Innate and adaptive immunity against Porcine Reproductive and Respiratory Syndrome Virus

Veterinary Immunology and Immunopathology

Volumn 167, Issue 1-2, 2015, Pages 1-14

  Loving, Crystal L ^a   Osorio, Fernando A ^b   Murtaugh, Michael P ^c   Zuckermann, Federico A ^d  

^a NATIONAL ANIMAL DISEASE CENTER   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Antibody; Cell mediated immunity; Immunology; Innate immunity; PRRSV

Indexed keywords

ALPHA INTERFERON; EPITOPE; GLYCAN; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY; VIRUS PROTEIN; VIRUS ANTIGEN; VIRUS VACCINE;

ADAPTIVE IMMUNITY; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; IMMUNE EVASION; IMMUNE RESPONSE; INNATE IMMUNITY; MEMORY T LYMPHOCYTE; NONHUMAN; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS; REGULATORY T LYMPHOCYTE; REVIEW; VIRAL CLEARANCE; VIRION; VIRUS INFECTIVITY; ANIMAL; BIOSYNTHESIS; CROSS REACTION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; PATHOGENICITY; PIG; T LYMPHOCYTE; VIROLOGY;

PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUIDAE;

ADAPTIVE IMMUNITY; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; CROSS REACTIONS; EPITOPES; HOST-PATHOGEN INTERACTIONS; IMMUNE EVASION; IMMUNITY, CELLULAR; IMMUNITY, INNATE; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUS SCROFA; SWINE; T-LYMPHOCYTES; VIRAL VACCINES;

EID: 84940453660     PISSN: 01652427     EISSN: 18732534     Source Type: Journal    
DOI: 10.1016/j.vetimm.2015.07.003     Document Type: Review

References (173)

1. Albina E. Porcine reproductive and respiratory syndrome: ten years of experience (1986-1996) with this undesirable viral infection. Vet. Res. 1997, 28:305-352.
2. Albina E., Piriou L., Hutet E., Cariolet R., L'Hospitalier R. Immune responses in pigs infected with porcine reproductive and respiratory syndrome virus (PRRSV). Vet. Immunol. Immunopathol. 1998, 61:49-66.
3. Allende R., Laegreid W.W., Kutish G.F., Galeota J.A., Wills R.W., Osorio F.A. Porcine reproductive and respiratory syndrome virus: description of persistence in individual pigs upon experimental infection. J. Virol. 2000, 74:10834-10837.
4. Ansari I.H., Kwon B., Osorio F.A., Pattnaik A.K. Influence of N-linked glycosylation of porcine reproductive and respiratory syndrome virus GP5 on virus infectivity, antigenicity, and ability to induce neutralizing antibodies. J. Virol. 2006, 80:3994-4004.
5. Bastos R.G., Dellagostin O.A., Barletta R.G., Doster A.R., Nelson E., Zuckermann F., Osorio F.A. Immune response of pigs inoculated with Mycobacterium bovis BCG expressing a truncated form of GP5 and M protein of porcine reproductive and respiratory syndrome virus. Vaccine 2004, 22:467-474.
6. Baum A., Garcia-Sastre A. Induction of type I interferon by RNA viruses: cellular receptors and their substrates. Amino Acids 2010, 38:1283-1299.
7. Baumann A., Mateu E., Murtaugh M.P., Summerfield A. Impact of genotype 1 and 2 of porcine reproductive and respiratory syndrome viruses on interferon-alpha responses by plasmacytoid dendritic cells. Vet. Res. 2013, 44:33.
8. Bautista E.M., Molitor T.W. Cell-mediated immunity to porcine reproductive and respiratory syndrome virus in swine. Viral Immunol. 1997, 10:83-94.
9. Bautista E.M., Suarez P., Molitor T.W. T cell responses to the structural polypeptides of porcine reproductive and respiratory syndrome virus. Arch. Virol. 1999, 144:117-134.
