Murine coronavirus neuropathogenesis: Determinants of virulence

Journal of NeuroVirology

Volumn 16, Issue 6, 2010, Pages 427-434

  Cowley, Timothy J ^a   Weiss, Susan R ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

JHM and A59 strains; mouse hepatitis virus; neurovirulence; viral spread

Indexed keywords

CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1; GAMMA INTERFERON; HEMAGGLUTININ; NONSTRUCTURAL PROTEIN 4; NUCLEOCAPSID PROTEIN; VIRUS RECEPTOR; VIRUS SPIKE PROTEIN; CEACAM1A PROTEIN; ESTERASE; NONSTRUCTURAL PROTEIN 2; UNCLASSIFIED DRUG; VIRUS HEMAGGLUTININ;

ADAPTIVE IMMUNITY; INNATE IMMUNITY; MURINE HEPATITIS CORONAVIRUS; NERVE CELL; NEUROPATHOLOGY; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; T LYMPHOCYTE; VIRUS REPLICATION; VIRUS TRANSMISSION; VIRUS VIRULENCE; ANTIGEN EXPRESSION; MURINE CORONAVIRUS; MURINE HEPATITIS VIRUS (STRAIN A59); VIRUS INFECTIVITY; VIRUS ISOLATION; VIRUS NUCLEOCAPSID;

ADAPTIVE IMMUNITY; ANIMALS; BRAIN; GENES, VIRAL; IMMUNITY, INNATE; MICE; MICE, INBRED C57BL; MURINE HEPATITIS VIRUS; NEURONS; NUCLEOCAPSID PROTEINS; RECEPTORS, VIRUS; T-LYMPHOCYTES; VIRULENCE; VIRUS REPLICATION;

MURINE HEPATITIS VIRUS;

EID: 78649693194     PISSN: 13550284     EISSN: None     Source Type: Journal    
DOI: 10.3109/13550284.2010.529238     Document Type: Review

References (78)

