Broadening the Heterologous Cross-Neutralizing Antibody Inducing Ability of Porcine Reproductive and Respiratory Syndrome Virus by Breeding the GP4 or M genes

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

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

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

^b CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

NEUTRALIZING ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIVIRUS; ARTERIVIRUS INFECTION; ARTICLE; CHIMERA; CONTROLLED STUDY; DNA LIBRARY; DNA SHUFFLING; EXPERIMENTAL PIG; GP4 GENE; IN VITRO STUDY; IN VIVO STUDY; M GENE; MOLECULAR CLONING; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCE ANALYSIS; VIRUS GENE; VIRUS GENOME; VIRUS NEUTRALIZATION; VIRUS REPLICATION; VIRUS STRAIN;

ANIMALS; ANTIBODIES, NEUTRALIZING; BASE SEQUENCE; CELL LINE; DNA, COMPLEMENTARY; GENES, VIRAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SEQUENCE HOMOLOGY, NUCLEIC ACID; SWINE;

PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUIDAE;

EID: 84879486470     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066645     Document Type: Article

References (79)

1. Wensvoort G, de Kluyver EP, Pol JM, Wagenaar F, Moormann RJ, et al. (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.
2. Neumann EJ, Kliebenstein JB, Johnson CD, Mabry JW, Bush EJ, et al. (2005) Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States. J Am Vet Med Assoc 227: 385-392.
3. Pejsak Z, Stadejek T, Markowska-Daniel I, (1997) Clinical signs and economic losses caused by porcine reproductive and respiratory syndrome virus in a large breeding farm. Vet Microbiol 55: 317-322.
4. Garner MG, Whan IF, Gard GP, Phillips D, (2001) The expected economic impact of selected exotic diseases on the pig industry of Australia. Rev Sci Tech 20: 671-685.
5. Lunney JK, Benfield DA, Rowland RR, (2010) Porcine reproductive and respiratory syndrome virus: an update on an emerging and re-emerging viral disease of swine. Virus Res 154: 1-6.
6. Keffaber K (1989) Reproductive failure of unknown etiology. Am Assoc Swine Pract Newslett 1, 9.
7. Wensvoort G, Terpstra C, Pol JM, ter Laak EA, Bloemraad M, et al. (1991) Mystery swine disease in The Netherlands: the isolation of Lelystad virus. Vet Q 13: 121-130.
8. Tian K, Yu X, Zhao T, Feng Y, Cao Z, et al. (2007) Emergence of fatal PRRSV variants: unparalleled outbreaks of atypical PRRS in China and molecular dissection of the unique hallmark. PLoS ONE 2: e526.
9. Zhou L, Zhang J, Zeng J, Yin S, Li Y, et al. (2009) 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 83: 5156-5167.
10. Guo B, Lager KM, Henningson JN, Miller LC, Schlink SN, et al. (2013) Experimental infection of United States swine with a Chinese highly pathogenic strain of porcine reproductive and respiratory syndrome virus. Virology 435: 372-384.
11. Cavanagh D, (1997) Nidovirales: a new order comprising Coronaviridae and Arteriviridae. Arch Virol 142: 629-633.
12. Benfield DA, Nelson E, Collins JE, Harris L, Goyal SM, et al. (1992) Characterization of swine infertility and respiratory syndrome (SIRS) virus (isolate ATCC VR-2332). J Vet Diagn Invest 4: 127-133.
13. Ropp SL, Wees CE, Fang Y, Nelson EA, Rossow KD, et al. (2004) Characterization of emerging European-like porcine reproductive and respiratory syndrome virus isolates in the United States. J Virol 78: 3684-3703.
14. Nelsen CJ, Murtaugh MP, Faaberg KS, (1999) Porcine reproductive and respiratory syndrome virus comparison: divergent evolution on two continents. J Virol 73: 270-280.
15. Han K, Seo HW, Oh Y, Kang I, Park C, et al. (2012) Comparison of the virulence of European and North American genotypes of porcine reproductive and respiratory syndrome virus in experimentally infected pigs. Vet J.
16. Forsberg R, Storgaard T, Nielsen HS, Oleksiewicz MB, Cordioli P, et al. (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.
17. Shi M, Lam TT, Hon CC, Murtaugh MP, Davies PR, et al. (2010) A Phylogeny-based Evolutionary, Demographical and Geographical Dissection of North American Type 2 Porcine Reproductive and Respiratory Syndrome Viruses. J Virol.
