Retargeting of coronavirus by substitution of the spike glycoprotein ectodomain: Crossing the host cell species barrier

Journal of Virology

Volumn 74, Issue 3, 2000, Pages 1393-1406

  Kuo, Lili ^a   Godeke, Gert Jan ^b   Raamsman, Martin J B ^b   Masters, Paul S ^a   Rottier, Peter J M ^b  

^a WADSWORTH CENTER   (United States)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS GLYCOPROTEIN; VIRUS RNA; VITRONECTIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHIMERA; CORONAVIRUS; GENETIC RECOMBINATION; MURINE HEPATITIS CORONAVIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN TARGETING; SPECIES DIFFERENCE; VIRION; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; BASE SEQUENCE; CATS; CELL LINE; CORONAVIRUS, FELINE; MEMBRANE GLYCOPROTEINS; MICE; MOLECULAR SEQUENCE DATA; MURINE HEPATITIS VIRUS; NEUTRALIZATION TESTS; PLASMIDS; RECEPTORS, VIRUS; RECOMBINANT FUSION PROTEINS; RECOMBINATION, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; SPECIES SPECIFICITY; VIRAL ENVELOPE PROTEINS; VIRION;

EID: 0033982337     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.3.1393-1406.2000     Document Type: Article

References (63)

1. Baric, R. S., B. Yount, L. Hensley, S. A. Peel, and W. Chen. 1997. Episodic evolution mediates interspecies transfer of a murine coronavirus. J. Virol. 71:1946-1955.
2. Baudoux, P., C. Carrat, L. Besnardeau, B. Charley, and H. Laude. 1998. Coronavirus pseudoparticles formed with recombinant M and E proteins induce alpha interferon synthesis by leukocytes. J. Virol. 72:8636-8643.
3. Bos, E. C. W., L. Heijnen, W. Luytjes, and W. J. M. Spaan. 1995. Mutational analysis of the murine coronavirus spike protein: effect on cell-to-cell fusion. Virology 214:453-463.
4. Bos, E. C. W., W. Luytjes, H. van der Meulen, H. K. Koerten, and W. J. M. Spaan. 1996. The production of recombinant infectious DI-particles of a murine coronavirus in the absence of helper virus. Virology 218:52-60.
5. Bos, E. C. W., W. Luytjes, and W. J. M. Spaan. 1997. The function of the spike protein of mouse hepatitis virus strain A59 can be studied on virus-like particles: cleavage is not required for infectivity. J. Virol. 71:9427-9433.
6. de Groot, R. J., J. Maduro, J. A. Lenstra, M. C. Horzinek, B. A. M. van der Zeijst, and W. J. M. Spaan. 1987. cDNA cloning and sequence analysis of the gene encoding the peplomer protein of feline infectious peritonitis virus. J. Gen. Virol. 68:2639-2646.
7. de Haan, C. A. M., L. Kuo, P. S. Masters, H. Vennema, and P. J. M. Rottier. 1998. Coronavirus particle assembly: primary structure requirements of the membrane protein. J. Virol. 72:6838-6850.
8. de Haan, C. A. M., P. Roestenberg, M. de Wit, A. A. F. de Vries, T. Nilsson, H. Vennema, and P. J. M. Rottier. 1998. Structural requirements for Oglycosylation of the mouse hepatitis virus membrane protein. J. Biol. Chem. 273:29905-29914.
9. Delmas, B., J. Gelfi, R. L'Haridon, L. K. Vogel, H. Sjöström, O. Norén, and H. Laude. 1992. Aminopeptidase N is a major receptor for the enteropathogenic coronavirus TGEV. Nature 357:417-420.
10. Dveksler, G. S., M. N. Pensiero, C. B. Cardellichio, R. W. Williams, G.-S. Jiang, K. V. Holmes, and C. W. Dieffenbach. 1991. Cloning of the mouse hepatitis virus (MHV) receptor: expression in human and hamster cell lines confers susceptibility to MHV. J. Virol. 65:6881-6891.
11. Fichot, O., and M. Girard. 1990. An improved method for sequencing of RNA templates. Nucleic Acids Res. 18:6162.
12. Fischer, F., D. Peng, S. T. Hingley, S. R. Weiss, and P. S. Masters. 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.
13. Fischer, F., C. F. Stegen, C. A. Koetzner, and P. S. Masters. 1997. Analysis of a recombinant mouse hepatitis virus expressing a foreign gene reveals a novel aspect of coronavirus transcription. J. Virol. 71:5148-5160.
14. Fischer, F., C. F. Stegen, P. S. Masters, and W. A. Samsonoff. 1998. Analysis of constructed E gene mutants of mouse hepatitis virus confirms a pivotal role for E protein in coronavirus assembly. J. Virol. 72:7885-7894.
15. Fleming. J. O., R. A. Shubin, M. A. Sussman, N. Casteel, and S. A. Stohlman. 1989. Monoclonal antibodies to the matrix (E1) glycoprotein of mouse hepatitis virus protect mice from encephalitis. Virology 168:162-167.
16. Godeke, G.-J., C. A. M. de Haan, J. W. A. Rossen, H. Vennema, and P. J. M. Rottier. 1999. Assembly of spikes into coronavirus particles is mediated by the carboxy-terminal domain of the spike protein. J. Virol. 74:1566-1571.
