the induction of nitric oxide synthase.
    J Virol. 1993 Oct;67(10):5786-91 PMID: 7690410
  15. Aminoguanidine, an inhibitor of inducible nitric oxide synthase, ameliorates experimental autoimmune encephalomyelitis in SJL mice.
    J Clin Invest. 1994 Jun;93(6):2684-90 PMID: 7515395
  16. Cytokine induction during T-cell-mediated clearance of mouse hepatitis virus from neurons in vivo.
    J Virol. 1994 Sep;68(9):5483-95 PMID: 8057431
  17. Nitric oxide synthases: roles, tolls, and controls.
    Cell. 1994 Sep 23;78(6):915-8 PMID: 7522969
  18. Expression of the inducible nitric oxide synthase. Correlation with neuropathology and clinical features in mice with lymphocytic choriomeningitis.
    J Immunol. 1994 Oct 15;153(8):3622-9 PMID: 7523499
  19. Gamma interferon-induced, nitric oxide-mediated inhibition of vaccinia virus replication.
    J Virol. 1995 Feb;69(2):910-5 PMID: 7529336
  20. Inhibition of vesicular stomatitis virus infection by nitric oxide.
    J Virol. 1995 Apr;69(4):2208-13 PMID: 7533852
  21. Utility of mouse cell line DBT for propagation and assay of mouse hepatitis virus.
    Jpn J Exp Med. 1978 Feb;48(1):71-5 PMID: 209230
  22. Mechanism of vascular smooth muscle relaxation by organic nitrates, nitrites, nitroprusside and nitric oxide: evidence for the involvement of S-nitrosothiols as active intermediates.
    J Pharmacol Exp Ther. 1981 Sep;218(3):739-49 PMID: 6115052
  23. Murine hepatitis virus-4 (strain JHM)-induced neurologic disease is modulated in vivo by monoclonal antibody.
    Virology. 1984 Jan 30;132(2):261-70 PMID: 6199889
  24. Cytoimmunotherapy for persistent virus infection reveals a unique clearance pattern from the central nervous system.
    Nature. 1986 May 15-21;321(6067):239-43 PMID: 3086743
  25. Site-specific alteration of murine hepatitis virus type 4 peplomer glycoprotein E2 results in reduced neurovirulence.
    J Virol. 1986 Aug;59(2):463-71 PMID: 3016306
  26. Human gamma interferon and tumor necrosis factor exert a synergistic blockade on the replication of herpes simplex virus.
    J Virol. 1989 Mar;63(3):1354-9 PMID: 2536838
  27. Macrophage oxidation of L-arginine to nitrite and nitrate: nitric oxide is an intermediate.
    Biochemistry. 1988 Nov 29;27(24):8706-11 PMID: 3242600
  28. T-cell-mediated clearance of mouse hepatitis virus strain JHM from the central nervous system.
    J Virol. 1989 Jul;63(7):3051-6 PMID: 2542613
  29. Establishment and characterization of multipotent neural cell lines using retrovirus vector-mediated oncogene transfer.
    J Neurobiol. 1990 Mar;21(2):356-75 PMID: 2307979
  30. Effective clearance of mouse hepatitis virus from the central nervous system requires both CD4+ and CD8+ T cells.
    J Virol. 1990 Sep;64(9):4589-92 PMID: 2166833
  31. Alteration of the pH dependence of coronavirus-induced cell fusion: effect of mutations in the spike glycoprotein.
    J Virol. 1991 Apr;65(4):1916-28 PMID: 1848311
  32. Role of nitric oxide synthesis in macrophage antimicrobial activity.
    Curr Opin Immunol. 1991 Feb;3(1):65-70 PMID: 1711326
  33. Nitric oxide: physiology, pathophysiology, and pharmacology.
    Pharmacol Rev. 1991 Jun;43(2):109-42 PMID: 1852778
  34. Antibody-mediated clearance of alphavirus infection from neurons.
    Science. 1991 Nov 8;254(5033):856-60 PMID: 1658936
  35. 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):5312-6 PMID: 7539914
  36. Gamma interferon is a major mediator of antiviral defense in experimental measles virus-induced encephalitis.
    J Virol. 1995 Sep;69(9):5469-74 PMID: 7636992
  37. Vesicular stomatitis virus infection of the central nervous system activates both innate and acquired immunity.
    J Virol. 1995 Oct;69(10):6466-72 PMID: 7545248
  38. An essential role for type 1 interferon-gamma in terminating persistent viral infection.
    Virology. 1995 Sep 10;212(1):244-50 PMID: 7676639
  39. Inhibitory effect of nitric oxide on the replication of a murine retrovirus in vitro and in vivo.
    J Virol. 1995 Nov;69(11):7001-5 PMID: 7474119
  40. Gamma interferon is critical for resistance to Theiler's virus-induced demyelination.
    J Virol. 1995 Nov;69(11):7286-90 PMID: 7474155
  41. Activation of astrocytes in the spinal cord of mice chronically infected with a neurotropic coronavirus.
    Virology. 1995 Nov 10;213(2):482-93 PMID: 7491773
  42. Inhibition of vaccinia virus DNA replication by inducible expression of nitric oxide synthase.
    J Immunol. 1995 Dec 15;155(12):5711-8 PMID: 7499858
  43. HIV suppression by interleukin-16.
    Nature. 1995 Dec 7;378(6557):563 PMID: 8524386
  44. Identification of RANTES, MIP-1 alpha, and MIP-1 beta as the major HIV-suppressive factors produced by CD8+ T cells.
    Science. 1995 Dec 15;270(5243):1811-5 PMID: 8525373
  45. Nitric oxide production is increased during murine vaccinia virus infection, but may not be essential for virus clearance.
    Virology. 1996 Mar 15;217(2):470-7 PMID: 8610438
  46. Nitric oxide inhibits viral replication in murine myocarditis.
    J Clin Invest. 1996 Apr 15;97(8):1837-43 PMID: 8621766
  47. 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):304-6 PMID: 8623546
  48. Nitric oxide, a novel neuronal messenger.
    Neuron. 1992 Jan;8(1):3-11 PMID: 1370373
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1997-03-00
Pages
2202-10
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC191327
Subset
IM
Grants
NIAID NIH HHS · AI 25913 · United States
NIMH NIH HHS · MH 19185 · United States
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