Broadly neutralizing antibodies against the rapidly evolving porcine reproductive and respiratory syndrome virus

Virus Research

Volumn 203, Issue , 2015, Pages 56-65

  Robinson, Sally R ^a   Li, Juan ^a,c   Nelson, Eric A ^b   Murtaugh, Michael P ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b SOUTH DAKOTA STATE UNIVERSITY   (United States)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Immunity; Infectious disease; Macrophage; PRRSV; Swine

Indexed keywords

IMMUNOGLOBULIN; MEMBRANE PROTEIN; NEUTRALIZING ANTIBODY; IMMUNOGLOBULIN G; VIRUS ANTIBODY;

ANIMAL CELL; ANTIBODY PRODUCTION; ANTIBODY TITER; ARTICLE; CELL CULTURE; CONTROLLED STUDY; CROSS PROTECTION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENOTYPE; LUNG ALVEOLUS MACROPHAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN ISOLATION; VIROGENESIS; VIRUS CONCENTRATION; VIRUS NEUTRALIZATION; VIRUS STRAIN; ANIMAL; BLOOD; CROSS REACTION; IMMUNOLOGY; PIG; SERODIAGNOSIS; VIROLOGY;

PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; RNA VIRUSES; SUIDAE; SUS;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CELLS, CULTURED; CROSS PROTECTION; CROSS REACTIONS; IMMUNOGLOBULIN G; MACROPHAGES, ALVEOLAR; NEUTRALIZATION TESTS; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SWINE;

EID: 84930816565     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2015.03.016     Document Type: Article

References (59)

