Identification of 5′ and 3′ cis-acting elements of the porcine reproductive and respiratory syndrome virus: Acquisition of novel 5′ AU-rich sequences restored replication of a 5′-proximal 7-nucleotide deletion mutant

Journal of Virology

Volumn 80, Issue 2, 2006, Pages 723-736

  Choi, Yu Jeong ^a   Yun, Sang Im ^a   Kang, Shien Young ^b   Lee, Young Min ^a  

^a Chungbuk National University College of Medicine   (South Korea)

^b Chungbuk National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; COMPLEMENTARY DNA; VIRUS RNA; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; LUCIFERASE;

ANIMAL CELL; ARTERIVIRUS; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; DELETION MUTANT; GENE EXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REPLICON; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSCRIPTION; SWINE DISEASE; VIRUS INFECTION; VIRUS RECOMBINANT; VIRUS REPLICATION; ANIMAL; BIOSYNTHESIS; CELL LINE; DNA FLANKING REGION; GENE VECTOR; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION;

ANIMALIA; ARTERIVIRUS; BACTERIA (MICROORGANISMS); PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUIDAE; SUS SCROFA;

3' FLANKING REGION; 5' FLANKING REGION; ANIMALS; CELL LINE; DNA, COMPLEMENTARY; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; LUCIFERASES; MUTATION; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; REPLICON; RNA, VIRAL;

EID: 30344481122     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.2.723-736.2006     Document Type: Article

References (62)

