DNA shuffling of the GP3 genes of porcine reproductive and respiratory syndrome virus (PRRSV) produces a chimeric virus with an improved cross-neutralizing ability against a heterologous PRRSV strain

Virology

Volumn 434, Issue 1, 2012, Pages 96-109

  Zhou, Lei ^a,b   Ni, Yan Yan ^a   Piñeyro, Pablo ^a   Sanford, Brenton J ^a   Cossaboom, Caitlin M ^a   Dryman, Barbara A ^a   Huang, Yao Wei ^a   Cao, Dian Jun ^a   Meng, Xiang Jin ^a  

^a VIRGINIA MARYLAND REGIONAL COLLEGE OF VETERINARY MEDICINE   (United States)

^b CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Cross neutralizing antibodies; GP3 gene; Porcine reproductive and respiratory syndrome virus (PRRSV); Synthetic DNA shuffling; Traditional DNA shuffling

Indexed keywords

OLIGONUCLEOTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIVIRUS; ARTICLE; CHIMERA; CONTROLLED STUDY; DNA LIBRARY; DNA SHUFFLING; GENE ACTIVITY; GENE FUNCTION; GENE SEQUENCE; GP3 GENE; IN VITRO STUDY; IN VIVO STUDY; JXA1 GENE; MN184B GENE; MOLECULAR CLONING; NADC20 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PRIORITY JOURNAL; SWINE; VIRUS GENE; VIRUS NEUTRALIZATION; VIRUS REPLICATION; VIRUS STRAIN;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; BASE SEQUENCE; CELL LINE; CROSS REACTIONS; DISEASE MODELS, ANIMAL; DNA SHUFFLING; GENOTYPE; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; PHYLOGENY; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SWINE; VIRAL LOAD; VIRAL STRUCTURAL PROTEINS; VIRUS REPLICATION;

PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUIDAE;

EID: 84868094739     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.09.005     Document Type: Article

References (72)

