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Molecular Basis of Neuropathogenicity of Mouse Hepatitis Virus

  • Michael M. C. Lai
  • Stephen A. Stohlman

Abstract

The JHM strain of mouse hepatitis virus (MHV), a member of the Coronaviridae, was one of the earliest recognized neurotropic viruses. It was isolated from a paralytic mouse by F. S. Cheever et al. in 1949 (1, 2), and subsequently shown to cause encephalitis and demyelinating lesions upon intracerebral injection into mice (1, 3, 4, 5). The virus has a predilection for oligodendrocytes, causing primary demyelination with axonal sparing (3). The neuropathogenic properties of the virus in mice vary with the genetic background of the mouse strains and appear to be controlled by one or more host genes (6, 7, 8). Furthermore, several different strains of MHV have been isolated that differ markedly in their neuropathogenic properties. Thus, this system offers an experimental model in which both the host and viral genes influencing neuropathogenesis can be examined. Coronavimses, particularly MHV, also exhibit several unique features of virion structure and replication strategy (9), which make the MHV model a particularly interesting system. This chapter will emphasize the role of viral genes and the molecular approaches to the problems of MHV neuropathogenesis. A recent review has examined the role of host responses in this system (10).

Keywords

Recombinant Virus Nonstructural Protein Nucleocapsid Protein Parental Virus Viral Pathogenesis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Bailey, O. T., A. M. Pappenheimer, F. S. Cheever, and J. B. Daniels (1949) A murine coronavirus (JHM) causing disseminated encephalomyelitis with extensive destruction of myelin. II. Pathology. J. Exp. Med. 90, 195–212.PubMedCrossRefGoogle Scholar
  2. 2.
    Cheever, F. S., J. B. Daniels, A. M. Pappenheimer, and O. T. Bailey (1949) Amurine virus (JHM) causing disseminated encephalomyelitis with extensive destruction of myelin. I. Isolation and biological properties of the virus. J. Exp. Med. 90, 181–194.PubMedCrossRefGoogle Scholar
  3. 3.
    Lampert, P. W., J. K. Sims, and A. J. Kniazeff (1973) Mechanism of demyelination in JHM virus encephalomyelitis: Electron microscope studies. Acta Neuropathol. 24, 76–85.PubMedCrossRefGoogle Scholar
  4. 4.
    Stohlman, S. A. and L. P. Weiner (1981) Chronic central nervous system demyelination in mice after JHM virus infection. Neurology 31, 38–44.PubMedCrossRefGoogle Scholar
  5. 5.
    Weiner, L. P. (1973) Pathogenesis of demyelination induced by a mouse hepatitis virus (JHM virus). Acta Neurol. 18, 298–303.Google Scholar
  6. 6.
    Bang, F. S (1981) The use of a genetically incompatible combination of host and virus (MHV) for the study of mechanisms of host resistance. Adv. Exp. Med. Biol. 142, 359–373.PubMedGoogle Scholar
  7. 7.
    Knobler, R. L., M. V. Haspel, and M. B. A. Oldstone (1981) Mouse hepatitis virus type 4 (JHM strain)-induced fatal central nervous system disease. I. Genetic control and the murine neuron as the susceptible site of disease. J. Exp. Med. 153, 832–843.PubMedCrossRefGoogle Scholar
  8. 8.
    Stohlman, S. A. and J. A. Frelinger (1978) Resistance to fatal central nervous system disease by mouse hepatitis virus, strain JHM. I. Genetic analysis. Immunogenetics 6, 277–281.CrossRefGoogle Scholar
  9. 9.
    Lai, M. M. C. (1990) Coronavirus: organization, replication and expression of genome. Ann. Rev. Microb. 44, 303–333.PubMedCrossRefGoogle Scholar
  10. 10.