1. Albina, E. 1997. Epidemiology of porcine reproductive and respiratory syndrome (PRRS): an overview. Vet. Microbiol. 55:309-316.
2. Allende, R., T. L. Lewis, Z. Lu, D. L. Rock, G. F. Kutish, A. Ali, A. R. Doster, and F. A. Osorio. 1999. North American and European porcine reproductive and respiratory syndrome viruses differ in non-structural protein coding regions. J. Gen. Virol. 80:307-315.
3. Almazan, F., C. Galan, and L. Enjuanes. 2004. The nucleoprotein is required for efficient coronavirus genome replication. J. Virol. 78:12683-12688.
4. Ball, L. A. 1994. Replication of the genomic RNA of a positive-strand RNA animal virus from negative-sense transcripts. Proc. Natl. Acad. Sci. USA 91:12443-12447.
5. Bautista, E. M., K. S. Faaberg, D. Mickelson, and E. D. McGruder. 2002. Functional properties of the predicted helicase of porcine reproductive and respiratory syndrome virus. Virology 298:258-270.
6. Benfield, D. A., E. Nelson, J. E. Collins, L. Harris, S. M. Goyal, D. Robison, W. T. Christianson, R. B. Morrison, D. Gorcyca, and D. Chladek. 1992. Characterization of swine infertility and respiratory syndrome (SIRS) virus (isolate ATCC VR-2332). J. Vet. Diagn. Investig. 4:127-133.
7. Boyer, J. C., and A. L. Haenni. 1994. Infectious transcripts and cDNA clones of RNA viruses. Virology 198:415-426.
8. Cavanagh, D. 1997. Nidovirales: a new order comprising Coronaviridae and Arteriviridae. Arch. Virol. 142:629-633.
9. Christianson, W. T., and H. S. Joo. 1994. Porcine reproductive and respiratory syndrome: a review. Swine Health Production 2:10-28.
10. Collins, J. E., D. A. Benfield, W. T. Christianson, L. Harris, J. C. Hennings, D. P. Shaw, S. M. Goyal, S. McCullough, R. B. Morrison, H. S. Joo, D. E. Gorcyca, and D. W. Chladek. 1992. Isolation of swine infertility and respiratory syndrome virus (isolate ATCC VR-2332) in North America and experimental reproduction of the disease in gnotobiotic pigs. J. Vet. Diagn. Investig. 4:117-126.
11. Contreras, R., H. Cheroutre, W. Degrave, and W. Fiers. 1982. Simple, efficient in vitro synthesis of capped RNA useful for direct expression of cloned eukaryotic genes. Nucleic Acids Res. 10:6353-6362.
12. Conzelmann, K. K., and G. Meyers. 1996. Genetic engineering of animal RNA viruses. Trends Microbiol. 4:386-393.
13. Conzelmann, K. K., N. Visser, P. van Woesel, and H. J. Thiel. 1993. Molecular characterization of porcine reproductive and respiratory syndrome virus, a member of the arterivirus group. Virology 193:329-339.
14. Dea, S., C. A. Gagnon, H. Mardassi, B. Pirzadeh, and D. Rogan. 2000. Current knowledge on the structural proteins of porcine reproductive and respiratory syndrome (PRRS) virus: comparison of the North American and European isolates. Arch. Virol. 145:659-688.
15. Dee, S. A., H. S. Joo, D. D. Poison, and W. E. Marsh. 1997. Evaluation of the effects of nursery depopulation of the profitability of 34 pig farms. Vet. Rec. 140:498-500.
16. de Vries, A. A. F., A. L. Glaser, M. J. B. Raamsman, C. A. de Haan, S. Sarnataro, G. J. Godeke, and P. J. M. Rottier. 2000. Genetic manipulation of equine arteritis virus using full-length cDNA clones: separation of overlapping genes and expression of a foreign epitope. Virology 270:84-97.
17. Done, S. H., and D. J. Paton. 1995. Porcine reproductive and respiratory syndrome: clinical disease, pathology and immunosuppression. Vet. Rec. 136:32-35.
18. Guan, H., C. Song, and A. E. Simon. 1997. RNA promoters located on (-)-strands of a subviral RNA associated with turnip crinkle virus. RNA 3:1401-1412.
19. Halbur, P. G., P. S. Paul, M. L. Frey, J. Landgraf, K. Eernisse, X. J. Meng, M. A. Lum, J. J. Andrews, and J. A. Rathje. 1995. Comparison of the pathogenicity of two US porcine reproductive and respiratory syndrome virus isolates with that of the Lelystad virus. Vet. Pathol. 32:648-660.
20. Kang, S.-Y., S.-I. Yun, H.-S. Park, C.-K. Park, H.-S. Choi, and Y.-M. Lee. 2004. Molecular characterization of PL97-1, the first Korean isolate of the porcine reproductive and respiratory syndrome virus. Virus Res. 104:165-179.
21. Keffaber, K. K. 1989. Reproductive failure of unknown etiology. Am. Assoc. Swine Practitioners Newsl. 1:1-9.
