Enhanced virulence mediated by the murine coronavirus, mouse hepatitis virus strain JHM, is associated with a glycine at residue 310 of the spike glycoprotein

Journal of Virology

Volumn 77, Issue 19, 2003, Pages 10260-10269

  Ontiveros, Evelena ^a   Kim, Taeg S ^a   Gallagher, Thomas M ^c   Perlman, Stanley ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; NEUTRALIZING ANTIBODY;

AMINO ACID ANALYSIS; AMINO ACID SUBSTITUTION; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORONAVIRUS; ENCEPHALITIS; HEPATITIS VIRUS; IN VITRO STUDY; MOUSE; MURINE HEPATITIS CORONAVIRUS; NEUROLOGIC DISEASE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN STABILITY; TECHNOLOGY; VIROGENESIS; VIRUS EXPRESSION; VIRUS RECOMBINANT; VIRUS STRAIN; VIRUS VIRULENCE;

ANIMALS; CRICETINAE; GLYCINE; MEMBRANE FUSION; MEMBRANE GLYCOPROTEINS; MICE; MURINE HEPATITIS VIRUS; STRUCTURE-ACTIVITY RELATIONSHIP; VIRAL ENVELOPE PROTEINS; VIRULENCE;

EID: 0141856400     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.19.10260-10269.2003     Document Type: Article

References (74)

