Emergence of novel European genotype porcine reproductive and respiratory syndrome virus in mainland China

Journal of General Virology

Volumn 92, Issue 4, 2011, Pages 880-892

  Chen, Nanhua ^a,b   Cao, Zhen ^a   Yu, Xiuling ^a   Deng, Xiaoyu ^a   Zhao, Tiezhu ^a,c   Wang, Lilin ^a,d   Liu, Qi ^a   Li, Xiaoxia ^a   Tian, Kegong ^a  

^a China Animal Disease Control Center   (China)

^b KANSAS STATE UNIVERSITY   (United States)

^c Beijing Anheal Laboratories Co Ltd   (China)

^d CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

NONSTRUCTURAL PROTEIN 2;

ARTERIVIRUS; ARTICLE; BLOOD; CHINA; CONTROLLED STUDY; GENE SEQUENCE; GENOTYPE; LUNG ALVEOLUS MACROPHAGE; LUNG PARENCHYMA; NONHUMAN; OPEN READING FRAME; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROMOTER REGION; SEQUENCE ANALYSIS; TRANSMISSION ELECTRON MICROSCOPY; VIRUS DETECTION; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS ISOLATION; VIRUS STRAIN;

ANIMALS; CARRIER STATE; CELLS, CULTURED; CHINA; CLUSTER ANALYSIS; CYTOPATHOGENIC EFFECT, VIRAL; EVOLUTION, MOLECULAR; GENOME, VIRAL; GENOTYPE; LUNG; MACROPHAGES; MOLECULAR SEQUENCE DATA; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; SERUM; SWINE;

PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUIDAE; SUS;

EID: 79955773883     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.027995-0     Document Type: Article

References (78)