10. Biron C.A. Interferons alpha and beta as immune regulators - a new look. Immunity 2001, 14:661-664.
11. Brockmeier S.L., Lager K.M., Grubman M.J., Brough D.E., Ettyreddy D., Sacco R.E., Gauger P.C., Loving C.L., Vorwald A.C., Kehrli M.E., Lehmkuhl H.D. Adenovirus-mediated expression of interferon-alpha delays viral replication and reduces disease signs in swine challenged with porcine reproductive and respiratory syndrome virus. Viral Immunol. 2009, 22:173-180.
12. Brockmeier S.L., Loving C.L., Nelson E.A., Miller L.C., Nicholson T.L., Register K.B., Grubman M.J., Brough D.E., Kehrli M.E. The presence of alpha interferon at the time of infection alters the innate and adaptive immune responses to porcine reproductive and respiratory syndrome virus. Clin. Vaccine Immunol.: CVI 2012, 19:508-514.
13. Brown E., Lawson S., Welbon C., Gnanandarajah J., Li J., Murtaugh M.P., Nelson E.A., Molina R.M., Zimmerman J.J., Rowland R.R., Fang Y. Antibody response to porcine reproductive and respiratory syndrome virus (PRRSV) nonstructural proteins and implications for diagnostic detection and differentiation of PRRSV types I and II. Clin. Vaccine Immunol.: CVI 2009, 16:628-635.
14. Buddaert W., Van Reeth K., Pensaert M. In vivo and in vitro interferon (IFN) studies with the porcine reproductive and respiratory syndrome virus (PRRSV). Adv. Exp. Med. Biol. 1998, 440:461-467.
15. Burgara-Estrella A., Díaz I., Rodríguez-Gómez I.M., Essler S.E., Hernández J., Mateu E. Predicted peptides from non-structural proteins of porcine reproductive and respiratory syndrome virus are able to induce IFN-γ and IL-10. Viruses 2013, 5:663-677.
16. Calzada-Nova G., Schnitzlein W., Husmann R., Zuckermann F.A. Characterization of the cytokine and maturation responses of pure populations of porcine plasmacytoid dendritic cells to porcine viruses and toll-like receptor agonists. Vet. Immunol. Immunopathol. 2010, 135:20-33.
17. Calzada-Nova G., Schnitzlein W.M., Husmann R.J., Zuckermann F.A. North American porcine reproductive and respiratory syndrome viruses inhibit type I interferon production by plasmacytoid dendritic cells. J. Virol. 2011, 85:2703-2713.
18. 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.
19. Cecere T.E., Todd S.M., Leroith T. Regulatory T cells in arterivirus and coronavirus infections: do they protect against disease or enhance it?. Viruses 2012, 4:833-846.
20. Cella M., Facchetti F., Lanzavecchia A., Colonna M. Plasmacytoid dendritic cells activated by influenza virus and CD40L drive a potent TH1 polarization. Nat. Immunol. 2000, 1:305-310.
21. Charerntantanakul W., Platt R., Johnson W., Roof M., Vaughn E., Roth J.A. Immune responses and protection by vaccine and various vaccine adjuvant candidates to virulent porcine reproductive and respiratory syndrome virus. Vet. Immunol. Immunopathol. 2006, 109:99-115.
22. Collins J.E. Porcine reproductive and respiratory syndrome: the disease. Proceedings of the 15th IPVS Congress 1998, 149-156.
23. Costers S., Lefebvre D.J., Goddeeris B., Delputte P.L., Nauwynck H.J. Functional impairment of PRRSV-specific peripheral CD3+ CD8high cells. Vet. Res. 2009, 40:46.
24. Cousens L.P., Orange J.S., Su H.C., Biron C.A. Interferon-alpha/beta inhibition of interleukin 12 and interferon-gamma production in vitro and endogenously during viral infection. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:634-639.
25. Cousens L.P., Peterson R., Hsu S., Dorner A., Altman J.D., Ahmed R., Biron C.A. Two roads diverged: interferon alpha/beta- and interleukin 12-mediated pathways in promoting T cell interferon gamma responses during viral infection. J. Exp. Med. 1999, 189:1315-1328.
26. 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, 84:1731-1740.