1. Almazan, F., J. M. Gonzalez, Z. Penzes, A. Izeta, E. Calvo, J. Plana-Duran, and L. Enjuanes. 2000. Engineering the largest RNA virus genome as an infectious bacterial artificial chromosome. Proc. Natl. Acad. Sci. USA 97:5516-5521.
2. Bang, F. B. 1978. Genetics of resistance of animals to viruses. I. Introduction and studies in mice. Adv. Virus Res. 1978:269-348.
3. Barnett, E., M. Cassell, and S. Perlman. 1993. Two neurotropic viruses, herpes simplex virus type 1 and mouse hepatitis virus, spread along different neural pathways from the main olfactory bulb. Neuroscience 57:1007-1025.
4. Boyle, J. F., 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.
5. Buchmeier, M. J., H. A. Lewicki, P. J. Talbot, and R. L. Knobler. 1984. Murine hepatitis virus-4 (strain JHM)-induced neurologic disease is modulated in vivo by monoclonal antibody. Virology 132:261-270.
6. Casais, R., V. Thiel, S. G. Siddell, D. Cavanagh, and P. Britton. 2001. Reverse genetics system for the avian coronavirus infectious bronchitis virus. J. Virol. 75:12359-12369.
7. Cavanagh, D. 1997. Nidovirales: a new order comprising Coronaviridae and Arteriviridae. Arch. Virol. 142:629-633.
8. Cheever, F. S., J. B. Daniels, A. M. Pappenheimer, and O. T. Bailey. 1949. A murine virus (JHM) causing disseminated encephalomyelitis with extensive destruction of myelin. J. Exp. Med. 90:181-194.
9. Chen, D., M. Asanaka, K. Yokomori, F. Wang, S. Hwang, H. Li, and M. M. C. Lai. 1995. A pregnancy-specific glycoprotein is expressed in the brain and serves as a receptor for mouse hepatitis virus. Proc. Natl. Acad. Sci. USA 92:12095-12099.
10. Collins, A. R., R. L. Knobler, H. Powell, and M. J. Buchmeier. 1982. Monoclonal antibodies to murine hepatitis virus-4 (strain JHM) define the viral glycoprotein responsible for attachment and cell-cell fusion. Virology 119:358-371.
11. de Groot, R. J., J. A. Lenstra, W. Luytjes, H. G. Niesters, M. C. Horzinek, B. A. van der Zeijst, and W. J. Spaan. 1987. Sequence and structure of the coronavirus peplomer protein. Adv. Exp. Med. Biol. 218:31-38.
12. Fingerote, R. J., M. Abecassis, M. J. Phillips, Y. S. Rao, E. H. Cole, J. Leibowitz, and G. A. Levy. 1996. Loss of resistance to murine hepatitis virus strain 3 infection after treatment with corticosteroids is associated with induction of macrophage procoagulant activity. J. Virol. 70:4275-4282.
13. Fleming, J. O., M. D. Trousdale, F. 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.
14. Gallagher, T., M. Buchmeier, and S. Perlman. 1992. Cell receptor-independent infection by a neurotropic murine coronavirus. Virology 191:517-522.
15. Gallagher, T. M. 1996. Murine coronavirus membrane fusion is blocked by modification of thiols buried within the spike protein. J. Virol. 70:4683-4690.
16. Gallagher, T. M. 1997. A role for naturally occurring variation of the murine coronavirus spike protein in stabilizing association with the cellular receptor. J. Virol. 71:3129-3137.
17. Gallagher, T. M., and M. J. Buchmeier. 2001. Coronavirus spike proteins in viral entry and pathogenesis. Virology 279:371-374.
18. Gallagher, T. M., C. Escarmis, and M. J. Buchmeier. 1991. Alteration of the pH dependence of coronavirus-induced cell fusion: effect of mutations in the spike glycoprotein. J. Virol. 65:1916-1928.
19. Godfraind, C., N. Havaux, K. V. Holmes, and J. P. Coutelier. 1997. Role of virus receptor-bearing endothelial cells of the blood-brain barrier in preventing the spread of mouse hepatitis virus-A59 into the central nervous system. J. Neurovirol. 3:428-434.
20. Godfraind, C., S. G. Langreth, C. B. Cardellichio, R. Knobler, J. P. Coute. lier, M. Dubois-Dalcq, and K. V. Holmes. 1995. Tissue and cellular distribution of an adhesion molecule in the carcinoembryonic antigen family that serves as a receptor for mouse hepatitis virus. Lab. Investig. 73:615-627.
21. Haring, J., and S. Perlman. 2001. Mouse hepatitis virus. Curr. Opin. Microbiol. 4:462-466.
22. 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.
23. Holmes, K. V., and G. S. Dveksler. 1994. Specificity of coronavirus/receptor interactions, p. 403-443. In E. Wimmer (ed.), Cell receptors for animal viruses, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
24. Karp, C. L., M. Wysocka, L. M. Wahl, J. M. Ahearn, P. J. Cuomo, B. Sherry, G. Trinchieri, and D. E. Griffin. 1996. Mechanism of suppression of cell-mediated immunity by measles virus. Science 273:228-231.
25. Knobler, R., M. Haspel, and M. B. A. Oldstone. 1981. Mouse hepatitis virus type-4 (JHM strain) induced fatal nervous system disease. Part I. Genetic control and the murine neuron as the susceptible site of disease. J. Exp. Med. 153:832-843.
