Transmissible gastroenteritis coronavirus packaging signal is located at the 5′ end of the virus genome

Journal of Virology

Volumn 77, Issue 14, 2003, Pages 7890-7902

  Escors, David ^a   Izeta, Ander ^a   Capiscol, Carmen ^a   Enjuanes, Luis ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLUCURONIDASE; MESSENGER RNA; VIRUS NUCLEOPROTEIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CORONAVIRUS; DNA PACKAGING; GASTROENTERITIS; GENE LOCATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE SPECIFICITY; VIRUS CAPSID; VIRUS DETECTION; VIRUS EXPRESSION; VIRUS GENOME; VIRUS PURIFICATION; VIRUS REPLICATION; VIRUS TRANSMISSION;

5' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; CAPSID; CELL LINE; GENOME, VIRAL; MOLECULAR SEQUENCE DATA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, VIRAL; SIGNAL TRANSDUCTION; SWINE; TRANSMISSIBLE GASTROENTERITIS VIRUS; VIRION; VIRUS ASSEMBLY; VIRUS REPLICATION;

EID: 0038758951     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.14.7890-7902.2003     Document Type: Article

References (76)

1. Adkins, B., and T. Hunter. 1981. Identification of a packaged cellular mRNA in virions of Rous sarcoma virus. J. Virol. 39:471-480.
2. Almazán, F., J. M. González, Z. Pénzes, A. Izeta, E. Calvo, J. Plana-Durán, and L. Enjuanes. 2000. Engineering the largest RNA virus genome as an infectious bacterial artificial chromosome. Proc. Natl. Acad. Sci. USA 97: 5516-5521.
3. Alonso, S., A. Izeta, I. Sola, and L. Enjuanes. 2002. Transcription regulatory sequences and mRNA expression levels in the coronavirus transmissible gastroenteritis virus. J. Virol. 76:1293-1308.
4. An, S., A. Maeda, and S. Makino. 1998. Coronavirus transcription early in infection. J. Virol. 72:8517-8524.
5. Bancroft, C. T., and T. G. Parslow. 2002. Evidence for segment-nonspecific packaging of the influenza A virus genome. J. Virol. 76:7133-7139.
6. Bos, E. C. W., J. C. Dobbe, W. Luytjes, and W. J. M. Spaan. 1997. A subgenomic mRNA transcript of the coronavirus mouse hepatitis virus strain A59 defective interfering (DI) RNA is packaged when it contains the DI packaging signal. J. Virol. 71:5684-5687.
7. 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.
8. Chang, R. Y., and D. A. Brian. 1996. cis requirement for N-specific protein sequence in bovine coronavirus defective interfering RNA replication. J. Virol. 70:2201-2207.
9. Charley, B., and H. Laude. 1988. Induction of alpha interferon by transmissible gastroenteritis coronavirus: role of transmembrane glycoprotein El. J. Virol. 62:8-10.
10. Cologna, R., and B. Hogue. 1998. Coronavirus nucleocapsid protein: RNA interactions. Adv. Exp. Med. Biol. 440:355-360.
11. Cologna, R., and B. G. Hogue. 2000. Identification of a bovine coronavirus packaging signal. J. Virol. 74:580-583.
12. Dalton, K., R. Casais, K. Shaw, K. Stirrups, S. Evans, P. Britton, T. D. K. Brown, and D. Cavanagh. 2001. cis-acting sequences required for coronavirus infectious bronchitis virus defective-RNA replication and packaging. J. Virol. 75:125-133.
13. Damayanti, T. A., H. Nagano, K. Mise, I. Furusawa, and T. Okuno. 2002. Positional effect of deletions on viability, especially on encapsidation, of Brome mosaic virus D-RNA in barley protoplasts. Virology 293:314-319.
14. Dannull, J., A. Surovoy, G. Jung, and K. Moelling. 1994. Specific binding of HIV-1 nucleocapsid protein to PSI RNA in vitro requires N-terminal zinc finger and flanking basic amino acid residues. EMBO J. 13:1525-1533.