27. Dawson H.D., Beshah E., Nishi S., Solano-Aguilar G., Morimoto M., Zhao A., Madden K.B., Ledbetter T.K., Dubey J.P., Shea-Donohue T., Lunney J.K., Urban J.F. Localized multigene expression patterns support an evolving Th1/Th2-like paradigm in response to infections with Toxoplasma gondii and Ascaris suum. Infect. Immun. 2005, 73:1116-1128.
28. 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.
29. 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. 2000, 145:659-688.
30. Delputte P.L., Meerts P., Costers S., Nauwynck H.J. 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.
31. Diaz 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 2009, 27:5603-5611.
32. Dobrescu I., Levast B., Lai K., Delgado-Ortega M., Walker S., Banman S., Townsend H., Simon G., Zhou Y., Gerdts V., Meurens F. In vitro and ex vivo analyses of co-infections with swine influenza and porcine reproductive and respiratory syndrome viruses. Vet. Microbiol. 2014, 169:18-32.
33. Dwivedi V., Manickam C., Binjawadagi B., Linhares D., Murtaugh M.P., Renukaradhya G.J. Evaluation of immune responses to porcine reproductive and respiratory syndrome virus in pigs during early stage of infection under farm conditions. Virol. J. 2012, 9:45.
34. Ebner F., Rausch S., Scharek-Tedin L., Pieper R., Burwinkel M., Zentek J., Hartmann S. A novel lineage transcription factor based analysis reveals differences in T helper cell subpopulation development in infected and intrauterine growth restricted (IUGR) piglets. Dev. Comp. Immunol. 2014, 46:333-340.
35. Faaberg K.S., Hocker J.D., Erdman M.M., Harris D.L., Nelson E.A., Torremorell M., Plagemann P.G. Neutralizing antibody responses of pigs infected with natural GP5 N-glycan mutants of porcine reproductive and respiratory syndrome virus. Viral Immunol. 2006, 19:294-304.
36. Fan B., Liu X., Bai J., Zhang T., Zhang Q., Jiang P. The amino acid residues at 102 and 104 in GP5 of porcine reproductive and respiratory syndrome virus regulate viral neutralization susceptibility to the porcine serum neutralizing antibody. Virus Res. 2015, 204:21-30.
37. Fang Y., Snijder E.J. The PRRSV replicase: exploring the multifunctionality of an intriguing set of nonstructural proteins. Virus Res. 2010, 154:61-76.
38. Feng W.H., Tompkins M.B., Xu J.S., Brown T.T., Laster S.M., Zhang H.X., McCaw M.B. Thymocyte and peripheral blood T lymphocyte subpopulation changes in piglets following in utero infection with porcine reproductive and respiratory syndrome virus. Virology 2002, 302:363-372.
39. Feng W.H., Tompkins M.B., Xu J.S., Zhang H.X., McCaw M.B. Analysis of constitutive cytokine expression by pigs infected in-utero with porcine reproductive and respiratory syndrome virus. Vet. Immunol. Immunopathol. 2003, 94:35-45.
40. Ferrari L., Martelli P., Saleri R., De Angelis E., Cavalli V., Bresaola M., Benetti M., Borghetti P. Lymphocyte activation as cytokine gene expression and secretion is related to the porcine reproductive and respiratory syndrome virus (PRRSV) isolate after in vitro homologous and heterologous recall of peripheral blood mononuclear cells (PBMC) from pigs vaccinated and exposed to natural infection. Vet. Immunol. Immunopathol. 2013, 151:193-206.
41. 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.
42. Fitzgerald-Bocarsly P. Natural interferon-alpha producing cells: the plasmacytoid dendritic cells. Biotechniques 2002, (Suppl.). 16-20, 22, 19-24.
43. Fitzgerald-Bocarsly P., Dai J., Singh S. Plasmacytoid dendritic cells and type I IFN: 50 years of convergent history. Cytokine Growth Factor Rev. 2008, 19:3-19.
44. Foss D.L., Zilliox M.J., Meier W., Zuckermann F., Murtaugh M.P. Adjuvant danger signals increase the immune response to porcine reproductive and respiratory syndrome virus. Viral Immunol. 2002, 15:557-566.
