The Coronavirus Membrane Glycoprotein

  • Peter J. M. Rottier
Part of the The Viruses book series (VIRS)

Abstract

Coronaviruses have a simple protein composition. While there is some variation among different members, a basic set of four protein species universally occurs: the nucleocapsid protein (N), the spike protein (S), a small membrane protein (SM), and the membrane glycoprotein (M). Some coronaviruses have an additional membrane glycoprotein (HE). The M protein, previously also called El, is the subject of this chapter. As will become clear, M is a peculiar glycoprotein, different from all other viral glycoproteins in its structural and biochemical features. These unique features may be responsible for important biological properties of coronaviruses, in particular for their intracellular budding.

Keywords

Carbohydrate Serine Lysine Oligomerization Diarrhea 

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References

  1. Armstrong, J., and Patel, S., 1991, The Golgi sorting domain of Coronavirus El protein, J. Cell Sci. 98:567.PubMedGoogle Scholar
  2. Armstrong, J., Niemann, H., Smeekens, S., Rottier, P., and Warren, G., 1984, Sequence and topology of a model intracellular membrane protein, El glycoprotein, from a Coronavirus, Nature 308:751.PubMedCrossRefGoogle Scholar
  3. Armstrong, J., McCrae, M., and Colman, A., 1987, Expression of Coronavirus El and rotavirus VP10 membrane proteins from synthetic RNA, J. Cell. Biochem. 35:129.PubMedCrossRefGoogle Scholar
  4. Armstrong, J., Patel, S., and Riddle, P., 1990, Lysosomal sorting mutants of Coronavirus El protein, a Golgi membrane protein, J. Cell Sci. 95:191.PubMedGoogle Scholar
  5. Becker, W. B., McIntosh, K., Dees, J. H., and Chanock, R. M., 1967, Morphogenesis of avian infectious bronchitis virus and a related human virus (strain 229E), J. Virol. 1:1019.PubMedGoogle Scholar
  6. Binns, M. M., Boursnell, M. E. G., Tomley, F. M., and Brown, T. D. K., 1986, Nucleotide sequence encoding the membrane protein of the IBV strain 6/82, Nucleic Acids Res. 14:5558.PubMedGoogle Scholar
  7. Boursnell, M. E. G., Brown, T. D. K., and Binns, M. M., 1984, Sequence of the membrane protein gene from avian Coronavirus IBV, Virus Res. 1:303.PubMedCrossRefGoogle Scholar
  8. Bradburne, A. F., 1970, Antigenic relationships amongst coronaviruses, Arch. Gesamte Virusforsch. 31:352.PubMedCrossRefGoogle Scholar
  9. Buchmeier, M. J., Lewicki, H. A., Talbot, P. J., and Knobler, R. L., 1984, Murine hepatitis virus-4 (strain JHM)-induced neurologic disease is modulated in vivo by monoclonal antibody, Virology 132:261.PubMedCrossRefGoogle Scholar
  10. Callebaut, P. E., and Pensaert, M. B., 1980, Characterization and isolation of structural polypeptides in haemagglutinating encephalomyelitis virus, J. Gen. Virol. 48:193.PubMedCrossRefGoogle Scholar
  11. Cavanagh, D., 1981, Structural polypeptides of Coronavirus IBV, J. Gen. Virol. 53:93.PubMedCrossRefGoogle Scholar
  12. Cavanagh, D., 1983, Coronavirus IBV glycopolypeptides: Size of their polypeptide moieties and nature of their oligosaccharides, J. Gen. Virol. 64:1187.PubMedCrossRefGoogle Scholar
  13. Cavanagh, D., and Davis, P. J., 1988. Evolution of avian Coronavirus IBV: Sequence of the matrix glycoprotein gene and intergenic region of several serotypes, J. Gen. Virol. 69:621.PubMedCrossRefGoogle Scholar
  14. Cavanagh, D., Davis, P. J., and Pappin, D. J. C., 1986a, Coronavirus IBV glycopolypeptides: Ideational studies using proteases and saponin, a membrane permeabilizer, Virus Res. 4:145.PubMedCrossRefGoogle Scholar
