A GP5 Mosaic T-cell vaccine for porcine reproductive and respiratory syndrome virus is immunogenic and confers partial protection to pigs

Vaccine Reports

Volumn 6, Issue , 2016, Pages 77-85

  Cui, J ^a   O'Connell, C M ^a   Smith, J D ^a   Pan, Y ^b   Smyth, J A ^a   Verardi, P H ^a   Garmendia, A E ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b GUANGXI VETERINARY RESEARCH INSTITUTE   (China)

Author keywords

Mosaic T cell vaccine; PRRS; PRRSV; Swine

Indexed keywords

DNA VACCINE; EPITOPE; GAMMA INTERFERON; GP5 MOSAIC T LYMPHOCYTE VACCINE; INTERLEUKIN 10; MESSENGER RNA; UNCLASSIFIED DRUG; VIRUS RNA; VIRUS VACCINE;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; ELECTROPORATION; ESCHERICHIA COLI; GENE DOSAGE; GENE EXPRESSION; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PIG; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS; PRIORITY JOURNAL; PROPHYLAXIS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; VACCINATION; VACCINE IMMUNOGENICITY; VIRUS LOAD; WESTERN BLOTTING;

EID: 85019590429     PISSN: 24057843     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vacrep.2016.11.003     Document Type: Article

References (48)

