PRRSV structure, replication and recombination: Origin of phenotype and genotype diversity

Virology

Volumn 479-480, Issue , 2015, Pages 475-486

  Kappes, Matthew A ^a   Faaberg, Kay S ^a  

^a NATIONAL ANIMAL DISEASE CENTER   (United States)

Author keywords

Arterivirus; Heteroclite; Porcine reproductive and respiratory syndrome virus; Recombination; Replication; Subgenomic RNA

Indexed keywords

ANIMAL; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENETICS; GENOTYPE; PHENOTYPE; PHYSIOLOGY; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS; ULTRASTRUCTURE; VIRION; VIRUS REPLICATION;

ANIMALS; GENETIC VARIATION; GENOTYPE; PHENOTYPE; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; RECOMBINATION, GENETIC; VIRION; VIRUS REPLICATION;

EID: 84937511147     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.02.012     Document Type: Review

References (182)

1. Albina E., Leforban Y., Baron T., Plana Duran J.P., Vannier P. An enzyme linked immunosorbent assay (ELISA) for the detection of antibodies to the porcine reproductive and respiratory syndrome (PRRS) virus. Ann. Rech. Vet. 1992, 23:167-176.
2. Baig T.T., Zakhartchouk A. New insights into RNA packaging in porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 2011, 92:2865-2870.
3. Baker S.C., Baric R.S., Balasuriya U.B., Brinton M.A., Bonami J.R., Crowley J.A., de Groot R.J., Enjuanes L., Faaberg K.S., Flegel T.W., Gorbalenya A.E., Holmes K.V., Leung F.C.-C., Lightner D.V., Nauwynck H., Perlman S., Poon L., Rottier P.J.M., Snijder E.J., Stadejk T., Talbot P.J., Walker R.M., Woo P.C.Y., Yang H., Yoo D., Ziebuhr J. Nidovirales, Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses 2012, 785-834. Elsevier, San Diego, CA, USA.
4. Baker S.C., Lai M.M. An in vitro system for the leader-primed transcription of coronavirus mRNAs. EMBO J. 1990, 9:4173-4179.
5. Banner L.R., Lai M.M. Random nature of coronavirus RNA recombination in the absence of selection pressure. Virology 1991, 185:441-445.
6. Baric R.S., Stohlman S.A., Lai M.M. Characterization of replicative intermediate RNA of mouse hepatitis virus: presence of leader RNA sequences on nascent chains. J. Virol. 1983, 48:633-640.
7. Baron T., Albina E., Leforban Y., Madec F., Guilmoto H., Plana Duran J., Vannier P. Report on the first outbreaks of the porcine reproductive and respiratory syndrome (PRRS) in France. Diagnosis and viral isolation. Ann. Rech. Vet. 1992, 23:161-166.
8. Bautista E.M., Faaberg K.S., Mickelson D., McGruder E.D. Functional properties of the predicted helicase of porcine reproductive and respiratory syndrome virus. Virology 2002, 298:258-270.
9. Bautista E.M., Meulenberg J.J., Choi C.S., Molitor T.W. Structural polypeptides of the American (VR-2332) strain of porcine reproductive and respiratory syndrome virus. Arch. Virol. 1996, 141:1357-1365.
10. Beerens N., Selisko B., Ricagno S., Imbert I., van der Zanden L., Snijder E.J., Canard B. De novo initiation of RNA synthesis by the arterivirus RNA-dependent RNA polymerase. J. Virol. 2007, 81:8384-8395.
11. Beerens N., Snijder E.J. An RNA pseudoknot in the 3' end of the arterivirus genome has a critical role in regulating viral RNA synthesis. J. Virol. 2007, 81:9426-9436.
12. Benfield D.A., Nelson E., Collins J.E., Harris L., Goyal S.M., Robison D., Christianson W.T., Morrison R.B., Gorcyca D., Chladek D. Characterization of swine infertility and respiratory syndrome (SIRS) virus (isolate ATCC VR-2332). J. Vet. Diagn. Investig. 1992, 4:127-133.
13. Breckenridge D.G., Germain M., Mathai J.P., Nguyen M., Shore G.C. Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 2003, 22:8608-8618.
14. Brockmeier S.L., Loving C.L., Vorwald A.C., Kehrli M.E., Baker R.B., Nicholson T.L., Lager K.M., Miller L.C., Faaberg K.S. Genomic sequence and virulence comparison of four Type 2 porcine reproductive and respiratory syndrome virus strains. Virus Res. 2012, 169:212-221.
15. Cavanagh D., Davis P.J. Sequence analysis of strains of avian infectious bronchitis coronavirus isolated during the 1960s in the U.K. Arch. Virol. 1993, 130:471-476.
16. Chen Q., Fang L., Wang D., Wang S., Li P., Li M., Luo R., Chen H., Xiao S. Induction of autophagy enhances porcine reproductive and respiratory syndrome virus replication. Virus Res. 2012, 163:650-655.
17. Choi Y.J., Yun S.I., Kang S.Y., Lee Y.M. 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. J. Virol. 2006, 80:723-736.
18. 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., Joo H.S., et al. 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. 1992, 4:117-126.
19. Costers S., Lefebvre D.J., Delputte P.L., Nauwynck H.J. Porcine reproductive and respiratory syndrome virus modulates apoptosis during replication in alveolar macrophages. Arch. Virol. 2008, 153:1453-1465.
20. Cottam E.M., Whelband M.C., Wileman T. Coronavirus NSP6 restricts autophagosome expansion. Autophagy 2014, 10:1426-1441.
21. Das P.B., Dinh P.X., Ansari I.H., de Lima M., Osorio F.A., Pattnaik A.K. The minor envelope glycoproteins GP2a and GP4 of porcine reproductive and respiratory syndrome virus interact with the receptor CD163. J. Virol. 2010, 84:1731-1740.