45. Francica J.R., Varela-Rohena A., Medvec A., Plesa G., Riley J.L., Bates P. Steric shielding of surface epitopes and impaired immune recognition induced by the ebola virus glycoprotein. PLoS Pathog. 2010, 6:e1001098.
46. Genini S., Delputte P.L., Malinverni R., Cecere M., Stella A., Nauwynck H.J., Giuffra E. Genome-wide transcriptional response of primary alveolar macrophages following infection with porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 2008, 89:2550-2564.
47. Gomez-Laguna J., Salguero F.J., De Marco M.F., Pallares F.J., Bernabe A., Carrasco L. Changes in lymphocyte subsets and cytokines during European porcine reproductive and respiratory syndrome: increased expression of IL-12 and IL-10 and proliferation of CD4(-)CD8(high). Viral Immunol. 2009, 22:261-271.
48. Gómez-Laguna J., Salguero F.J., Fernández de Marco M., Barranco I., Rodríguez-Gómez I.M., Quezada M., Carrasco L. Type 2 Porcine Reproductive and Respiratory Syndrome Virus infection mediated apoptosis in B- and T-cell areas in lymphoid organs of experimentally infected pigs. Transbound. Emerg. Dis. 2013, 60:273-278.
49. Gu W., Guo L., Yu H., Niu J., Huang M., Luo X., Li R., Tian Z., Feng L., Wang Y. Involvement of CD16 in antibody-dependent enhancement of porcine reproductive and respiratory syndrome virus infection. J. Gen. Virol. 2015.
50. Han K., Seo H.W., Park C., Chae C. Vaccination of sows against type 2 Porcine Reproductive and Respiratory Syndrome Virus (PRRSV) before artificial insemination protects against type 2 PRRSV challenge but does not protect against type 1 PRRSV challenge in late gestation. Vet. Res. 2014, 45:12.
51. Hesse R., Couture L., Lau M., Wunder K., Wasmoen T. Efficacy of Prime Pac PRRS in controlling PRRS reproductive disease: heterologous challenge. Proceedings 27th Annual Meetg American Association of Swine Practitioners 1996, 107-110.
52. Honda K., Sakaguchi S., Nakajima C., Watanabe A., Yanai H., Matsumoto M., Ohteki T., Kaisho T., Takaoka A., Akira S., Seya T., Taniguchi T. Selective contribution of IFN-alpha/beta signaling to the maturation of dendritic cells induced by double-stranded RNA or viral infection. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:10872-10877.
53. Jeong H.J., Song Y.J., Lee S.W., Lee J.B., Park S.Y., Song C.S., Ha G.W., Oh J.S., Oh Y.K., Choi I.S. Comparative measurement of cell-mediated immune responses of swine to the M and N proteins of porcine reproductive and respiratory syndrome virus. Clin. Vaccine Immunol.: CVI 2010, 17:503-512.
54. Jiang W., Jiang P., Wang X., Li Y., Du Y. Influence of porcine reproductive and respiratory syndrome virus GP5 glycoprotein N-linked glycans on immune responses in mice. Virus Genes 2007, 35:663-671.
55. 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.
56. Johnson C.R., Griggs T.F., Gnanandarajah J., Murtaugh M.P. Novel structural protein in porcine reproductive and respiratory syndrome virus encoded by an alternative ORF5 present in all arteriviruses. J. Gen. Virol. 2011, 92:1107-1116.
57. Johnson C.R., Yu W., Murtaugh M.P. Cross-reactive antibody responses to nsp1 and nsp2 of Porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 2007, 88:1184-1195.
58. Jung K., Renukaradhya G.J., Alekseev K.P., Fang Y., Tang Y., Saif L.J. Porcine reproductive and respiratory syndrome virus modifies innate immunity and alters disease outcome in pigs subsequently infected with porcine respiratory coronavirus: implications for respiratory viral co-infections. J. Gen. Virol. 2009, 90:2713-2723.
59. Kadowaki N., Antonenko S., Lau J.Y., Liu Y.J. Natural interferon alpha/beta-producing cells link innate and adaptive immunity. J. Exp. Med. 2000, 192:219-226.