18. Kim WI, Yoon KJ, (2008) Molecular assessment of the role of envelope-associated structural proteins in cross neutralization among different PRRS viruses. Virus Genes 37: 380-391.
19. Kim WI, Kim JJ, Cha SH, Yoon KJ, (2008) Different biological characteristics of wild-type porcine reproductive and respiratory syndrome viruses and vaccine viruses and identification of the corresponding genetic determinants. J Clin Microbiol 46: 1758-1768.
20. Chang CC, Yoon KJ, Zimmerman JJ, Harmon KM, Dixon PM, et al. (2002) Evolution of porcine reproductive and respiratory syndrome virus during sequential passages in pigs. J Virol 76: 4750-4763.
21. Meng XJ, (2000) Heterogeneity of porcine reproductive and respiratory syndrome virus: implications for current vaccine efficacy and future vaccine development. Vet Microbiol 74: 309-329.
22. Dwivedi V, Manickam C, Patterson R, Dodson K, Murtaugh M, et al. (2011) Cross-protective immunity to porcine reproductive and respiratory syndrome virus by intranasal delivery of a live virus vaccine with a potent adjuvant. Vaccine.
23. Han K, Seo HW, Oh Y, Kang I, Park C, et al. (2012) Effects of North American porcine reproductive and respiratory syndrome virus (PRRSV)-based modified live vaccines on preimmunized sows artificially inseminated with European PRRSV-spiked semen. Clin Vaccine Immunol 19: 319-324.
24. Dwivedi V, Manickam C, Binjawadagi B, Joyappa D, Renukaradhya GJ, (2012) Biodegradable nanoparticle-entrapped vaccine induces cross-protective immune response against a virulent heterologous respiratory viral infection in pigs. PLoS One 7: e51794.
25. Murtaugh MP, Faaberg KS, Laber J, Elam M, Kapur V, (1998) Genetic variation in the PRRS virus. Adv Exp Med Biol 440: 787-794.
26. Fang Y, Schneider P, Zhang WP, Faaberg KS, Nelson EA, et al. (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.
27. Renukaradhya GJ, Dwivedi V, Manickam C, Binjawadagi B, Benfield D, (2012) Mucosal vaccines to prevent porcine reproductive and respiratory syndrome: a new perspective. Anim Health Res Rev 13: 21-37.
28. Conzelmann KK, Visser N, Van Woensel P, Thiel HJ, (1993) Molecular characterization of porcine reproductive and respiratory syndrome virus, a member of the arterivirus group. Virology 193: 329-339.
29. Meulenberg JJ, Hulst MM, de Meijer EJ, Moonen PL, den Besten A, et al. (1993) Lelystad virus, the causative agent of porcine epidemic abortion and respiratory syndrome (PEARS), is related to LDV and EAV. Virology 192: 62-72.
30. Snijder EJ, Meulenberg JJ, (1998) The molecular biology of arteriviruses. J Gen Virol 79 (Pt 5): 961-979.
31. Meulenberg JJ, Petersen-den Besten A, (1996) Identification and characterization of a sixth structural protein of Lelystad virus: the glycoprotein GP2 encoded by ORF2 is incorporated in virus particles. Virology 225: 44-51.
32. van Nieuwstadt AP, Meulenberg JJ, van Essen-Zanbergen A, Petersen-den Besten A, Bende RJ, et al. (1996) Proteins encoded by open reading frames 3 and 4 of the genome of Lelystad virus (Arteriviridae) are structural proteins of the virion. J Virol 70: 4767-4772.
33. Wu WH, Fang Y, Farwell R, Steffen-Bien M, Rowland RR, et al. (2001) A 10-kDa structural protein of porcine reproductive and respiratory syndrome virus encoded by ORF2b. Virology 287: 183-191.
34. Mardassi H, Mounir S, Dea S, (1995) Molecular analysis of the ORFs 3 to 7 of porcine reproductive and respiratory syndrome virus, Quebec reference strain. Arch Virol 140: 1405-1418.
35. Meulenberg JJ, Petersen-den Besten A, De Kluyver EP, Moormann RJ, Schaaper WM, et al. (1995) Characterization of proteins encoded by ORFs 2 to 7 of Lelystad virus. Virology 206: 155-163.
36. Nelson EA, Christopher-Hennings J, Benfield DA, (1995) Structural proteins of porcine reproductive and respiratory syndrome virus (PRRSV). Adv Exp Med Biol 380: 321-323.
37. Johnson CR, Griggs TF, Gnanandarajah JS, Murtaugh MP (2011) 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.