22. Dea S., Bilodeau R., Athanaseous R., Sauvageau R.A., Martineau G.P. PRRS syndrome in Quebec: isolation of a virus serologically related to Lelystad virus. Vet. Rec. 1992, 130:167.
23. Dea S., Gagnon C.A., Mardassi H., Pirzadeh B., Rogan D. Current knowledge on the structural proteins of porcine reproductive and respiratory syndrome (PRRS) virus: comparison of the North American and European isolates. Arch. Virol. 2000, 145:659-688.
24. den Boon J.A., Kleijnen M.F., Spaan W.J., Snijder E.J. Equine arteritis virus subgenomic mRNA synthesis: analysis of leader-body junctions and replicative-form RNAs. J. Virol. 1996, 70:4291-4298.
25. den Boon J.A., Snijder E.J., Chirnside E.D., de Vries A.A., Horzinek M.C., Spaan W.J. Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily. J. Virol. 1991, 65:2910-2920.
26. Deng Z., Lehmann K.C., Li X., Feng C., Wang G., Zhang Q., Qi X., Yu L., Zhang X., Feng W., Wu W., Gong P., Tao Y., Posthuma C.C., Snijder E.J., Gorbalenya A.E., Chen Z. Structural basis for the regulatory function of a complex zinc-binding domain in a replicative arterivirus helicase resembling a nonsense-mediated mRNA decay helicase. Nucleic Acids Res. 2014, 42:3464-3477.
27. Doan D.N., Dokland T. Structure of the nucleocapsid protein of porcine reproductive and respiratory syndrome virus. Structure 2003, 11:1445-1451.
28. Drew T.W., Lowings J.P., Yapp F. Variation in open reading frames 3, 4 and 7 among porcine reproductive and respiratory syndrome virus isolates in the UK. Vet. Microbiol. 1997, 55:209-221.
29. Drew T.W., Meulenberg J.J., Sands J.J., Paton D.J. Production, characterization and reactivity of monoclonal antibodies to porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 1995, 76(Pt 6):1361-1369.
30. Duan X., Nauwynck H.J., Pensaert M.B. Effects of origin and state of differentiation and activation of monocytes/macrophages on their susceptibility to porcine reproductive and respiratory syndrome virus (PRRSV). Arch. Virol. 1997, 142:2483-2497.
31. Dunowska M., Biggs P.J., Zheng T., Perrott M.R. Identification of a novel nidovirus associated with a neurological disease of the Australian brushtail possum (Trichosurus vulpecula). Vet. Microbiol. 2012, 156:418-424.
32. Faaberg K.S. Arterivirus structural proteins and assembly. The Nidoviruses 2007, 211-234. ASM Press, Washington, DC. S. Perlman, T. Gallaher, E. Snjder (Eds.).
33. Faaberg K.S., Balasuriya U.B., Brinton M.A., Gorbalenya A.E., Leung F.C., Nauwynck H., Snijder E.J., Stadejek T., Yang H., Yoo D. Family arteriviridae. Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses 2012, 796-805. Elsevier/Academic Press, Amsterdam. A.M.Q. King (Ed.).
34. Faaberg K.S., Even C., Palmer G.A., Plagemann P.G. Disulfide bonds between two envelope proteins of lactate dehydrogenase-elevating virus are essential for viral infectivity. J. Virol. 1995, 69:613-617.
35. Fang Y., Snijder E.J. The PRRSV replicase: exploring the multifunctionality of an intriguing set of nonstructural proteins. Virus Res. 2010, 154:61-76.
36. Fang Y., Treffers E.E., Li Y., Tas A., Sun Z., van der Meer Y., de Ru A.H., van Veelen P.A., Atkins J.F., Snijder E.J., Firth A.E. Efficient-2 frameshifting by mammalian ribosomes to synthesize an additional arterivirus protein. Proc. Natl. Acad. Sci. USA 2012, 109:E2920-E2928.
37. Ferrer-Orta C., Arias A., Escarmis C., Verdaguer N. A comparison of viral RNA-dependent RNA polymerases. Curr. Opin. Struct. Biol. 2006, 16:27-34.
38. Forsberg R. Divergence time of porcine reproductive and respiratory syndrome virus subtypes. Mol. Biol. Evol. 2005, 22:2131-2134.
39. Forsberg R., Oleksiewicz M.B., Petersen A.M., Hein J., Botner A., Storgaard T. A molecular clock dates the common ancestor of European-type porcine reproductive and respiratory syndrome virus at more than 10 years before the emergence of disease. Virology 2001, 289:174-179.
40. Forsberg R., Storgaard T., Nielsen H.S., Oleksiewicz M.B., Cordioli P., Sala G., Hein J., Botner A. The genetic diversity of European type PRRSV is similar to that of the North American type but is geographically skewed within Europe. Virology 2002, 299:38-47.
41. Frossard J.P., Hughes G.J., Westcott D.G., Naidu B., Williamson S., Woodger N.G., Steinbach F., Drew T.W. Porcine reproductive and respiratory syndrome virus: genetic diversity of recent British isolates. Vet. Microbiol. 2013, 162:507-518.
42. Gao F., Lu J., Yao H., Wei Z., Yang Q., Yuan S. Cis-acting structural element in 5' UTR is essential for infectivity of porcine reproductive and respiratory syndrome virus. Virus Res. 2012, 163:108-119.
43. Gauger P.C., Faaberg K.S., Guo B., Kappes M.A., Opriessnig T. Genetic and phenotypic characterization of a 2006 United States porcine reproductive and respiratory virus isolate associated with high morbidity and mortality in the field. Virus Res. 2012, 163:98-107.