  15. Cavanagh, D., Davis, P. J., Pappin, D. J. C., Binns, M. M., Boursnell, M. E. G., and Brown, T. D. K., 1986b, Coronavirus IBV: Partial amino terminal sequencing of spike polypeptide S2 identifies the sequence Arg-Arg-Phe-Arg-Arg at the cleavage site of the spike precursor propolypeptide of IBV strains Beaudette and M41, Virus Res. 4:133.PubMedCrossRefGoogle Scholar
  16. Charley, B., and Laude, H., 1988, Induction of alpha interferon by transmissible gastroenteritis Coronavirus: Role of transmembrane glycoprotein El, J. Virol. 62:8.PubMedGoogle Scholar
  17. Chasey, D., and Alexander, D. J., 1976. Morphogenesis of avian infectious bronchitis virus in primary chick kidney cells, Arch. Virol. 52:101.PubMedCrossRefGoogle Scholar
  18. Collins, A. R., Knobler, R. L., Powell, H., and Buchmeier, M. J., 1982, Monoclonal antibodies to murine hepatitis virus 4 (strain JHM) define the viral glycoprotein responsible for attachment and cell-cell fusion, Virology 119:358.PubMedCrossRefGoogle Scholar
  19. David-Ferreira, J. F., and Manaker, R. A., 1965, An electron microscope study of the development of a mouse hepatitis virus in tissue culture cells, J. Cell Biol. 24:57.PubMedCrossRefGoogle Scholar
  20. Deregt, D., and Babiuk, L. A., 1987, Monoclonal antibodies to bovine Coronavirus: Characteristics and topographical mapping of neutralizing epitopes on the E2 and E3 glycoproteins, Virology 161:410.PubMedCrossRefGoogle Scholar
  21. Deregt, D., Sahara, M., and Babiuk, L. A., 1987, Structural proteins of bovine Coronavirus and their intracellular processing, J. Gen. Virol. 68:2863.PubMedCrossRefGoogle Scholar
  22. Doyle, C., Sambrook, J., and Gething, M.-J., 1986, Analysis of progressive deletions of the transmembrane and cytoplasmic domains of influenza hemagglutinin, J. Cell Biol. 103:1193.PubMedCrossRefGoogle Scholar
  23. Dubois-Dalcq, M. E., Doller, E. W., Haspel, M. V., and Holmes, K. V., 1982, Cell tropism and expression of mouse hepatitis viruses (MHV) in mouse spinal cord cultures, Virology 119:317.PubMedCrossRefGoogle Scholar
  24. Dubois-Dalcq, M. E., Holmes, K. V., and Rentier, B., 1984, Assembly of RNA Viruses, Springer Verlag, New York.CrossRefGoogle Scholar
  25. Earl, P. L., Moss, B., and Doms, R. W., 1991, Folding, interaction with GRP78-BiP, assembly, and transport of the human immunodeficiency virus type 1 envelope protein, J. Virol. 65:2047.PubMedGoogle Scholar
  26. Fiscus, S. A., and Teramoto, Y. A., 1987, Antigenic comparison of feline Coronavirus isolates: Evidence for markedly different peplomer glycoproteins, J. Virol. 61:2607.PubMedGoogle Scholar
  27. Fleming, J. O., Shubin, R. A., Sussman, M. A., Casteel, N., and Stohlman, S. A., 1989, Monoclonal antibodies to the matrix (El) glycoprotein of mouse hepatitis virus protect mice from encephalitis, Virology 168:162.PubMedCrossRefGoogle Scholar
  28. Gallagher, T. M., Parker, S. E., and Buchmeier, M. J., 1990, Neutralization-resistant variants of the neurotropic Coronavirus are generated by deletions within the amino-terminal half of the spike glycoprotein, J. Virol. 64:731.PubMedGoogle Scholar
  29. Garwes, D. J., Pocock, D. H., and Pike, B. V., 1976, Isolation of subviral components from transmissible gastroenteritis virus, J. Gen. Virol. 32:283.PubMedCrossRefGoogle Scholar
  30. Geyer, H., Holschbach, C., Hunsmann, G., and Schneider, J., 1988, Carbohydrates of human immunodeficiency virus. Structures of olisosaccharides linked to the envelope glycoprotein 120, J. Biol. Chem. 263:1 1760.Google Scholar