1. Done, S.H., Paton, D.J., Porcine reproductive and respiratory syndrome: clinical disease, pathology and immunosuppression. Vet. Rec. 136:2 (1995), 32–35.
2. Bøtner, A., Diagnosis of PRRS veterinary. Microbiology 55:1–4 (1997), 295–301.
3. Holtkamp, D.J., Kliebenstein, J.B., Neumann, E.J., Zimmerman, J.J., Rotto, H.F., Yoder, T.K., Wang, C., Yeske, P.E., Mowrer, C.L., Haley, C.A., Assessment of the economic impact of porcine reproductive and respiratory syndrome virus on United States pork producers. J. Swine Health Prod. 21:2 (2013), 72–84.
4. Conzelmann, Karl-Klaus, Visser, Nico, Van Woensel, Peter, Thiel, Heinz-Jürgen, Molecular characterization of porcine reproductive and respiratory syndrome virus, a member of the arterivirus group. Virology 193:1 (1993), 329–339.
5. Snijder, E.J., Meulenberg, J., The molecular biology of arteriviruses. J. Gen. Virol. 79:Pt 5 (1998), 961–979 5.
6. Wensvoort, G., Terpstra, C., Pol, J.M.A., ter Laak, E.A., Bloemraad, M., de Kluyver, E.P., Kragten, C., van Buiten, L., den Besten, A., Wagenaar, F., Broekhuijsen, J.M., Moonen, P.L.J.M., Zetstra, T., de Boer, E.A., Tibben, H.J., de Jong, M.F., van ‘t Veld, P., Greenland, G.J.R., van Gennep, J.A., Th Voets, M., Verheijden, J.H.M., Braamskamp, J., Mystery swine disease in the Netherlands: the isolation of Lelystad virus. Vet. Q. 13:3 (1991), 121–130.
7. Collins, James E., Benfield, David A., Christianson, William T., Harris, Louis, Hennings, Jane C., Shaw, Daniel P., Goyal, Sagar M., McCullough, Sam., Morrison, Robert B., Joo, Han Soo, Gorcyca, David, Chladek, Dan, 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. 4:2 (1992), 117–126.
8. 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. 145:4 (2000), 659–688.
9. Meulenberg, J.J., PRRSV, the virus. Vet. Res. 31:1 (2000), 11–21.
10. Mateu, E., Martín, M., Vidal, D., Genetic diversity and phylogenetic analysis of glycoprotein 5 of European-type porcine reproductive and respiratory virus strains in Spain. J. Gen. Virol. 84:3 (2003), 529–534.
11. Kim, H.K., Yang, J.S., Moon, H.J., Park, S.J., Luo, Y., Lee, C.S., Song, D.S., Kang, B.K., Ann, S.K., Jun, C.H., Park, B.K., Genetic analysis of ORF5 of recent Korean porcine reproductive and respiratory syndrome viruses (PRRSVs) in viremic sera collected from MLV-vaccinating or non-vaccinating farms. J. Vet. Sci. 10:2 (2009), 121–130.
12. 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. 84:17 (2010), 8700–8711.
13. Brar, M.S., Shi, M., Ge, L., Carman, S., Murtaugh, M.P., Leung, F.C., Porcine reproductive and respiratory syndrome virus in Ontario, Canada 1999 to 2010: genetic diversity and restriction fragment length polymorphisms. J. Gen. Virol. 92:6 (2011), 1391–1397.
14. Martín-Valls, G.E., Kvisgaard, L.K., Tello, M., Darwich, L., Cortey, M., Burgara-Estrella, A.J., Hernández, 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. 88:6 (2014), 3170–3181.
15. 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. 147:12 (2002), 2327–2347.
16. 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. 76:9 (2002), 4241–4250.
17. Vashisht, K., Goldberg, T.L., Husmann, R.J., Schnitzlein, W., Zuckermann, F.A., Identification of immunodominant T-cell epitopes present in glycoprotein 5 of the North American Genotype of porcine reproductive and respiratory syndrome virus. Vaccine 26:36 (2008), 4747–4753.
18. Díaz, I., Pujols, J., Ganges, L., Gimeno, M., Darwich, L., Domingo, M., Mateu, E., In silico prediction and ex vivo evaluation of potential T-cell epitopes in glycoproteins 4 and 5 and nucleocapsid protein of genotype-I (European) of porcine reproductive and respiratory syndrome virus. Vaccine 27:41 (2009), 5603–5611.
19. Xia, P., Dang, Z., Qiu, H., Fan, X., Zhou, B., Cui, B., Chen, P., Function of PRRSV GP5 envelope protein by using pseudotyped virus. Vet. Microbiol. 138:3–4 (2009), 297–303.
20. Wu, F., Peng, K., Tian, J., Xu, X., Zhou, E., Chen, H., Immune response to Fc tagged GP5 glycoproteins of porcine reproductive and respiratory syndrome virus. Viral Immunol. 27:7 (2014), 343–349.
21. Ren, J.Q., Sun, W.C., Lu, H.J., Wen, S.B., Jing, J., Yan, F.L., Liu, H., Liu, C.X., Xiao, P.P., Chen, X., Du, S.W., Du, R., Jin, N.Y., Construction and immunogenicity of a DNA vaccine coexpressing GP3 and GP5 of Genotype-I porcine reproductive and respiratory syndrome virus. BMC Vet. Res., 10(1), 2014, 128.
22. Lee, J.A., Kwon, B., Osorio, F.A., Pattnaik, A.K., Lee, N.H., Lee, S.W., Park, S.Y., Song, C.S., Choi, I.S., Lee, J.B., Protective humoral immune response induced by an inactivated porcine reproductive and respiratory syndrome virus expressing the hypo-glycosylated glycoprotein 5. Vaccine 32:29 (2014), 3617–3622.
23. Tian, D., Ni, Y.Y., Zhou, L., Opriessnig, T., Cao, D., Piñeyro, P., Yugo, D.M., Overend, C., Cao, Q., Lynn Heffron, C., Halbur, P.G., Pearce, D.S., Calvert, J.G., Meng, X.J., Chimeric porcine reproductive and respiratory syndrome virus containing shuffled multiple envelope genes confers cross-protection in pigs. Virology 485 (2015), 402–413.
24. Meng, X.J., Paul, P.S., Halbur, P.G., Lum, M.A., Phylogenetic analyses of the putative M (ORF 6) and N (ORF 7) genes of porcine reproductive and respiratory syndrome virus (PRRSV): implication for the existence of two Genotypes of PRRSV in the U.S.A. and Europe. Arch. Virol. 140:4 (1995), 745–755.
25. 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. 123:1–3 (2007), 1–14.
26. Kimman, T.G., Cornelissen, L.A., Moormann, R.J., Rebel, J.M., Stockhofe-Zurwieden, N., Challenges for porcine reproductive and respiratory syndrome virus (PRRSV) vaccinology. Vaccine 27:28 (2009), 3704–3718.