38. Firth AE, Zevenhoven-Dobbe JC, Wills NM, Go YY, Balasuriya UB, et al. (2011) Discovery of a small arterivirus gene that overlaps the GP5 coding sequence and is important for virus production. J Gen Virol 92: 1097-1106.
39. Dea S, Gagnon CA, 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.
40. Lee C, Bachand A, Murtaugh MP, Yoo D, (2004) Differential host cell gene expression regulated by the porcine reproductive and respiratory syndrome virus GP4 and GP5 glycoproteins. Vet Immunol Immunopathol 102: 189-198.
41. Wissink EH, Kroese MV, van Wijk HA, Rijsewijk FA, Meulenberg JJ, et al. (2005) Envelope protein requirements for the assembly of infectious virions of porcine reproductive and respiratory syndrome virus. J Virol 79: 12495-12506.
42. de Lima M, Ansari IH, Das PB, Ku BJ, Martinez-Lobo FJ, et al. (2009) GP3 is a structural component of the PRRSV type II (US) virion. Virology 390: 31-36.
43. Das PB, Vu HL, Dinh PX, Cooney JL, Kwon B, et al. (2011) Glycosylation of minor envelope glycoproteins of porcine reproductive and respiratory syndrome virus in infectious virus recovery, receptor interaction, and immune response. Virology 410: 385-394.
44. Tian D, Wei Z, Zevenhoven-Dobbe JC, Liu R, Tong G, et al. (2012) Arterivirus minor envelope proteins are a major determinant of viral tropism in cell culture. J Virol 86: 3701-3712.
45. Das PB, Dinh PX, Ansari IH, de Lima M, Osorio FA, et al. (2010) The minor envelope glycoproteins GP2a and GP4 of porcine reproductive and respiratory syndrome virus interact with the receptor CD163. J Virol 84: 1731-1740.
46. Du Y, Pattnaik AK, Song C, Yoo D, Li G, (2012) Glycosyl-phosphatidylinositol (GPI)-anchored membrane association of the porcine reproductive and respiratory syndrome virus GP4 glycoprotein and its co-localization with CD163 in lipid rafts. Virology 424: 18-32.
47. Vanhee M, Van Breedam W, Costers S, Geldhof M, Noppe Y, et al. (2011) Characterization of antigenic regions in the porcine reproductive and respiratory syndrome virus by the use of peptide-specific serum antibodies. Vaccine 29: 4794-4804.
48. Vanhee M, Costers S, Van Breedam W, Geldhof MF, Van Doorsselaere J, et al. (2010) A variable region in GP4 of European-type porcine reproductive and respiratory syndrome virus induces neutralizing antibodies against homologous but not heterologous virus strains. Viral Immunol 23: 403-413.
49. Weiland E, Wieczorek-Krohmer M, Kohl D, Conzelmann KK, Weiland F, (1999) Monoclonal antibodies to the GP5 of porcine reproductive and respiratory syndrome virus are more effective in virus neutralization than monoclonal antibodies to the GP4. Vet Microbiol 66: 171-186.
50. Costers S, Vanhee M, Van Breedam W, Van Doorsselaere J, Geldhof M, et al. (2010) GP4-specific neutralizing antibodies might be a driving force in PRRSV evolution. Virus Res 154: 104-113.
51. Wieringa R, de Vries AA, van der Meulen J, Godeke GJ, Onderwater JJ, et al. (2004) Structural protein requirements in equine arteritis virus assembly. J Virol 78: 13019-13027.
52. Mardassi H, Massie B, Dea S, (1996) Intracellular synthesis, processing, and transport of proteins encoded by ORFs 5 to 7 of porcine reproductive and respiratory syndrome virus. Virology 221: 98-112.
53. Yang L, Frey ML, Yoon KJ, Zimmerman JJ, Platt KB, (2000) Categorization of North American porcine reproductive and respiratory syndrome viruses: epitopic profiles of the N, M, GP5 and GP3 proteins and susceptibility to neutralization. Arch Virol 145: 1599-1619.
54. Jiang Y, Xiao S, Fang L, Yu X, Song Y, et al. (2006) DNA vaccines co-expressing GP5 and M proteins of porcine reproductive and respiratory syndrome virus (PRRSV) display enhanced immunogenicity. Vaccine 24: 2869-2879.
55. Cancel-Tirado SM, Evans RB, Yoon KJ, (2004) Monoclonal antibody analysis of porcine reproductive and respiratory syndrome virus epitopes associated with antibody-dependent enhancement and neutralization of virus infection. Vet Immunol Immunopathol 102: 249-262.
56. Soong NW, Nomura L, Pekrun K, Reed M, Sheppard L, et al. (2000) Molecular breeding of viruses. Nat Genet 25: 436-439.