44. Goldberg T.L., Lowe J.F., Milburn S.M., Firkins L.D. Quasispecies variation of porcine reproductive and respiratory syndrome virus during natural infection. Virology 2003, 317:197-207.
45. Gorbalenya A.E., Enjuanes L., Ziebuhr J., Snijder E.J. Nidovirales: evolving the largest RNA virus genome. Virus Res. 2006, 117:17-37.
46. Goyal S.M. Porcine reproductive and respiratory syndrome. J. Vet. Diagn. Investig. 1993, 5:656-664.
47. Guo B., Lager K.M., Henningson J.N., Miller L.C., Schlink S.N., Kappes M.A., Kehrli M.E., Brockmeier S.L., Nicholson T.L., Yang H.C., Faaberg K.S. Experimental infection of United States swine with a Chinese highly pathogenic strain of porcine reproductive and respiratory syndrome virus. Virology 2013, 435:372-384.
48. Guo B., Lager K.M., Schlink S.N., Kehrli M.E., Brockmeier S.L., Miller L.C., Swenson S.L., Faaberg K.S. Chinese and Vietnamese strains of HP-PRRSV cause different pathogenic outcomes in United States high health swine. Virology 2013, 446:238-250.
49. Halbur P.G., Paul P.S., Frey M.L., Landgraf J., Eernisse K., Meng X.J., Lum M.A., Andrews J.J., Rathje J.A. Comparison of the pathogenicity of two US porcine reproductive and respiratory syndrome virus isolates with that of the Lelystad virus. Vet. Pathol. 1995, 32:648-660.
50. Halbur P.G., Paul P.S., Meng X.J., Lum M.A., Andrews J.J., Rathje J.A. Comparative pathogenicity of nine US porcine reproductive and respiratory syndrome virus (PRRSV) isolates in a five-week-old cesarean-derived, colostrum-deprived pig model. J. Vet. Diagn. Investig. 1996, 8:11-20.
51. Han J., Rutherford M.S., Faaberg K.S. The porcine reproductive and respiratory syndrome virus nsp2 cysteine protease domain possesses both trans- and cis-cleavage activities. J. Virol. 2009, 83:9449-9463.
52. Han J., Rutherford M.S., Faaberg K.S. Proteolytic products of the porcine reproductive and respiratory syndrome virus nsp2 replicase protein. J. Virol. 2010, 84:10102-10112.
53. Han J., Wang Y., Faaberg K.S. Complete genome analysis of RFLP 184 isolates of porcine reproductive and respiratory syndrome virus. Virus Res. 2006, 122:175-182.
54. Hanada K., Suzuki Y., Nakane T., Hirose O., Gojobori T. The origin and evolution of porcine reproductive and respiratory syndrome viruses. Mol. Biol. Evol. 2005, 22:1024-1031.
55. Hilgenfeld R., Peiris M. From SARS to MERS: 10 years of research on highly pathogenic human coronaviruses. Antivir. Res. 2013, 100:286-295.
56. Holtkamp, D., 2011. Industry Study: Assessment of the Economic Impact of Porcine Reproductive and Respiratory Syndrome Virus on U.S. Pork Producers.
57. Hopper S.A., White M.E., Twiddy N. An outbreak of blue-eared pig disease (porcine reproductive and respiratory syndrome) in four pig herds in Great Britain. Vet. Rec. 1992, 131:140-144.
58. Huo Y., Fan L., Yin S., Dong Y., Guo X., Yang H., Hu H. Involvement of unfolded protein response, p53 and Akt in modulation of porcine reproductive and respiratory syndrome virus-mediated JNK activation. Virology 2013, 444:233-240.
59. Johnson C.R., Griggs T.F., Gnanandarajah J., Murtaugh M.P. Novel structural protein in porcine reproductive and respiratory syndrome virus encoded by an alternative ORF5 present in all arteriviruses. J. Gen. Virol. 2011, 92:1107-1116.
60. Kappes M.A., Miller C.L., Faaberg K.S. Highly divergent strains of porcine reproductive and respiratory syndrome virus incorporate multiple isoforms of nonstructural protein 2 into virions. J. Virol. 2013, 87:13456-13465.
61. Kappes M.A., Miller C.L., Faaberg K.S. Porcine reproductive and respiratory syndrome virus nonstructural protein2 (nsp2) topology and selective isoform integration in artificial membranes. J. Virol. 2015, in press. 10.1016/j.virol.2015.01.028.
62. Kapur V., Elam M.R., Pawlovich T.M., Murtaugh M.P. Genetic variation in porcine reproductive and respiratory syndrome virus isolates in the midwestern United States. J. Gen. Virol. 1996, 77(Pt 6):1271-1276.
63. Karniychuk U.U., Geldhof M., Vanhee M., Van Doorsselaere J., Saveleva T.A., Nauwynck H.J. Pathogenesis and antigenic characterization of a new East European subtype 3 porcine reproductive and respiratory syndrome virus isolate. BMC Vet. Res. 2010, 6:30.
64. Keffaber K.K. Reproductive failure of unknown etiology. Am. Assoc. Swine Pract. Newsl. 1989, 1:1-9.
65. Knoops K., Barcena M., Limpens R.W., Koster A.J., Mommaas A.M., Snijder E.J. Ultrastructural characterization of arterivirus replication structures: reshaping the endoplasmic reticulum to accommodate viral RNA synthesis. J. Virol. 2012, 86:2474-2487.
66. Koonin E.V. The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J. Gen. Virol. 1991, 72(Pt 9):2197-2206.
67. Kottier S.A., Cavanagh D., Britton P. Experimental evidence of recombination in coronavirus infectious bronchitis virus. Virology 1995, 213:569-580.
68. Labarque G., Van Gucht S., Nauwynck H., Van Reeth K., Pensaert M. Apoptosis in the lungs of pigs infected with porcine reproductive and respiratory syndrome virus and associations with the production of apoptogenic cytokines. Vet. Res. 2003, 34:249-260.