    Kyuwa, S. and S. A. Stohlman (1990) Pathogenesis of a neurotropic murine coronavirus, strain JHM in the central nervous system of mice. Seminar in Virology 1, 273–280.Google Scholar
  11. 11.
    Lee, H.-J., C.-K. Shieh, A. E. Gorbalenya, E. V. Koonin, N. La Monica, J. Tuler, A. Bagdzyahdzhyan, and M. M.-C. Lai (1991) The complete sequence (22 kilobases) of murine coronavirus gene 1 encoding the putative proteases and RNA polymerase. Virology 180, 567–582.PubMedCrossRefGoogle Scholar
  12. 12.
    Pachuk, C. J., P. J. Bredenbeek, P. W. Zoltick, W. J. M. Spaan, and S. R. Weiss (1989) Molecular cloning of the gene encoding the putative polymerase of mouse hepatitis coronavirus strain A59. Virology 171, 141–148.PubMedCrossRefGoogle Scholar
  13. 13.
    Lai, M. M. C., P. R. Brayton, R. C. Armen, C. D. Patton, C. Pugh, and S. A. Stohlman (1981) Mouse hepatitis virus A59: Messenger RNA structure and genetic localization of the sequence divergence from the hepatotropic strain MHV 3. J. Virol. 39, 823–834.PubMedGoogle Scholar
  14. 14.
    Leibowitz, J. L., S. R. Weiss, E. Paavola, and C. W. Bond (1982) Cell-free translation of murine coronavirus RNA. J. Virol. 43, 905–913.PubMedGoogle Scholar
  15. 15.
    Sturman, L. S. and K. V. Holmes (1983) The molecular biology of coronaviruses. Adv. Virus Res. 28, 35–112.PubMedCrossRefGoogle Scholar
  16. 16.
    Frana, M. F., J. N. Behnke, L. S. Sturman, and K. V. Holmes (1985) Proteolytic cleavage of the E2 glycoprotein of murine coronavirus: Host-dependent differences in proteolytic cleavage and cell fusion. J. Virol. 56, 912–920.PubMedGoogle Scholar
  17. 17.
    Sturman, L. S., K. V. Holmes, and J. Behnke (1980) Isolation of coronavirus envelope glycoproteins and interaction with the viral nucleocapsid. J. Virol. 33, 449–462.PubMedGoogle Scholar
  18. 18.
    Holmes, K. V., E. W. Doller, and L. S. Sturman (1981) Tunicamycin-resistant glycosylation of coronavirus glycoprotein: Demonstration of a novel type of viral glycoprotein. Virology 115, 334–344.PubMedCrossRefGoogle Scholar
  19. 19.
    Niemann, H., T. Mayer, M. Wirth, and T. Tamura (1987) Expression of the El gene of mouse hepatitis virus (MHV A59) in vivo and in vitro}. Adv. Exp. Med. Biol. 218, 83–97.PubMedCrossRefGoogle Scholar
  20. 20.
    Rottier, P. J. M., M. C. Horzinek, and B. A. M. van der Zeijst (1981) Viral protein synthesis in mouse hepatitis virus strain A59-infected cells: Effect of tunicamycin. J. Virol. 40, 350–357.PubMedGoogle Scholar
  21. 21.
    Makino, S., F. Taguchi, M. Hayami, and K. Fujiwara (1983) Characterization of small plaque mutants of mouse hepatitis virus, JHM strain. Microbiol. Immunol. 27, 445–454.PubMedGoogle Scholar
  22. 22.
    Siddell, S. G. (1982) Coronavirus JHM: Tryptic peptide fingerprinting of virion proteins and intracellular polypeptides. J. Gen. Virol. 62, 259–269.PubMedCrossRefGoogle Scholar
  23. 23.
    Yokomori, K., N. La Monica, S. Makino, C.-K. Shieh, and M. M.-C. Lai (1989) Biosynthesis, structure, and biological activities of envelope protein gp65 of murine coronavirus. Virology 173, 683–691.PubMedCrossRefGoogle Scholar
  24. 24.