22. Kirkegaard, K., and D. Baltimore. 1986. The mechanism of RNA recombination in poliovirus. Cell 47:433-443.
23. Lee, C., J. G. Calvert, S. K. Welch, and D. Yoo. 2005. A DNA-launched reverse genetics system for porcine reproductive and respiratory syndrome virus reveals that homodimerization of the nucleocapsid protein is essential for virus infectivity. Virology 331:47-62.
24. Markoff, L. 2003. 5′- and 3′-noncoding regions in flavivirus RNA. Adv. Virus Res. 59:177-228.
25. Meng, X. J., P. S. Paul, P. G. Halbur, and M. A. Lum. 1995. Phylogenetic analyses of the putative M (ORF 6) and N (ORF 7) genes of porcine reproductive and respiratory syndrome virus (PRRSV): implication for the existence of two genotypes of PRRSV in the USA and Europe. Arch. Virol. 140:745-755.
26. Messerle, M., I. Crnkovic, W. Hammerschmidt, H. Ziegler, and U. H. Koszinowski. 1997. Cloning and mutagenesis of a herpesvirus genome as an infectious bacterial artificial chromosome. Proc. Natl. Acad. Sci. USA 94: 14759-14763.
27. Meulenberg, J. J., D. B. Petersen, E. de Kluyver, A. van Nieuwstadt, G. Wensvoort, and R. J. Moormann. 1997. Molecular characterization of Lelystad virus. Vet. Microbiol. 55:197-202.
28. Meulenberg, J. J., J. N. Bos-de Ruijter, R. van de Graaf, G. Wensvoort, and R. J. Moormann. 1998. Infectious transcripts from cloned genome-length cDNA of porcine reproductive and respiratory syndrome virus. J. Virol. 72:380-387.
29. Meulenberg, J. J. M., M. M. Hulst, E. J. de Meyer, P. L. J. M. Moonen, A. den Besten, E. P. De Kluyver, G. Wensvoort, and R. J. M. Moormann. 1993. Lelystad virus, the causative agent of porcine epidemic abortion and respiratory syndrome (PEARS), is related to lactate dehydrogenase-elevating virus and equine arteritis virus. Virology 192:62-72.
30. Meyers, G., and H. J. Thiel. 1996. Molecular characterization of pestiviruses. Adv. Virus Res. 47:53-118.
31. Molenkamp, R., H. van Tol, B. C. Rozier, Y. van der Meer, W. J. Spaan, and E. J. Snijder. 2000. The arterivirus replicase is the only viral protein required for genome replication and subgenomic mRNA transcription. J. Gen. Virol. 81:2491-2496.
32. Nelsen, C. J., M. P. Murtaugh, and K. S. Faaberg, 1999. Porcine reproductive and respiratory syndrome virus comparison: divergent evolution on two continents. J. Virol. 73:270-280.
33. Nelson, E. A., J. Christopher-Hennings, T. Drew, G. Wensvoort, J. E. Collins, and D. A. Benfield. 1993. Differentiation of U.S. and European isolates of porcine reproductive and respiratory syndrome virus by monoclonal antibodies. J. Clin. Microbiol. 31:3184-3189.
34. Nielsen, H. S., G. Liu, J. Nielsen, M. B. Oleksiewici, A. Botner, T. Storgaard, and K. S. Faaberg. 2003. Generation of an infectious clone of VR-2332, a highly virulent North American-type isolate of porcine reproductive and respiratory syndrome virus. J. Virol. 77:3702-3711.
35. Paton, D. J., I. H. Brown, S. Edwards, and G. Wensvoort. 1991. 'Blue ear' disease of pigs. Vet. Rec. 128:617.
36. Pugachev, K. V., and T. K. Frey. 1998. Effects of defined mutations in the 5′ nontranslated region of rubella virus genomic RNA on virus viability and macromolecule synthesis. J. Virol. 72:641-650.
37. Rice, C. M., A. Grakoui, R. Galler, and T. J. Chambers. 1989. Transcription of infectious yellow fever virus RNA from full-length cDNA templates produced by in vitro ligation. New Biol. 1:285-296.
38. 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.
39. Schelle, B., N. Karl, B. Ludewig, S. G. Siddell, and V. Thiel. 2005. Selective replication of coronavirus genomes that express nucleocapsid protein. J. Virol. 79:6620-6630.
40. Schlesinger, S. 1995. RNA viruses as vectors for the expression of heterologous proteins. Mol. Biotechnol. 3:155-165.
41. Schmittgen, T. D., B. A. Zakrajsek, A. G. Mills, V. Gorn, M. J. Singer, and M. W. Reed. 2000. Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal. Biochem. 285:194-204.
42. Shizuya, H., B. Birren, U. J. Kim, V. Mancino, T. Slepak, Y. Tachiiri, and M. Simon. 1992. Cloning and stable maintenance of 300-kilobase-pair fragments of human DNA in Escherichia coli using an F-factor-based vector. Proc. Natl. Acad. Sci. USA 89:8794-8797.
43. Snijder, E. J. 1998. The arterivirus replicase. The road from RNA to protein(s), and back again. Adv. Exp. Med. Biol. 440:97-108.
