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 Immunology

Volumn 23, Issue 4, 2010, Pages 403-413

  Vanhee, Merijn ^a   Costers, Sarah ^a   Van Breedam, Wander ^a   Geldhof, Marc F ^a   Van Doorsselaere, Jan ^b   Nauwynck, Hans J ^a  

^a GHENT UNIVERSITY   (Belgium)

^b KATHO Catholic University   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; GLYCOPROTEIN GP4; NEUTRALIZING ANTIBODY; PROTEIN ORF4; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ARTERIVIRUS INFECTION; ARTICLE; CONTROLLED STUDY; CROSS REACTION; EUROPE; GENE SEQUENCE; HUMAN; HUMAN CELL; LELYSTAD VIRUS; LUNG ALVEOLUS MACROPHAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; SERODIAGNOSIS; SWINE; VIRAL GENETICS; VIREMIA; VIRUS STRAIN;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY SPECIFICITY; CROSS REACTIONS; EPITOPES; GENETIC VARIATION; MOLECULAR SEQUENCE DATA; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SEQUENCE ALIGNMENT; SWINE; VIRAL STRUCTURAL PROTEINS;

LELYSTAD VIRUS; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUIDAE; SUS;

EID: 77955855300     PISSN: 08828245     EISSN: None     Source Type: Journal    
DOI: 10.1089/vim.2010.0025     Document Type: Article

References (56)