    Luytjes, W., P. J. Bredenbeek, A. F. H. Noten, M. C. Horzinek, and W. J. Spaan (1988) Sequence of mouse hepatitis virus A59 mRNA 2: Indications for RNA-recombination between coronavirus and influenza C virus. Virology 166, 415–422.PubMedCrossRefGoogle Scholar
  25. 25.
    Baric, R. S., G. W. Nelson, J. O. Fleming, R. J. Deans, J. G. Keck, N. Casteel, and S. A. Stohlman (1988) Interactions between coronavirus nucleocapsid protein and viral RNAs: Implications for viral transcription. J. Virol. 62, 4280–4287.PubMedGoogle Scholar
  26. 26.
    Stohlman, S. A., R. S. Baric, G. N. Nelson, L. H. Soe, L. M. Welter, and R. J. Deans (1988) Specific interaction between coronavirus leader RNA and nucleocapsid protein. J. Virol. 62, 4288–4295.PubMedGoogle Scholar
  27. 27.
    Bredenbeek, P. J., C. J. Pachuk, A. F. H. Noten, J. Charite, W. Luytjes, S. R. Weiss, and W. J. M. Spaan (1990) The primary structure and expression of the second open reading frame of the polymerase gene of the coronavirus MHV-A59: A highly conserved polymerase is expressed by an efficient ribosomal frameshifting mechanism. Nucleic Acids Res. 18, 1825–1832.PubMedCrossRefGoogle Scholar
  28. 28.
    Baker, S. C., C.-K. Shieh, L. H. Soe, M.-F. Chang, D. M. Vannier, and M. M.-C. Lai (1989) Identification of a domain required for the autoproteolytic cleavage of murine coronavirus gene A polyprotein. J. Virol. 63, 3693–3699.PubMedGoogle Scholar
  29. 29.
    Baric, R. S., K. Fu, M. C. Schaad, and S. A. Stohlman (1990) Establishing a genetic recombination map for murine coronavirus strain A59 complementation groups. Virology 177, 646–656.PubMedCrossRefGoogle Scholar
  30. 30.
    Leibowitz, J. L., J. R. DeVries, and M. V. Haspel (1982) Genetic analysis of murine hepatitis virus strain JHM. J. Virol. 42, 1080–1087.PubMedGoogle Scholar
  31. 31.
    Schaad, M. C., S. A. Stohlman, J. Egbert, K. Lum, K. Fu, T. Wei, and R. S. Baric (1990) Genetics of mouse hepatitis virus transcription: Identification of cistrons which may function in positive and negative strand RNA synthesis. Virology 177, 634–645.PubMedCrossRefGoogle Scholar
  32. 32.
    Schwarz, B., E. Routledge, and S. G. Siddell (1990) Murine coronavirus nonstructural protein ns2 is not essential for virus replication in transformed cells. J. Virol. 64, 4784–4791.PubMedGoogle Scholar
  33. 32a.
    Yokomori, K. and M. M. C. Lai (1991) Mouse hepatitis virus RNA sequence reveals that nonstructural proteins ns4 and ns5a are not essential for murine coronavirus replication. J. Virol, (in press).Google Scholar
  34. 33.
    Shieh, C.-K., L. H. Soe, S. Makino, M.-F. Chang, S. A. Stohlman, and M. M. C. Lai (1987) The 5′-end sequence of the murine coronavirus genome: Implications for multiple fusion sites in leader-primed transcription. Virology 156, 321–330.PubMedCrossRefGoogle Scholar
  35. 34.
    Tooze, J. and S. A. Tooze (1985) Infection of AtT20 murine pituitary tumour cells by mouse hepatitis virus strain A59: Virus budding is restricted to the Golgi region. Eur. J. Cell. Biol. 37, 203–212.PubMedGoogle Scholar
  36. 35.