60. Kapsenberg M.L. Dendritic-cell control of pathogen-driven T-cell polarization. Nat. Rev. Immunol. 2003, 3:984-993.
61. Kawashima K., Narita M., Yamada S. Changes in macrophage and lymphocyte subpopulations of lymphoid tissues from pigs infected with the porcine reproductive and respiratory syndrome virus (PRRSV). Vet. Immunol. Immunopathol. 1999, 71:257-262.
62. Kim W.I., Kim J.J., Cha S.H., Wu W.H., Cooper V., Evans R., Choi E.J., Yoon K.J. Significance of genetic variation of PRRSV ORF5 in virus neutralization and molecular determinants corresponding to cross neutralization among PRRS viruses. Vet. Microbiol. 2013, 162:10-22.
63. 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.
64. 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.
65. Labarque G.G., Nauwynck H.J., Van Reeth K., Pensaert M.B. 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.
66. Lamontagne L., Page C., Larochelle R., Magar R. Porcine reproductive and respiratory syndrome virus persistence in blood, spleen, lymph nodes, and tonsils of experimentally infected pigs depends on the level of CD8high T cells. Viral Immunol. 2003, 16:395-406.
67. Lee S.M., Schommer S.K., Kleiboeker S.B. Porcine reproductive and respiratory syndrome virus field isolates differ in in vitro interferon phenotypes. Vet. Immunol. Immunopathol. 2004, 102:217-231.
68. Levy D.E., Marie I., Prakash A. Ringing the interferon alarm: differential regulation of gene expression at the interface between innate and adaptive immunity. Curr. Opin. Immunol. 2003, 15:52-58.
69. 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, 433:367-376.
70. 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.
71. Linhares D.C., Cano J.P., Torremorell M., Morrison R.B. Comparison of time to PRRSv-stability and production losses between two exposure programs to control PRRSv in sow herds. Prev. Vet. Med. 2014, 116:111-119.
72. Liu C.H., Chaung H.C., Chang H.L., Peng Y.T., Chung W.B. Expression of Toll-like receptor mRNA and cytokines in pigs infected with porcine reproductive and respiratory syndrome virus. Vet. Microbiol. 2009, 136:266-276.
73. Liu M., Chen H., Luo F., Li P., Pan Q., Xia B., Qi Z., Ho W.Z., Zhang X.L. Deletion of N-glycosylation sites of hepatitis C virus envelope protein E1 enhances specific cellular and humoral immune responses. Vaccine 2007, 25:6572-6580.
74. Loemba H.D., Mounir S., Mardassi H., Archambault D., 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.
75. Lohse L., Nielsen J., Eriksen L. Temporary CD8+ T-cell depletion in pigs does not exacerbate infection with porcine reproductive and respiratory syndrome virus (PRRSV). Viral Immunol. 2004, 17:594-603.
76. Lopez Fuertes L., Domenech N., Alvarez B., Ezquerra A., Dominguez J., Castro J.M., Alonso F. Analysis of cellular immune response in pigs recovered from porcine respiratory and reproductive syndrome infection. Virus Res. 1999, 64:33-42.
77. 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.: CVI 2007, 14:269-275.
78. Lopez O.J., Osorio F.A. Role of neutralizing antibodies in PRRSV protective immunity. Vet. Immunol. Immunopathol. 2004, 102:155-163.
79. Loving C.L., Brockmeier S.L., Sacco R.E. Differential type I interferon activation and susceptibility of dendritic cell populations to porcine arterivirus. Immunology 2007, 120:217-229.
80. Lowe J.E., Husmann R., Firkins L.D., Zuckermann F.A., Goldberg T.L. Correlation of cell-mediated immunity against porcine reproductive and respiratory syndrome virus with protection against reproductive failure in sows during outbreaks of porcine reproductive and respiratory syndrome in commercial herds. J. Am. Vet. Med. Assoc. 2005, 226:1707-1711.
81. Mair K.H., Koinig H., Gerner W., Hohne A., Bretthauer J., Kroll J.J., Roof M.B., Saalmuller A., Stadler K., Libanova R. Carbopol improves the early cellular immune responses induced by the modified-life vaccine Ingelvac PRRS MLV. Vet. Microbiol. 2015, 176:352-357.