44. Snijder, E. J., and J. J. Meulenberg. 1998. The molecular biology of arteri-viruses. J. Gen. Virol. 79:961-979.
45. th ed. Lippincott Williams & Wilkins Publisher, Philadelphia, Pa.
46. Thiel, V., N. Karl, B. Schelle, P. Disterer, I. Klagge, and S. G. Siddell. 2003. Multigene RNA vector based on coronavirus transcription. J. Virol. 77:9790-9798.
47. Truong, H. M., Z. Lu, G. F. Kutish, J. Galeota, F. A. Osorio, and A. K. Pattnaik. 2004. A highly pathogenic porcine reproductive and respiratory syndrome virus generated from an infectious cDNA clone retains the in vivo virulence and transmissibility properties of the parental virus. Virology 325: 308-319.
48. Van den born, E., A. P. Gultyaev, and E. J. Snijder. 2004. Secondary structure and function of the 5′-proximal region of the equine arteritis virus RNA genome. RNA. 10:424-437.
49. van Dinten, L. C., S. Rensen, A. E. Gorbalenya, and E. J. Snijder. 1999. Proteolytic processing of the open reading frame 1b-encoded part of arteri-virus replicase is mediated by nsp4 serine protease and is essential for virus replication. J. Virol. 73:2027-2037.
50. van Dinten, L. C., J. A. den Boon, A. L. M. Wassenaar, W. J. M. Spaan, and E. J. Snijder. 1997. An infectious arterivirus cDNA clone: identification of a replicase point mutation that abolishes discontinuous mRNA transcription. Proc. Natl. Acad. Sci. USA 94:991-996.
51. Verheije, M. H., R. C. Olsthoorn, M. V. Kroese, P. J. Rottier, and J. J. Meulenberg. 2002. Kissing interaction between 3′ noncoding and coding sequences is essential for porcine arterivirus RNA replication. J. Virol. 76:1521-1526.
52. Wang, K., C. Boysen, H. Schizuya, M. I. Simon, and L. Hood. 1997. Complete nucleotide sequence of two generations of a bacterial artificial chromosome cloning vector. BioTechniques 23:992-994.
53. Wensvoort, G., C. Terpstra, J. M. Pol, E. A. ter Laak, M. Bloemraad, E. P. de Kluyver, C. Kragten, L. van Buiten, A. den Besten, F. Wagenaar, J. M. Broekhuijsen, P. L. J. M. Moonen, T. Zetstra, E. A. de Boer, H. J. Tibben, M. F. de Jong, P. van't Veld, G. J. R. Groenland, J. A. van Gennep, M. T. Voets, J. H. M. Verbeijden, and J. Braamskamp. 1991. Mystery swine disease in The Netherlands: the isolation of Lelystad virus. Vet. Q. 13:121-130.
54. Wensvoort, G., E. P. de Kluyver, E. A. Luijtze, A. den Besten, L. Harris, J. E. Collins, W. T. Christianson, and D. Chladek. 1992. Antigenic comparison of Lelystad virus and swine infertility and respiratory syndrome (SIRS) virus. J. Vet. Diagn. Investig. 4:134-138.
55. Wieringa, R., A. A. de Vries, J. van der Meulen, G. J. Godeke, J. J. Onderwater, H. van Tol, H. K. Koerten, A. M. Mommaas, E. J. Snijder, and P. J. Rottier. 2004. Structural protein requirements in equine arteritis virus assembly. J. Virol. 78:13019-13027.
56. Winer, J., C. K. S. Jung, I. Shackel, and P. M. Williams. 1999. Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal. Biochem. 270:41-49.
57. Wootton, S., D. Yoo, and D. Rogan. 2000. Full-length sequence of a Canadian porcine reproductive and respiratory syndrome virus (PRRSV) isolate. Arch. Virol. 145:2297-2323.
58. Wootton, S. K., E. A. Nelson, and D. Yoo. 1998. Antigenic structure of the nucleocapsid protein of porcine reproductive and respiratory syndrome virus. Clin. Diagn. Lab. Immunol. 5:773-779.
59. Wu, W. H., Y. Fang, R. Farwell, M. Steffen-Bien, R. R. Rowland, J. Christopher-Hennings, and E. A. Nelson. 2001. A 10-kDa structural protein of porcine reproductive and respiratory syndrome virus encoded by ORF2b. Virology 287:183-191.
60. Yamshchikov, V., V. Mishin, and F. Cominelli. 2001. A new strategy in design of (+)RNA virus infectious clones enabling their stable propagation in E. coli. Virology 281:272-280.
61. Yun, S.-I., S.-Y. Kim, C. M. Rice, and Y.-M. Lee. 2003. Development and application of a reverse genetics system for Japanese encephalitis virus. J. Virol. 77:6450-6465.
62. Zevenhoven-Dobbe, J. C, S. Greve, H. van Tol, W. J. Spaan, and E. J. Snijder. 2004. Rescue of disabled infectious single-cycle (DISC) equine arteritis virus by using complementing cell lines that express minor structural glycoproteins. J. Gen. Virol. 85:3709-3714.