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PMID: 8057431 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Cytokine induction during T-cell-mediated clearance of mouse hepatitis virus from neurons in vivo.

Journal of virology ·Vol. 68 ·No. 9 ·1994-09-00 ·Pages 5483-95

Pearce BD, Hobbs MV, McGraw TS, Buchmeier MJ

Abstract

To investigate the mechanism by which viruses are cleared from neurons in the central nervous system, we have utilized a mouse model involving infection with a neurotropic variant of mouse hepatitis virus (OBLV60). After intranasal inoculation, OBLV60 grew preferentially in the olfactory bulbs of BALB/c mice. Using in situ hybridization, we found that viral RNA localized primarily in the outer layers of the olfactory bulb, including neurons of the mitral cell layer. Virus was cleared rapidly from the olfactory bulb between 5 and 11 days. Athymic nude mice failed to eliminate the virus, demonstrating a requirement for T lymphocytes. Immunosuppression of normal mice with cyclophosphamide also prevented clearance. Both CD4+ and CD8+ T-cell subsets were important, as depletion of either of these subsets delayed viral clearance. Gliosis and infiltrates of CD4+ and CD8+ cells were detected by immunohistochemical analysis at 6 days. The role of cytokines in clearance was investigated by using an RNase protection assay for interleukin-1 alpha (IL-1 alpha), IL-1 beta, IL-2, IL-3, IL-4, IL-5, IL-6, tumor necrosis factor alpha (TNF-alpha), TNF-beta, and gamma interferon (IFN-gamma). In immunocompetent mice there was upregulation of RNA for IL-1 alpha, IL-1 beta, IL-6, TNF-alpha, and IFN-gamma at the time of clearance. Nude mice had comparable increases in these cytokine messages, with the exception of IFN-gamma. Induction of major histocompatibility complex class I (MHC-I) molecules on cells in infected brains was demonstrated by immunohistochemical analyses in normal and nude mice, suggesting that IFN-gamma may not be necessary for induction of MHC-I on neural cells in vivo.

