Targeted recombination demonstrates that the spike gene of transmissible gastroenteritis coronavirus is a determinant of its enteric tropism and virulence

Journal of Virology

Volumn 73, Issue 9, 1999, Pages 7607-7618

  Sánchez, Carlos M ^a   Izeta, Ander ^a   Sánchez Morgado, Jose M ^a   Alonso, Sara ^a   Sola, Isabel ^a   Balasch, Mónica ^b   Plana Durán, Juan ^b   Enjuanes, Luis ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b Dept of Research and Development ^*  (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CORONAVIRUS; GASTROENTERITIS; GENE SEQUENCE; GENE TARGETING; GENETIC RECOMBINATION; GENETIC TRANSFECTION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; VIROGENESIS; VIRULENCE; VIRUS REPLICATION;

EID: 0344069787     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.9.7607-7618.1999     Document Type: Article

References (75)

1. Bai, M., L. Campisi, and P. Freimuth. 1994. Vitronectin receptor antibodies inhibit infection of HeLa and A549 cells by adenovirus type 12 but not by adenovirus type 2. J. Virol. 68:5925-5932.
2. Ballesteros, M. L., C. M. Sanchez, and L. Enjuanes. 1997. Two amino acid changes at the N-terminus of transmissible gastroenteritis coronavirus spike protein result in the loss of enteric tropism. Virology 227:378-388.
3. Benbacer, L., E. Kut, L. Besnardeau, H. Laude, and B. Delmas. 1997. Interspecies aminopeptidase-N chimeras reveal species-specific receptor recognition by canine coronavirus, feline infectious peritonitis virus, and transmissible gastroenteritis virus. J. Virol. 71:734-737.
4. Bergelson, J. M., J. A. Cunningham, G. Droguett, E. A. Kurt-Jones, A. Krithivas, J. S. Hong, M. S. Horwitz, R. L. Crowell, and R. W. Finberg. 1997. Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320-1323.
5. Bergelson, J. M., J. G. Mohanty, R. L. Crowell, N. F. St. John, D. M. Lublin, and R. W. Finberg. 1995. Coxsackievirus B3 adapted to growth in RD cells binds to decay-accelerating factor (CD55). J. Virol. 69:1903-1906.
6. Bernard, S., and H. Laude. 1995. Site-specific alteration of transmissible gastroenteritis virus spike protein results in markedly reduced pathogenicity. J. Gen. Virol. 76:2235-2241.
7. Bloom, D. C., and J. G. Stevens. 1994. Neuron-specific restriction of a herpes simplex virus recombinant maps to the UL5 gene. J. Virol. 68:3761-3772.
8. Bohl, E. H., and R. F. Cross. 1971. Clinical and pathological differences in enteric infections in pigs caused by Escherichia coli. Ann. N. Y. Acad. Sci. 176:150-161.
9. Bohl, E. H., P. Gupta, F. Olquin, and L. J. Saif. 1972. Antibody responses in serum, colostrum, and milk of swine after infection or vaccination with transmissible gastroenteritis virus. Infect. Immun. 6:289-301.
10. Bohl, E. H., and T. Kumagai. 1965. The use of cell cultures for the study of TGE virus of swine. Proc. U. S. Livestock Sanitary Assoc. 69:343-350.
11. Britton, P., K. L. Mawditt, and K. W. Page. 1991. The cloning and sequencing of the virion protein genes from a British isolate of porcine respiratory coronavirus: comparison with transmissible gastroenteritis virus genes. Virus Res. 21:181-198.
12. Callebaut, P., I. Correa, M. Pensaert, G. Jiménez, and L. Enjuanes. 1988. Antigenic differentiation between transmissible gastroenteritis virus of swine and a related porcine respiratory coronavirus. J. Gen. Virol. 69:1725-1730.
13. Cavanagh, D., D. A. Brian, P. Britton, L. Enjuanes, M. C. Horzinek, M. M. C. Lai, H. Laude, P. G. W. Plagemann, S. Siddell, W. Spaan, and P. J. Talbot. 1997. Nidovirales: a new order comprising Coronaviridae and Arteriviridae. Arch. Virol. 142:629-635.