1. Allende, R., Lewis, T. L., Lu, Z., Rock, D. L., Kutish, G. F., Ali, A., Doster, A. R. & Osorio, F. A. (1999). North American and European porcine reproductive and respiratory syndrome viruses differ in nonstructural protein coding regions. J Gen Virol 80, 307-315.
2. Amonsin, A., Kedkovid, R., Puranaveja, S., Wongyanin, P., Suradhat, S. & Thanawongnuwech, R. (2009). Comparative analysis of complete nucleotide sequence of porcine reproductive and respiratory syndrome virus (PRRSV) isolates in Thailand (US and EU genotypes). Virol J 6, 143.
3. Balka, G., Hornyák, A., Bálint, A., Kiss, I., Kecskeméti, S., Bakonyi, T. & Rusvai, M. (2008). Genetic diversity of porcine reproductive and respiratory syndrome virus strains circulating in Hungarian swine herds. Vet Microbiol 127, 128-135.
4. Bøtner, A., Strandbygaard, B., Sørensen, K. J., Have, P., Madsen, K. G., Madsen, E. S. & Alexandersen, S. (1997). Appearance of acute PRRS-like symptoms in sow herds after vaccination with a modified live PRRS vaccine. Vet Rec 141, 497-499.
5. Cavanagh, D. (1997). Nidovirales: a new order comprising Coronaviridae and Arteriviridae. Arch Virol 142, 629-633.
6. Chen, N. H., Chen, X. Z., Hu, D. M., Yu, X. L., Wang, L. L., Han, W., Wu, J. J., Cao, Z., Wang, C. B. & Zhang, Q. (2009). apid differential detection of classical and highly pathogenic North American Porcine Reproductive and Respiratory Syndrome virus in China by a duplex real-time RT-PCR. J Virol Methods 161, 192-198.
7. Chen, Z., Zhou, X., Lunney, J. K., Lawson, S., Sun, Z., Brown, E., Christopher-Hennings, J., Knudsen, D., Nelson, E. & Fang, Y. (2010). Immunodominant epitopes in Nsp2 of porcine reproductive and respiratory syndrome virus are dispensable for replication, but play an important role in modulation of the host immune response. J Gen Virol 91, 1047-1057.
8. Collins, J. E., Benfield, D. A., Christianson, W. T., Harris, L., Hennings, J. C., Shaw, D. P., Goyal, S. M., McCullough, S., Morrison, R. B. & other authors (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 Invest 4, 117-126.
9. Conzelmann, K. K., Visser, N., Van Woensel, P. & Thiel, H. J. (1993). Molecular characterization of porcine reproductive and respiratory syndrome virus, a member of the arterivirus group. Virology 193, 329-339.
10. Dea, S., Gagnon, C. A., Mardassi, H., Pirzadeh, B. & Rogan, D. (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.
11. de Lima, M., Pattnaik, A. K., Flores, E. F. & Osorio, F. A. (2006). Serologic marker candidates identified among B-cell linear epitopes of Nsp2 and structural proteins of a North American strain of porcine reproductive and respiratory syndrome virus. Virology 353, 410-421.
12. Dewey, C., Charbonneau, G., Carman, S., Hamel, A., Nayar, G., Friendship, R., Eernisse, K. & Swenson, S. (2000). Lelystad-like strain of porcine reproductive and respiratory syndrome virus (PRRSV) identified in Canadian swine. Can Vet J 41, 493-494.
13. Drew, T. W., Lowings, J. P. & Yapp, F. (1997). Variation in open reading frames 3, 4 and 7 among porcine reproductive and respiratory syndrome virus isolates in the UK. Vet Microbiol 55, 209-221.
14. Fang, Y. & Snijder, E. J. (2010). The PRRSV replicase: exploring the multifunctionality of an intriguing set of nonstructural proteins. Virus Res 154, 61-76.
15. Fang, Y., Kim, D. Y., Ropp, S., Steen, P., Christopher-Hennings, J., Nelson, E. A. & Rowland, R. R. (2004). Heterogeneity in Nsp2 of European-like porcine reproductive and respiratory syndrome viruses isolated in the United States. Virus Res 100, 229-235.