MeSH Terms
Animals Central Nervous System Diseases/microbiology Coronavirus Infections/physiopathology Cytokines/biosynthesis,genetics Gene Expression Regulation, Viral H-2 Antigens/immunology Immunosuppression Therapy Mice Mice, Inbred BALB C Mice, Nude Murine hepatitis virus/growth & development,immunology Neurons/microbiology RNA, Messenger/genetics RNA, Viral/genetics T-Lymphocyte Subsets/immunology Time Factors
Chemicals
Cytokines H-2 Antigens RNA, Messenger RNA, Viral
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Pearce B D
Scripps Research Institute, La Jolla, California 92037.
Hobbs M V
McGraw T S
Buchmeier M J
References (68)
68 references, click to expand
  1. Studies on the synthesis and secretion of interleukin 1. I. A 33,000 molecular weight precursor for interleukin 1.
    J Immunol. 1985 Jan;134(1):343-9 PMID: 2578046
  2. Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain.
    Neuroscience. 1985 Jun;15(2):313-26 PMID: 3895031
  3. Responses of mice susceptible or resistant to lethal infection with mouse hepatitis virus, strain JHM, after exposure by a natural route.
    Lab Anim Sci. 1985 Oct;35(5):469-72 PMID: 2414512
  4. In vivo effects of coronavirus-specific T cell clones: DTH inducer cells prevent a lethal infection but do not inhibit virus replication.
    J Immunol. 1986 Apr 15;136(8):3052-6 PMID: 2420882
  5. Viremic dissemination of mouse hepatitis virus-JHM following intranasal inoculation of mice.
    Arch Virol. 1992;122(1-2):35-44 PMID: 1309644
  6. The V5A13.1 envelope glycoprotein deletion mutant of mouse hepatitis virus type-4 is neuroattenuated by its reduced rate of spread in the central nervous system.
    Virology. 1992 Mar;187(1):178-88 PMID: 1310555
  7. A case for cytokines as effector molecules in the resolution of virus infection.
    Immunol Today. 1993 Apr;14(4):155-7 PMID: 8499074
  8. Rous-Whipple Award Lecture. Viruses and diseases of the twenty-first century.
    Am J Pathol. 1993 Nov;143(5):1241-9 PMID: 8238240
  9. Mechanism of demyelination in JHM virus encephalomyelitis. Electron microscopic studies.
    Acta Neuropathol. 1973 Mar 30;24(1):76-85 PMID: 4349379
  10. Enhancement by interferon of the expression of surface antigens on murine leukemia L 1210 cells.
    Proc Natl Acad Sci U S A. 1973 Oct;70(10):2785-8 PMID: 4517933
  11. Extrathymic T cell maturation. Phenotypic analysis of T cell subsets in nude mice as a function of age.
    J Immunol. 1992 Mar 15;148(6):1620-9 PMID: 1347303
  12. Immune response to a murine coronavirus: identification of a homing receptor-negative CD4+ T cell subset that responds to viral glycoproteins.
    Virology. 1992 Apr;187(2):443-52 PMID: 1347668
  13. The role of nasopharyngeal lymphoid tissue.
    Immunol Today. 1992 Jun;13(6):219-24 PMID: 1627250
  14. Inflammatory cytokines within the central nervous system: sources, function, and mechanism of action.
    Am J Physiol. 1992 Jul;263(1 Pt 1):C1-16 PMID: 1636671
  15. Leucocyte recruitment and inflammation in the CNS.
    Trends Neurosci. 1992 Aug;15(8):276-8 PMID: 1384194
  16. SJL/J resistance to mouse hepatitis virus-JHM-induced neurologic disease can be partially overcome by viral variants of S and host immunosuppression.
    Microb Pathog. 1992 Jul;13(1):1-15 PMID: 1331698
  17. In vivo depletion of interferon-gamma leads to susceptibility of A/J mice to mouse hepatitis virus 3 infection.
    Immunobiology. 1992 Sep;185(5):475-82 PMID: 1360445
  18. Cervical lymphatics, the blood-brain barrier and the immunoreactivity of the brain: a new view.
    Immunol Today. 1992 Dec;13(12):507-12 PMID: 1463583
  19. Major histocompatibility complex genes have an increased brain expression after scrapie infection.
    Proc Natl Acad Sci U S A. 1993 Jan 1;90(1):114-7 PMID: 7678332
  20. Interleukin-6 induction in vitro in mouse brain endothelial cells and astrocytes by exposure to mouse hepatitis virus (MHV-4, JHM).
    J Neuroimmunol. 1993 Jan;42(1):47-52 PMID: 8380807
  21. The cellular and molecular pathogenesis of coronaviruses.
    Lab Anim Sci. 1993 Feb;43(1):15-28 PMID: 8384676
  22. Patterns of cytokine gene expression by CD4+ T cells from young and old mice.
    J Immunol. 1993 Apr 15;150(8 Pt 1):3602-14 PMID: 8096853
  23. The olfactory nerve and not the trigeminal nerve is the major site of CNS entry for mouse hepatitis virus, strain JHM.
    Virology. 1993 May;194(1):185-91 PMID: 8386871
  24. Mouse hepatitis virus A59 increases steady-state levels of MHC mRNAs in primary glial cell cultures and in the murine central nervous system.
    Microb Pathog. 1992 Dec;13(6):493-505 PMID: 1338798
  25. Virus-specific T cells in the central nervous system following infection with an avirulent neurotropic mouse hepatitis virus.
    Reg Immunol. 1992 May-Jun;4(3):145-52 PMID: 1338891
  26. The role of circulating interferon in the modifications of immune responsiveness by mouse hepatitis virus (MHV-3).
    J Immunol. 1976 Sep;117(3):748-53 PMID: 182881
  27. Mouse hepatitis virus type 4 (JHM strains). induced fatal central nervous system disease. I. genetic control and murine neuron as the susceptible site of disease.
    J Exp Med. 1981 Apr 1;153(4):832-43 PMID: 6265583
  28. Pathogenicity of antigenic variants of murine coronavirus JHM selected with monoclonal antibodies.
    J Virol. 1986 Jun;58(3):869-75 PMID: 3701929
  29. 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
  30. Inducibility of Ia antigen on astrocytes by murine coronavirus JHM is rat strain dependent.
    J Exp Med. 1987 Jul 1;166(1):259-64 PMID: 3036995
  31. In vitro anti-human immunodeficiency virus activities of tumor necrosis factor-alpha and interferon-gamma.
    J Immunol. 1988 Jan 1;140(1):120-4 PMID: 3121735
  32. Limbic encephalitis after inhalation of a murine coronavirus.
    Lab Invest. 1988 Jan;58(1):31-6 PMID: 2826881