1. Allende R, Lewis TL, Lu Z, et al.: North American and European porcine reproductive and respiratory syndrome viruses differ in non-structural protein coding regions. J Gen Virol 1999;80(Pt 2):307-315.
2. Calvert JG, Slade DE, Shields SL, Jolie R, Mannan RM, Ankenbauer RG, and Welch SK: CD163 expression confers susceptibility to porcine reproductive and respiratory syndrome viruses. J Virol 2007;81:7371-7379.
3. Cancel-Tirado SM, Evans RB, and Yoon KJ: 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.
4. Chen C, and Okayama H: High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 1987;7: 2745-2752.
5. Christianson WT, Collins JE, Benfield DA, et al.: Experimental reproduction of swine infertility and respiratory syndrome in pregnant sows. Am J Vet Res 1992;53:485-488.
6. Collins JE, Benfield DA, Christianson WT, 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 Invest 1992;4:117-126.
7. Costers S, Lefebvre DJ, Van Doorsselaere J, Vanhee M, Delputte PL, and Nauwynck HJ: GP4 of porcine reproductive and respiratory syndrome virus contains a neutralizing epitope that is susceptible to immunoselection in vitro. Arch Virol 2010;155:371-378.
8. de Lima M, Ansari IH, Das PB, Ku BJ, Martinez-Lobo FJ, Pattnaik AK, and Osorio FA: GP3 is a structural component of the PRRSV type II (US) virion. Virology 2009;390:31-36.
9. de Lima M, Pattnaik AK, Flores EF, and Osorio FA: 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.
10. Delputte PL, Meerts P, Costers S, and Nauwynck HJ: Effect of virus-specific antibodies on attachment, internalization and infection of porcine reproductive and respiratory syndrome virus in primary macrophages. Vet Immunol Immunopathol 2004;102:179-188.
11. Diaz I, Darwich L, Pappaterra G, Pujols J, and Mateu E: Immune responses of pigs after experimental infection with a European strain of porcine reproductive and respiratory syndrome virus. J Gen Virol 2005;86:1943-1951.
12. Drew TW, Lowings JP, and 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.
13. Duan X, Nauwynck HJ, and Pensaert MB: 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.
14. Duan X, Nauwynck HJ, and Pensaert MB: Virus quantification and identification of cellular targets in the lungs and lymphoid tissues of pigs at different time intervals after inoculation with porcine reproductive and respiratory syndrome virus (PRRSV). Vet Microbiol 1997;56:9-19.
15. Forsberg R, Storgaard T, Nielsen HS, et al.: 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.
16. Geysen MH, Meloen RH, and Barteling SJ: Use of peptide synthesis to probe viral antigens for epitopes to a resolution of a single amino acid. Proc Natl Acad Sci USA 1984; 81:3398-4002.
17. Gonin P, Pirzadeh B, Gagnon CA, and Dea S: Seroneutralization of porcine reproductive and respiratory syndrome virus correlates with antibody response to the GP5 major envelope glycoprotein. J Vet Diagn Invest 1999;11:20-26.
18. Gorbalenya AE, Enjuanes L, Ziebuhr J, and Snijder EJ: Nidovirales: evolving the largest RNA virus genome. Virus Res 2006;117:17-37.
19. Kim HS, Kwang J, Yoon IJ, Joo HS, and Frey ML: Enhanced replication of porcine reproductive and respiratory syndrome (PRRS) virus in a homogeneous subpopulation of MA-104 cell line. Arch Virol 1993;133:477-483.
20. Kim JK, Fahad AM, Shanmukhappa K, and Kapil S: Defining the cellular target(s) of porcine reproductive and respiratory syndrome virus blocking monoclonal antibody 7G10. J Virol 2006;80:689-696.
21. Klasse PJ, and Sattentau QJ: Occupancy and mechanism in antibody-mediated neutralization of animal viruses. J Gen Virol 2002;83:2091-2108.
22. Labarque GG, Nauwynck HJ, Van Reeth K, and Pensaert MB: Effect of cellular changes and onset of humoral immunity on the replication of porcine reproductive and respiratory syndrome virus in the lungs of pigs. J Gen Virol 2000; 81:1327-1334.
23. Loemba HD, Mounir S, Mardassi H, Archambault D, and 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.
24. Lopez OJ, Oliveira MF, Garcia EA, Kwon BJ, Doster A, and Osorio FA: Protection against porcine reproductive and respiratory syndrome virus (PRRSV) infection through passive transfer of PRRSV-neutralizing antibodies is dose dependent. Clin Vaccine Immunol 2007;14:269-275.
25. Lopez OJ, and Osorio FA: Role of neutralizing antibodies in PRRSV protective immunity. Vet Immunol Immunopathol 2004;102:155-163.
26. Mardassi H, Mounir S, and 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.
27. Meulenberg JJ, Petersen-den Besten A, De Kluyver EP, Moormann RJ, Schaaper WM, and Wensvoort G: Characterization of proteins encoded by ORFs 2 to 7 of Lelystad virus. Virology 1995;206:155-163.
28. Meulenberg JJ, van Nieuwstadt AP, van Essen-Zandbergen A, and Langeveld JP: Posttranslational processing and identification of a neutralization domain of the GP4 protein encoded by ORF4 of Lelystad virus. J Virol 1997;71: 6061-6067.
29. Mulupuri P, Zimmerman JJ, Hermann J, et al.: Antigenspecific B-cell responses to porcine reproductive and respiratory syndrome virus infection. J Virol 2008;82:358-370.