69. Lai M.M. Genetic recombination in RNA viruses. Curr. Top. Microbiol. Immunol. 1992, 176:21-32.
70. Lai M.M., Baric R.S., Makino S., Keck J.G., Egbert J., Leibowitz J.L., Stohlman S.A. Recombination between nonsegmented RNA genomes of murine coronaviruses. J. Virol. 1985, 56:449-456.
71. Lauber C., Goeman J.J., Parquet Mdel C., Nga P.T., Snijder E.J., Morita K., Gorbalenya A.E. The footprint of genome architecture in the largest genome expansion in RNA viruses. PLoS Pathog. 2013, 9:e1003500.
72. Li B., Fang L., Xu Z., Liu S., Gao J., Jiang Y., Chen H., Xiao S. Recombination in vaccine and circulating strains of porcine reproductive and respiratory syndrome viruses. Emerg. Infect. Dis. 2009, 15:2032-2035.
73. Li Y., Tas A., Sun Z., Snijder E.J., Fang Y. Proteolytic processing of the porcine reproductive and respiratory syndrome virus replicase. Virus Res. 2015, in press. 10.1016/j.virusres.2014.12.027.
74. Li Y., Treffers E.E., Napthine S., Tas A., Zhu L., Sun Z., Bell S., Mark B.L., van Veelen P.A., van Hemert M.J., Firth A.E., Brierley I., Snijder E.J., Fang Y. Transactivation of programmed ribosomal frameshifting by a viral protein. Proc. Natl. Acad. Sci. USA 2014, 66:E2172-E2181.
75. Liao C.L., Lai M.M. RNA recombination in a coronavirus: recombination between viral genomic RNA and transfected RNA fragments. J. Virol. 1992, 66:6117-6124.
76. Liao C.L., Lai M.M. Requirement of the 5'-end genomic sequence as an upstream cis-acting element for coronavirus subgenomic mRNA transcription. J. Virol. 1994, 68:4727-4737.
77. Lin Y.C., Chang R.Y., Chueh L.L. Leader-body junction sequence of the viral subgenomic mRNAs of porcine reproductive and respiratory syndrome virus isolated in Taiwan. J. Vet. Med. Sci. 2002, 64:961-965.
78. Liu D., Zhou R., Zhang J., Zhou L., Jiang Q., Guo X., Ge X., Yang H. Recombination analyses between two strains of porcine reproductive and respiratory syndrome virus in vivo. Virus Res. 2011, 155:473-486.
79. Loemba H.D., Mounir S., Mardassi H., Archambault D., Dea S. Kinetics of humoral immune response to the major structural proteins of the porcine reproductive and respiratory syndrome virus. Arch. Virol. 1996, 141:751-761.
80. Lu J., Gao F., Wei Z., Liu P., Liu C., Zheng H., Li Y., Lin T., Yuan S. A 5'-proximal stem-loop structure of 5' untranslated region of porcine reproductive and respiratory syndrome virus genome is key for virus replication. Virol. J. 2011, 8:172.
81. Makino S., Keck J.G., Stohlman S.A., Lai M.M. High-frequency RNA recombination of murine coronaviruses. J. Virol. 1986, 57:729-737.
82. Mardassi H., Athanassious R., Mounir S., Dea S. Porcine reproductive and respiratory syndrome virus: morphological, biochemical and serological characteristics of Quebec isolates associated with acute and chronic outbreaks of porcine reproductive and respiratory syndrome. Can. J. Vet. Res. 1994, 58:55-64.
83. Mardassi H., Massie B., Dea S. Intracellular synthesis, processing, and transport of proteins encoded by ORFs 5 to 7 of porcine reproductive and respiratory syndrome virus. Virology 1996, 221:98-112.
84. Mardassi H., Mounir S., Dea S. Identification of major differences in the nucleocapsid protein genes of a Quebec strain and European strains of porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 1994, 75(Pt 3):681-685.
85. Mardassi H., Mounir S., Dea S. Molecular analysis of the ORFs 3 to 7 of porcine reproductive and respiratory syndrome virus, Quebec reference strain. Arch. Virol. 1995, 140:1405-1418.
86. Martin-Valls G.E., Kvisgaard L.K., Tello M., Darwich L., Cortey M., Burgara-Estrella A.J., Hernandez J., Larsen L.E., Mateu E. Analysis of ORF5 and full-length genome sequences of porcine reproductive and respiratory syndrome virus isolates of genotypes 1 and 2 retrieved worldwide provides evidence that recombination is a common phenomenon and may produce mosaic isolates. J. Virol. 2014, 88:3170-3181.
87. Masters P.S. The molecular biology of coronaviruses. Adv. Virus Res. 2006, 66:193-292.
88. Meng X.J. Spread like a wildfire-the omnipresence of porcine circovirus type 2 (PCV2) and its ever-expanding association with diseases in pigs. Virus Res. 2012, 164:1-3.
89. Meng X.J., Paul P.S., Halbur P.G. Molecular cloning and nucleotide sequencing of the 3'-terminal genomic RNA of the porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 1994, 75(Pt 7):1795-1801.
90. Meng X.J., Paul P.S., Halbur P.G., Lum M.A. Characterization of a high-virulence US isolate of porcine reproductive and respiratory syndrome virus in a continuous cell line, ATCC CRL11171. J. Vet. Diagn. Investig. 1996, 8:374-381.
91. Meng X.J., Paul P.S., Morozov I., Halbur P.G. A nested set of six or seven subgenomic mRNAs is formed in cells infected with different isolates of porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 1996, 77(Pt 6):1265-1270.