26. + T cells. J. Immunol. 147:2317-2323.
27. Krueger, D. K., S. M. Kelly, D. N. Lewicki, R. Ruffolo, and T. M. Gallagher. 2001. Variations in disparate regions of the murine coronavirus spike protein impact the initiation of membrane fusion. J. Virol. 75:2792-2802.
28. Kubo, H., Y. K. Yamada, and F. Taguchi. 1994. Localization of neutralizing epitopes and the receptor-binding site within the amino-terminal 330 amino acids of the murine coronavirus spike protein. J. Virol. 68:5403-5410.
29. Kuo, L., G. J. Godeke, M. J. Raamsman, P. S. Masters, and P. J. Rottier. 2000. Retargeting of coronavirus by substitution of the spike glycoprotein ectodomain: crossing the host cell species barrier. J. Virol. 74:1393-1406.
30. Lai, M. M. C., and D. Cavanagh. 1997. The molecular biology of coronaviruses. Adv. Virus Res. 48:1-100.
31. 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.
32. Leparc-Goffart, I., S. T. Hingley, M. M. Chua, X. Jiang, E. Lavi, and S. R. Weiss. 1997. Altered pathogenesis of a mutant of the murine coronavirus MHV-A59 is associated with a Q159L amino acid substitution in the spike protein. Virology 239:1-10.
33. Luo, Z., and S. R. Weiss. 1998. Roles in cell-to-cell fusion of two conserved hydrophobic regions in the murine coronavirus spike protein. Virology 244:483-494.
34. Luytjes, W., L. S. Sturman, P. J. Bredenbeek, J. Charite, B. A. M. van der Zeijst, M. C. Horzinek, and W. J. M. Spaan. 1987. Primary structure of the glycoprotein E2 of coronavirus MHV-A59 and identification of the trypsin cleavage site. Virology 161:479-487.
35. Masters, P. S. 1999. Reverse genetics of the largest RNA viruses. Adv. Virus Res. 53:245-264.
36. Matsuyama, S., and F. Taguchi. 2002. Communication between S1N330 and a region in S2 of murine coronavirus spike protein is important for virus entry into cells expressing CEACAM1b receptor. Virology 295:160-171.
37. Moore, J. P., J. A. McKeating, R. A. Weiss, and Q. J. Sattentau. 1990. Dissociation of gp120 from HIV-1 virions induced by soluble CD4. Science 250:1139-1142.
38. Moskophidis, D., F. Lechner, H. Pircher, and R. M. Zinkernagel. 1993. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature 362:758-761.
39. 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.
40. Nash, T., and M. J. Buchmeier. 1997. Entry of mouse hepatitis virus into cells by endosomal and nonendosomal pathways. Virology 233:1-8.
41. Nash, T., and M. J. Buchmeier. 1996. Spike glycoprotein-mediated fusion in biliary glycoprotein-independent cell-associated spread of mouse hepatitis virus infection. Virology 223:68-78.
42. Navas, S., S. H. Seo, M. M. Chua, J. D. Sarma, E. Lavi, S. T. Hingley, and S. R. Weiss. 2001. Murine coronavirus spike protein determines the ability of the virus to replicate in the liver and cause hepatitis. J. Virol. 75:2452-2457.
43. Nedellec, P., G. S. Dveksler, E. Daniels, C. Turbide, B. Chow, A. A. Basile, K. V. Holmes, and N. Beauchemin. 1994. Bgp2, a new member of the carcinoembryonic antigen-related gene family, encodes an alternative receptor for mouse hepatitis viruses. J. Virol. 68:4525-4537.
44. Ohtsuka, N., Y. K. Yamada, and F. Taguchi. 1996. Difference in virus-binding activity of two distinct receptor proteins for mouse hepatitis virus. J. Gen. Virol. 77:1683-1692.
45. Ontiveros, E., L. Kuo, P. S. Masters, and S. Perlman. 2001. Inactivation of expression of gene 4 of mouse hepatitis virus strain JHM does not affect virulence in the murine CNS. Virology 290:230-238.
46. Parker, S. E., T. M. Gallagher, and M. J. Buchmeier. 1989. 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.
47. Perlman, S., G. Jacobsen, A. L. Olson, and A. Afifi. 1990. Identification of the spinal cord as a major site of persistence during chronic infection with a murine coronavirus. Virology 175:418-426.
48. Perlman, S., R. Schelper, E. Bolger, and D. Ries. 1987. Late onset, symptomatic, demyelinating encephalomyelitis in mice infected with MHV-JHM in the presence of maternal antibody. Microb. Pathog. 2:185-194.
49. Pewe, L., G. Wu, E. M. Barnett, R. Castro, and S. Perlman. 1996. Cytotoxic T cell-resistant variants are selected in a virus-induced demyelinating disease. Immunity 5:253-262.
50. Pewe, L., S. Xue, and S. Perlman. 1997. Cytotoxic T cell-resistant variants arise at early times after infection in C57BL/6 but not in SCID mice infected with a neurotropic coronavirus. J. Virol. 71:7640-7647.
51. Phillips, J. J., M. M. Chua, E. Lavi, and S. R. Weiss. 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.