1. Andrewes C.H., Elford W.J. Observations on anti-phage sera. I. The percentage law. Br. J. Exp. Pathol. 1933, 14(6):367-376.
2. Bautista E.M., Goyal S.M., Yoon I.J., Joo H.S., Collins J.E. Comparison of porcine alveolar macrophages and CL 2621 for the detection of porcine reproductive and respiratory syndrome (PRRS) virus and anti-PRRS antibody. J. Vet. Diagn. Invest. 1993, 5(2):163-165.
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. Diagn. Invest. 1992, 4(2):127-133.
4. Binjawadagi B., Dwivedi V., Manickam C., Ouyang K., Wu Y., Lee L.J., Torrelles J.B., Renukaradhya G.J. Adjuvanted poly(lactic-co-glycolic) acid nanoparticle-entrapped inactivated porcine reproductive and respiratory syndrome virus vaccine elicits cross-protective immune response in pigs. Int. J. Nanomed. 2014, 9:679-694.
5. Burton D.R., Poignard P., Stanfield R.L., Wilson I.A. Broadly neutralizing antibodies present new prospects to counter highly antigenically diverse viruses. Science 2012, 337(6091):183-186.
6. Calvert J.G., Slade D.E., Shields S.L., Jolie R., Mannan R.M., Ankenbauer R.G., Welch S.K. CD163 expression confers susceptibility to porcine reproductive and respiratory syndrome viruses. J. Virol. 2007, 81(14):7371-7379.
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. 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. Invest. 1992, 4(2):117-126.
9. Darwich L., Diaz I., Mateu E. Certainties, doubts and hypotheses in porcine reproductive and respiratory syndrome virus immunobiology. Virus Res. 2010, 154(1-2):123-132.
10. 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(4):1731-1740.
11. de Abin M.F., Spronk G., Wagner M., Fitzsimmons M., Abrahante J.E., Murtaugh M.P. Comparative infection efficiency of porcine reproductive and respiratory syndrome virus field isolates on MA104 cells and porcine alveolar macrophages. Can. J. Vet. Res. 2009, 73(3):200-204.
12. Halstead S.B. Neutralization and antibody-dependent enhancement of dengue viruses. Advances in Virus Research 2003, vol. 60:421-467. Academic Press.
13. Islam Z.U., Bishop S.C., Savill N.J., Rowland R.R., Lunney J.K., Trible B., Doeschl-Wilson A.B. Quantitative analysis of porcine reproductive and respiratory syndrome (PRRS) viremia profiles from experimental infection: a statistical modelling approach. PLOS ONE 2014, 8(12):e83567.
14. Karush F. The affinity of antibody: range, variability, and the role of multivalence. Immunoglobulins 1978, 85-116. Plenum Press, New York. G.W. Litman, R.A. Good (Eds.).
15. Kim H.S., Kwang J., Yoon I.J., Joo H.S., Frey M.L. Enhanced replication of porcine reproductive and respiratory syndrome (PRRS) virus in a homogeneous subpopulation of MA-104 cell line. Arch. Virol. 1993, 133(3-4):477-483.
16. Kim W.-I., Lee D.-S., Johnson W., Roof M., Cha S.-H., Yoon K.-J. Effect of genotypic and biotypic differences among PRRS viruses on the serologic assessment of pigs for virus infection. Vet. Microbiol. 2007, 123(1-3):1-14.
17. Klasse P.J., Moore J.P. Quantitative model of antibody- and soluble CD4-mediated neutralization of primary isolates and T-cell line-adapted strains of human immunodeficiency virus type 1. J. Virol. 1996, 70(6):3668-3677.
18. Klasse P.J., Sattentau Q.J. Occupancy and mechanism in antibody-mediated neutralization of animal viruses. J. Gen. Virol. 2002, 83(Pt 9):2091-2108.
19. Klinge K.L., Vaughn E.M., Roof M.B., Bautista E.M., Murtaugh M.P. Age-dependent resistance to porcine reproductive and respiratory syndrome virus replication in swine. Virol. J. 2009, 6:177.
20. Li J., Murtaugh M.P. Dissociation of porcine reproductive and respiratory syndrome virus neutralization from antibodies specific to major envelope protein surface epitopes. Virology 2012, 433(2):367-376.
21. Li X., Galliher-Beckley A., Pappan L., Trible B., Kerrigan M., Beck A., Hesse R., Blecha F., Nietfeld J.C., Rowland R.R., Shi J. Comparison of host immune responses to homologous and heterologous type II porcine reproductive and respiratory syndrome virus (PRRSV) challenge in vaccinated and unvaccinated pigs. Biomed. Res. Int. 2014, 2014:416727.