30. Nelsen CJ, Murtaugh MP, and Faaberg KS: Porcine reproductive and respiratory syndrome virus comparison: divergent evolution on two continents. J Virol 1999;73:270-280.
31. Nelson EA, Christopher-Hennings J, and Benfield DA: Serum immune responses to the proteins of porcine reproductive and respiratory syndrome (PRRS) virus. J Vet Diagn Invest 1994;6:410-415.
32. Oleksiewicz MB, Botner A, Toft P, Grubbe T, Nielsen J, Kamstrup S, and Storgaard T: 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 2000;267:135-140.
33. Oleksiewicz MB, Botner A, Toft P, Normann P, and Storgaard T: 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 2001;75:3277-3290.
34. Oleksiewicz MB, Stadejek T, Mackiewicz Z, Porowski M, and Pejsak Z: Discriminating between serological responses to European-genotype live vaccine and European-genotype field strains of porcine reproductive and respiratory syndrome virus (PRRSV) by peptide ELISA. J Virol Methods 2005;129:134-144.
35. Ostrowski M, Galeota JA, Jar AM, Platt KB, Osorio FA, and Lopez OJ: Identification of neutralizing and nonneutralizing epitopes in the porcine reproductive and respiratory syndrome virus GP5 ectodomain. J Virol 2002;76: 4241-4250.
36. Pirzadeh B, and Dea S: Monoclonal antibodies to the ORF5 product of porcine reproductive and respiratory syndrome virus define linear neutralizing determinants. J Gen Virol 1997;78(Pt 8):1867-1873.
37. Plagemann PG, Rowland RR, and Faaberg KS: 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.
38. Reading SA, and Dimmock NJ: Neutralization of animal virus infectivity by antibody. Arch Virol 2007;152:1047-1059.
39. Snijder EJ, and Meulenberg JJ: The molecular biology of arteriviruses. J Gen Virol 1998;79:961-979.
40. Stadejek T, Oleksiewicz MB, Scherbakov AV, Timina AM, Krabbe JS, Chabros K, and Potapchuk D: Definition of subtypes in the European genotype of porcine reproductive and respiratory syndrome virus: nucleocapsid characteristics and geographical distribution in Europe. Arch Virol 2008;153:1479-1488.
41. Terpstra C, Wensvoort G, and Pol JM: Experimental reproduction of porcine epidemic abortion and respiratory syndrome (mystery swine disease) by infection with Lelystad virus: Koch's postulates fulfilled. Vet Q 1991;13:131-136.
42. Thacker EL: Immunology of the porcine respiratory disease complex. Vet Clin North Am Food Anim Pract 2001; 17:551-565.
43. Van Gorp H, Van Breedam W, Delputte PL, and Nauwynck HJ: Sialoadhesin and CD163 join forces during entry of the porcine reproductive and respiratory syndrome virus. J Gen Virol 2008;89:2943-2953.
44. Van Gucht S, Labarque G, and Van Reeth K: The combination of PRRS virus and bacterial endotoxin as a model for multifactorial respiratory disease in pigs. Vet Immunol Immunopathol 2004;102:165-178.
45. van Nieuwstadt AP, Meulenberg JJ, van Essen-Zanbergen A, Petersen-den Besten A, Bende RJ, Moormann RJ, and 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.
46. Vanderheijden N, Delputte PL, Favoree, HW, Vandekerckhove J, Van Damme J, van Woensel PA, and Nauwynck HJ: Involvement of sialoadhesin in entry of porcine reproductive and respiratory syndrome virus into porcine alveolar macrophages. J Virol 2003;77:8207-8215.
47. Vanhee M, Delputte PL, Delrue I, Geldhof MF, and Nauwynck HJ: Development of an experimental inactivated PRRSV vaccine that induces virus-neutralizing antibodies. Vet Res 2009;40:63.
48. Weiland E, Wieczorek-Krohmer M, Kohl D, Conzelmann KK, and Weiland F: 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 1999;66:171-186.
49. Wensvoort G, Terpstra C, Pol JM, et al.: Mystery swine disease in The Netherlands: the isolation of Lelystad virus. Vet Q 1991;13:121-130.
50. Wieczorek-Krohmer M, Weiland F, Conzelmann K, et al.: Porcine reproductive and respiratory syndrome virus (PRRSV): monoclonal antibodies detect common epitopes on two viral proteins of European and U.S. isolates. Vet Microbiol 1996;51:257-266.
51. Wissink EH, van Wijk HA, Kroese MV, Weiland E, Meulenberg JJ, Rottier PJ, and van Rijn PA: The major envelope protein, GP5, of a European porcine reproductive and respiratory syndrome virus contains a neutralization epitope in its N-terminal ectodomain. J Gen Virol 2003;84:1535-1543.
52. Wu WH, Fang Y, Farwell R, Steffen-Bien M, Rowland RR, Christopher-Hennings J, and Nelson EA: A 10-kDa structural protein of porcine reproductive and respiratory syndrome virus encoded by ORF2b. Virology 2001;287:183-191.
53. Yang L, Frey ML, Yoon KJ, Zimmerman JJ, and Platt KB: 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 2000;145:1599-1619.
54. Yoon IJ, Joo HS, Goyal SM, and Molitor TW: A modified serum neutralization test for the detection of antibody to porcine reproductive and respiratory syndrome virus in swine sera. J Vet Diagn Invest 1994;6:289-292.
55. Yoon KJ, Zimmerman JJ, Swenson SL, et al.: Characterization of the humoral immune response to porcine reproductive and respiratory syndrome (PRRS) virus infection. J Vet Diagn Invest 1995;7:305-312.
56. Zhang Y, Sharma RD, and Paul PS: Monoclonal antibodies against conformationally dependent epitopes on porcine reproductive and respiratory syndrome virus. Vet Microbiol 1998;63:125-136.