52. Sanchez, C. M., A. Izeta, J. M. Sanchez-Morgado, S. Alonso, I. Sola, M. Balasch, J. Plana-Duran, and L. Enjuanes. 1999. Targeted recombination demonstrates that the spike gene of transmissible gastroenteritis coronavirus is a determinant of its enteric tropism and virulence. J. Virol. 73:7607-7618.
53. Sevilla, N., S. Kunz, A. Holz, H. Lewicki, D. Homann, H. Yamada, K. P. Campbell, J. C. de La Torre, and M. B. Oldstone. 2000. Immunosuppression and resultant viral persistence by specific viral targeting of dendritic cells. J. Exp. Med. 192:1249-1260.
54. Spaan, W., D. Cavanagh, and M. C. Horzinek. 1988. Coronaviruses: structure and genome expression. J. Gen. Virol. 69:2939-2952.
55. Stohlman, S. A., C. C. Bergmann, and S. Perlman. 1998. Mouse hepatitis virus, p. 537-557. In R. Ahmed and I. Chen (ed.), Persistent viral infections. John Wiley & Sons, Ltd., New York, N.Y.
56. Stohlman, S. A., and D. R. Hinton. 2001. Viral induced demyelination. Brain Pathol. 11:92-106.
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.
58. Sturman, L., and K. Holmes. 1985. The novel glycoproteins of coronaviruses. Trends Biochem. Res. 10:17-20.
59. Sturman, L. S., C. S. Ricard, and K. V. Holmes. 1990. Conformational change of the coronavirus peplomer glycoprotein at pH 8.0 and 37 degrees C correlates with virus aggregation and virus-induced cell fusion. J. Virol. 64:3042-3050.
60. Sun, N., D. Grzybicki, R. Castro, S. Murphy, and S. Perlman. 1995. Activation of astrocytes in the spinal cord of mice chronically infected with a neurotropic coronavirus. Virology 213:482-493.
61. Suzuki, H., and F. Taguchi. 1996. Analysis of the receptor-binding site of murine coronavirus spike protein. J. Virol. 70:2632-2636.
62. Taguchi, F., T. Ikeda, and H. Shida. 1992. Molecular cloning and expression of a spike protein of neurovirulent murine coronavirus JHMV variant cl-2. J. Gen. Virol. 73:1065-1072.
63. Taguchi, F., and Y. K. Shimazaki. 2000. Functional analysis of an epitope in the S2 subunit of the murine coronavirus spike protein: involvement in fusion activity. J. Gen. Virol. 81:2867-2871.
64. Tan, K., B. D. Zelus, R. Meijers, J. H. Liu, J. M. Bergelson, N. Duke, R. Zhang, A. Joachimiak, K. V. Holmes, and J. H. Wang. 2002. Crystal structure of murine sCEACAM1a[1,4]: a coronavirus receptor in the CEA family. EMBO J. 21:2076-2086.
65. Thiel, V., J. Herold, B. Schelle, and S. G. Siddell. 2001. Infectious RNA transcribed in vitro from a cDNA copy of the human coronavirus genome cloned in vaccinia virus. J. Gen. Virol. 82:1273-1281.
66. Tsai, J. C., B. D. Zelus, K. V. Holmes, and S. R. Weiss. 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.
67. Weismiller, D. G., L. S. Sturman, M. J. Buchmeier, J. O. Fleming, and K. V. Holmes. 1990. Monoclonal antibodies to the peplomer glycoprotein of coronavirus mouse hepatitis virus identify two subunits and detect a conformational change in the subunit released under mild alkaline conditions. J. Virol. 64:3051-3055.
68. Wu, S. J., G. Grouard-Vogel, W. Sun, J. R. Mascola, E. Brachtel, R. Putvatana, M. K. Louder, L. Filgueira, M. A. Marovich, H. K. Wong, A. Blauvelt, G. S. Murphy, M. L. Robb, B. L. Innes, D. L. Birx, C. G. Hayes, and S. S. Frankel. 2000. Human skin Langerhans cells are targets of dengue virus infection. Nat. Med. 6:816-820.
69. Yamaguchi, K., N. Goto, S. Kyuwa, M. Hayami, and Y. Toyoda. 1991. Protection of mice from a lethal coronavirus infection in the central nervous system by adoptive transfer of virus-specific T cell clones. J. Neuroimmunol. 32:1-9.
70. Yount, B., K. M. Curtis, and R. S. Baric. 2000. Strategy for systematic assembly of large RNA and DNA genomes: transmissible gastroenteritis virus model. J. Virol. 74:10600-10611.
71. Yount, B., M. R. Denison, S. R. Weiss, and R. S. Baric. 2002. Systematic assembly of a full-length infectious cDNA of mouse hepatitis virus strain A59. J. Virol. 76:11065-11078.
72. Zajac, A. J., J. N. Blattman, K. Murali-Krishna, D. Sourdive, M. Suresh, J. D. Altman, and R. Ahmed. 1998. Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 188:2205-2213.
73. Zelus, B. D., J. H. Schickli, D. M. Blau, S. R. Weiss, and K. V. Holmes. 2003. Conformational changes in the spike glycoprotein of murine coronavirus are induced at 37 degrees C either by soluble murine CEACAM1 receptors or by pH 8. J. Virol. 77:830-840.
74. Zelus, B. D., D. R. Wessner, R. K. Williams, M. N. Pensiero, F. T. Phibbs, M. de Souza, G. S. Dveksler, and K. V. Holmes. 1998. Purified, soluble recombinant mouse hepatitis virus receptor, Bgp1(b), and Bgp2 murine coronavirus receptors differ in mouse hepatitis virus binding and neutralizing activities. J. Virol. 72:7237-7244.