22. Liao H.X., Lynch R., Zhou T., Gao F., Alam S.M., Boyd S.D., Fire A.Z., Roskin K.M., Schramm C.A., Zhang Z., Zhu J., Shapiro L., Mullikin J.C., Gnanakaran S., Hraber P., Wiehe K., Kelsoe G., Yang G., Xia S.M., Montefiori D.C., Parks R., Lloyd K.E., Scearce R.M., Soderberg K.A., Cohen M., Kamanga G., Louder M.K., Tran L.M., Chen Y., Cai F., Chen S., Moquin S., Du X., Joyce M.G., Srivatsan S., Zhang B., Zheng A., Shaw G.M., Hahn B.H., Kepler T.B., Korber B.T., Kwong P.D., Mascola J.R., Haynes B.F. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 2013, 496(7446):469-476.
23. Lopez O.J., Oliveira M.F., Garcia E.A., Kwon B.J., Doster A., Osorio F.A. 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(3):269-275.
24. Ludemann L.R., Lager K.M. Porcine reproductive and respiratory syndrome. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals (Mammals, Birds and Bees), Paris 2010, 1-13. sixth ed. OIE, W.O.F.A.H. (Eds.).
25. Martinez-Lobo F.J., Diez-Fuertes F., Simarro I., Castro J.M., Prieto C. Porcine reproductive and respiratory syndrome virus isolates differ in their susceptibility to neutralization. Vaccine 2011, 29(40):6928-6940.
26. McEwan W.A., Hauler F., Williams C.R., Bidgood S.R., Mallery D.L., Crowther R.A., James L.C. Regulation of virus neutralization and the persistent fraction by TRIM21. J. Virol. 2012, 86(16):8482-8491.
27. Molina R.M., Cha S.H., Chittick W., Lawson S., Murtaugh M.P., Nelson E.A., Christopher-Hennings J., Yoon K.J., Evans R., Rowland R.R.R., Zimmerman J.J. Immune response against porcine reproductive and respiratory syndrome virus during acute and chronic infection. Vet. Immunol. Immunopathol. 2008, 126:283-292.
28. Mulupuri P., Zimmerman J.J., Hermann J., Johnson C.R., Cano J.P., Yu W., Dee S.A., Murtaugh M.P. Antigen-specific B-cell responses to porcine reproductive and respiratory virus infection. J. Virol. 2008, 82:358-370.
29. 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(8):1451-1460.
30. Murtaugh M.P., Genzow M. Immunological solutions for treatment and prevention of porcine reproductive and respiratory syndrome (PRRS). Vaccine 2011, 29(46):8192-8204.
31. 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.
32. 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(1):270-280.
33. 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. Invest. 1994, 6(4):410-415.
34. Nishimura Y., Igarashi T., Haigwood N., Sadjadpour R., Plishka R.J., Buckler-White A., Shibata R., Martin M.A. Determination of a statistically valid neutralization titer in plasma that confers protection against simian-human immunodeficiency virus challenge following passive transfer of high-titered neutralizing antibodies. J. Virol. 2002, 76(5):2123-2130.
35. Osorio F.A., Galeota J.A., Nelson E., Brodersen B., Doster A., Wills R., Zuckermann F., Laegreid W.W. Passive transfer of virus-specific antibodies confers protection against reproductive failure induced by a virulent strain of porcine reproductive and respiratory syndrome virus and establishes sterilizing immunity. Virology 2002, 302(1):9-20.
36. Pestka J.M., Zeisel M.B., Bläser E., Schürmann P., Bartosch B., Cosset F.-L., Patel A.H., Meisel H., Baumert J., Viazov S., Rispeter K., Blum H.E., Roggendorf M., Baumert T.F. Rapid induction of virus-neutralizing antibodies and viral clearance in a single-source outbreak of hepatitis C. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(14):6025-6030.
37. Prather R.S., Rowland R.R., Ewen C., Trible B., Kerrigan M., Bawa B., Teson J.M., Mao J., Lee K., Samuel M.S., Whitworth K.M., Murphy C.N., Egen T., Green J.A. An intact sialoadhesin (Sn/SIGLEC1/CD169) is not required for attachment/internalization of the Porcine reproductive and respiratory syndrome virus. J. Virol. 2013, 87(17):9538-9546.
38. Reed L.J., Muench H. A simple method of estimating fifty per cent endpoints. Am. J. Epidemiol. 1938, 27(3):493-497.
39. Reverberi R., Reverberi L. Factors affecting the antigen-antibody reaction. Blood Transfus. 2007, 5(4):227-240.
40. Robinson S.R., Figueiredo M.C., Abrahante J.E., Murtaugh M.P. Immune response to ORF5a protein immunization is not protective against porcine reproductive and respiratory syndrome virus infection. Vet. Microbiol. 2013, 164:281-285.
41. Roehrig J.T., Hombach J., Barrett A.D. Guidelines for plaque-reduction neutralization testing of human antibodies to dengue viruses. Viral Immunol. 2008, 21(2):123-132.