15. 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. 2000. Coronaviridae, p. 835-849. In M. H. V. van Regenmortel, C. M. Fauquet, D. H. L. Bishop, E. B. Carsten, M. K. Estes, S. M. Lemon, D. J. McGeoch, J. Maniloff, M. A. Mayo, C. R. Pringle, and R. B. Wickner (ed.), Virus taxonomy. Classification and nomenclature of viruses. Academic Press, San Diego, Calif.
16. Escors, D., E. Camafeita, J. Ortego, H. Laude, and L. Enjuanes. 2001. Organization of two transmissible gastroenteritis coronavirus membrane protein topologies within the virion and core. J. Virol. 75:12228-12240.
17. Escors, D., J. Ortego, H. Laude, and L. Enjuanes. 2001. The membrane M protein carboxy terminus binds to transmissible gastroenteritis coronavirus core and contributes to core stability. J. Virol. 75:1312-1324.
18. Flodell, S., J. Cromsigt, J. Schleucher, K. Kidd-Ljunggren, and S. Wijmenga. 2002. Structure elucidation of the hepatitis B virus encapsidation signal by NMR on selectively labeled RNAs. J. Biomol. Struct. Dyn. 19:627-636.
19. Fosmire, J. A., K. Hwang, and S. Makino. 1992. Identification and characterization of a coronavirus packaging signal. J. Virol. 66:3522-3530.
20. Fujimura, T., and R. Esteban. 2000. Recognition of RNA encapsidation signal by the yeast L-A double-strander RNA virus. J. Biol. Chem. 275:37118-37126.
21. Fujimura, T., R. Esteban, L. M. Esteban, and R. B. Wickner. 1990. Portable encapsidation signal of the L-A double-stranded RNA virus of S. cerevisiae. Cell 62:819-828.
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. González, J. M., Z. Penzes, F. Almazán, E. Calvo, and L. Enjuanes. 2002. Stabilization of a full-length infectious cDNA clone of transmissible gastroenteritis coronavirus by the insertion of an intron. J. Virol. 76:4655-4661.
24. Griffin, S. D. C., J. F. Allen, and A. M. L. Lever. 2001. The major human immunodeficiency virus type 2 (HIV-2) packaging signal is present on all HIV-2 RNA species: cotranslational RNA encapsidation and limitation of gag protein confer specificity. J. Virol. 75:12058-12069.
25. Hofmann, M. A., P. B. Sethna, and D. A. Brian. 1990. Bovine coronavirus mRNA replication continues throughout persistent infection in cell culture. J. Virol. 64:4108-4114.
26. Huang, P., and M. M. C. Lai. 2001. Heterogeneous nuclear ribonucleoprotein A1 binds to the 3′-untranslated region and mediates potential 5′-3′-end cross talks of mouse hepatitis virus RNA. J. Virol. 75:5009-5017.
27. Izeta, A., C. Smerdou, S. Alonso, Z. Penzes, A. Méndez, J. Plana-Durán, and L. Enjuanes. 1999. Replication and packaging of transmissible gastroenteritis coronavirus-derived synthetic minigenomes. J. Virol. 73:1535-1545.
28. Jeong, Y. S., and S. Makino. 1994. Evidence for coronavirus discontinuous transcription. J. Virol. 68:2615-2623.
29. Jewell, N. A., and L. M. Mansky. 2000. In the beginning: genome recognition, RNA encapsidation and the initiation of complex retrovirus assembly. J. Gen. Virol. 81:1889-1899.
30. 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.
31. Joo, M., S. Banerjee, and S. Makino. 1996. Replication of murine coronavirus defective interfering RNA from negative-strand transcripts. J. Virol. 70:5769-5776.
32. Khromykh, A. A., A. N. Varnavski, P. L. Sedlak, and E. G. Westaway. 2001. Coupling between replication and packaging of flavivirus RNA: evidence derived from the use of DNA-based full-length cDNA clones of Kunjin virus. J. Virol. 75:4633-4640.
33. Khromykh, A. A., A. N. Varnavski, and E. G. Westaway. 1998. Encapsidation of the flavivirus Kunjin replicon RNA by using a complementation system providing Kunjin virus structural proteins in trans. J. Virol. 72:5967-5977.