92. Mengeling W.L., Lager K.M., Vorwald A.C. Clinical consequences of exposing pregnant gilts to strains of porcine reproductive and respiratory syndrome (PRRS) virus isolated from field cases of "atypical" PRRS. Am. J. Vet. Res. 1998, 59:1540-1544.
93. Meulenberg J.J., de Meijer E.J., Moormann R.J. Subgenomic RNAs of Lelystad virus contain a conserved leader-body junction sequence. J. Gen. Virol. 1993, 74(Pt 8):1697-1701.
94. 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. Lelystad virus, the causative agent of porcine epidemic abortion and respiratory syndrome (PEARS), is related to LDV and EAV. Virology 1993, 192:62-72.
95. 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. Lelystad virus belongs to a new virus family, comprising lactate dehydrogenase-elevating virus, equine arteritis virus, and simian hemorrhagic fever virus. Arch. Virol. Suppl. 1994, 9:441-448.
96. Meulenberg J.J., Petersen-den Besten A., De Kluyver E.P., Moormann R.J., Schaaper W.M., Wensvoort G. Characterization of proteins encoded by ORFs 2 to 7 of Lelystad virus. Virology 1995, 206:155-163.
97. Molenkamp R., Rozier B.C., Greve S., Spaan W.J., Snijder E.J. Isolation and characterization of an arterivirus defective interfering RNA genome. J. Virol. 2000, 74:3156-3165.
98. Molenkamp R., van Tol H., Rozier B.C., van der Meer Y., Spaan W.J., Snijder E.J. The arterivirus replicase is the only viral protein required for genome replication and subgenomic mRNA transcription. J. Gen. Virol. 2000, 81:2491-2496.
99. Morin M., Elazhary Y., Girard C. Porcine reproductive and respiratory syndrome in Quebec. Vet. Rec. 1991, 129:252.
100. Morrison R.B., Collins J.E., Harris L., Christianson W.T., Benfield D.A., Chladek D.W., Gorcyca D.E., Joo H.S. Serologic evidence incriminating a recently isolated virus (ATCC VR-2332) as the cause of swine infertility and respiratory syndrome (SIRS). J. Vet. Diagn. Investig. 1992, 4:186-188.
101. Murtaugh M.P., Elam M.R., Kakach L.T. Comparison of the structural protein coding sequences of the VR-2332 and Lelystad virus strains of the PRRS virus. Arch. Virol. 1995, 140:1451-1460.
102. Murtaugh M.P., Stadejek T., Abrahante J.E., Lam T.T., Leung F.C. The ever-expanding diversity of porcine reproductive and respiratory syndrome virus. Virus Res. 2010, 154:18-30.
103. Murtaugh M.P., Yuan S., Nelson E.A., Faaberg K.S. Genetic interaction between porcine reproductive and respiratory syndrome virus (PRRSV) strains in cell culture and in animals. J. Swine Health Prod. 2001, 10:15-21.
104. Nedialkova D.D., Ulferts R., van den Born E., Lauber C., Gorbalenya A.E., Ziebuhr J., Snijder E.J. Biochemical characterization of arterivirus nonstructural protein 11 reveals the nidovirus-wide conservation of a replicative endoribonuclease. J. Virol. 2009, 83:5671-5682.
105. Nelsen C.J., Murtaugh M.P., Faaberg K.S. Porcine reproductive and respiratory syndrome virus comparison: divergent evolution on two continents. J. Virol. 1999, 73:270-280.
106. Nelson E.A., Christopher-Hennings J., Benfield D.A. Serum immune responses to the proteins of porcine reproductive and respiratory syndrome (PRRS) virus. J. Vet. Diagn. Investig. 1994, 6:410-415.
107. O'Reilly E.K., Kao C.C. Analysis of RNA-dependent RNA polymerase structure and function as guided by known polymerase structures and computer predictions of secondary structure. Virology 1998, 252:287-303.
108. Oleksiewicz M.B., Botner A., Nielsen J., Storgaard T. Determination of 5'-leader sequences from radically disparate strains of porcine reproductive and respiratory syndrome virus reveals the presence of highly conserved sequence motifs. Arch. Virol. 1999, 144:981-987.
109. Ostrowski M., Galeota J.A., Jar A.M., Platt K.B., Osorio F.A., Lopez O.J. Identification of neutralizing and nonneutralizing epitopes in the porcine reproductive and respiratory syndrome virus GP5 ectodomain. J. Virol. 2002, 76:4241-4250.
110. Otake S., Dee S.A., Moon R.D., Rossow K.D., Trincado C., Farnham M., Pijoan C. Survival of porcine reproductive and respiratory syndrome virus in houseflies. Can. J. Vet. Res. 2003, 67:198-203.
111. Otake S., Dee S.A., Moon R.D., Rossow K.D., Trincado C., Pijoan C. Evaluation of mosquitoes, Aedes vexans, as biological vectors of porcine reproductive and respiratory syndrome virus. Can. J. Vet. Res. 2003, 67:265-270.
112. Pasternak A.O., Gultyaev A.P., Spaan W.J., Snijder E.J. Genetic manipulation of arterivirus alternative mRNA leader-body junction sites reveals tight regulation of structural protein expression. J. Virol. 2000, 74:11642-11653.
113. Pasternak A.O., Spaan W.J., Snijder E.J. Regulation of relative abundance of arterivirus subgenomic mRNAs. J. Virol. 2004, 78:8102-8113.
114. Pasternak A.O., Spaan W.J., Snijder E.J. Nidovirus transcription: how to make sense. .?. J. Gen. Virol 2006, 87:1403-1421.
115. Pasternak A.O., van den Born E., Spaan W.J., Snijder E.J. Sequence requirements for RNA strand transfer during nidovirus discontinuous subgenomic RNA synthesis. EMBO J. 2001, 20:7220-7228.