  31. Hasony, H. J., and Macnaughton, M. R., 1981, Antigenicity of mouse hepatitis virus strain 3 subcomponents in C57 strain mice, Arch. Virol. 69:33.PubMedCrossRefGoogle Scholar
  32. Hauri, H.-P., and Schweizer, A., 1992, The endoplasmic reticulum-Golgi intermediate compartment, Curr. Opin. Cell Biol. 4:600.PubMedCrossRefGoogle Scholar
  33. Hogue, B. G., and Brian, D. A., 1986, Structural proteins of human respiratory Coronavirus OC43, Virus Res. 5:131.PubMedCrossRefGoogle Scholar
  34. Holmes, K. V., and Behnke, J. N., 1981, Evolution of a Coronavirus during persistent infection in vitro, Adv. Exp. Med. Biol. 142:287.CrossRefGoogle Scholar
  35. Holmes, K. V., Doller, E. W., and Behnke, J. N., 1981a, Analysis of the functions of Coronavirus glycoproteins by differential inhibition of synthesis with tunicamycin, Adv. Exp. Med. Biol. 142:133.PubMedCrossRefGoogle Scholar
  36. Holmes, K. V., Doller, E. W., and Sturman, L. S., 1981b, Tunicamycin resistant glycosylation of a Coronavirus glycoprotein: Demonstration of a novel type of viral glycoprotein, Virology 115:334.PubMedCrossRefGoogle Scholar
  37. Horsburgh, B. C., Brierley, I., and Brown, T. D. K., 1992, Analysis of a 9.6 kb sequence from the 3′ end of canine Coronavirus genomic RNA, J. Gen. Virol. 73:2849.PubMedCrossRefGoogle Scholar
  38. Horzinek, M. C., Lutz, H., and Pedersen, N. C., 1982, Antigenic relationships among homologous structural polypeptides of porcine, feline, and canine coronaviruses. Infect, Immunology 37:1148.Google Scholar
  39. Jacobs, L., Van der Zeijst, B. A. M., and Horzinek, M. C., 1986, Characterization and translation of transmissible gastroenteritis virus mRNAs, J. Virol. 57:1010.PubMedGoogle Scholar
  40. Kapke, P. A., Tung, F. Y. T., Hogue, B. G., Brian, D. A., Woods, R. D., and Wesley, R., 1988, The amino-terminal signal peptide on the porcine transmissible gastroenteritis Coronavirus matrix protein is not an absolute requirement for membrane translocation and glycosylation, Virology 165:367.PubMedCrossRefGoogle Scholar
  41. King, B., and Brian, D. A., 1982, Bovine Coronavirus structural proteins, J. Virol. 42:700.PubMedGoogle Scholar
  42. Klumperman, J., Krijnse Locker, J., Meijer, A., Horzinek, M. C., Geuze, H. J., and Rottier, P. J. M., 1994, Coronavirus M proteins accumulate in the Golgi complex beyond the site of virion budding, J. Virol. 68:6523.PubMedGoogle Scholar
  43. Krijnse Locker, J., Griffiths, G., Horzinek, M. C., and Rottier, P. J. M., 1992a, O-glycosylation of the Coronavirus M protein, J. Biol. Chem. 267:14094.Google Scholar
  44. Krijnse Locker, J., Rose, J. K., Horzinek, M. C., and Rottier, P. J. M., 1992b, Membrane assembly of the triple-spanning Coronavirus M protein, J. Biol. Chem. 267:2 1911.Google Scholar
  45. Krijnse Locker, J., Ericsson, M., Rottier, P. J. M., and Griffiths, G., 1994, Characterization of the budding compartment of mouse hepatitis virus, J. Cell Biol. 124:55.PubMedCrossRefGoogle Scholar
  46. Krijnse Locker, J., Klumperman, J., Oorschot, V., Geuze, H. J., Horzinek, M. C., and Rottier, P. J. M., 1995, The cytoplasmic tail of mouse hepatitis virus M protein is essential but not sufficient for its retention in the Golgi complex, J. Biol. Chem. 269:28263.Google Scholar
  47. Kyte, J., and Doolittle, R. F., 1982, A simple method for displaying the hydropathic character of a protein, J. Mol. Biol. 157:105.PubMedCrossRefGoogle Scholar
  48. Lanser, J. A., and Howard, C. R., 1980, The polypeptides of infectious bronchitis virus (IBV-41 strain). J. Gen. Virol. 46:349.PubMedCrossRefGoogle Scholar