1. Barnett EM, Perlman S (1993). The olfactory nerve and not the trigeminal nerve is the major site of CNS entry for mouse hepatitis virus, strain JHM. Virology 194: 185-191.
2. Bender SJ, Phillips JM, Scott EP, Weiss SR (2010). Murine coronavirus receptors are differentially expressed in the central nervous system and play virus strain-dependent roles in neuronal spread. J Virol 84: 11030-11044.
3. Bender SJ, Weiss SR (2010). Pathogenesis of murine coro-navirus in the central nervous system. J Neuroimmune Pharmacol 5: 336-354.
4. Bergmann CC, Parra B, Hinton DR, Chandran R, Morrison M, Stohlman SA (2003). Perforin-mediated effector function within the central nervous system requires IFN-gamma-mediated MHC up-regulation. J Immunol 170: 3204-3213.
5. Cheever FS, Daniels JB, Pappenheimer AM, Baily OT (1949). A murine virus (JHM) causing disseminated encephalo-myelitis with extensive destruction of myelin. I. Isolation and biological properties of the virus. J ExpMed 90: 181-194.
6. Cowley TJ, Long SY, Weiss SR (2010). The murine coro-navirus nucleocapsid gene is a determinant of virulence. J Virol 84: 1752-1763.
7. De Albuquerque N, Baig E, Ma X, Zhang J, He W, Rowe A, Habal M, Liu M, Shalev I, Downey GP, Gorczynski R, Butany J, Leibowitz J, Weiss SR, McGilvray ID, Phillips MJ, Fish EN, Levy GA (2006). Murine hepatitis virus strain 1 produces a clinically relevant model of severe acute respiratory syndrome in A/J mice. J Virol 80: 10382-10394.
8. Dorries R (2001). The role of T-cell-mediated mechanisms in virus infections of the nervous system. Curr Top Microbiol Immunol 253: 219-245.
9. Eriksson KK, Cervantes-Barragan L, Ludewig B, Thiel V (2008). Mouse hepatitis virus liver pathology is dependent on ADP-ribose-1¢¢ -phosphatase, a viral function conserved in the alpha-like supergroup. J Virol 82: 12325-12334.
10. Fazakerley JK, Parker SE, Bloom F, Buchmeier MJ (1992). 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. Virol 187: 178-188.
11. Fischer F, Peng D, Hingley ST, Weiss SR, Masters PS (1997). The internal open reading frame within the nucleocapsid gene of mouse hepatitis virus encodes a structural protein that is not essential for viral replication. J Virol 71: 996-1003.
12. Fishman PS, Gass JS, Swoveland PT, Lavi E, Highkin MK, Weiss SR (1985). Infection of the basal ganglia by a murine coronavirus. Science 229: 877-879.
13. Gallagher TM, Buchmeier MJ (2001). Coronavirus spike proteins in viral entry and pathogenesis. Virology 279: 371-374.
14. Gallagher TM, Buchmeier MJ, Perlman S (1992). Cell receptor-independent infection by a neurotropic murine coronavirus. Virology 191: 517-522.
15. Gallagher TM, Parker SE, Buchmeier MJ (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.
16. Gombold JL, Sutherland RM, Lavi E, Paterson Y, Weiss SR (1995). Mouse hepatitis virus A59-induced demyelin-ation can occur in the absence of CD8+ T cells. Microb Pathog 18: 211-221.
17. Gorbalenya AE, Koonin EV, Lai MM (1991). Putative papain-related thiol proteases of positive-strand RNA viruses. Identification of rubi- and aphthovirus proteases and delineation of a novel conserved domain associated with proteases of rubi-, alpha- and corona-viruses. FEBS Lett 288: 201-205.
18. Haspel MV, Lampert PW, Oldstone MB (1978). Temperature-sensitive mutants of mouse hepatitis virus produce a high incidence of demyelination. Proc Natl Acad Sci USA 75: 4033-4036.
19. Houtman JJ, Fleming JO (1996a). Dissociation of demye-lination and viral clearance in congenitally immunode-ficient mice infected with murine coronavirus JHM. J NeuroVirol 2: 101-110.
20. Houtman JJ, Fleming JO (1996b). Pathogenesis of mouse hepatitis virus-induced demyelination. J NeuroVirol 2: 361-376.
21. Iacono KT, Kazi L, Weiss SR (2006). Both spike and background genes contribute to murine coronavirus neurovirulence. J Virol 80: 6834-6843.
22. Karman J, Ling C, Sandor M, Fabry Z (2004). Initiation of immune responses in brain is promoted by local dendritic cells. J Immunol 173: 2353-2361.
23. Kazi L, Lissenberg A, Watson R, de Groot RJ, Weiss SR (2005). Expression of hemagglutinin esterase protein from recombinant mouse hepatitis virus enhances neu-rovirulence. J Virol 79: 15064-15073.
24. Knobler RL, Haspel MV, Oldstone MB (1981). 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 153: 832-843.
25. Koetzner CA, Kuo L, Goebel SJ, Dean AB, Parker MM, Masters PS (2010). Accessory protein 5a is a major antagonist of the antiviral action of interferon against murine coronavirus. J Virol 84: 8262-8274.
26. Krueger DK, Kelly SM, Lewicki DN, Ruffolo R, Gallagher TM (2001). Variations in disparate regions of the murine coronavirus spike protein impact the initiation of membrane fusion. J Virol 75: 2792-2802.
27. LaMonica N, Banner LR, Morris VL, Lai MMC (1991). Localization of extensive deletions in the structural genes of two neurotropic variants of murine coronavirus JHM. Virology 182: 883-888.