    Fishman, P. S., J. S. Gass, P. T. Sworeland, E. Lavi, M. Highkin, and S. R. Weiss (1985) Infection of the basal ganglia by a murine coronavirus. Science 229, 877–879.PubMedCrossRefGoogle Scholar
  37. 36.
    Knobler, R. L., M. Dubois-Dalcq, M. V. Haspel, S. P. Claysmith, P. W. Lampert, and M. B. A. Oldstone (1981) Selective localization of wild type and mutant mouse hepatitis virus (JHM strain) antigens in CNS tissue by fluorescence, light and electron microscopy. J. Neuroimmunol. 1, 81–92.PubMedCrossRefGoogle Scholar
  38. 37.
    Perlman, S. and D. Ries (1987) The astrocyte is a target cell in mice persistently infected with mouse hepatitis virus, strain JHM. Microb. Pathogen. 3, 309–314.CrossRefGoogle Scholar
  39. 38.
    Haspel, M. V., P. W. Lampert, and M. B. A. Oldstone (1978) Temperature-sensitive mutants of mouse hepatitis virus produce a high incidence of demyelination. Proc. Natl. Acad. Sci. USA 75, 4033–4036.PubMedCrossRefGoogle Scholar
  40. 39.
    Koolen, M. J. M., A. D. M. E. Osterhaus, G. van Steenis, M. C. Horzinek, and B. A. M. van der Zeijst (1983) Temperature-sensitive mutants of mouse hepatitis virus strain A59: Isolation, characterization and neuropathogenic properties. Virology 125, 393–402.PubMedCrossRefGoogle Scholar
  41. 40.
    Stohlman, S. A., P. R. Brayton, J. O. Fleming, L. P. Weiner, and M. M. C. Lai (1982) Murine coronaviruses: Isolation and characterization of two plaque morphology variants of the JHM neurotropic strain. J. Gen. Virol. 63, 265–275.CrossRefGoogle Scholar
  42. 41.
    Banner, L. R., J. G. Keck, and M. M.-C. Lai (1990) A clustering of RNA recombination sites adjacent to a hypervariable region of the peplomer gene of murine coronavirus. Virology 175, 548–555.PubMedCrossRefGoogle Scholar
  43. 42.
    Parker, S. E., T. M. Gallagher, and M. J. Buchmeier (1990) Sequence analysis reveals extensive polymorphism and evidence of deletions within the E2 glycoprotein gene of several strains of murine hepatitis virus. Virology 173, 664–673.CrossRefGoogle Scholar
  44. 43.
    Lavi, E., E. M. Murray, S. Makino, S. A. Stohlman, M. M. C. Lai, and S. R. Weiss (1990) Determinants of coronavirus MHV pathogenesis are localized to 3′-portions of the genome as determined by ribonucleic acid-ribonucleic acid recombination. Lab. Invest. 62, 570–578.PubMedGoogle Scholar
  45. 44.
    Knobler, R. L., B. A. Taylor, M. K. Wooddell, W G. Beamer, and M. B. A. Oldstone (1984) Host genetic control of mouse hepatitis virus type-4 (JHM strain) replication. II. The gene locus for susceptibility is linked to the Svp-2 locus on mouse chromosome 7. Exp. Clin. Immunogenet. 1, 217–222.PubMedGoogle Scholar
  46. 45.
    Stohlman, S. A., J. A. Frelinger, and L. P. Weiner (1980) Resistance to fatal central nervous system disease by mouse hepatitis virus, strain JHM. II. Adherent cell-mediated protection. J. Immunol. 124, 1733–1739.PubMedGoogle Scholar
  47. 46.
    Wilson, G. A. R. and S. Dales (1988) In vivo and in vitro models of demyelinating disease: Efficiency of virus spread and formation of infectious centers among glial cells is genetically determined by the murine host. J. Virol. 62, 3371–3377.PubMedGoogle Scholar
  48. 47.