42. Schwartz E.J., Smith R.J. Identifying the conditions under which antibodies protect against infection by equine infectious anemia virus. Vaccines 2014, 2(2):397-421.
43. Shingai M., Donau O.K., Plishka R.J., Buckler-White A., Mascola J.R., Nabel G.J., Nason M.C., Montefiori D., Moldt B., Poignard P., Diskin R., Bjorkman P.J., Eckhaus M.A., Klein F., Mouquet H., Cetrulo Lorenzi J.C., Gazumyan A., Burton D.R., Nussenzweig M.C., Martin M.A., Nishimura Y. Passive transfer of modest titers of potent and broadly neutralizing anti-HIV monoclonal antibodies block SHIV infection in macaques. J. Exp. Med. 2014, 211(10):2061-2074.
44. Simek M.D., Rida W., Priddy F.H., Pung P., Carrow E., Laufer D.S., Lehrman J.K., Boaz M., Tarragona-Fiol T., Miiro G., Birungi J., Pozniak A., McPhee D.A., Manigart O., Karita E., Inwoley A., Jaoko W., DeHovitz J., Bekker L.-G., Pitisuttithum P., Paris R., Walker L.M., Poignard P., Wrin T., Fast P.E., Burton D.R., Koff W.C. Human Immunodeficiency virus type 1 elite neutralizers: individuals with broad and potent neutralizing activity identified by using a high-throughput neutralization assay together with an analytical selection algorithm. J. Virol. 2009, 83(14):7337-7348.
45. Smith D.M., Strain M.C., Frost S.D.W., Pillai S.K., Wong J.K., Wrin T., Liu Y., Petropolous C.J., Daar E.S., Little S.J., Richman D.D. Lack of neutralizing antibody response to HIV-1 predisposes to superinfection. Virology 2006, 355(1):1-5.
46. To K.K., Zhang A.J., Hung I.F., Xu T., Ip W.C., Wong R.T., Ng J.C., Chan J.F., Chan K.H., Yuen K.Y. High titer and avidity of nonneutralizing antibodies against influenza vaccine antigen are associated with severe influenza. Clin. Vaccine Immunol. 2012, 19(7):1012-1018.
47. Tyrrell D.A. Neutralization of viruses by homologous immune serum. II. Theoretical study of the equilibrium state. J. Exp. Med. 1953, 97(6):863-870.
48. 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(7):1659-1667.
49. Van Gorp H., Van Breedam W., Delputte P.L., Nauwynck H.J. Sialoadhesin and CD163 join forces during entry of the porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 2008, 89(Pt 12):2943-2953.
50. Vincent A.L., Ma W., Lager K.M., Richt J.A., Janke B.H., Sandbulte M.R., Gauger P.C., Loving C.L., Webby R.J., Garcia-Sastre A. Live attenuated influenza vaccine provides superior protection from heterologous infection in pigs with maternal antibodies without inducing vaccine-associated enhanced respiratory disease. J. Virol. 2012, 86(19):10597-10605.
51. von Hahn T., Yoon J.C., Alter H., Rice C.M., Rehermann B., Balfe P., McKeating J.A. Hepatitis C virus continuously escapes from neutralizing antibody and T-cell responses during chronic infection in vivo. Gastroenterology 2007, 132(2):667-678.
52. Walker L.M., Phogat S.K., Chan-Hui P.Y., Wagner D., Phung P., Goss J.L., Wrin T., Simek M.D., Fling S., Mitcham J.L., Lehrman J.K., Priddy F.H., Olsen O.A., Frey S.M., Hammond P.W., Kaminsky S., Zamb T., Moyle M., Koff W.C., Poignard P., Burton D.R. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 2009, 326(5950):285-289.
53. Wei X., Decker J.M., Wang S., Hui H., Kappes J.C., Wu X., Salazar-Gonzalez J.F., Salazar M.G., Kilby J.M., Saag M.S., Komarova N.L., Nowak M.A., Hahn B.H., Kwong P.D., Shaw G.M. Antibody neutralization and escape by HIV-1. Nature 2003, 422(6929):307-312.
54. Welch S.K., Calvert J.G. A brief review of CD163 and its role in PRRSV infection. Virus Res. 2010, 154(1-2):98-103.
55. 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. Invest. 1992, 4(2):134-138.
56. 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(3):121-130.
57. Willey R., Nason M.C., Nishimura Y., Follmann D.A., Martin M.A. Neutralizing antibody titers conferring protection to macaques from a simian/human immunodeficiency virus challenge using the TZM-bl assay. AIDS Res. Hum. Retroviruses 2010, 26(1):89-98.
58. Yoon K.J., Wu L.L., Zimmerman J.J., Hill H.T., Platt K.B. Antibody-dependent enhancement (ADE) of porcine reproductive and respiratory syndrome virus (PRRSV) infection in pigs. Viral Immunol. 1996, 9(1):51-63.
59. Yoon K.J., Wu L.L., Zimmerman J.J., Platt K.B. Field isolates of porcine reproductive and respiratory syndrome virus (PRRSV) vary in their susceptibility to antibody dependent enhancement. Vet. Microbiol. 1997, 55:277-287.