27. Vu, H.L., Ma, F., Laegreid, W.W., Pattnaik, A.K., Steffen, D., Doster, A.R., Osorio, F.A., A synthetic porcine reproductive and respiratory syndrome virus strain confers unprecedented levels of heterologous protection. J. Virol. 89:23 (2015), 12070–12083.
28. Jiang, Y., Xiao, S., Fang, L., Yu, X., Song, Y., Niu, C., Chen, H., DNA vaccines co-expressing GP5 and M proteins of porcine reproductive and respiratory syndrome virus (PRRSV) display enhanced immunogenicity. Vaccine 24:15 (2006), 2869–2879.
29. Zhou, L., Ni, Y.Y., Piñeyro, P., Sanford, B.J., Cossaboom, C.M., Dryman, B.A., Huang, Y.W., Cao, D.J., Meng, X.J., 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 434:1 (2012), 96–109.
30. Fischer, W., Perkins, S., Theiler, J., Bhattacharya, T., Yusim, K., Funkhouser, R., Kuiken, C., Haynes, B., Letvin, N.L., Walker, B.D., Hahn, B.H., Korber, B.T., Polyvalent vaccines for optimal coverage of potential T-cell epitopes in global HIV-1 variants. Nat. Med. 13:1 (2007), 100–106.
31. Thurmond, J., Yoon, H., Kuiken, C., Yusim, K., Perkins, S., Theiler, J., Bhattacharya, T., Korber, B., Fischer, W., Web-based design and evaluation of T-cell vaccine candidates. Bioinformatics 24:14 (2008), 1639–1640.
32. Barouch, D.H., O'Brien, K.L., Simmons, N.L., King, S.L., Abbink, P., Maxfield, L.F., Sun, Y.H., La Porte, A., Riggs, A.M., Lynch, D.M., Clark, S.L., Backus, K., Perry, J.R., Seaman, M.S., Carville, A., Mansfield, K.G., Szinger, J.J., Fischer, W., Muldoon, M., Korber, B., Mosaic HIV-1 vaccines expand the breadth and depth of cellular immune responses in rhesus monkeys. Nat. Med. 16:3 (2010), 319–323.
33. Santra, S., Liao, H.X., Zhang, R., Muldoon, M., Watson, S., Fischer, W., Theiler, J., Szinger, J., Balachandran, H., Buzby, A., Quinn, D., Parks, R.J., Tsao, C.Y., Carville, A., Mansfield, K.G., Pavlakis, G.N., Felber, B.K., Haynes, B.F., Korber, B.T., Letvin, N.L., Mosaic vaccines elicit CD8+ T lymphocyte responses that confer enhanced immune coverage of diverse HIV strains in monkeys. Nat. Med. 16:3 (2010), 324–328.
34. 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. 133:3–4 (1993), 477–483.
35. 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. Invest. 8:1 (1996), 11–20.
36. Ren, J., Lu, H., Wen, S., Sun, W., Yan, F., Chen, X., Jing, J., Liu, H., Liu, C., Xue, F., Xiao, P., Xin, S., Jin, N., Enhanced immune responses in pigs by DNA vaccine coexpressing GP3 and GP5 of European type porcine reproductive and respiratory syndrome virus. J. Virol. Methods 206 (2014), 27–37.
37. Du, Y., Lu, Y., Wang, X., Qi, J., Liu, J., Hu, Y., Li, F., Wu, J., Guo, L., Liu, J., Tao, H., Sun, W., Chen, L., Cong, X., Ren, S., Shi, J., Li, J., Wang, J., Huang, B., Wan, R., Highly efficient expression of interleukin-2 under the control of rabbit beta-globin intron II gene enhances protective immune responses of porcine reproductive and respiratory syndrome (PRRS) DNA vaccine in pigs. PLoS ONE, 9, 2014, 3.
38. Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:4 (2001), 402–408.
39. Patel, D., Nan, Y., Shen, M., Ritthipichai, K., Zhu, X., Zhang, Y.J., Porcine reproductive and respiratory syndrome virus inhibits type I interferon signaling by blocking STAT1/STAT2 nuclear translocation. J. Virol. 84:21 (2010), 11045–11055.
40. Chen, Z., Lawson, S., Sun, Z., Zhou, X., Guan, X., Christopher-Hennings, J., Nelson, E.A., Fang, Y., Identification of two auto-cleavage products of nonstructural protein 1 (nsp1) in porcine reproductive and respiratory syndrome virus infected cells: nsp1 function as interferon antagonist. Virology 398:1 (2010), 87–97.
41. Renukaradhya, G.J., Alekseev, K., Jung, K., Fang, Y., Saif, L.J., Porcine reproductive and respiratory syndrome virus-induced immunosuppression exacerbates the inflammatory response to porcine respiratory coronavirus in pigs. Viral Immunol. 23:5 (2010), 457–466.
42. Meier, W.A., Galeota, J., Osorio, F.A., Husmann, R.J., Schnitzlein, W.M., Zuckermann, F.A., Gradual development of the interferon-gamma response of swine to porcine reproductive and respiratory syndrome virus infection or vaccination. Virology 309 (2003), 18–31.
43. Go, N., Bidot, C., Belloc, C., Touzeau, S., Integrative model of the immune response to a pulmonary macrophage infection: what determines the infection duration?. PLoS ONE, 9, 2014, 9.
44. Morgan, S.B., Graham, S.P., Salguero, F.J., Sánchez Cordón, P.J., Mokhtar, H., Rebel, J.M., Weesendorp, E., Bodman-Smith, K.B., Steinbach, F., Frossard, J.P., Increased pathogenicity of European porcine reproductive and respiratory syndrome virus is associated with enhanced adaptive responses and viral clearance. Vet. Microbiol. 163:1 (2013), 13–22.
45. Díaz, I., Darwich, L., Pappaterra, G., Pujols, J., Mateu, E., Different European-type vaccines against porcine reproductive and respiratory syndrome virus have different immunological properties and confer different protection to pigs. Virology 351:2 (2006), 249–259.
46. Rossow, K., Porcine reproductive and respiratory syndrome. Vet. Pathol. 35:1 (1998), 1–20.
47. Rovira, A., Balasch, M., Segalés, J., García, L., Plana-Durán, J., Rosell, C., Ellerbrok, H., Mankertz, A., Domingo, M., Experimental inoculation of conventional pigs with porcine reproductive and respiratory syndrome virus and porcine circovirus 2. J. Virol. 76:7 (2002), 3232–3239.
48. Ahlén, G., Söderholm, J., Tjelle, T., Kjeken, R., Frelin, L., Höglund, U., Blomberg, P., Fons, M., Mathiesen, I., Sällberg, M., In vivo electroporation enhances the immunogenicity of hepatitis C virus nonstructural 3/4A DNA by increased local DNA uptake, protein expression, inflammation, and infiltration of CD3+ T cells. J. Immunol. 179:7 (2007), 4741–4753.