    Boyle, J. R., D. G. Weismiller, and K. V. Holmes (1987) Genetic resistance to mouse hepatitis virus correlates with absence of virus-binding activity on target tissues. J. Virol. 61, 185–189.PubMedGoogle Scholar
  49. 47a.
    Williams, R. K., G.-S. Jiang, and K. V. Holmes (1991) Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins. Proc. Natl. Acad. Sci. USA 88, 5533–5536.PubMedCrossRefGoogle Scholar
  50. 48.
    Lucas, A., W. Flintoff, R. Anderson, D. Percy, M. Coulter, and S. Dales (1977) In vivo and in vitro models of demyelinating diseases: Tropism of the JHM strain of murine hepatitis virus for cells of glial origin. Cell 12, 553–560.PubMedCrossRefGoogle Scholar
  51. 49.
    Massa, P. T., R. Brinkmann, and V. ter Meulen (1987) Inducibility of la antigen on astrocytes by murine coronavirus JHM is rat strain-dependent. J. Exp. Med. 166, 259–264.PubMedCrossRefGoogle Scholar
  52. 50.
    Suzumura, A., E. Lavi, S. Bhat, D. Murasko, S. R. Weiss, and D. H. Silberberg (1988) 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. 140, 2068–2072.PubMedGoogle Scholar
  53. 51.
    Suzumura, A., E. Lavi, S. R. Weiss, and D. H. Silberberg (1986) Coronavirus infection induces H-2 antigen expression on oligodendrocytes and astrocytes. Science 232, 991–993.PubMedCrossRefGoogle Scholar
  54. 52.
    Buchmeier, M. J., H. A. Lewicki, P. J. Talbot, and R. L. Knobler (1984) Murine hepatitis virus (strain JHM)-induced neurologic disease is modulated in vivo by monoclonal antibody. Virology 132, 261–270.PubMedCrossRefGoogle Scholar
  55. 53.
    Fleming, J. O., R. A. Shubin, M. A. Sussman, N. Casteel, and S. A. Stohlman (1989) Monoclonal antibodies to the matrix (El) glycoprotein of mouse hepatitis virus protect mice from encephalitis. Virology 168, 162–167.PubMedCrossRefGoogle Scholar
  56. 54.
    Lecomte, J., V. Cainelli-Gebara, G. Mercier, S. Mansour, P. J. Talbot, G. Lussier, and D. Oth (1987) Protection from mouse hepatitis virus type 3-induced acute disease by an anti-nucleoprotein monoclonal antibody. Arch. Virol. 97, 123–130.PubMedCrossRefGoogle Scholar
  57. 55.
    Nakanaga, K., K. Yamanouchi, and K. Fujiwara (1986) Protective effect of monoclonal antibodies on lethal mouse hepatitis virus infection in mice. J. Virol. 59, 168–171.PubMedGoogle Scholar
  58. 56.
    Wege, H., J. Winter, and R. Meyermann (1988) The peplomer protein E2 of coronavirus JHM as a determinant of neurovirulence: Definition of critical epitopes by variant analysis. J. Gen. Virol. 69, 87–98.PubMedCrossRefGoogle Scholar
  59. 57.
    Stohlman, S. A., G. K. Matsushima, N. Casteel, and L. P. Weiner (1986) In vivo effects of coronavirus-specific T cell clones: DTH inducer cells prevent a lethal infection but do not inhibit virus replication. J. Immunol. 136, 3052–3056.PubMedGoogle Scholar
  60. 58.
    Stohlman, S. A., M. A. Sussman, G. K. Matsushima, R. A. Shubin, and S. S. Erlich (1988) Delayed-type hypersensitivity response in the central nervous system during JHM virus infection requires viral specificity for protection. J. Neuroimmunol. 19, 255–268.PubMedCrossRefGoogle Scholar
  61. 59.