16. Fang, Y., Schneider, P., Zhang, W. P., Faaberg, K. S., Nelson, E. A. & Rowland, R. R. (2007). Diversity and evolution of a newly emerged North American Type 1 porcine arterivirus: analysis of isolates collected between 1999 and 2004. Arch Virol 152, 1009-1017.
17. Fang, Y., Christopher-Hennings, J., Brown, E., Liu, H., Chen, Z., Lawson, S. R., Breen, R., Clement, T., Gao, X. & other authors (2008). Development of genetic markers in the non-structural protein 2 region of a US type 1 porcine reproductive and respiratory syndrome virus: implications for future recombinant marker vaccine development. J Gen Virol 89, 3086-3096.
18. Forsberg, R., Storgaard, T., Nielsen, H. S., Oleksiewicz, M. B., Cordioli, P., Sala, G., Hein, J. & Bøtner, A. (2002). The genetic diversity of European type PRRSV is similar to that of the North American type but is geographically skewed within Europe. Virology 299, 38-47.
19. Gao, Z. Q., Guo, X. & Yang, H. C. (2004). Genomic characterization of two Chinese isolates of porcine respiratory and reproductive syndrome virus. Arch Virol 149, 1341-1351.
20. Gorbalenya, A. E., Enjuanes, L., Ziebuhr, J. & Snijder, E. J. (2006). Nidovirales: evolving the largest RNA virus genome. Virus Res 117, 17-37.
21. Guo, B. Q., Chen, Z. S., Liu, W. X. & Cui, Y. Z. (1996). Isolation of PRRSV from aborted fetus with typical clinical PRRS manifestations. Chin J Prev Vet Med 2, 1-5 (in Chinese).
22. Han, J., Wang, Y. & Faaberg, K. S. (2006). Complete genome analysis of RFLP 184 isolates of porcine reproductive and respiratory syndrome virus. Virus Res 122, 175-182.
23. Han, J., Liu, G., Wang, Y. & Faaberg, K. S. (2007). Identification of nonessential regions of the Nsp2 replicase protein of porcine reproductive and respiratory syndrome virus strain VR-2332 for replication in cell culture. J Virol 81, 9878-9890.
24. Han, W., Wu, J. J., Deng, X. Y., Cao, Z., Yu, X. L., Wang, C. B., Zhao, T. Z., Chen, N. H., Hu, H. H. & other authors (2009). Molecular mutations associated with the in vitro passage of virulent porcine reproductive and respiratory syndrome virus. Virus Genes 38, 276-284.
25. Jeanmougin, F., Thompson, J. D., Gouy, M., Higgins, D. G. & Gibson, T. J. (1998). Multiple sequence alignment with CLUSTAL X. Trends Biochem Sci 23, 403-405.
26. Kapur, V., Elam, M. R., Pawlovich, T. M. & Murtaugh, M. P. (1996). Genetic variation in porcine reproductive and respiratory syndrome virus isolates in the midwestern United States. J Gen Virol 77, 1271-1276
27. Katz, J. B., Shafer, A. L., Eernisse, K. A., Landgraf, J. G. & Nelson, E. A. (1995). Antigenic differences between European and American isolates of porcine reproductive and respiratory syndrome virus (PRRSV) are encoded by the carboxyterminal portion of viral open reading frame 3. Vet Microbiol 44, 65-76.
28. Keffaber, K. K. (1989). Reproductive failure of unknown etiology. Am Assoc Swine Prac Newsl 1, 1-10.
29. Kim, H. S., Kwang, J., Yoon, I. J., Joo, H. S. & Frey, M. L. (1993). Enhanced replication of porcine reproductive and respiratory syndrome (PRRS) virus in a homogeneous subpopulation of MA-104 cell line. Arch Virol 133, 477-483.
30. Kim, D. Y., Kaiser, T. J., Horlen, K., Keith, M. L., Taylor, L. P., Jolie, R., Calvert, J. G. & Rowland, R. R. (2009a). Insertion and deletion in a non-essential region of the nonstructural protein 2 (Nsp2) of porcine reproductive and respiratory syndrome (PRRS) virus: effects on virulence and immunogenicity. Virus Genes 38, 118-128.
31. Kim, H. K., Yang, J. S., Moon, H. J., Park, S. J., Luo, Y., Lee, C. S., Song, D. S., Kang, B. K., Ann, S. K. & other authors (2009b). Genetic analysis of ORF5 of recent Korean porcine reproductive and respiratory syndrome viruses (PRRSVs) in viremic sera collected from MLV-vaccinating or non-vaccinating farms. J Vet Sci 10, 121-130.