57. Pekrun K, Shibata R, Igarashi T, Reed M, Sheppard L, et al. (2002) Evolution of a human immunodeficiency virus type 1 variant with enhanced replication in pig-tailed macaque cells by DNA shuffling. J Virol 76: 2924-2935.
58. Callison S, Hilt D, Jackwood M, (2005) Using DNA shuffling to create novel infectious bronchitis virus S1 genes: implications for S1 gene recombination. Virus Genes 31: 5-11.
59. Locher CP, Paidhungat M, Whalen RG, Punnonen J, (2005) DNA shuffling and screening strategies for improving vaccine efficacy. DNA Cell Biol 24: 256-263.
60. Apt D, Raviprakash K, Brinkman A, Semyonov A, Yang S, et al. (2006) Tetravalent neutralizing antibody response against four dengue serotypes by a single chimeric dengue envelope antigen. Vaccine 24: 335-344.
61. Li W, Asokan A, Wu Z, Van Dyke T, DiPrimio N, et al. (2008) Engineering and selection of shuffled AAV genomes: a new strategy for producing targeted biological nanoparticles. Mol Ther 16: 1252-1260.
62. Yang L, Jiang J, Drouin LM, Agbandje-McKenna M, Chen C, et al. (2009) A myocardium tropic adeno-associated virus (AAV) evolved by DNA shuffling and in vivo selection. Proc Natl Acad Sci U S A 106: 3946-3951.
63. Ni YY, Opriessnig T, Zhou L, Cao D, Huang YW, et al. (2013) Attenuation of porcine reproductive and respiratory syndrome virus by molecular breeding of virus envelope genes from genetically divergent strains. J Virol 87: 304-313.
64. Zhou L, Ni YY, Piñeyro P, Sanford B, Cossaboom C, et al. (2012) 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 434: 96-109.
65. Ni YY, Huang YW, Cao D, Opriessnig T, Meng XJ, (2011) 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 160: 264-273.
66. Shi M, Lam TT, Hon CC, Murtaugh MP, Davies PR, et al. (2010) Phylogeny-based evolutionary, demographical, and geographical dissection of North American type 2 porcine reproductive and respiratory syndrome viruses. J Virol 84: 8700-8711.
67. Truong HM, Lu Z, Kutish GF, Galeota J, Osorio FA, et al. (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.
68. Fang Y, Rowland RR, Roof M, Lunney JK, Christopher-Hennings J, et al. (2006) 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 80: 11447-11455.
69. Meng XJ, Paul PS, Halbur PG, Lum MA, (1996) 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 8: 374-381.
70. Meulenberg JJ, Bos-de Ruijter JN, Wensvoort G, Moormann RJ, (1998) An infectious cDNA clone of porcine reproductive and respiratory syndrome virus. Adv Exp Med Biol 440: 199-206.
71. Zhang JH, Dawes G, Stemmer WP, (1997) Directed evolution of a fucosidase from a galactosidase by DNA shuffling and screening. Proc Natl Acad Sci U S A 94: 4504-4509.
72. Chang CC, Chen TT, Cox BW, Dawes GN, Stemmer WP, et al. (1999) Evolution of a cytokine using DNA family shuffling. Nat Biotechnol 17: 793-797.
73. Opriessnig T, Halbur PG, Yoon KJ, Pogranichniy RM, Harmon KM, et al. (2002) 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 76: 11837-11844.
74. Huang YW, Meng XJ, (2010) Novel strategies and approaches to develop the next generation of vaccines against porcine reproductive and respiratory syndrome virus (PRRSV). Virus Res 154: 141-149.
75. Costers S, Lefebvre DJ, Van Doorsselaere J, Vanhee M, Delputte PL, et al. (2010) GP4 of porcine reproductive and respiratory syndrome virus contains a neutralizing epitope that is susceptible to immunoselection in vitro. Arch Virol 155: 371-378.
76. Dokland T, (2010) The structural biology of PRRSV. Virus Res 154: 86-97.
77. Li J, Murtaugh MP, (2012) Dissociation of porcine reproductive and respiratory syndrome virus neutralization from antibodies specific to major envelope protein surface epitopes. Virology 433: 367-376.
78. Burton DR, (2002) Antibodies, viruses and vaccines. Nat Rev Immunol 2: 706-713.
79. Lopez OJ, Oliveira MF, Garcia EA, Kwon BJ, Doster A, et al. (2007) Protection against porcine reproductive and respiratory syndrome virus (PRRSV) infection through passive transfer of PRRSV-neutralizing antibodies is dose dependent. Clin Vaccine Immunol 14: 269-275.