    Erlich, S. S., G. K. Matsushima, and S. A. Stohlman (1989) Studies on the mechanism of protection from acute viral encephalomyelitisby delayed-type hypersensitivity inducer T cell clones. J. Neurol. Sci. 90, 203–216.PubMedCrossRefGoogle Scholar
  62. 60.
    Kyuwa, S. and K. Fujiwara (1984) Delayed-type hypersensitivity in mouse hepatitis virus infection in mice. Jpn. J. Exp. Med. 54, 81–86.PubMedGoogle Scholar
  63. 61.
    Sussman, M. A., J. O. Fleming, H. Allen, and S. A. Stohlman (1987) Immune mediated clearance of JHM virus from the central nervous system. Adv. Exp. Med. Biol. 218, 399–410.PubMedCrossRefGoogle Scholar
  64. 62.
    Sussman, M. A., R. A. Shubin, S. Kyuwa, and S. A. Stohlman (1989) T cell-mediated clearance of mouse hepatitis virus strain JHM from the central nervous system. J. Virol. 63, 3051–3056.PubMedGoogle Scholar
  65. 63.
    Williamson, J. S. P. and S. A. Stohlman (1990) Effective clearance of mouse hepatitis virus from the central nervous system requires both CD4+ and DC8+ T. cells. J. Virol. 64, 4589–4592.PubMedGoogle Scholar
  66. 63a.
    Williamson, J. S. P., K. C. Sykes, and S. A. Stohlman (1991) Characterization of brain-infiltrating mononuclear cells during infectiion with mouse hepatitis virus strain JHM. J. Neuroimmunol. 32, 199–207.PubMedCrossRefGoogle Scholar
  67. 63b.
    Wang, F.-I., S. A. Stohlman, and J. A. Fleming (1990) Demyelination induced by murine hepatitis virus JHM strain (MHV-4) is immunologically mediated. J. Neuroimmunol. 30, 31–41.PubMedCrossRefGoogle Scholar
  68. 64.
    Buchmeier, M. J., R. G. Dalziel, and M. J. M. Koolen (1988) Coronavirus-induced CNS disease: A model for virus-induced demyelination. J. Neuroimmunol. 20, 111–116.PubMedCrossRefGoogle Scholar
  69. 65.
    Dalziel, R. G., P. W. Lampert, P. J. Talbot, and M. J. Buchmeier (1986) Site-specific alteration of murine hepatitis virus type-4 (MHV-4) peplomer glycoprotein E2 results in reduced neurovirulence. J. Virol. 59, 463–471.PubMedGoogle Scholar
  70. 66.
    Fleming, J. O., M. D. Trousdale, J. Bradbury, S. A. Stohlman, and L. P. Weiner (1987) Experimental demyelination induced by coronavirus JHM (MHV-4): Molecular identification of a viral determinant of paralytic disease. Microb. Pathogen. 3, 9–20.CrossRefGoogle Scholar
  71. 67.
    Fleming, J. O., M. D. Trousdale, F. A. K. El-Zaatari, S. A. Stohlman, and L. P. Weiner (1986) Pathogenicity of antigenic variants of murine coronavirus JHM selected with monoclonal antibodies. J. Virol. 58, 869–875.PubMedGoogle Scholar
  72. 67a.
    Wang, F.-I., J. O. Fleming, and M. M. C. Lai (1991) Sequence analysis of the spike protein genes of murine coronavirus variants: Study of genetic sites affecting neuropathogenicity. Virology (submitted).Google Scholar
  73. 68.
    Gallagher, T. M., S. E. Parker, and M. J. Buchmeier (1990) Neutralization-resistant variants of a neurotropic coronavirus are generated by deletions within the amino-terminal half of the spike glycoprotein. J. Virol. 64, 731–741.PubMedGoogle Scholar
  74. 69.