  49. Lapps, W., Hogue, B. G., and Brian, D. A., 1987, Sequence analysis of the bovine Coronavirus nucleocapsid and matrix protein genes, Virology 157:47.PubMedCrossRefGoogle Scholar
  50. Laude, H., Chapsal, J.-M., Gelfi, J., Labiau, S., and Grosclaude, J., 1986, Antigenic structure of transmissible gastroenteritis virus. I. Properties of monoclonal antibodies directed against virion proteins, J. Gen. Virol. 67:119.PubMedCrossRefGoogle Scholar
  51. Laude, H., Rasschaert, D., and Huet, J.-C., 1987, Sequence and N-terminal processing of the transmissible protein El of the Coronavirus transmissible gastroenteritis virus, J. Gen. Virol. 68:1687.PubMedCrossRefGoogle Scholar
  52. Laude, H., Gelfi, J., Lavenant, L., and Charley, B., 1992, Single amino acid changes in the viral glycoprotein M affect induction of alpha interferon by the Coronavirus transmissible gastroenteritis virus, J. Virol. 66:743.PubMedGoogle Scholar
  53. Laviada, M. D., Videgain, S. P., Moreno, L., Alonso, F., Enjuanes, L., and Escribano, J. M., 1990, Expression of swine transmissible gastroenteritis virus envelope antigens on the surface of infected cells: Epitopes externally exposed, Virus Res. 16:247.PubMedCrossRefGoogle Scholar
  54. Luytjes, W., Sturman, L. S., Bredenbeek, P. J., Charité, J., Van der Zeijst, B. A. M., Horzinek, M. C., and Spaan, W. J. M., 1987, Primary structure of the glycoprotein E2 of Coronavirus MHV-A59 and identification of the trypsin cleavage site, Virology 161:479.PubMedCrossRefGoogle Scholar
  55. Machamer, C. E., and Rose, J. K., 1987, A specific transmembrane domain of a Coronavirus El glycoprotein is required for its retention in the Golgi region, J. Cell Biol. 105:1205.PubMedCrossRefGoogle Scholar
  56. Machamer, C. E., Mentone, S. A., Rose, J. K., and Farquhar, M. G., 1990, The El glycoprotein of an avian Coronavirus is targeted to the cis Golgi complex, Proc. Natl. Acad. Sci. USA 87:6944.PubMedCrossRefGoogle Scholar
  57. Machamer, C. E., Grim, M. G., Esquela, A., Chung, S. W., Rolls, M., Ryan, K., and Swift, A. M., 1993, Retention of a cis Golgi protein requires polar residues on one face of a predicted a-helix in the transmembrane domain, Mol. Biol. Cell 4:695.PubMedGoogle Scholar
  58. Macnaughton, M. R., 1981, Structural and antigenic relationships between human, murine and avian coronaviruses, Adv. Exp. Med. Biol. 142:19.PubMedCrossRefGoogle Scholar
  59. Mayer, T., Tamura, T., Falk, M., and Niemann, H., 1988, Membrane integration and intracellular transport of the Coronavirus glycoprotein El, a class III membrane glycoprotein, J. Biol. Chem. 263:14956.PubMedGoogle Scholar
  60. Mcintosh, K., Kapikian, A. Z., Hardison, K. A., Hartley, J. W., and Chanock, R. M., 1969, Antigenic relationships among the coronaviruses of man and between human and animal coronaviruses, J. Immunol. 102:1109.PubMedGoogle Scholar
  61. Mobley, J., Evans, G., Dailey, M. O., and Perlman, S., 1992, Immune response to a murine coronavirus: Identification of a homing receptor-negative CD4+ T cell subset that responds to viral glycoproteins, Virology 187:443.PubMedCrossRefGoogle Scholar
  62. Mounir, S., and Talbot, P. J., 1992, Sequence analysis of the membrane protein gene of human Coronavirus OC43 and evidence for O-glycosylation, J. Gen. Virol. 73:2731.PubMedCrossRefGoogle Scholar
  63. Niemann, H., and Klenk, H.-D., 1981, Coronavirus glycoprotein El, a new type of viral glycoprotein, J. Mol. Biol. 153:993.PubMedCrossRefGoogle Scholar
  64. Niemann, H., Boschek, B., Evans, D., Rosing, M., Tamura, T., and Klenk, H.-D., 1982, Post-translational glycosylation of Coronavirus glycoprotein El: Inhibition by monensin, EMBO J. 1:1499.PubMedGoogle Scholar