34. Kouznetzoff, A., M. Buckle, and N. Tordo. 1998. Identification of a region of the rabies virus N protein involved in direct binding to the viral RNA. J. Gen. Virol. 79:1005-1013.
35. Kuo, L., and P. S. Masters. 2002. Genetic evidence for a structural interaction between the carboxy termini of the membrane and nucleocapsid proteins of mouse hepatitis virus. J. Virol. 76:4987-4999.
36. Laude, H., J. Gelfi, L. Lavenant, and B. Charley. 1992. Single amino acid changes in the viral glycoprotein M affect induction of alpha interferon by the coronavirus transmissible gastroenteritis virus. J. Virol. 66:743-749.
37. Laude, H., K. Vanreeth, and M. Pensaert. 1993. Porcine respiratory coronavirus - molecular features and virus host interactions. Vet. Res. 24:125-150.
38. Levin, J. G., and J. G. Seidman. 1979. Selective packaging of host tRNA's by murine leukemia virus particles does not require genomic RNA. J. Virol. 29:328-335.
39. Li, H.-P., X. Zhang, R. Duncan, L. Comai, and M. M. C. Lai. 1997. Heterogeneous nuclear ribonucleoprotein A1 binds to the transcription-regulatory region of mouse hepatitis virus RNA. Proc. Natl. Acad. Sci. USA 94:9544-9549.
40. Luytjes, W., H. Gerritsma, and W. J. M. Spaan. 1996. Replication of synthetic defective interfering RNAs derived from coronavirus mouse hepatitis virus-A59. Virology 216:174-183.
41. 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.
42. McVoy, M. A., D. E. Nixon, J. K. Hur, and S. P. Adler. 2000. The ends on herpesvirus DNA replicative concatemers contain pac2 cis cleavage/packaging elements and their formation is controlled by terminal cis sequences. J. Virol. 74:1587-1592.
43. Motulsky, H. 1995. Comparing two paired groups: paired t and Wilcoxon tests, p. 225-229. Intuitive Biostatistics. Oxford University Press, New York, N.Y.
44. Mougel, M., and E. Barklis. 1997. A role for two hairpin structures as a core RNA encapsidation signal in murine leukemia virus virions. J. Virol. 71:8061-8065.
45. Mougel, M., Y. Zhang, and E. Barklis. 1996. cis-active structural motifs involved in specific encapsidation of Moloney murine leukemia virus RNA. J. Virol. 70:5043-5050.
46. Muriaux, D., J. Mirro, D. Harvin, and A. Rein. 2001. RNA is a structural element in retrovirus particles. Proc. Natl. Acad. Sci. USA 98:5246-5251.
47. Narayanan, K., C.-J. Chen, J. Maeda, and S. Makino. 2003. Nucleocapsid-independent specific viral RNA packaging via viral envelope protein and viral RNA signal. J. Virol. 77:2922-2927.
48. Narayanan, K., A. Maeda, J. Maeda, and S. Makino. 2000. Characterization of the coronavirus M protein and nucleocapsid interaction in infected cells. J. Virol. 74:8127-8134.
49. Narayanan, K., and S. Makino. 2001. Cooperation of an RNA packaging signal and a viral envelope protein in coronavirus RNA packaging. J. Virol. 75:9059-9067.
50. Nguyen, V.-P., and B. G. Hogue. 1997. Protein interactions during coronavirus assembly. J. Virol. 71:9278-9284.
51. Nugent, C. I., K. L. Johnson, P. Sarnow, and K. Kirkegaard. 1999. Functional coupling between replication and packaging of poliovirus replicon RNA. J. Virol. 73:427-435.
52. Ortego, J., D. Escors, H. Laude, and L. Enjuanes. 2002. Generation of a replication-competent, propagation-deficient virus vector based on the transmissible gastroenteritis coronavirus genome. J. Virol. 76:11518-11529.
53. Osborne, J. C., and R. M. Elliott. 2000. RNA binding properties of bunyamwera virus nucleocapsid protein and selective binding to an element in the 5′ terminus of the negative-sense S segment. J. Virol. 74:9946-9952.