1. Albina E. Epidemiology of porcine reproductive and respiratory syndrome (PRRS): an overview. Vet. Microbiol. 1997, 55:309-316.
2. Apt D., Raviprakash K., Brinkman A., Semyonov A., Yang S., Skinner C., Diehl L., Lyons R., Porter K., Punnonen J. Tetravalent neutralizing antibody response against four dengue serotypes by a single chimeric dengue envelope antigen. Vaccine 2006, 24:335-344.
3. 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. Diag. Invest. 1992, 4:127-133.
4. Botner A., Nielsen J., Bille-Hansen V. Isolation of porcine reproductive and respiratory syndrome (PRRS) virus in a Danish swine herd and experimental infection of pregnant gilts with the virus. Vet. Microbiol. 1994, 40:351-360.
5. Burton D.R. Antibodies, viruses and vaccines. Nat. Rev. Immunol. 2002, 2:706-713.
6. Callison S., Hilt D., Jackwood M. Using DNA shuffling to create novel infectious bronchitis virus S1 genes: implications for S1 gene recombination. Virus Genes 2005, 31:5-11.
7. Cancel-Tirado S.M., Evans R.B., Yoon K.J. Monoclonal antibody analysis of porcine reproductive and respiratory syndrome virus epitopes associated with antibody-dependent enhancement and neutralization of virus infection. Vet. Immunol. Immunopathol. 2004, 102:249-262.
8. Cavanagh D. Nidovirales: a new order comprising Coronaviridae and Arteriviridae. Arch Virol. 1997, 142:629-633.
9. Chang C.C., Chen T.T., Cox B.W., Dawes G.N., Stemmer W.P., Punnonen J., Patten P.A. Evolution of a cytokine using DNA family shuffling. Nat. Biotechnol. 1999, 17:793-797.
10. Christopher-Hennings J., Nelson E.A., Nelson J.K., Benfield D.A. Effects of a modified-live virus vaccine against porcine reproductive and respiratory syndrome in boars. Am. J. Vet. Res. 1997, 58:40-45.
11. Conzelmann K.K., Visser N., Van Woensel P., Thiel H.J. Molecular characterization of porcine reproductive and respiratory syndrome virus, a member of the arterivirus group. Virology 1993, 193:329-339.
12. Das P.B., Vu H.L., Dinh P.X., Cooney J.L., Kwon B., Osorio F.A., Pattnaik A.K. Glycosylation of minor envelope glycoproteins of porcine reproductive and respiratory syndrome virus in infectious virus recovery, receptor interaction, and immune response. Virology 2011, 410:385-394.
13. de Lima M., Ansari I.H., Das P.B., Ku B.J., Martinez-Lobo F.J., Pattnaik A.K., Osorio F.A. GP3 is a structural component of the PRRSV type II (US) virion. Virology 2009, 390:31-36.
14. de Lima M., Pattnaik A.K., Flores E.F., Osorio F.A. 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 2006, 353:410-421.
15. Dwivedi V., Manickam C., Patterson R., Dodson K., Murtaugh M., Torrelles J.B., Schlesinger L.S., Renukaradhya G.J. Cross-protective immunity to porcine reproductive and respiratory syndrome virus by intranasal delivery of a live virus vaccine with a potent adjuvant. Vaccine 2011.
16. Fang Y., Rowland R.R., Roof M., Lunney J.K., Christopher-Hennings J., Nelson E.A. A full-length cDNA infectious clone of North American type 1 porcine reproductive and respiratory syndrome virus: expression of green fluorescent protein in the Nsp2 region. J. Virol. 2006, 80:11447-11455.
17. Firth A.E., Zevenhoven-Dobbe J.C., Wills N.M., Go Y.Y., Balasuriya U.B., Atkins J.F., Snijder E.J., Posthuma C.C. Discovery of a small arterivirus gene that overlaps the GP5 coding sequence and is important for virus production. J. Gen. Virol. 2011, 92:1097-1106.
18. 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.
19. Garner M.G., Whan I.F., Gard G.P., Phillips D. The expected economic impact of selected exotic diseases on the pig industry of Australia. Rev. Sci. Tech. 2001, 20:671-685.
20. 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.
21. Jiang W., Jiang P., Li Y., Wang X., Du Y. Analysis of immunogenicity of minor envelope protein GP3 of porcine reproductive and respiratory syndrome virus in mice. Virus Genes 2007, 35:695-704.
22. Jiang W., Jiang P., Wang X., Li Y., Du Y. Enhanced immune responses of mice inoculated recombinant adenoviruses expressing GP5 by fusion with GP3 and/or GP4 of PRRS virus. Virus Res. 2008, 136:50-57.
23. Johnson C.R., Griggs T.F., Gnanandarajah J.S., Murtaugh M.P. Novel structural protein in porcine reproductive and respiratory syndrome virus encoded in an alternative open reading frame 5 present in all arteriviruses. J. Gen. Virol 2011.
24. 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.
25. Keffaber K. Reproductive failure of unknown etiology. Am. Assoc. Swine Pract. Newslett. 1989, 1:9.