17. Godet, M., J. Grosclaude, B. Delmas, and H. Laude. 1994. Major receptor-binding and neutralization determinants are located within the same domain of the transmissible gastroenteritis virus (coronavirus) spike protein. J. Virol. 68:8008-8016.
18. Godet, M., R. L'haridon, J.-F. Vautherot, and H. Laude. 1992. TGEV corona virus ORF4 encodes a membrane protein that is incorporated into virions. Virology 188:666-675.
19. Hansen, G. H., B. Delmas, L. Besnardeau, L. K. Vogel, H. Laude, H. Sjöström, and O. Norén. 1998. The coronavirus transmissible gastroenteritis virus causes infection after receptor-mediated endocytosis and acid-dependent fusion with an intracellular compartment. J. Virol. 72:527-534.
20. Hegyi, A., and A. F. Kolb. 1998. Characterization of determinants involved in the feline infectious peritonitis virus receptor function of feline aminopeptidase N. J. Gen. Virol. 79:1387-1391.
21. Hohdatsu, T., Y. Izumiya, Y. Yokoyama, K. Kida, H. Koyama. 1998. Differences in virus receptor for type I and type II feline infectious peritonitis virus. Arch. Virol. 143:839-850.
22. Holmes, K. V., E. W. Dollar, and L. S. Sturman. 1981. Tunicamycin resistant glycosylation of a coronavirus glycoprotein: demonstration of a novel type of viral glycoprotein. Virology 115:334-344.
23. Horton, R. M., and L. R. Pease. 1991. Recombination and mutagenesis of DNA sequences using PCR, p. 217-247. In M. J. McPherson (ed.), Directed mutagenesis: a practical approach. IRL Press, New York, N.Y.
24. Hsue, B., and P. S. Masters. 1997. A bulged stem-loop structure in the 3′ untranslated region of the genome of the coronavirus mouse hepatitis virus is essential for replication. J. Virol. 71:7567-7578.
25. Hsue, B., and P. S. Masters. 1999. Insertion of a new transcriptional unit into the genome of mouse hepatitis virus. J. Virol. 73:6128-6135.
26. Kingsman, S. M., and C. E. Samuel. 1980. Mechanism of interferon action. Interferon-mediated inhibition of simian virus-40 early RNA accumulation. Virology 101:458-465.
27. Klumperman, J., J. Krijnse Locker, A. Meijer, M. C. Horzinek, H. J. Geuze, and P. J. M. Rottier. 1994. Coronavirus M proteins accumulate in the Golgi complex beyond the site of virion budding. J. Virol. 68:6523-6534.
28. Koetzner, C. A., M. M. Parker, C. S. Ricard, L. S. Sturman, and P. S. Masters. 1992. Repair and mutagenesis of the genome of a deletion mutant of the coronavirus mouse hepatitis virus by targeted RNA recombination. J. Virol. 66:1841-1848.
29. Kolb, A. F., A. Hegyi, and S. G. Siddell. 1997. Identification of residues critical for the human coronavirus 229E receptor function of human amino-peptidase N. J. Gen. Virol. 78:2795-2802.
30. 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.
31. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
32. Laude, H., and P. S. Masters. 1995. The coronavirus nucleocapsid protein, p. 141-163. In S. G. Siddell (ed.), The Coronaviridae. Plenum Press. New York, N.Y.
33. Leparc-Goffart, I., S. T. Hingley, M. M. Chua, J. Phillips, E. Lavi, and S. R. Weiss. 1998. Targeted recombination within the spike gene of murine coronavirus mouse hepatitis virus-A59: Q159 is a determinant of hepatotropism. J. Virol. 72:9628-9636.
34. Liu, D. X., and S. C. Inglis. 1991. Association of the infectious bronchitis virus 3c protein with the virion envelope. Virology 185:911-917.
35. Luytjes, W., P. J. Bredenbeek, A. F. H. Noten, M. C. Horzinek, and W. J. M. Spaan. 1988. Sequence of mouse hepatitis virus A59 mRNA2: Indications for RNA recombination between coronaviruses and influenza C virus. Virology 166:415-422.
36. Masters, P. S., C. A. Koetzner, C. A. Kerr, and Y. Heo. 1994. Optimization of targeted RNA recombination and mapping of a novel nucleocapsid gene mutation in the coronavirus mouse hepatitis virus. J. Virol. 68:328-337.
37. Nguyen, V.-P., and B. Hogue. 1997. Protein interactions during coronavirus assembly. J. Virol. 71:9278-9284.
38. Olsen, C. W., W. V. Corapi, C. K. Ngichabe, J. D. Baines, and F. W. Scott. 1992. Monoclonal antibodies to the spike protein of feline infectious peritonitis virus mediate antibody-dependent enhancement of infection of feline macrophages. J. Virol. 66:956-965.
39. Opstelten, D.-J. E., P. de Groote, M. C. Horzinek, H. Vennema, and P. J. M. Rottier. 1993. Disulfide bonds in folding and transport of mouse hepatitis coronavirus glycoproteins. J. Virol. 67:7394-7401.