  65. Niemann, H., Geyer, R., Klenk, H.-D., Linder, D., Stirm, S., and Wirth, M., 1984, The carbohydrates of mouse hepatitis virus (MHV) A59: Structures of the O-glycosidically linked oligosaccharides of glycoprotein El, EMBO J. 3:665.PubMedGoogle Scholar
  66. Opstelten, D.-J. E., Horzinek, M. C., and Rottier, P. J. M., 1993a, Complex formation between the spike protein and the membrane protein during mouse hepatitis virus assembly, Adv. Exp. Med. Biol. 342:189.PubMedCrossRefGoogle Scholar
  67. Opstelten, D.-J. E., De Groote, P., Horzinek, M. C., Vennema, H., and Rottier, P. J. M., 1993b, Disulfide bonds in folding and transport of mouse hepatitis Coronavirus glycoproteins, J. Virol. 67:7394.PubMedGoogle Scholar
  68. Opstelten, D.-J. E., De Groote, P., Horzinek, M. C., and Rottier, P. J. M., 1994, Folding of the mouse hepatitis virus spike protein and its association with the membrane protein, Arch. Virol. (Suppl) 9:319.Google Scholar
  69. Parker, S. E., Gallagher, T. M., and Buchmeier, M. J., 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.PubMedCrossRefGoogle Scholar
  70. Pedersen, N. C., Ward, I., and Mengeling, W. L., 1978, Antigenic relationships of the feline infectious peritonitis virus to coronaviruses of other species, Arch. Virol. 58:45.PubMedCrossRefGoogle Scholar
  71. Pfleiderer, M., Skinner, M. A., and Siddell, S. G., 1986, Coronavirus MHV-JHM: Nucleotide sequence of the mRNA that encodes the membrane protein, Nucleic Acids Res. 14:6338.PubMedCrossRefGoogle Scholar
  72. Pulford, D. J., and Britton, P., 1990, Expression and cellular localisation of porcine transmissible gastroenteritis virus N and M proteins by recombinant vaccinia viruses, Virus Res. 18:203.CrossRefGoogle Scholar
  73. Raabe, T., and Siddell, S. G., 1989, Nucleotide sequence of the gene encoding the membrane protein of human Coronavirus 229 E, Arch. Virol. 107:323.PubMedCrossRefGoogle Scholar
  74. Rasschaert, D., Duarte, M., and Laude, H., 1990, Porcine respiratory Coronavirus differs from transmissible gastroenteritis virus by a few genomic deletions, J. Gen. Virol. 71:2599.PubMedCrossRefGoogle Scholar
  75. Rottier, P. J. M., and Rose, J. K., 1987, Coronavirus El glycoprotein expressed from cloned cDNA localizes in the Golgi region, J. Virol. 61:2042.PubMedGoogle Scholar
  76. Rottier, P. J. M., Spaan, W. J. M., Horzinek, M. C., and Van der Zeijst, B. A. M., 1981a, Translation of three mouse hepatitis virus strain A59 subgenomic RNAs in Xenopus laevis oocytes, J. Virol. 38:20.PubMedGoogle Scholar
  77. Rottier, P. J. M., Horzinek, M. C., and Van der Zeijst, B. A. M., 1981b, Viral protein synthesis in mouse hepatitis virus strain A59-infected cells: Effect of tunicamycin, J. Virol. 40:350.PubMedGoogle Scholar
  78. Rottier, P., Brandenburg, D., Armstrong, J., Van der Zeijst, B., and Warren, G., 1984, Assembly in vitro of a spanning membrane protein of the endoplasmic reticulum: The El glycoprotein of Coronavirus mouse hepatitis virus A59, Proc. Natl. Acad. Sci. USA 81:1421.PubMedCrossRefGoogle Scholar
  79. Rottier, P., Armstrong, J., and Meyer, D. I., 1985, Signal recognition particle-dependent insertion of Coronavirus El, an intracellular membrane glycoprotein, J. Biol. Chem. 260:4648.PubMedGoogle Scholar
  80. Rottier, P. J. M., Welling, G. W., Welling-Wester, S., Niesters, H. G. M., Lenstra, J. A., and Van der Zeijst, B. A. M., 1986, Predicted membrane topology of the Coronavirus protein El, Biochemistry 25:1335.PubMedCrossRefGoogle Scholar