26. Kim W.I., Yoon K.J. Molecular assessment of the role of envelope-associated structural proteins in cross neutralization among different PRRS viruses. Virus Genes 2008, 37:380-391.
27. Kuwahara H., Nunoya T., Tajima M., Kato A., Samejima T. An outbreak of porcine reproductive and respiratory syndrome in Japan. J. Vet. Med. Sci. 1994, 56:901-909.
28. Li W., Asokan A., Wu Z., Van Dyke T., DiPrimio N., Johnson J.S., Govindaswamy L., Agbandje-McKenna M., Leichtle S., Redmond D.E., McCown T.J., Petermann K.B., Sharpless N.E., Samulski R.J. Engineering and selection of shuffled AAV genomes: a new strategy for producing targeted biological nanoparticles. Mol. Ther. 2008, 16:1252-1260.
29. Locher C.P., Paidhungat M., Whalen R.G., Punnonen J. DNA shuffling and screening strategies for improving vaccine efficacy. DNA Cell Biol. 2005, 24:256-263.
30. Lopez O.J., Osorio F.A. Role of neutralizing antibodies in PRRSV protective immunity. Vet. Immunol. Immunopathol. 2004, 102:155-163.
31. Lunney J.K., Benfield D.A., Rowland R.R. Porcine reproductive and respiratory syndrome virus: an update on an emerging and re-emerging viral disease of swine. Virus Res. 2010, 154:1-6.
32. 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.
33. Meng X.J. Heterogeneity of porcine reproductive and respiratory syndrome virus: implications for current vaccine efficacy and future vaccine development. Vet. Microbiol. 2000, 74:309-329.
34. 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. Invest. 1996, 8:374-381.
35. Meng X.J., Paul P.S., Halbur P.G., Morozov I. Sequence comparison of open reading frames 2 to 5 of low and high virulence United States isolates of porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 1995, 76(Pt 12):3181-3188.
36. 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(6):1265-1270.
37. Meulenberg J.J., Bos-de Ruijter J.N., Wensvoort G., Moormann R.J. An infectious cDNA clone of porcine reproductive and respiratory syndrome virus. Adv. Exp. Med. Biol. 1998, 440:199-206.
38. 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.
39. Meulenberg J.J., Petersen-den Besten A. Identification and characterization of a sixth structural protein of Lelystad virus: the glycoprotein GP2 encoded by ORF2 is incorporated in virus particles. Virology 1996, 225:44-51.
40. 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.
41. Morozov I., Meng X.J., Paul P.S. Sequence analysis of open reading frames (ORFs) 2 to 4 of a U.S. isolate of porcine reproductive and respiratory syndrome virus. Arch Virol. 1995, 140:1313-1319.
42. 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.
43. 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.
44. Neumann E.J., Kliebenstein J.B., Johnson C.D., Mabry J.W., Bush E.J., Seitzinger A.H., Green A.L., Zimmerman J.J. Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States. J. Am. Vet. Med. Assoc. 2005, 227:385-392.
45. Ni Y.Y., Huang Y.W., Cao D., Opriessnig T., Meng X.J. Establishment of a DNA-launched infectious clone for a highly pneumovirulent strain of type 2 porcine reproductive and respiratory syndrome virus: identification and in vitro and in vivo characterization of a large spontaneous deletion in the nsp2 region. Virus Res. 2011, 160:264-273.
46. Opriessnig T., Halbur P.G., Yoon K.J., Pogranichniy R.M., Harmon K.M., Evans R., Key K.F., Pallares F.J., Thomas P., Meng X.J. Comparison of molecular and biological characteristics of a modified live porcine reproductive and respiratory syndrome virus (PRRSV) vaccine (ingelvac PRRS MLV), the parent strain of the vaccine (ATCC VR2332), ATCC VR2385, and two recent field isolates of PRRSV. J. Virol. 2002, 76:11837-11844.
47. Pejsak Z., Stadejek T., Markowska-Daniel I. Clinical signs and economic losses caused by porcine reproductive and respiratory syndrome virus in a large breeding farm. Vet. Microbiology 1997, 55:317-322.
48. Pekrun K., Shibata R., Igarashi T., Reed M., Sheppard L., Patten P.A., Stemmer W.P., Martin M.A., Soong N.W. Evolution of a human immunodeficiency virus type 1 variant with enhanced replication in pig-tailed macaque cells by DNA shuffling. J. Virol. 2002, 76:2924-2935.
49. Plana Duran J., Climent I., Sarraseca J., Urniza A., Cortes E., Vela C., Casal J.I. Baculovirus expression of proteins of porcine reproductive and respiratory syndrome virus strain Olot/91. Involvement of ORF3 and ORF5 proteins in protection. Virus Genes 1997, 14:19-29.
50. Powell S.K., Kaloss M.A., Pinkstaff A., McKee R., Burimski I., Pensiero M., Otto E., Stemmer W.P., Soong N.W. Breeding of retroviruses by DNA shuffling for improved stability and processing yields. Nat.Biotechnol. 2000, 18:1279-1282.