14. Chen, C.-M., D. Caranagh, and P. Britton. 1995. Cloning and sequencing of an 8.4-kb region from the 3′-end of a Taiwanese virulent isolate of the coronavirus transmissible gastroenteritis virus. Virus Res. 38:83-89.
15. Dayton, E. T., D. A. M. Konings, S. Y. Lim, R. K. S. Hsu, L. Butini, G. Pantaleo, and A. I. Dayton. 1993. The RRE of human immunodeficiency virus type 1 contributes to cell-type-specific viral tropism. J. Virol. 67:2871-2878.
16. Delmas, B., J. Gelfi, R. L'Haridon, L. K. Vogel, O. Norén, and H. Laude. 1992. Aminopeptidase N is a major receptor for the enteropathogenic coronavirus TGEV. Nature 357:417-420.
17. Eleouet, J. F., D. Rasschaert, P. Lambert, L. Levy, P. Vende, and H. Laude. 1995. Complete sequence (20 kilobases) of the polyprotein-encoding gene 1 of transmissible gastroenteritis virus. Virology 206:817-822.
18. Enjuanes, L., D. Brian, D. Cavanagh, K. Holmes, M. M. C. Lai, H. Laude, P. Masters, P. Rottier, S. G. Siddell, W. J. M. Spaan, F. Taguchi, and P. Talbot. Coronaviridae. In C. M. Fauquet, M. H. V. Van Regenmortel, D. H. L. Bishop and C. R. Pringle (ed.), Virus taxonomy, in press. Academic Press, New York, N.Y.
19. Enjuanes, L., and B. A. M. Van der Zeijst. 1995. Molecular basis of transmissible gastroenteritis coronavirus epidemiology, p. 337-376. In S. G. Siddell (ed.), The Coronaviridae. Plenum Press, New York, N.Y.
20. Fichot, O., and M. Girard. 1990. An improved method for sequencing of RNA templates. Nucleic Acids Res. 18:6162.
21. Fox, G., N. R. Parry, P. V. Barnett, B. McGinn, D. J. Rowlands, and F. Brown. 1989. The cell attachment site on foot-and-mouth disease virus includes the amino acid sequence RGD (arginine-glycine-aspartic acid). J. Gen. Virol. 70:625-637.
22. Gebauer, F., W. A. P. Posthumus, I. Correa, C. Suñé, C. M. Sánchez, C. Smerdou, J. A. Lenstra, R. Meloen, and L. Enjuanes. 1991. Residues involved in the formation of the antigenic sites of the S protein of transmissible gastroenteritis coronavirus. Virology 183:225-238.
23. Godet, M., J. Grosclaude, B. Delmas, and H. Laude. 1994. Major receptorbinding and neutralization determinants are located within the same domain of the transmissible gastroenteritis virus (coronavirus) spike protein. J. Virol. 68:8008-8016.
24. Haelterman, E. O., and M. B. Pensaert. 1967. Pathogenesis of transmissible gastroenteritis of swine, p. 569-572. Proceedings of the 18th World Veterinary Congress, Paris, France.
25. Holmes, K. V., and M. M. C. Lai. 1996. Coronaviridae: the viruses and their replication, p. 541-559. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fundamental virology, 3rd ed. Lippincott-Raven, Philadelphia, Pa.
26. Hong, S. S., L. Karayan, J. Tournier, D. T. Curiel, and P. A. Boulanger. 1997. Adenovirus type 5 fiber knob binds to MHC class I α2 domain at the surface of human epithelial and B lymphoblastoid cells. EMBO J. 16:2294-2306.
27. Izeta, A., C. Smerdou, S. Alonso, Z. Penzes, A. Mendez, J. Plana-Duran, and L. Enjuanes. 1999. Replication and packaging of transmissible gastroenteritis coronavirus-derived synthetic minigenomes. J. Virol. 73:1535-1545.
28. Jiménez, G., I. Correa, M. P. Melgosa, M. J. Bullido, and L. Enjuanes. 1986. Critical epitopes in transmissible gastroenteritis virus neutralization. J. Virol. 60:131-139.
29. Kapke, P. A., and D. A. Brian. 1986. Sequence analysis of the porcine transmissible gastroenteritis coronavirus nucleocapsid protein gene. Virology 151:41-49.
30. 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.