116. Pasternak A.O., van den Born E., Spaan W.J., Snijder E.J. The stability of the duplex between sense and antisense transcription-regulating sequences is a crucial factor in arterivirus subgenomic mRNA synthesis. J. Virol. 2003, 77:1175-1183.
117. Paton D.J., Brown I.H., Edwards S., Wensvoort G. 'Blue ear' disease of pigs. Vet. Rec. 1991, 128:617.
118. Pattnaik A.K., Ball L.A., LeGrone A.W., Wertz G.W. Infectious defective interfering particles of VSV from transcripts of a cDNA clone. Cell 1992, 69:1011-1020.
119. Pedersen K.W., van der Meer Y., Roos N., Snijder E.J. Open reading frame 1a-encoded subunits of the arterivirus replicase induce endoplasmic reticulum-derived double-membrane vesicles which carry the viral replication complex. J. Virol. 1999, 73:2016-2026.
120. Pesch S., Meyer C., Ohlinger V.F. New insights into the genetic diversity of European porcine reproductive and respiratory syndrome virus (PRRSV). Vet. Microbiol. 2005, 107:31-48.
121. Plagemann P.G. Porcine reproductive and respiratory syndrome virus: origin hypothesis. Emerg. Infect. Dis. 2003, 9:903-908.
122. Plagemann P.G., Moennig V. Lactate dehydrogenase-elevating virus, equine arteritis virus, and simian hemorrhagic fever virus: a new group of positive-strand RNA viruses. Adv. Virus Res. 1992, 41:99-192.
123. Plagemann P.G., Rowland R.R., Faaberg K.S. The primary neutralization epitope of porcine respiratory and reproductive syndrome virus strain VR-2332 is located in the middle of the GP5 ectodomain. Arch. Virol. 2002, 147:2327-2347.
124. Plana J., Vayreda M., Vilarrasa J., Bastons M., Rosell R., Martinez M., San Gabriel A., Pujols J., Badiola J.L., Ramos J.A., et al. Porcine epidemic abortion and respiratory syndrome (mystery swine disease). Isolation in Spain of the causative agent and experimental reproduction of the disease. Vet. Microbiol. 1992, 33:203-211.
125. Posthuma C.C., Nedialkova D.D., Zevenhoven-Dobbe J.C., Blokhuis J.H., Gorbalenya A.E., Snijder E.J. Site-directed mutagenesis of the Nidovirus replicative endoribonuclease NendoU exerts pleiotropic effects on the arterivirus life cycle. J. Virol. 2006, 80:1653-1661.
126. Razi M., Chan E.Y., Tooze S.A. Early endosomes and endosomal coatomer are required for autophagy. J. Cell Biol. 2009, 185:305-321.
127. Robinson S.R., Abrahante J.E., Johnson C.R., Murtaugh M.P. Purifying selection in porcine reproductive and respiratory syndrome virus ORF5a protein influences variation in envelope glycoprotein 5 glycosylation. Infect. Genet. Evol. 2013, 20:362-368.
128. Rossow K.D., Shivers J.L., Yeske P.E., Polson D.D., Rowland R.R., Lawson S.R., Murtaugh M.P., Nelson E.A., Collins J.E. Porcine reproductive and respiratory syndrome virus infection in neonatal pigs characterised by marked neurovirulence. Vet. Rec. 1999, 144:444-448.
129. Sabanadzovic S., Ghanem-Sabanadzovic N.A., Gorbalenya A.E. Permutation of the active site of putative RNA-dependent RNA polymerase in a newly identified species of plant alpha-like virus. Virology 2009, 394:1-7.
130. Sagripanti J.L., Zandomeni R.O., Weinmann R. The cap structure of simian hemorrhagic fever virion RNA. Virology 1986, 151:146-150.
131. Sawicki S.G., Sawicki D.L. Coronaviruses use discontinuous extension for synthesis of subgenome-length negative strands. Adv. Exp. Med. Biol. 1995, 380:499-506.
132. Schurrer J.A., Dee S.A., Moon R.D., Murtaugh M.P., Finnegan C.P., Deen J., Kleiboeker S.B., Pijoan C.B. Retention of ingested porcine reproductive and respiratory syndrome virus in houseflies. Am. J. Vet. Res. 2005, 66:1517-1525.
133. Schurrer J.A., Dee S.A., Moon R.D., Rossow K.D., Mahlum C., Mondaca E., Otake S., Fano E., Collins J.E., Pijoan C. Spatial dispersal of porcine reproductive and respiratory syndrome virus-contaminated flies after contact with experimentally infected pigs. Am. J. Vet. Res. 2004, 65:1284-1292.
134. Shi M., Holmes E.C., Brar M.S., Leung F.C. Recombination is associated with an outbreak of novel highly pathogenic porcine reproductive and respiratory syndrome viruses in china. J. Virol. 2013, 87:10904-10907.
135. Shi M., Lam T.T., Hon C.C., Hui R.K., Faaberg K.S., Wennblom T., Murtaugh M.P., Stadejek T., Leung F.C. Molecular epidemiology of PRRSV: a phylogenetic perspective. Virus Res. 2010, 154:7-17.
136. Shi M., Lam T.T., Hon C.C., Murtaugh M.P., Davies P.R., Hui R.K., Li J., Wong L.T., Yip C.W., Jiang J.W., Leung F.C. Phylogeny-based evolutionary, demographical, and geographical dissection of North American type 2 porcine reproductive and respiratory syndrome viruses. J. Virol. 2010, 84:8700-8711.
137. Shi M., Lemey P., Singh Brar M., Suchard M.A., Murtaugh M.P., Carman S., D'Allaire S., Delisle B., Lambert M.E., Gagnon C.A., Ge L., Qu Y., Yoo D., Holmes E.C., Chi-Ching Leung F. The spread of type 2 porcine reproductive and respiratory syndrome virus (PRRSV) in North America: a phylogeographic approach. Virology 2013, 447:146-154.