32. Kim, S. H., Roh, I. S., Choi, E. J., Lee, C., Lee, C. H., Lee, K. H., Lee, K. K., Song, Y. K., Lee, O. S. & Park, C. K. (2010). A molecular analysis of European porcine reproductive and respiratory syndrome virus isolated in South Korea. Vet Microbiol 143, 394-400.
33. Kleiboeker, S. B., Schommer, S. K., Lee, S. M., Watkins, S., Chittick, W. & Polson, D. (2005). Simultaneous detection of North American and European porcine reproductive and respiratory syndrome virus using real-time quantitative reverse transcriptase-PCR. J Vet Diagn Invest 17, 165-170.
34. Labarque, G., Reeth, K. V., Nauwynck, H., Drexler, C., Van Gucht, S. & Pensaert, M. (2004). Impact of genetic diversity of European-type porcine reproductive and respiratory syndrome virus strains on vaccine efficacy. Vaccine 22, 4183-4190.
35. Li, Y., Wang, X., Jiang, P., Chen, W. & Wang, X. (2008). Genetic analysis of two porcine reproductive and respiratory syndrome viruses with different virulence isolated in China. Arch Virol 153, 1877-1884.
36. Li, B., Fang, L., Xu, Z., Liu, S., Gao, J., Jiang, Y., Chen, H. & Xiao, S. (2009a). Recombination in vaccine and circulating strains of porcine reproductive and respiratory syndrome viruses. Emerg Infect Dis 15, 2032-2035.
37. Li, Y., Wang, X., Jiang, P., Wang, X., Chen, W., Wang, X. & Wang, K. (2009b). Genetic variation analysis of porcine reproductive and respiratory syndrome virus isolated in China from 2002 to 2007 based on ORF5. Vet Microbiol 138, 150-155.
38. Meng, X. J., Paul, P. S., Halbur, P. G. & Lum, M. A. (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 U.S.A. and Europe. Arch Virol 140, 745-755.
39. Mengeling, W. L., Lager, K. M. & Vorwald, A. C. (1995). Diagnosis of porcine reproductive and respiratory syndrome. J Vet Diagn Invest 7, 3-16.
40. Meulenberg, J. J., Hulst, M. M., de Meijer, E. J., Moonen, P. L., den Besten, A., de Kluyver, E. P., Wensvoort, G. & Moormann, R. J. (1993). Lelystad virus, the causative agent of porcine epidemic abortion and respiratory syndrome (PEARS), is related to LDV and EAV. Virology 192, 62-72.
41. Meulenberg, J. J., Petersen-den Besten, A., De Kluyver, E. P., Moormann, R. J., Schaaper, W. M. & Wensvoort, G. (1995). Characterization of proteins encoded by ORFs 2 to 7 of Lelystad virus. Virology 206, 155-163.
42. Murtaugh, M. P., Elam, M. R. & Kakach, L. T. (1995). Comparison of the structural protein coding sequences of the VR-2332 and Lelystad virus strains of the PRRS virus. Arch Virol 140, 1451-1460.
43. Nam, E., Park, C. K., Kim, S. H., Joo, Y. S., Yeo, S. G. & Lee, C. (2009). Complete genomic characterization of a European type 1 porcine reproductive and respiratory syndrome virus isolate in Korea. Arch Virol 154, 629-638.
44. Nelsen, C. J., Murtaugh, M. P. & Faaberg, K. S. (1999). Porcine reproductive and respiratory syndrome virus comparison: divergent evolution on two continents. J Virol 73, 270-280.
45. Oleksiewicz, M. B., Bøtner, A., Madsen, K. G. & Storgaard, T. (1998). Sensitive detection and typing of porcine reproductive and respiratory syndrome virus by RT-PCR amplification of whole viral genes. Vet Microbiol 64, 7-22.
46. Oleksiewicz, M. B., Bøtner, A., Toft, P., Grubbe, T., Nielsen, J., Kamstrup, S. & Storgaard, T. (2000). Emergence of porcine reproductive and respiratory syndrome virus deletion mutants: correlation with the porcine antibody response to a hypervariable site in the ORF 3 structural glycoprotein. Virology 267, 135-140.