  81. Rottier, P. J. M., Krijnse Locker, J., Horzinek, M. C., and Spaan, W. J. M., 1990, Expression of MHV-A59 M glycoprotein: Effects of deletions on membrane integration and intracellular transport, Adv. Exp. Med. Biol. 276:127.PubMedCrossRefGoogle Scholar
  82. Sanchez, C. M., Jimenez, G., Laviada, M. D., Correa, I., Sune, C., Bullido, M. J., Gebauer, F., Smerdou, C., Callebaut, P., Escribano, J. M., and Enjuanes, L., 1990, Antigenic homology among coronaviruses related to transmissible gastroenteritis virus, Virology 174:410.PubMedCrossRefGoogle Scholar
  83. Schmidt, I., Skinner, M., and Siddell, S., 1987, Nucleotide sequence of the gene encoding the surface projection glycoprotein of Coronavirus MHV-JHM, J. Gen. Virol. 68:47.PubMedCrossRefGoogle Scholar
  84. Schmidt, M. F. G., 1982, Acylation of viral spike glycoproteins, a feature of enveloped RNA viruses, Virology 116:327.PubMedCrossRefGoogle Scholar
  85. Schmidt, O. W., and Kenny, G. E., 1982, Polypeptides and functions of antigens from human coronaviruses 229E and OC43, Infect. Immun. 35:515.PubMedGoogle Scholar
  86. Siddell, S. G., Wege, H., Barthel, A., and Ter Meulen, V., 1981, Coronavirus JHM. Intracellular protein synthesis, J. Gen. Virol. 53:145.PubMedCrossRefGoogle Scholar
  87. Stern, D. F., and Sefton, B. M., 1982a, Coronavirus proteins: Biogenesis of avian infectious bronchitis virus virion proteins, J. Virol. 44:794.PubMedGoogle Scholar
  88. Stern, D. F., and Sefton, B. M., 1982b, Coronavirus proteins: Structure and function of the oligosaccharides of the avian infectious bronchitis virus glycoproteins, J. Virol. 44:804.PubMedGoogle Scholar
  89. Stern, D. F., Burgess, L., and Sefton, B. M., 1982, Structural analysis of virion proteins of the avian Coronavirus infectious bronchitis virus, J. Virol. 42:208.PubMedGoogle Scholar
  90. Stohlman, S. A., and Lai, M. M. C., 1979, Phosphoproteins of murine hepatitis viruses, J. Virol. 32:672.PubMedGoogle Scholar
  91. Sturman, L. S., 1977, Characterization of a Coronavirus. I. Structural proteins: Effects of preparative conditions on the migration of protein in Polyacrylamide gels, Virology 77:637.PubMedCrossRefGoogle Scholar
  92. Sturman, L. S., 1981, The structure and behaviour of Coronavirus A59 glycoproteins, Adv. Exp. Med. Biol. 142:1.PubMedCrossRefGoogle Scholar
  93. Sturman, L. S., and Holmes, K. V., 1977, Characterization of a Coronavirus. II. Glycoproteins of the viral envelope: Tryptic peptide analysis, Virology 77:650.PubMedCrossRefGoogle Scholar
  94. Sturman, L. S., Holmes, K. V., and Behnke, J., 1980, Isolation of Coronavirus envelope glycoproteins and interaction with the viral nucleocapsid, J. Virol. 33:449.PubMedGoogle Scholar
  95. Sugiyama, K., and Amano, Y., 1981, Morphological and biological properties of a new Coronavirus associated with diarrhea in infant mice, Arch. Virol. 67:241.PubMedCrossRefGoogle Scholar
  96. Swift, A. M., and Machamer, C. E., 1991, A Golgi retention signal in a membrane-spanning domain of Coronavirus El protein, J. Cell Biol. 115:19.PubMedCrossRefGoogle Scholar
  97. Tooze, J., Tooze, S., and Warren, G., 1984, Replication of Coronavirus MHV-A59 in sac” cells: Determination of the first site of budding of progeny virions, Eur. J. Cell Biol. 33:281.PubMedGoogle Scholar
  98. Tooze, J., Tooze, S. A., and Warren, G., 1985, Laminated cisternae of the rough endoplasmic reticulum induced by Coronavirus MHV-A59 infection, Eur. J. Cell Biol. 36:108.PubMedGoogle Scholar