51. Ropp S.L., Wees C.E., Fang Y., Nelson E.A., Rossow K.D., Bien M., Arndt B., Preszler S., Steen P., Christopher-Hennings J., Collins J.E., Benfield D.A., Faaberg K.S. Characterization of emerging European-like porcine reproductive and respiratory syndrome virus isolates in the United States. J. Virol. 2004, 78:3684-3703.
52. 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. A Phylogeny-based Evolutionary, Demographical and Geographical Dissection of North American Type 2 Porcine Reproductive and Respiratory Syndrome Viruses. J Virol 2010.
53. Snijder E.J., Meulenberg J.J. The molecular biology of arteriviruses. J. Gen. Virol. 1998, 79(Pt 5):961-979.
54. Soong N.W., Nomura L., Pekrun K., Reed M., Sheppard L., Dawes G., Stemmer W.P. Molecular breeding of viruses. Nat. Genet. 2000, 25:436-439.
55. Tian D., Wei Z., Zevenhoven-Dobbe J.C., Liu R., Tong G., Snijder E.J., Yuan S. Arterivirus minor envelope proteins are a major determinant of viral tropism in cell culture. J. Virol. 2012, 86:3701-3712.
56. 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.
57. Truong H.M., Lu Z., Kutish G.F., Galeota J., Osorio F.A., Pattnaik A.K. 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 2004, 325:308-319.
58. van Nieuwstadt A.P., Meulenberg J.J., van Essen-Zanbergen A., Petersen-den Besten A., Bende R.J., Moormann R.J., Wensvoort G. Proteins encoded by open reading frames 3 and 4 of the genome of Lelystad virus (Arteriviridae) are structural proteins of the virion. J. Virol. 1996, 70:4767-4772.
59. Vanhee M., Van Breedam W., Costers S., Geldhof M., Noppe Y., Nauwynck H. Characterization of antigenic regions in the porcine reproductive and respiratory syndrome virus by the use of peptide-specific serum antibodies. Vaccine 2011, 29:4794-4804.
60. Vu H.L., Kwon B., Yoon K.J., Laegreid W.W., Pattnaik A.K., Osorio F.A. Immune evasion of porcine reproductive and respiratory syndrome virus through glycan shielding involves both glycoprotein 5 as well as glycoprotein 3. J. Virol 2011.
61. 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. Lelystad virus, the cause of porcine epidemic abortion and respiratory syndrome: a review of mystery swine disease research at Lelystad. Vet. Microbiol. 1992, 33:185-193.
62. 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.
63. 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.
64. Wu W.H., Fang Y., Farwell R., Steffen-Bien M., Rowland R.R., Christopher-Hennings J., Nelson E.A. A 10-kDa structural protein of porcine reproductive and respiratory syndrome virus encoded by ORF2b. Virology 2001, 287:183-191.
65. Yang L., Jiang J., Drouin L.M., Agbandje-McKenna M., Chen C., Qiao C., Pu D., Hu X., Wang D.Z., Li J., Xiao X. A myocardium tropic adeno-associated virus (AAV) evolved by DNA shuffling and in vivo selection. Proc. Natl. Acad. Sci. USA 2009, 106:3946-3951.
66. Yu X., Chen N., Wang L., Wu J., Zhou Z., Ni J., Li X., Zhai X., Shi J., Tian K. New genomic characteristics of highly pathogenic porcine reproductive and respiratory syndrome viruses do not lead to significant changes in pathogenicity. Vet. Microbiol 2012.
67. Zhang J.H., Dawes G., Stemmer W.P. Directed evolution of a fucosidase from a galactosidase by DNA shuffling and screening. Proc. Natl. Acad. Sci. USA 1997, 94:4504-4509.
68. Zhou L., Chen S., Zhang J., Zeng J., Guo X., Ge X., Zhang D., Yang H. Molecular variation analysis of porcine reproductive and respiratory syndrome virus in China. Virus Res. 2009, 145:97-105.
69. Zhou L., Yang H. Porcine reproductive and respiratory syndrome in China. Virus Res 2010.
70. Zhou L., Zhang J., Zeng J., Yin S., Li Y., Zheng L., Guo X., Ge X., Yang H. The 30-amino-acid deletion in the Nsp2 of highly pathogenic porcine reproductive and respiratory syndrome virus emerging in China is not related to its virulence. J. Virol. 2009, 83:5156-5167.
71. Zhou Y.J., An T.Q., He Y.X., Liu J.X., Qiu H.J., Wang Y.F., Tong G. Antigenic structure analysis of glycosylated protein 3 of porcine reproductive and respiratory syndrome virus. Virus Res. 2006, 118:98-104.
72. Zuckermann F.A., Garcia E.A., Luque I.D., Christopher-Hennings J., Doster A., Brito M., Osorio F. Assessment of the efficacy of commercial porcine reproductive and respiratory syndrome virus (PRRSV) vaccines based on measurement of serologic response, frequency of gamma-IFN-producing cells and virological parameters of protection upon challenge. Vet. Microbiol. 2007, 123:69-85.