    Morris, V. L., C. Tieszer, J. Mackinnon, and D. Percy (1989) Characterization of coronavirus JHM variants isolated from Wistar Furth rats with a viral-induced demyelinating disease. Virology 169, 127–136.PubMedCrossRefGoogle Scholar
  75. 70.
    Taguchi, F., S. G. Siddell, H. Wege, and V. ter Meulen (1985) Characterization of a variant virus selected in rat brains after infection by coronavirus mouse hepatitis virus JHM. J. Virol. 54, 429–435.PubMedGoogle Scholar
  76. 71.
    Taguchi, F., P. T. Massa, and V. ter Meulen (1986) Characterization of a variant virus isolated from neural cell culture after infection of mouse coronavirus JHMV. Virology 155, 267–270.PubMedCrossRefGoogle Scholar
  77. 71a.
    La Monica, N., L. R. Banner, V. L. Morris, and M. M. C. Lai (1991) Localization of extensive deletions in the structural genes of two neurotropic variants of murine coronavirus JHM. Virology 182, 883–888.PubMedCrossRefGoogle Scholar
  78. 72.
    Keck, J. G., L. H. Soe, S. Makino, S. A. Stohlman, and M. M. C. Lai (1988) RNA recombination of murine coronaviruses: Recombination between fusion-positive MHV-A59 and fusion-negative MHV-2. J. Virol. 62, 1989–1998.PubMedGoogle Scholar
  79. 73.
    Keck, J. G., S. A. Stohlman, L. H. Soe, S. Makino, and M. M. C. Lai (1987) Multiple recombination sites at the 5′-end of murine coronavirus RNA. Virology 156, 331–341.PubMedCrossRefGoogle Scholar
  80. 74.
    Lai, M. M. C., R. S. Baric, S. Makino, J. G. Keck, J. Egbert, J. L. Leibowitz, and S. A. Stohlman (1985) Recombination between nonsegmented RNA genomes of murine coronaviruses. J. Virol. 56, 449–456.PubMedGoogle Scholar
  81. 75.
    Keck, J. G., G. K. Matsushima, S. Makino, J. O. Fleming, D. M. Vannier, S. A. Stohlman, and M. M. C. Lai (1988) In vivo RNA-RNA recombination of coronavirus in mouse brain. J. Virol. 62, 1810–1813.PubMedGoogle Scholar
  82. 76.
    Makino, S., J. O. Fleming, J. G. Keck, S. A. Stohlman, and M. M. C. Lai (1987) RNA recombination of coronaviruses: Localization of neutralizing epitopes and neuropathogenic determinants on the carboxyl terminus of peplomers. Proc. Natl. Acad. Sci. USA 84, 6567–6571.PubMedCrossRefGoogle Scholar
  83. 77.
    Shieh, C.-K., H.-J. Lee, K. Yokomori, N. La Monica, S. Makino, and M. M. C. Lai (1989) Identification of a new transcriptional initiation site and the corresponding functional gene 2b in the murine coronavirus RNA genome. J. Virol. 63, 3729–3736.PubMedGoogle Scholar
  84. 77a.
    Yokomori, K., L. R. Banner, and M. M. C. Lai (1991) Heterogeneity of gene expression of the hemagglutinin-esterase (HE) protein of murine coronaviruses. Virology 183, 647–657.PubMedCrossRefGoogle Scholar
  85. 78.
    Makino, S. and M. M.-C. Lai (1989) Evolution of the 5′-end of genomic RNA of murine coronaviruses during passages in vitro. Virology 169, 227–232.PubMedCrossRefGoogle Scholar
  86. 79.
    Hogue, B. G. and D. A. Brian (1986) Structural proteins of human respiratory coronavirus OC43. Virus Res. 5, 131–144.PubMedCrossRefGoogle Scholar
  87. 80.
    King, B., B. J. Potts, and D. A. Brian (1985) Bovine coronavirus hemagglutinin protein. Virus Res. 2, 53–59.PubMedCrossRefGoogle Scholar
  88. 81.