28. Lampert PW, Sims JK, Kniazeff AJ (1973). Mechanism of demyelination in JHM virus encephalomyelitis. Acta Neurophathol (Berl) 24: 76-85.
29. Lavi E, Fishman PS, Highkin MK, Weiss SR (1988). Limbic encephalitis after inhalation of a murine coronavirus. Lab Invest 58: 31-36.
30. Lavi E, Gilden DH, Highkin MK, Weiss SR (1986). The organ tropism of mouse hepatitis virus A59 in mice is dependent on dose and route of inoculation. Lab Anim Sci 36: 130-135.
31. Lavi E, Gilden DH, Wroblewska Z, Rorke LB, Weiss SR (1984). Experimental demyelination produced by the A59 strain of mouse hepatitis virus. Neurology 34: 597-603.
32. Lin MT, Hinton DR, Marten NW, Bergmann CC, Stohlman SA (1999). Antibody prevents virus reactivation within the central nervous system. J Immunol 162: 7358-7368.
33. Lin MT, Stohlman SA, Hinton DR (1997). Mouse hepatitis virus is cleared from the central nervous systems of mice lacking perforin-mediated cytolysis. J Virol 71: 383-391.
34. Macnamara KC, Bender SJ, Chua MM, Watson R, Weiss SR (2008). Priming of CD8+ T cells during central nervous system infection with a murine coronavirus is strain-dependent. J Virol 82: 6150-6160.
35. MacNamara KC, Chua MM, Phillips JJ, Weiss SR (2005). Contributions of the viral genetic background and a single amino acid substitution in an immunodominant CD8+ T-cell epitope to murine coronavirus neuroviru-lence. J Virol 79: 9108-9118.
36. Marten NW, Stohlman SA, Bergmann CC (2001). MHV infection of the CNS: mechanisms of immune-mediated control. Viral Immunol 14: 1-18.
37. Marten NW, Stohlman SA, Zhou J, Bergmann CC (2003). Kinetics of virus-specific CD8+-T-cell expansion and trafficking following central nervous system infection. J Virol 77: 2775-2778.
38. Matsubara Y, Watanabe R, Taguchi F (1991). Neuroviru-lence of six different murine coronavirus JHMV variants for rats. Virus Res 20: 45-58.
39. Matthews AE, Weiss SR, Shlomchik MJ, Hannum LG, Gombold JL, Paterson Y (2001). Antibody is required for clearance of infectious murine hepatitis virus A59 from the central nervous system, but not the liver. J Immunol 167: 5254-5263.
40. Miura TA, Travanty EA, Oko L, Bielefeldt-Ohmann H, Weiss SR, Beauchemin N, Holmes KV (2008). The spike glycoprotein of murine coronavirus MHV-JHM mediates receptor-independent infection and spread in the central nervous system of Ceacam1a-/- mice. J Virol 82: 755-763.
41. Nakagaki K, Taguchi F (2005). Receptor-independent spread of a highly neurotropic murine coronavirus JHMV strain from initially infected microglial cells in mixed neural cultures. J Virol 79: 6102-6110.
42. Navas S, Weiss SR (2003). Murine coronavirus-induced hepatitis: JHM genetic background eliminates A59 spike-determined hepatotropism. J Virol 77: 4972-4978.
43. Ontiveros E, Kim TS, Gallagher TM, Perlman S (2003). Enhanced virulence mediated by the murine coronavirus, mouse hepatitis virus strain JHM, is associated with a glycine at residue 310 of the spike glycoprotein. J Virol 77: 10260-10269.
44. Ontiveros E, Kuo L, Masters PS, Perlman S (2001). Inacti-vation of expression of gene 4 of mouse hepatitis virus strain JHM does not affect virulence in the murine CNS. Virology 289: 230-238.
45. Parham D, Tereba A, Talbot PJ, Jackson DP, Morris VL (1986). Analysis of JHM central nervous system infections in rats. Arch Neurol 43: 702-708.
46. Parra B, Hinton DR, Marten NW, Bergmann CC, Lin MT, Yang CS, Stohlman SA (1999). IFN-gamma is required for viral clearance from central nervous system oligo-dendroglia. J Immunol 162: 1641-1647.
47. Parra B, Lin MT, Stohlman SA, Bergmann CC, Atkinson R, Hinton DR (2001). Contributions of Fas-Fas ligand interactions to the pathogenesis of mouse hepatitis virus in the central nervous system. J Virol 74: 2447-2450.
48. Pasick JM, Kalicharran K, Dales S (1994). Distribution and trafficking of JHM coronavirus structural proteins and virions in primary neurons and the OBL-21 neuronal cell line. J Virol 68: 2915-2928.
49. Perlman S, Jacobsen G, Afifi A (1989). Spread of a neurotropic murine coronavirus into the CNS via the trigeminal and olfactory nerves. Virology 170: 556-560.
50. Perlman S, Schelper R, Bolger E, Ries D (1987). Late onset, symptomatic, demyelinating encephalomyelitis in mice infected with MHV-JHM in the presence of maternal antibody. Microb Pathog 2: 185-194.
51. Perlman S, Sun N, Barnett EM (1995). Spread of MHV-JHM from nasal cavity to white matter of spinal cord. Trans-neuronal movement and involvement of astrocytes. Adv Exp Med Biol 380: 73-78.
52. Phillips JJ, Chua MM, Lavi E, Weiss SR (1999). Pathogenesis of chimeric MHV4/MHV-A59 recombinant viruses: the murine coronavirus spike protein is a major determinant of neurovirulence. J Virol 73: 7752-7760.