138. Snijder E.J., Kikkert M., Fang Y. Arterivirus molecular biology and pathogenesis. J. Gen. Virol. 2013, 2141-2163.
139. Snijder E.J., van Tol H., Roos N., Pedersen K.W. Non-structural proteins 2 and 3 interact to modify host cell membranes during the formation of the arterivirus replication complex. J. Gen. Virol. 2001, 82:985-994.
140. Spilman M.S., Welbon C., Nelson E., Dokland T. Cryo-electron tomography of porcine reproductive and respiratory syndrome virus: organization of the nucleocapsid. J. Gen. Virol. 2009, 90:527-535.
141. Stadejek T., Stankevicius A., Murtaugh M.P., Oleksiewicz M.B. Molecular evolution of PRRSV in Europe: current state of play. Vet. Microbiol. 2013, 165:21-28.
142. Sun M.X., Huang L., Wang R., Yu Y.L., Li C., Li P.P., Hu X.C., Hao H.P., Ishag H.A., Mao X. Porcine reproductive and respiratory syndrome virus induces autophagy to promote virus replication. Autophagy 2012, 8:1434-1447.
143. Tahara S.M., Dietlin T.A., Bergmann C.C., Nelson G.W., Kyuwa S., Anthony R.P., Stohlman S.A. Coronavirus translational regulation: leader affects mRNA efficiency. Virology 1994, 202:621-630.
144. Tan C., Chang L., Shen S., Liu D.X., Kwang J. Comparison of the 5' leader sequences of North American isolates of reference and field strains of porcine reproductive and respiratory syndrome virus (PRRSV). Virus Genes 2001, 22:209-217.
145. Tian K., Yu X., Zhao T., Feng Y., Cao Z., Wang C., Hu Y., Chen X., Hu D., Tian X., Liu D., Zhang S., Deng X., Ding Y., Yang L., Zhang Y., Xiao H., Qiao M., Wang B., Hou L., Wang X., Yang X., Kang L., Sun M., Jin P., Wang S., Kitamura Y., Yan J., Gao G.F. Emergence of fatal PRRSV variants: unparalleled outbreaks of atypical PRRS in China and molecular dissection of the unique hallmark. PLoS One 2007, 2:e526.
146. Tijms M.A., Nedialkova D.D., Zevenhoven-Dobbe J.C., Gorbalenya A.E., Snijder E.J. Arterivirus subgenomic mRNA synthesis and virion biogenesis depend on the multifunctional nsp1 autoprotease. J. Virol. 2007, 81:10496-10505.
147. Tijms M.A., Snijder E.J. Equine arteritis virus non-structural protein 1, an essential factor for viral subgenomic mRNA synthesis, interacts with the cellular transcription co-factor p100. J. Gen. Virol. 2003, 84:2317-2322.
148. Tijms M.A., van Dinten L.C., Gorbalenya A.E., Snijder E.J. A zinc finger-containing papain-like protease couples subgenomic mRNA synthesis to genome translation in a positive-stranded RNA virus. Proc. Natl. Acad. Sci. USA 2001, 98:1889-1894.
149. Toro H., van Santen V.L., Jackwood M.W. Genetic diversity and selection regulates evolution of infectious bronchitis virus. Avian Dis. 2012, 56:449-455.
150. Ulferts R., Ziebuhr J. Nidovirus ribonucleases: structures and functions in viral replication. RNA Biol. 2011, 8:295-304.
151. van Berlo M.F., Horzinek M.C., van der Zeijst B.A. Equine arteritis virus-infected cells contain six polyadenylated virus-specific RNAs. Virology 1982, 118:345-352.
152. Van Breedam W., Delputte P.L., Van Gorp H., Misinzo G., Vanderheijden N., Duan X., Nauwynck H.J. Porcine reproductive and respiratory syndrome virus entry into the porcine macrophage. J. Gen. Virol. 2010, 91:1659-1667.
153. van Dinten L.C., Rensen S., Gorbalenya A.E., Snijder E.J. Proteolytic processing of the open reading frame 1b-encoded part of arterivirus replicase is mediated by nsp4 serine protease and Is essential for virus replication. J. Virol. 1999, 73:2027-2037.
154. van Dinten L.C., van Tol H., Gorbalenya A.E., Snijder E.J. The predicted metal-binding region of the arterivirus helicase protein is involved in subgenomic mRNA synthesis, genome replication, and virion biogenesis. J. Virol. 2000, 74:5213-5223.
155. Van Doorsselaere J., Brar M.S., Shi M., Karniychuk U., Leung F.C., Nauwynck H.J. Complete genome characterization of a East European Type 1 subtype 3 porcine reproductive and respiratory syndrome virus. Virus Genes 2012, 44:51-54.
156. van Hemert M.J., de Wilde A.H., Gorbalenya A.E., Snijder E.J. The in vitro RNA synthesizing activity of the isolated arterivirus replication/transcription complex is dependent on a host factor. J. Biol. Chem. 2008, 283:16525-16536.
157. van Marle G., Dobbe J.C., Gultyaev A.P., Luytjes W., Spaan W.J., Snijder E.J. Arterivirus discontinuous mRNA transcription is guided by base pairing between sense and antisense transcription-regulating sequences. Proc. Natl. Acad. Sci. USA 1999, 96:12056-12061.
158. van Marle G., van Dinten L.C., Spaan W.J., Luytjes W., Snijder E.J. Characterization of an equine arteritis virus replicase mutant defective in subgenomic mRNA synthesis. J. Virol. 1999, 73:5274-5281.
159. van Vugt J.J., Storgaard T., Oleksiewicz M.B., Botner A. High frequency RNA recombination in porcine reproductive and respiratory syndrome virus occurs preferentially between parental sequences with high similarity. J. Gen. Virol. 2001, 82:2615-2620.