82. Mardassi H., Massie B., Dea S. Intracellular synthesis, processing, and transport of proteins encoded by ORFs 5-7 of porcine reproductive and respiratory syndrome virus. Virology 1996, 221:98-112.
83. Martelli P., Gozio S., Ferrari L., Rosina S., De Angelis E., Quintavalla C., Bottarelli E., Borghetti P. Efficacy of a modified live porcine reproductive and respiratory syndrome virus (PRRSV) vaccine in pigs naturally exposed to a heterologous European (Italian cluster) field strain: clinical protection and cell-mediated immunity. Vaccine 2009, 27:3788-3799.
84. 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, 29:6928-6940.
85. Meier W., Wheeler J.G., Husmann R.J., Osorio F.A., Zuckermann F. Charcateristics of the immune response of pigs to PRRS virus. Vet. Res. 2000, 31:41.
86. 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 2003, 309:18-31.
87. Meier W.A., Husmann R.J., Schnitzlein W.M., Osorio F.A., Lunney J.K., Zuckermann F.A. Cytokines and synthetic double-stranded RNA augment the T helper 1 immune response of swine to porcine reproductive and respiratory syndrome virus. Vet. Immunol. Immunopathol. 2004, 102:299-314.
88. Meulenberg J.J., Bende R.J., Pol J.M., Wensvoort G., Moormann R.J. Nucleocapsid protein N of Lelystad virus: expression by recombinant baculovirus, immunological properties, and suitability for detection of serum antibodies. Clin. Diagn. Lab. Immunol. 1995, 2:652-656.
89. Miller L.C., Lager K.M., Kehrli M.E. Role of Toll-like receptors in activation of porcine alveolar macrophages by porcine reproductive and respiratory syndrome virus. Clin. Vaccine Immunol.: CVI 2009, 16:360-365.
90. Molitor T. Immune response to PRRS virus. Proc. Allen D. Leman Confer. 1993, 20.
91. Molitor T.W., Bautista E.M., Choi C.S. Immunity to PRRSV: double-edged sword. Vet. Microbiol. 1997, 55:265-276.
92. Montoya M., Schiavoni G., Mattei F., Gresser I., Belardelli F., Borrow P., Tough D.F. Type I interferons produced by dendritic cells promote their phenotypic and functional activation. Blood 2002, 99:3263-3271.
93. 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 syndrome virus infection. J. Virol. 2008, 82:358-370.
94. Murtaugh M.P., Genzow M. Immunological solutions for treatment and prevention of porcine reproductive and respiratory syndrome (PRRS). Vaccine 2011, 29:8192-8204.
95. Murtaugh M.P., Johnson C.R., Xiao Z., Scamurra R.W., Zhou Y. Species specialization in cytokine biology: is interleukin-4 central to the T(H)1-T(H)2 paradigm in swine?. Dev. Comp. Immunol. 2009, 33:344-352.
96. Murtaugh M.P., Xiao Z., Zuckermann F. Immunological responses of swine to porcine reproductive and respiratory syndrome virus infection. Viral Immunol. 2002, 15:533-547.
97. 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, 6:410-415.
98. Nielsen J., Botner A. Hematological and immunological parameters of 4 1/2-month old pigs infected with PRRS virus. Vet. Microbiol. 1997, 55:289-294.
99. Nielsen J., Botner A., Tingstedt J.E., Aasted B., Johnsen C.K., Riber U., Lind P. In utero infection with porcine reproductive and respiratory syndrome virus modulates leukocyte subpopulations in peripheral blood and bronchoalveolar fluid of surviving piglets. Vet. Immunol. Immunopathol. 2003, 93:135-151.
100. Oleksiewicz M.B., Botner A., Toft P., Normann P., 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.
101. Olin M.R., Batista L., Xiao Z., Dee S.A., Murtaugh M.P., Pijoan C.C., Molitor T.W. Gammadelta lymphocyte response to porcine reproductive and respiratory syndrome virus. Viral Immunol. 2005, 18:490-499.
102. 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, 302:9-20.