  99. Tooze, J., Tooze, S. A., and Fuller, S. D., 1987, Sorting of progeny Coronavirus from condensed secretory proteins at the exit from the trans-Golgi network of AtT20 cells, J. Cell Biol. 105:1215.PubMedCrossRefGoogle Scholar
  100. Tooze, S. A., and Stanley, K. K., 1986, Identification of two epitopes in the carboxyterminal 15 amino acids of the El glycoprotein of mouse hepatitis virus A59 by using hybrid proteins, J. Virol. 60:928.PubMedGoogle Scholar
  101. Tooze, S. A., Tooze, J., and Warren, G., 1988, Site of addition of N-acetyl-galactosamine to the El glycoprotein of mouse hepatitis virus-A59, J. Cell. Biol. 106:1475.PubMedCrossRefGoogle Scholar
  102. Vennema, H., De Groot, R. J., Harbour, D. A., Dalderup, M., Gruffydd-Jones, T., Horzinek, M. C., and Spaan, W. J. M., 1990a, Early death after feline infectious peritonitis virus challenge due to recombinant vaccinia virus immunization, J. Virol. 64:1407.PubMedGoogle Scholar
  103. Vennema, H., Heijnen, L., Zijderveld, A., Horzinek, M. C., and Spaan, W. J. M., 1990b, Intracellular transport of recombinant Coronavirus spike proteins: Implications for virus assembly, J. Virol. 64:339.PubMedGoogle Scholar
  104. Vennema, H., De Groot, R. J., Harbour, D. A., Horzinek, M. C., and Spaan, W. J. M., 1991a, Primary structure of the membrane and nucleocapsid protein genes of feline infectious peritonitis virus and immunogenicity of recombinant vaccinia viruses in kittens, Virology 181:327.PubMedCrossRefGoogle Scholar
  105. Vennema, H., Rijnbrand, R., Heijnen, L., Horzinek, M. C., and Spaan, W. J. M., 1991b, Enhancement of the vaccinia virus/phage T7 RNA polymerase expression system using encephalomyocarditis virus 5′-untranslated region sequences, Gene 108:201.PubMedCrossRefGoogle Scholar
  106. Verbeek, A., and Tijssen, P., 1991, Sequence analysis of the turkey enteric Coronavirus nucleocapsid and membrane protein genes: A close genomic relationship with bovine Coronavirus, J. Gen. Virol. 72:1659.PubMedCrossRefGoogle Scholar
  107. Wang, F.-I., Fleming, J. O., and Lai, M. M. C., 1992, Sequence analysis of the spike protein gene of murine Coronavirus variants: Study of genetic sites affecting neuropathogenicity, Virology 186:742.PubMedCrossRefGoogle Scholar
  108. Wege, H., Wege, H., Nagashima, K., and Ter Meulen, V., 1979, Structural polypeptides of the murine Coronavirus JHM, J. Gen. Virol. 42:37.PubMedCrossRefGoogle Scholar
  109. Weisz, O. A., Swift, A. M., and Machamer, C. E., 1993, Oligomerization of a membrane protein correlates with its retention in the Golgi complex, J. Cell Biol. 122:1185.PubMedCrossRefGoogle Scholar
  110. Wesseling, J. G., Godeke, G.-J., Schijns, V. E. C. J., Prevec, L., Graham, F. L., Horzinek, M. C., and Rottier, P. J. M., 1993, Mouse hepatitis virus spike and nucleocapsid proteins expressed by adenovirus vectors protect mice against a lethal infection, J. Gen. Virol. 74:2061.PubMedCrossRefGoogle Scholar
  111. Wesseling, J. G., Vennema, H., Godeke, G.-J., Horzinek, M. C., and Rottier, P. J. M., 1994, Nucleotide sequence and expression of the spike (S) gene of canine Coronavirus and comparison with the S proteins of feline and porcine coronaviruses, J. Gen. Virol. 75:1789.PubMedCrossRefGoogle Scholar
  112. Woods, R. D., Wesley, R. D., and Kapke, P. A., 1988, Neutralization of porcine transmissible gastroenteritis virus by complement-dependent monoclonal antibodies, Am. f. Vet. Res. 49:300.Google Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • Peter J. M. Rottier
    • 1
  1. 1.Institute of Virology, Department of Infectious Diseases and ImmunologyUniversity of UtrechtUtrechtThe Netherlands

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