54. Penzes, Z., J. M. González, E. Calvo, A. Izeta, C. Smerdou, A. Mendez, C. M. Sánchez, I. Sola, F. Almazán, and L. Enjuanes. 2001. Complete genome sequence of transmissible gastroenteritis coronavirus PUR46-MAD clone and evolution of the Purdue virus cluster. Virus Genes 23:105-118.
55. Peters, G. G., and J. Hu. 1980. Reverse transcriptase as the major determinant for selective packaging of tRNA's into avian sarcoma virus particles. J. Virol. 36:692-700.
56. Pirttimaa, M. J., and D. H. Bamford. 2000. RNA secondary structures of the bacteriophage phi6 packaging regions. RNA 6:880-889.
57. Repass, J. F., and S. Makino. 1998. Importance of the positive-strand RNA secondary structure of a murine coronavirus defective interfering RNA internal replication signal in positive-strand RNA synthesis. J. Virol. 72:7926-7933.
58. 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.
59. Rumenapf, T., D. T. Brown, E. G. Strauss, M. König, R. Ramirez-Mitchel, and J. H. Strauss. 1995. Aura alphavirus subgenomic RNA is packaged into virions of two sizes. J. Virol. 69:1741-1746.
60. Rumenapf, T., E. G. Strauss, and J. H. Strauss. 1994. Subgenomic mRNA of Aura alphavirus is packaged into virions. J. Virol. 68:56-62.
61. Sánchez, 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.
62. Sawicki, S. G., and D. L. Sawicki. 1998. A new model for coronavirus transcription. Adv. Exp. Med. Biol. 440:215-220.
63. Sethna, P. B., M. A. Hofmann, and D. A. Brian. 1991. Minus-strand copies of replicating coronavirus mRNAs contain antileaders. J. Virol. 65:320-325.
64. Sethna, P. B., S.-L. Hung, and D. A. Brian. 1989. Coronavirus subgenomic minus-strand RNAs and the potential for mRNA replicons. Proc. Natl. Acad. Sci. USA 86:5626-5630.
65. Severson, W. E., X. Xu, and C. B. Jonsson. 2001. cis-acting signals in encapsidation of Hantaan virus S-segment viral genomic RNA by its N protein. J. Virol. 75:2646-2652.
66. Shi, S. T., P. Huang, H.-P. Li, and M. M. C. Lai. 2000. Heterogeneous nuclear ribonucleoprotein A1 regulates RNA synthesis of a cytoplasmic virus. EMBO J. 19:4701-4711.
67. Shin, H. J., S. S. Kim, Y. H. Cho, S. G. Lee, and H. M. Rho. 2002. Host cell proteins binding to the encapsidation signal c in hepatitis B virus RNA. Arch. Virol. 147:471-491.
68. Spagnolo, J. F., and B. G. Hogue. 2000. Host protein interactions with the 3′ end of bovine coronavirus RNA and the requirement of the poly(A) tail for coronavirus defective genome replication. J. Virol. 74:5053-5065.
69. Sturman, L. S., K. V. Holmes, and J. Behnke. 1980. Isolation of coronavirus envelope glycoproteins and interaction with the viral nucleocapsid. J. Virol. 33:449-462.
70. Thiel, V., J. Herold, B. Schelle, and S. 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.
71. van der Most, R. G., P. J. Bredenbeek, and W. J. M. Spaan. 1991. A domain at the 3′ end of the polymerase gene is essential for encapsidation of coronavirus defective interfering RNAS. J. Virol. 65:3219-3226.
72. Woo, K., M. Joo, K. Narayanan, K. H. Kim, and S. Makino. 1997. Murine coronavirus packaging signal confers packaging to nonviral RNA. J. Virol. 71:824-827.
73. Yount, B., K. M. Curtis, and R. S. Baric. 2000. Strategy for systematic assembly of large RNA and DNA genomes: the transmissible gastroenteritis virus model. J. Virol. 74:10600-10611.
74. 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.
75. Zhang, C., C. S. Lee, and P. Guo. 1994. The proximate 5′ and 3′ ends of the 120-base viral RNA (pRNA) are crucial for the packaging of bacteriophage phi 29 DNA. Virology 201:77-85.
76. Zhao, X., K. Shaw, and D. Cavanagh. 1993. Presence of subgenomic mRNAs in virions of coronavirus IBV. Virology 196:172-178.