40. Opstelten, D.-J. E., M. J. B. Raamsman. K. Wolfs, M. C. Horzinek, and P. J. M. Rottier. 1995. Envelope glycoprotein interactions in coronavirus assembly. J. Cell Biol. 131:339-349.
41. Peng, D., C. A. Koetzner, and P. S. Masters. 1995. Analysis of second-site revertants of a murine coronavirus nucleocapsid protein deletion mutant and construction of nucleocapsid protein mutants by targeted RNA recombination. J. Virol. 69:3449-3457.
42. Peng, D., C. A. Koetzner, T. McMahon, Y. Zhu, and P. S. Masters. 1995. Construction of murine coronavirus mutants containing interspecies chimeric nucleocapsid proteins. J. Virol. 69:5475-5484.
43. 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.
44. Risco, C., I. M. Antón, L. Enjuanes, and J. L. Carrascosa. 1996. The transmissible gastroenteritis coronavirus contains a spherical core shell consisting of M and N proteins. J. Virol. 70:4773-4777.
45. Risco, C., M. Muntión, L. Enjuanes, and J. L. Carrascosa. 1998. Two types of virus-related particles are found during transmissible gastroenteritis virus morphogenesis. J. Virol. 72:4022-4031.
46. Rossen, J. W. A., C. P. J. Bekker, G. J. A. M. Strous, M. C. Horzinek, G. S. Dveksler, K. V. Holmes, and P. J. M. Rottier. 1996. A murine and a porcine coronavirus are released from opposite surfaces of the same epithelial cells. Virology 224:345-351.
47. Rossen, J. W. A., W. F. Voorhoul, M. C. Horzinek, A. van der Ende, G. J. A. M. Strous, and P. J. M. Rottier. 1995. MHV-A59 enters polarized murine epithelial cells through the apical surface but is released basolaterally. Virology 210:54-66.
48. Rottier, P., J. Armstrong, and D. I. Meyer. 1985. Signal recognition particle-dependent insertion of coronavirus E1, an intracellular membrane glycoprotein. J. Biol. Chem. 260:4648-4652.
49. Rottier, P. J. M. 1995. The coronavirus membrane glycoprotein, p. 115-139. In S. G. Siddell (ed.), The Coronaviridae. Plenum Press, New York, N.Y.
50. 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: effects of tunicamycin. J. Virol. 40:350-357.
51. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
52. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
53. Schickli, J. H., B. D. Zelus, D. E. Wentworth, S. G. Sawicki, and K. V. Holmes. 1997. The murine coronavirus mouse hepatitis virus strain A59 from persistently infected murine cells exhibits an extended host range. J. Virol. 71:9499-9507.
54. Senanayake, S. D., M. A. Hofmann, J. L. Maki, and D. A. Brian. 1992. The nucleocapsid protein gene of bovine coronavirus is bicistronic. J. Virol. 66:5277-5283.
55. Shieh, C.-K., H.-J. Lee, K. Yokomori, N. La Monica, S. Makino, and M. M. C. Lai. 1989. Identification of a new transcription initiation site and the corresponding functional gene 2b in the murine coronavirus RNA genome. J. Virol. 63:3729-3736.
56. Siddell, S. G. 1995. The Coronaviridae: an introduction, p. 1-10. In S. G. Siddell (ed.), The Coronaviridae. Plenum Press, New York, N.Y.
57. Sturman, L. S. 1977. Characterization of a coronavirus. I. Structural proteins: effects of preparative conditions on the migration of protein in polyacrylamide gels. Virology 77:637-649.
58. - cells: determination of the first site of budding of progeny virions. Eur. J. Cell Biol. 33:281-293.
59. Tresnan, D. B., R. Levis, and K. V. Holmes. 1996. Feline aminopeptidase N serves as a receptor for feline, canine, porcine and human coronaviruses in serogroup I. J. Virol. 70:8669-8674.
60. van der Most, R. G., L. Heijnen, W. J. M. Spaan, and R. J. de Groot. 1992. Homologous RNA recombination allows efficient introduction of site-specific mutations into the genome of coronavirus MHV-A59 via synthetic co-replicating RNAs. Nucleic Acids Res. 20:3375-3381.
61. Vennema, H., G.-J. Godeke, J. W. A. Rossen, W. F. Voorhout, M. C. Horzinek, D.-J. E. Opstelten, and P. J. M. Rottier. 1996. Nucleocapsid-independent assembly of coronavirus-like particles by co-expression of viral envelope protein genes. EMBO J. 15:2020-2028.
62. Yeager, C. L., R. A. Ashmun, R. K. Williams, C. B. Cardellichio, L. H. Shapiro, A. T. Look, and K. V. Holmes. 1992. Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 357:420-422.
63. Yu, X., W. Bi, S. R. Weiss, and J. L. Leibowitz. 1994. Mouse hepatitis virus gene 5b protein is a new virion envelope protein. Virology 202:1018-1023.