53. Phillips JJ, Chua MM, Rall GF, Weiss SR (2002). Murine coronavirus spike glycoprotein mediates degree of viral spread, inflammation, and virus-induced immunopa-thology in the central nervous system. Virology 301: 109-120.
54. Putics A, Filipowicz W, Hall J, Gorbalenya AE, Ziebuhr J (2005). ADP-ribose-1¢¢ -monophosphatase: a conserved coronavirus enzyme that is dispensable for viral replication in tissue culture. J Virol 79: 12721-12731.
55. Putics A, Gorbalenya AE, Ziebuhr J (2006). Identification of protease and ADP-ribose 1¢¢ -monophosphatase activities associated with transmissible gastroenteritis virus non-structural protein 3. J Gen Virol 87: 651-656.
56. Ramakrishna C, Bergmann CC, Holmes KV, Stohlman SA (2004). Expression of the mouse hepatitis virus receptor by central nervous system microglia. J Virol 78: 7828-7832.
57. Rempel JD, Murray SJ, Meisner J, Buchmeier MJ (2004a). Differential regulation of innate and adaptive immune responses in viral encephalitis. Virology 318: 381-392.
58. Rempel JD, Murray SJ, Meisner J, Buchmeier MJ (2004b). Mouse hepatitis virus neurovirulence: evidence of a linkage between S glycoprotein expression and immu-nopathology. Virology 318: 45-54.
59. Roth-Cross JK, Stokes H, Chang G, Chua MM, Thiel V, Weiss SR, Gorbalenya AE, Siddell SG (2009). Organ-specific attenuation of murine hepatitis virus strain A59 by replacement of catalytic residues in the putative viral cyclic phosphodiesterase ns2. J Virol 83: 3743-3753.
60. Schwarz B, Routledge E, Siddell SG (1990). Murine coro-navirus nonstructural protein ns2 is not essential for virus replication in transformed cells. J Virol 64: 4784-4791.
61. Scott EP, Branigan PJ, Del Vecchio AM, Weiss SR (2008). Chemokine expression during mouse hepatitis virus-induced encephalitis: contributions of the spike and background genes. J NeuroVirol 14: 5-16.
62. Stevenson PG, Hawke S, Sloan DJ, Bangham CR (1997). The immunogenicity of intracerebral virus infection depends on anatomical site. J Virol 71: 145-151.
63. Stohlman SA, Bergmann CC, Lin MT, Cua DJ, Hinton DR (1998). CTL effector function within the central nervous system requires CD4+ T cells. J Immunol 160: 2896-2904.
64. Sun N, Perlman S (1995). Spread of a neurotropic corona-virus to spinal cord white matter via neurons and astrocytes. J Virol 69: 633-641.
65. Sussman MA, Shubin RA, Kyuwa S, Stohlman SA (1989). T-cell-mediated clearance of mouse hepatitis virus strain JHM from the central nervous system. J Virol 63: 3051-3061.
66. Sutherland RM, Chua MM, Lavi E, Weiss SR, Paterson Y (1997). CD4+ and CD8+ T cells are not major effectors of mouse hepatitis virus A59-induced demyelinating disease. J NeuroVirol 3: 225-228.
67. Taguchi F, Matsuyama S, Saeki K (1999). Difference in Bgp-independent fusion activity among mouse hepatitis viruses. Arch Virol 144: 2041-2049.
68. Taguchi F, Siddell SG, Wege H, ter Meulen V (1985). Characterization of a variant virus selected in rat brains after infection by a coronavirus mouse hepatitis virus JHM. J Virol 54: 429-435.
69. Tsai JC, Zelus BD, Holmes KV, Weiss SR (2003). The N-terminal domain of the murine coronavirus spike glycoprotein determines the CEACAM1 receptor specificity of the virus strain. J Virol 77: 841-850.
70. Wang FI, Hinton DR, Gilmore W, Trousdale MD, Fleming JO (1992). Sequential infection of glial cells by the murine hepatitis virus JHM strain (MHV-4) leads to a characteristic distribution of demyelination. Lab Invest 66: 744-754.
71. Weiner LP (1973). Pathogenesis of demyelination induced by a mouse hepatitis. Arch Neurol 28: 298-303.
72. Weiss SR, Navas-Martin S (2005). Coronavirus pathogen-esis and the emerging pathogen severe acute respiratory syndrome coronavirus. Microbiol Mol Biol Rev 69: 635-664.
73. Yokomori K, Asanaka M, Stohlman SA, Makino S, Shubin RA, Gilmore W, Weiner LP, Wang FI, Lai MM (1995). Neuropathogenicity of mouse hepatitis virus JHM isolates differing in hemagglutinin-esterase protein expression. J NeuroVirol 1: 330-339.
74. Yokomori K, Baker SC, Stohlman SA, Lai MM (1992). Hemagglutinin-esterase- specific monoclonal antibodies alter the neuropathogenicity of mouse hepatitis virus. J Virol 66: 2865-2874.
75. Yokomori K, Lai MM (1991). Mouse hepatitis virus S RNA sequence reveals that nonstructural proteins ns4 and ns5a are not essential for murine coronavirus replication. J Virol 65: 5605-5608.
76. Yokomori K, Stohlman SA, Lai MM (1993). The detection and characterization of multiple hemagglutinin-esterase (HE)-defective viruses in the mouse brain during sub-acute demyelination induced by mouse hepatitis virus. Virology 192: 170-178.
77. Zhou J, Stohlman SA, Atkinson R, Hinton DR, Marten NW (2002). Matrix metalloproteinase expression correlates with virulence following neurotropic mouse hepatitis virus infection. J Virol 76: 7374-7384.
78. Zhou J, Stohlman SA, Hinton DR, Marten NW (2003). Neutrophils promote mononuclear cell infiltration during viral-induced encephalitis. J Immunol 170: 3331-3336.