31. Kolb, A. F., A. Hegui, and S. G. Siddell. 1997. Identification of residues critical for the human coronavirus 229E receptor function of human aminopeptidase N. J. Gen. Virol. 78:2795-2802.
32. Krempl, C., B. Schultze, H. Laude, and G. Herrler. 1997. Point mutations in the S protein connect the sialic acid binding activity with the enteropathogenicity of transmissible gastroenteritis coronavirus. J. Virol. 71:3285-3287.
33. 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.
34. Lee, K. M., M. Moro, and J. A. Baker. 1954. Transmissible gastroenteritis in pigs. Am. J. Vet. Res. 15:364-372.
35. 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.
36. Levine, A. J. 1984. Viruses and differentiation: the molecular basis of viral tissue tropism, p. 130-134. In A. L. Notkins and M. B. S. Oldstone (ed.), Concepts in viral pathogenesis. Springer-Verlag, New York, N.Y.
37. Lunney, J. K., M. D. Pescovitz, and D. H. Sachs. 1986. The swine major histocompatibility complex: its structure and function, p. 1821-1836. In M. E. Tumbleson (ed.), Swine in biomedical research. Plenum Press, New York, N.Y.
38. 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.
39. Matloubian, M., S. R. Kolhekar, T. Somasundaram, and R. Ahmed. 1993. Molecular determinants of macrophage tropism and viral persistence: importance of single amino acid changes in the polymerase and glycoprotein of lymphocytic choriomeningitis virus. J. Virol. 67:7340-7349.
40. McClurkin, A. W., and J. O. Norman. 1966. Studies on transmissible gastroenteritis of swine. II. Selected characteristics of a cytopathogenic virus common to five isolates from transmissible gastroenteritis. Can. J. Comp. Med. Vet. Sci. 30:190-198.
41. McKittrick, S. P., A. M. Georgalis, and B. A. Atchison. 1993. Efficient extraction of viral RNA for PCR amplification. BioTechniques 15:802-805.
42. Mendez, A., C. Smerdou, A Izeta, F. Gebauer, and L. Enjuanes. 1996. Molecular characterization of transmissible gastroenteritis coronavirus defective interfering genomes: packaging and heterogeneity. Virology 217:495-507.
43. Peng, D., C. A. Koetzner, T. McMahon, Y. Zhu, and P. Masters, 1995. Construction of murine coronavirus mutants containing interspecies chimeric nucleocapsid proteins. J. Virol. 69:5475-5484.
44. Penzes, Z., A. Izeta, C. Smerdou. A. Mendez, M. L. Ballesteros, and L. Enjuanes. Complete nucleotide sequence of transmissible gastroenteritis coronavirus strain PUR46-MAD. Submitted for publication.
45. Rasschaert, D., M. Duarte, and H. Laude. 1990. Porcine respiratory coronavirus differs from transmissible gastroenteritis virus by a few genomic deletions. J. Gen. Virol. 71:2599-2607.
46. Rasschaert, D., J. Gelfi, and H. Laude. 1987. Enteric coronavirus TGEV: partial sequence of the genomic RNA, its organization and expression. Biochimie 69:591-600.
47. Rasschaert, D., and L. Laude. 1987. The predicted primary structure of the peplomer protein E2 of the porcine coronavirus transmissible gastroenteritis virus. J. Gen. Virol. 68:1883-1890.
48. Register, K. B., and R. D. Wesley. 1994. Molecular characterization of attenuated vaccine strains of transmissible gastroenteritis virus. J. Vet. Diagn. Investig. 6:16-22.
49. Sachs, D., G. Leight, J. Cone, S. Schwarz, L. Stuart, and S. Rosemberg. 1976. Transplantation in miniature swine. I. Fixation of the major histocompatibility complex. Transplantation 22:559-567.
50. Saif, L. J., and E. H. Bohl. 1979. Passive immunity in transmissible gastroenteritis of swine: immunoglobulin classes of milk antibodies after oral-intranasal inoculation of sows with a live low cell culture-passaged virus. Am. J. Vet. Res. 40:115-117.
51. Saif, L. J., and R. D. Wesley. 1992. Transmissible gastroenteritis, p. 362-386. In A. D. Leman, B. E. Straw, W. L. Mengeling, S. D'Allaire, and D. J. Taylor (ed.), Diseases of swine, 7th ed. Wolfe Publishing Ltd., Ames, Iowa.
52. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
53. Sanchez, C. M., F. Gebauer, C. Suñé, A. Mendez, J. Dopazo, and L. Enjuanes. 1992. Genetic evolution and tropism of transmissible gastroenteritis coronaviruses. Virology 190:92-105.
54. Sanchez, C. M., G. Jiménez, M. D. Laviada, I. Correa, C. Suñé, M. J. Bullido, F. Gebauer, C. Smerdou, P. Callebaut, J. M. Escribano, and L. Enjuanes. 1990. Antigenic homology among coronaviruses related to transmissible gastroenteritis virus. Virology 174:410-417.
55. Shafren, D. R., R. C. Bates, M. V. Agrez, R. L. Herd, G. F. Furns, and R. D. Barry. 1995. Coxsackieviruses B1, B3, and B5 use decay accelerating factor as a receptor for cell attachment. J. Virol. 69:3873-3877.
56. Shafren, D. R., D. J. Dorahy, R. A. Ingham, G. F. Burns, and R. D. Barry. 1997. Coxsackievirus A21 binds to decay-accelerating factor but requires intercellular adhesion molecule 1 for cell entry. J. Virol. 71:4736-4743.
57. Sinzger, C., and G. Jahn. 1996. Human cytomegalovirus cell tropism and pathogenesis. Intervirology 39:302-319.
58. Suñe, C., G. Jiménez, I. Correa, M. J. Bullido, F. Gebauer, C. Smerdou, and L. Enjuanes. 1990. Mechanisms of transmissible gastroenteritis coronavirus neutralization. Virology 177:559-569.
59. Suzuki, H., and F. Taguchi. 1996. Analysis of the receptor binding site of murine coronavirus spike protein. J. Virol. 70:2632-2636.
60. Takahashi, H., M. Tatsumi, M. Matsuda, K. Nagashima, T. Kurata, and W. W. Hall. 1997. The role of topoisomerase I in HIV-1 replication. Leukemia (Baltimore) 11:26-28.
61. 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.
62. van der Most, R. G., L. Heijnen, W. J. M. Spaan, and R. J. Degroot. 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.
63. Ward, T., and P. A. Pipkin. 1994. Decay-accelerating factor CD55 is identified as the receptor for echovirus 7 using CELICS, a rapid immuno-focal cloning method. EMBO J. 13:5070-5074.
64. Ward, T., R. M. Powell, P. A. Pipkin, D. J. Evans, P. D. Minor, and J. W. Almond. 1998. Role for β2-microglobulin in echovirus infection of rhabdomyosarcoma cells, J. Virol. 72:5360-5365.
65. Weiss, R. A., and P. R. Clapham. 1996. Hot fusion of HIV. Nature 381:647-648.
66. Welter, C. J. 1987. Strategies for a successful coi onavirus (TGE) vaccine for swine, p. 551-557. In M. M. C. Lai and S. A. Stohlman (ed.), Coronaviruses. Plenum Press, New York, N.Y.
67. Wesley, R. D. 1999. Personal communication.
68. Wesley, R. D., R. D. Woods, and A. K. Cheung. 1991. Genetic analysis of porcine respiratory coronavirus, an attenuated variant of transmissible gastroenteritis virus. J. Virol. 65:3369-3373.
69. Wesley, R. D., R. D. Woods, and A. K. Cheung. 1990. Genetic basis for the pathogenesis of transmissible gastroenteritis virus. J. Virol. 64:4761-4766.
70. 5 promote adenovirus internalization but not virus attachment. Cell 73:309-319.
71. Woods, R. D. 1978. Small plaque variant of transmissible gastroenteritis virus. J. Am. Vet. Med. Assoc. 173:643-647.
72. WuDunn, D., and P. G. Spear. 1989. Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J. Virol. 63:52-58.
73. 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.
74. Yokomori, K., M. Asanaka, S. A. Stohlman, and M. M. C. Lai. 1993. A spike protein-dependent cellular factor other than the viral receptor is required for mouse hepatitis virus entry. Virology 196:45-56.
75. Zhang, L., F. Homberger, W. Spaan, and W. Luytjes. 1997. Recombinant genomic RNA of coronavirus MHV-A59 after coreplication with a DI RNA containing the MHV-R1 spike gene. Virology 230:93-102.