47. Oleksiewicz, M. B., Bøtner, A., Toft, P., Normann, P. & Storgaard, T. (2001). Epitope mapping porcine reproductive and respiratory syndrome virus by phage display: the Nsp2 fragment of the replicase polyprotein contains a cluster of B-cell epitopes. J Virol 75, 3277-3290.
48. Ostrowski, M., Galeota, J. A., Jar, A. M., Platt, K. B., Osorio, F. A. & Lopez, O. J. (2002). Identification of neutralizing and nonneutralizing epitopes in the porcine reproductive and respiratory syndrome virus GP5 ectodomain. J Virol 76, 4241-4250.
49. Pol, J. M., Wagenaar, F. & Reus, J. E. (1997). Comparative morphogenesis of three PRRS virus strains. Vet Microbiol 55, 203-208.
50. Ropp, S. L., Wees, C. E., Fang, Y., Nelson, E. A., Rossow, K. D., Bien, M., Arndt, B., Preszler, S., Steen, P. & other authors (2004). Characterization of emerging European-like porcine reproductive and respiratory syndrome virus isolates in the United States. J Virol 78, 3684-3703.
51. Rossow, K. D. (1998). Porcine reproductive and respiratory syndrome. Vet Pathol 35, 1-20.
52. Shen, S., Kwang, J., Liu, W. & Liu, D. X. (2000). Determination of the complete nucleotide sequence of a vaccine strain of porcine reproductive and respiratory syndrome virus and identification of the Nsp2 gene with a unique insertion. Arch Virol 145, 871-883.
53. Snijder, E. J. (1998). The arterivirus replicase. The road from RNA to protein(s), and back again. Adv Exp Med Biol 440, 97-108.
54. Snijder, E. J. & Meulenberg, J. J. (1998). The molecular biology of arteriviruses. J Gen Virol 79, 961-979.
55. Snijder, E. J., den Boon, J. A., Horzinek, M. C. & Spaan, W. J. (1991). Comparison of the genome organization of toro- and coronaviruses: evidence for two nonhomologous RNA recombination events during Berne virus evolution. Virology 180, 448-452.
56. Snijder, E. J., Wassenaar, A. L., Spaan, W. J. & Gorbalenya, A. E. (1995). The arterivirus Nsp2 protease. An unusual cysteine protease with primary structure similarities to both papain-like and chymotrypsin-like proteases. J Biol Chem 270, 16671-16676.
57. Snijder, E. J., Wassenaar, A. L., van Dinten, L. C., Spaan, W. J. & Gorbalenya, A. E. (1996). The arterivirus Nsp4 protease is the prototype of a novel group of chymotrypsin-like enzymes, the 3C-like serine proteases. J Biol Chem 271, 4864-4871.
58. Stadejek, T., Oleksiewicz, M. B., Potapchuk, D. & Podgórska, K. (2006). Porcine reproductive and respiratory syndrome virus strains of exceptional diversity in eastern Europe support the definition of new genetic subtypes. J Gen Virol 87, 1835-1841.
59. Stadejek, T., Oleksiewicz, M. B., Scherbakov, A. V., Timina, A. M., Krabbe, J. S., Chabros, K. & Potapchuk, D. (2008). Definition of subtypes in the European genotype of porcine reproductive and respiratory syndrome virus: nucleocapsid characteristics and geographical distribution in Europe. Arch Virol 153, 1479-1488.
60. Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24, 1596-1599.
61. Thanawongnuwech, R., Amonsin, A., Tatsanakit, A. & Damrongwatanapokin, S. (2004). Genetics and geographical variation of porcine reproductive and respiratory syndrome virus (PRRSV) in Thailand. Vet Microbiol 101, 9-21.
62. Tian, K., Yu, X., Zhao, T., Feng, Y., Cao, Z., Wang, C., Hu, Y., Chen, X., Hu, D. & other authors (2007). Emergence of fatal PRRSV variants: unparalleled outbreaks of atypical PRRS in China and molecular dissection of the unique hallmark. PLoS ONE 2, e526.
63. Urniza, A., Climent, I., Duran, J. P., Cortés, E., Sarraseca, J., Casal, J. I. & Vela, C. (1997). Baculovirus expression of proteins of porcine reproductive and respiratory syndrome virus strain Olot/91. Involvement of ORF3 and ORF5 proteins in protection. Virus Genes 14, 19-29.