  33. Simultaneous localization of calcitonin mRNA and peptide in a medullary thyroid carcinoma.
    Virchows Arch B Cell Pathol Incl Mol Pathol. 1987;54(3):144-51 PMID: 2894088
  34. Induction of glial cell MHC antigen expression in neurotropic coronavirus infections. Characterization of the H-2-inducing soluble factor elaborated by infected brain cells.
    J Immunol. 1988 Mar 15;140(6):2068-72 PMID: 2831279
  35. A novel form of TNF/cachectin is a cell surface cytotoxic transmembrane protein: ramifications for the complex physiology of TNF.
    Cell. 1988 Apr 8;53(1):45-53 PMID: 3349526
  36. Impaired clonal expansion in athymic nude CD8+CD4- T cells.
    J Immunol. 1988 Jun 1;140(11):3727-35 PMID: 3131418
  37. Spontaneous production of interleukin-2 and interleukin-3 by spleen cells from mice infected with mouse hepatitis virus type 4.
    J Virol. 1988 Sep;62(9):3506-8 PMID: 2841500
  38. Olfactory neural pathway in mouse hepatitis virus nasoencephalitis.
    Acta Neuropathol. 1988;76(5):502-6 PMID: 2847476
  39. Experimental demyelination induced by coronavirus JHM (MHV-4): molecular identification of a viral determinant of paralytic disease.
    Microb Pathog. 1987 Jul;3(1):9-20 PMID: 2848172
  40. Coronavirus-induced CNS disease: a model for virus-induced demyelination.
    J Neuroimmunol. 1988 Dec;20(2-3):111-6 PMID: 2848860
  41. 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
  42. Peripheral nerve injury causes transient expression of MHC class I antigens in rat motor neurons and skeletal muscles.
    Brain Res. 1989 Mar 6;481(2):368-72 PMID: 2720389
  43. 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
  44. On the cellular source and function of interleukin 6 produced in the central nervous system in viral diseases.
    Eur J Immunol. 1989 Apr;19(4):689-94 PMID: 2543584
  45. Manganous superoxide dismutase is essential for cellular resistance to cytotoxicity of tumor necrosis factor.
    Cell. 1989 Sep 8;58(5):923-31 PMID: 2476237
  46. Establishment and characterization of multipotent neural cell lines using retrovirus vector-mediated oncogene transfer.
    J Neurobiol. 1990 Mar;21(2):356-75 PMID: 2307979
  47. Processing of precursor interleukin 1 beta and inflammatory disease.
    J Biol Chem. 1990 Apr 15;265(11):6318-22 PMID: 2156847
  48. Duration of mouse hepatitis virus infection: studies in immunocompetent and chemically immunosuppressed mice.
    Lab Anim Sci. 1990 Mar;40(2):133-7 PMID: 2157090
  49. Tumor necrosis factor-alpha production by astrocytes. Induction by lipopolysaccharide, IFN-gamma, and IL-1 beta.
    J Immunol. 1990 Apr 15;144(8):2999-3007 PMID: 2109008
  50. Immortalization of hypothalamic GnRH neurons by genetically targeted tumorigenesis.
    Neuron. 1990 Jul;5(1):1-10 PMID: 2196069
  51. 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
  52. Induction and regulation of interleukin-6 gene expression in rat astrocytes.
    J Neuroimmunol. 1990 Dec;30(2-3):201-12 PMID: 2121800
  53. Protection of mice from a lethal coronavirus infection in the central nervous system by adoptive transfer of virus-specific T cell clones.
    J Neuroimmunol. 1991 Apr;32(1):1-9 PMID: 1705943
  54. 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
  55. Tumour necrosis factor-alpha, interferon-gamma and interferon-beta exert antiviral activity in nervous tissue cells.
    J Gen Virol. 1991 Apr;72 ( Pt 4):809-15 PMID: 1849968
  56. Characterization of brain-infiltrating mononuclear cells during infection with mouse hepatitis virus strain JHM.
    J Neuroimmunol. 1991 Jun;32(3):199-207 PMID: 1851765
  57. Acquired immunity of A/J mice to mouse hepatitis virus 3 infection: dependence on interferon-gamma synthesis and macrophage sensitivity to interferon-gamma.
    J Gen Virol. 1991 Jun;72 ( Pt 6):1317-22 PMID: 1646275
  58. Manganese superoxide dismutase is induced by IFN-gamma in multiple cell types. Synergistic induction by IFN-gamma and tumor necrosis factor or IL-1.
    J Immunol. 1991 Jul 1;147(1):149-54 PMID: 1904900
  59. Mouse hepatitis virus (MHV-4, JHM) blocks gamma-interferon-induced major histocompatibility complex class II antigen expression on murine cerebral endothelial cells.
    J Neuroimmunol. 1991 Sep;33(3):181-90 PMID: 1651958
  60. Immunopathogenesis of demyelination induced by MHV-4.
    Adv Exp Med Biol. 1990;276:565-72 PMID: 1966450
  61. Regulation of MHC class I and II antigens on cerebral endothelial cells and astrocytes following MHV-4 infection.
    Adv Exp Med Biol. 1990;276:579-91 PMID: 1966452
  62. Vacuolar degeneration induced by JHM-CC virus in the CNS of cyclophosphamide-treated mice.
    Adv Exp Med Biol. 1990;276:601-7 PMID: 1966455
  63. Viral persistence in neurons explained by lack of major histocompatibility class I expression.
    Science. 1991 Sep 13;253(5025):1283-5 PMID: 1891717
  64. Infection of BALB/cByJ mice with the JHM strain of mouse hepatitis virus alters in vitro splenic T cell proliferation and cytokine production.
    Lab Anim Sci. 1991 Apr;41(2):99-105 PMID: 1658457
  65. Antibody-mediated clearance of alphavirus infection from neurons.
    Science. 1991 Nov 8;254(5033):856-60 PMID: 1658936
  66. 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
  67. Activation of natural killer cells and induction of interferon after injection of mouse hepatitis virus type 3 in mice.
    Infect Immun. 1982 Mar;35(3):869-73 PMID: 6175579
  68. Experimental demyelination produced by the A59 strain of mouse hepatitis virus.
    Neurology. 1984 May;34(5):597-603 PMID: 6324031
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1994-09-00
Pages
5483-95
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC236949
Subset
IM
Grants
NIAID NIH HHS · AI25913 · United States
NINDS NIH HHS · NS12428 · United States
NINDS NIH HHS · NS22347 · United States
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