    Deregt, D., G. A. Gifford, M. Khalid Ijaz, T. C. Watts, J. E. Gilchrist, D. M. Haines, and L. A. Babiuk (1989) Monoclonal antibodies to bovine coronavirus glycoproteins E2 and E3, demonstration of in vivo neutralizing activity. J. Gen. Virol. 70, 993–998.PubMedCrossRefGoogle Scholar
  89. 82.
    Vlasak, R., W. Luytjes, J. Lieder, W. Spaan, and P. Palese (1988) The E3 protein of bovine coronavirus is a receptor-destroying enzyme with acetyltransferase activity. J. Virol. 62, 4686–4690.PubMedGoogle Scholar
  90. 82a.
    Pfleiderer, M., E. Routledge, G. Herrler, and S. G. Siddell (1991) High level transient expression of the murine coronavirus hemagglutinin-esterase. J. Gen. Virol. 72, 1309–1315.PubMedCrossRefGoogle Scholar
  91. 83.
    Makino, S., J. G. Keck, S. A. Stohlman, and M. M. C. Lai (1986) High-frequency RNA recombination of murine coronaviruses. J. Virol. 57, 729–737.PubMedGoogle Scholar
  92. 84.
    Bennink, J. R., J. W. Yewdell, G. L. Smith, and B. Moss (1987) Anti-influenza virus cytotoxic T lymphocytes recognize the three viral polymerases and a nonstructural protein: Responsiveness to individual viral antigens is MHC controlled. J. Virol. 61, 1098–1102.PubMedGoogle Scholar
  93. 85.
    Koszinowski, U. H., G. M. Keil, H. Schwarz, J. Schickedanz, and M. J. Reddehase (1987) A nonstructural polypeptide encoded by immediate-early transcription unit 1 of murine cytomegalovirus is recognized by cytolytic T lymphocytes. J. Exp. Med. 166, 289–294.PubMedCrossRefGoogle Scholar
  94. 86.
    Holland, J., K. Spindler, F. Horodyski, E. Grabau, S. Nichol, and S. VandePol (1982) Rapid evolution of RNA genomes. Science 215, 1577–1585.PubMedCrossRefGoogle Scholar
  95. 87.
    Erlich, S. S., J. O. Fleming, S. A. Stohlman, and L. P. Weiner (1987) Experimental neuropathology of chronic demyelination induced by a JHM virus variant (DS). Arch. Neurol. 44, 839–842.PubMedCrossRefGoogle Scholar
  96. 88.
    Baric, R. S., C.-K. Shieh, S. A. Stohlman, and M. M. C. Lai (1987) Analysis of intracellular small RNAs of mouse hepatitis virus: Evidence for discontinuous transcription. Virology 156, 342–354.PubMedCrossRefGoogle Scholar
  97. 89.
    Javier, R. T., F. Sedarati, and J. G. Stevens (1986) Two avirulent herpes simplex viruses generate lethal recombinants in vivo. Science 234, 746–748.PubMedCrossRefGoogle Scholar
  98. 90.
    Katz, J. B., L. M. Henderson, and G. A. Erickson (1990) Recombination in vivo of pseudorabies vaccine strains to produce new virus strains. Vaccine 8, 286–288.PubMedCrossRefGoogle Scholar
  99. 91.
    Makino, S., F. Taguchi, and K. Fujiwara (1984) Defective interfering particles of mouse hepatitis virus. Virology 133, 9–17.PubMedCrossRefGoogle Scholar
  100. 92.
    Makino, S., C.-K. Shieh, J. G. Keck, and M. M. C. Lai (1988) Defective interfering particles of murine coronavirus: Mechanism of synthesis of defective viral RNAs. Virology 163, 104–111.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media New York 1992

Authors and Affiliations

  • Michael M. C. Lai
  • Stephen A. Stohlman

There are no affiliations available

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