64. van Dinten, L. C., Wassenaar, A. L., Gorbalenya, A. E., Spaan, W. J. & Snijder, E. J. (1996). Processing of the equine arteritis virus replicase ORF1b protein: identification of cleavage products containing the putative viral polymerase and helicase domains. J Virol 70, 6625-6633.
65. van Vugt, J. J., Storgaard, T., Oleksiewicz, M. B. & Bøtner, A. (2001). High frequency RNA recombination in porcine reproductive and respiratory syndrome virus occurs preferentially between parentalsequences with high similarity. J Gen Virol 82, 2615-2620.
66. Wassenaar, A. L., Spaan, W. J., Gorbalenya, A. E. & Snijder, E. J. (1997). Alternative proteolytic processing of the arterivirus replicase ORF1a polyprotein: evidence that NSP2 acts as a cofactor for the NSP4 serine protease. J Virol 71, 9313-9322.
67. Wensvoort, G., Terpstra, C., Pol, J. M., ter Laak, E. A., Bloemraad, M., de Kluyver, E. P., Kragten, C., van Buiten, L., den Besten, A. & other authors (1991). Mystery swine disease in The Netherlands: the isolation of Lelystad virus. Vet Q 13, 121-130.
68. Wensvoort, G., de Kluyver, E. P., Pol, J. M., Wagenaar, F., Moormann, R. J., Hulst, M. M., Bloemraad, R., den Besten, A., Zetstra, T. & Terpstra, C. (1992). Lelystad virus, the cause of porcine epidemic abortion and respiratory syndrome: a review of mystery swine disease research at Lelystad. Vet Microbiol 33, 185-193.
69. Wissink, E. H., van Wijk, H. A., Kroese, M. V., Weiland, E., Meulenberg, J. J., Rottier, P. J. & van Rijn, P. A. (2003). The major envelope protein, GP5, of a European porcine reproductive and respiratory syndrome virus contains a neutralization epitope in its Nterminal ectodomain. J Gen Virol 84, 1535-1543.
70. Wootton, S., Yoo, D. & Rogan, D. (2000). Full-length sequence of a Canadian porcine reproductive and respiratory syndrome virus (PRRSV) isolate. Arch Virol 145, 2297-2323.
71. Yoon, K. J., Wu, L. L., Zimmerman, J. J., Hill, H. T. & Platt, K. B. (1996). Antibody-dependent enhancement (ADE) of porcine reproductive and respiratory syndrome virus (PRRSV) infection in pigs. Viral Immunol 9, 51-63.
72. Yuan, S. & Wei, Z. (2008). Construction of infectious cDNA clones of PRRSV: separation of coding regions for nonstructural and structural proteins. Sci China C Life Sci 51, 271-279.
73. Yuan, S., Nelsen, C. J., Murtaugh, M. P., Schmitt, B. J. & Faaberg, K. S. (1999). Recombination between North American strains of porcine reproductive and respiratory syndrome virus. Virus Res 61, 87-98.
74. Zeman, D., Neiger, R., Yaeger, M., Nelson, E., Benfield, D., Leslie-Steen, P., Thomson, J., Miskimins, D., Daly, R. & Minehart, M. (1993). Laboratory investigation of PRRS virus infection in three swine herds. J Vet Diagn Invest 5, 522-528.
75. Zhou, L. & Yang, H. (2010). Porcine reproductive and respiratory syndrome in China. Virus Res 154, 31-37.
76. Zhou, L., Chen, S., Zhang, J., Zeng, J., Guo, X., Ge, X., Zhang, D. & Yang, H. (2009a). Molecular variation analysis of porcine reproductive and respiratory syndrome virus in China. Virus Res 145, 97-105.
77. Zhou, Y. J., Yu, H., Tian, Z. J., Li, G. X., Hao, X. F., Yan, L. P., Peng, J. M., An, T. Q., Xu, A. T. & Wang, Y.-X. (2009b). Genetic diversity of the ORF5 gene of porcine reproductive and respiratory syndrome virus isolates in China from 2006 to 2008. Virus Res 144, 136-144.
78. Ziebuhr, J., Snijder, E. J. & Gorbalenya, A. E. (2000). Virus-encoded proteinases and proteolytic processing in the Nidovirales. J Gen Virol 81, 853-879.