160. Veit M., Matczuk A.K., Sinhadri B.C., Krause E., Thaa B. Membrane proteins of arterivirus particles: structure, topology, processing and function. Virus Res. 2014, 16-36.
161. Verheije M.H., Olsthoorn R.C., Kroese M.V., Rottier P.J., Meulenberg J.J. Kissing interaction between 3' noncoding and coding sequences is essential for porcine arterivirus RNA replication. J. Virol. 2002, 76:1521-1526.
162. Villarreal L.P., Defilippis V.R., Gottlieb K.A. Acute and persistent viral life strategies and their relationship to emerging diseases. Virology 2000, 272:1-6.
163. Wang G., He Y., Tu Y., Liu Y., Zhou E.M., Han Z., Jiang C., Wang S., Shi W., Cai X. Comparative analysis of apoptotic changes in peripheral immune organs and lungs following experimental infection of piglets with highly pathogenic and classical porcine reproductive and respiratory syndrome virus. Virol. J. 2014, 11:2.
164. Wang L., Junker D., Collisson E.W. Evidence of natural recombination within the S1 gene of infectious bronchitis virus. Virology 1993, 192:710-716.
165. Wang R., Xiao Y., Opriessnig T., Ding Y., Yu Y., Nan Y., Ma Z., Halbur P.G., Zhang Y.J. Enhancing neutralizing antibody production by an interferon-inducing porcine reproductive and respiratory syndrome virus strain. Vaccine 2013, 31:5537-5543.
166. Wang Y., Liang Y., Han J., Burkhart K.M., Vaughn E.M., Roof M.B., Faaberg K.S. Attenuation of porcine reproductive and respiratory syndrome virus strain MN184 using chimeric construction with vaccine sequence. Virology 2008, 371:418-429.
167. Wensvoort G., de Kluyver E.P., Luijtze E.A., den Besten A., Harris L., Collins J.E., Christianson W.T., Chladek D. Antigenic comparison of Lelystad virus and swine infertility and respiratory syndrome (SIRS) virus. J. Vet. Diagn. Investig. 1992, 4:134-138.
168. 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., Wagenaar F., et al. Mystery swine disease in The Netherlands: the isolation of Lelystad virus. Vet. Q. 1991, 13:121-130.
169. Wissink E.H., Kroese M.V., van Wijk H.A., Rijsewijk F.A., Meulenberg J.J., Rottier P.J. Envelope protein requirements for the assembly of infectious virions of porcine reproductive and respiratory syndrome virus. J. Virol. 2005, 79:12495-12506.
170. Wootton S.K., Yoo D. Homo-oligomerization of the porcine reproductive and respiratory syndrome virus nucleocapsid protein and the role of disulfide linkages. J. Virol. 2003, 77:4546-4557.
171. Xiao C.T., Liu Z.H., Yu X.L., Ge M., Li R.C., Xiao B.R., Zhou H.R. Identification of new defective interfering RNA species associated with porcine reproductive and respiratory syndrome virus infection. Virus Res. 2011, 158:33-36.
172. Yin S., Huo Y., Dong Y., Fan L., Yang H., Wang L., Ning Y., Hu H. Activation of c-Jun NH(2)-terminal kinase is required for porcine reproductive and respiratory syndrome virus-induced apoptosis but not for virus replication. Virus Res. 2012, 166:103-108.
173. Yin Y., Liu C., Liu P., Yao H., Wei Z., Lu J., Tong G., Gao F., Yuan S. Conserved nucleotides in the terminus of the 3' UTR region are important for the replication and infectivity of porcine reproductive and respiratory syndrome virus. Arch. Virol. 2013, 158:1719-1732.
174. Yoon S.H., Kim H., Kim J., Lee H.K., Park B., Kim H. Complete genome sequences of porcine reproductive and respiratory syndrome viruses: perspectives on their temporal and spatial dynamics. Mol. Biol. Rep. 2013, 6843-6853.
175. Yu Z., Luo H., Fu W., Mattson M.P. The endoplasmic reticulum stress-responsive protein GRP78 protects neurons against excitotoxicity and apoptosis: suppression of oxidative stress and stabilization of calcium homeostasis. Exp. Neurol. 1999, 155:302-314.
176. Yuan S., Murtaugh M.P., Faaberg K.S. Heteroclite subgenomic RNAs are produced in porcine reproductive and respiratory syndrome virus infection. Virology 2000, 275:158-169.
177. Yuan S., Murtaugh M.P., Schumann F.A., Mickelson D., Faaberg K.S. Characterization of heteroclite subgenomic RNAs associated with PRRSV infection. Virus Res. 2004, 105:75-87.
178. Yuan S., Nelsen C.J., Murtaugh M.P., Schmitt B.J., Faaberg K.S. Recombination between North American strains of porcine reproductive and respiratory syndrome virus. Virus Res. 1999, 61:87-98.
179. Yun S.I., Lee Y.M. Overview: replication of porcine reproductive and respiratory syndrome virus. J. Microbiol. 2013, 51:711-723.
180. Zhang X., Liao C.L., Lai M.M. Coronavirus leader RNA regulates and initiates subgenomic mRNA transcription both in trans and in cis. J. Virol. 1994, 68:4738-4746.
181. Zhou Y., Zheng H., Gao F., Tian D., Yuan S. Mutational analysis of the SDD sequence motif of a PRRSV RNA-dependent RNA polymerase. Sci. China Life Sci. 2011, 54:870-879.
182. Zimmerman J.J., Yoon K.J., Pirtle E.C., Wills R.W., Sanderson T.J., McGinley M.J. Studies of porcine reproductive and respiratory syndrome (PRRS) virus infection in avian species. Vet. Microbiol. 1997, 55:329-336.