103. Osorio F.A., Zuckermann F., Wills R., Meier W., Christian S., Galeota J., Doster A. PRRSV: comparison of commercial vaccines in their ability to induce protection against current PRRSV strains of high virulence. Allen D. Leman Swine Conference, vol. 25 1998, 176-182.
104. 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. 2002, 76:4241-4250.
105. Parida R., Choi I.S., Peterson D.A., Pattnaik A.K., Laegreid W., Zuckermann F.A., Osorio F.A. Location of T-cell epitopes in nonstructural proteins 9 and 10 of type-II porcine reproductive and respiratory syndrome virus. Virus Res. 2012.
106. Pirzadeh B., 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.
107. Pirzadeh B., Dea S. Immune response in pigs vaccinated with plasmid DNA encoding ORF5 of porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 1998, 79(Pt 5):989-999.
108. 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. 2002, 147:2327-2347.
109. 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.
110. Plotkin S.A., Gilbert P.B. Nomenclature for immune correlates of protection after vaccination. Clin. Infect. Dis.: Off. Publ. Infect. Dis. Soc. Am. 2012, 54:1615-1617.
111. Reitter J.N., Means R.E., Desrosiers R.C. A role for carbohydrates in immune evasion in AIDS. Nat. Med. 1998, 4:679-684.
112. 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.
113. Robinson S.R., Li J., Nelson E.A., Murtaugh M.P. Broadly neutralizing antibodies against the rapidly evolving porcine reproductive and respiratory syndrome virus. Virus Res. 2015, 203:56-65.
114. Roca M., Gimeno M., Bruguera S., Segales J., Diaz I., Galindo-Cardiel I.J., Martinez E., Darwich L., Fang Y., Maldonado J., March R., Mateu E. Effects of challenge with a virulent genotype II strain of porcine reproductive and respiratory syndrome virus on piglets vaccinated with an attenuated genotype I strain vaccine. Vet. J. 2012, 193:92-96.
115. Rodriguez-Gomez I.M., Kaser T., Gomez-Laguna J., Lamp B., Sinn L., Rumenapf T., Carrasco L., Saalmuller A., Gerner W. PRRSV-infected monocyte-derived dendritic cells express high levels of SLA-DR and CD80/86 but do not stimulate PRRSV-naive regulatory T cells to proliferate. Vet. Res. 2015, 46:54.
116. Rowland R.R., Robinson B., Stefanick J., Kim T.S., Guanghua L., Lawson S.R., Benfield D.A. Inhibition of porcine reproductive and respiratory syndrome virus by interferon-gamma and recovery of virus replication with 2-aminopurine. Arch. Virol. 2001, 146:539-555.
117. Royaee A.R., Husmann R.J., Dawson H.D., Calzada-Nova G., Schnitzlein W.M., Zuckermann F.A., Lunney J.K. Deciphering the involvement of innate immune factors in the development of the host response to PRRSV vaccination. Vet. Immunol. Immunopathol. 2004, 102:199-216.
118. Samsom J.N., de Bruin T.G., Voermans J.J., Meulenberg J.J., Pol J.M., Bianchi A.T. Changes of leukocyte phenotype and function in the broncho-alveolar lavage fluid of pigs infected with porcine reproductive and respiratory syndrome virus: a role for CD8(+) cells. J. Gen. Virol. 2000, 81:497-505.
119. Sang Y., Rowland R.R., Blecha F. Antiviral regulation in porcine monocytic cells at different activation states. J. Virol. 2014, 88:11395-11410.
120. Sang Y., Shi J., Sang W., Rowland R.R., Blecha F. Replication-competent recombinant porcine reproductive and respiratory syndrome (PRRS) viruses expressing indicator proteins and antiviral cytokines. Viruses 2012, 4:102-116.
121. Scortti M., Prieto C., Simarro I., Castro J.M. Reproductive performance of gilts following vaccination and subsequent heterologous challenge with European strains of porcine reproductive and respiratory syndrome virus. Theriogenology 2006, 66:1884-1893.
122. Shimizu M., Yamada S., Kawashima K., Ohashi S., Shimizu S., Ogawa T. Changes of lymphocyte subpopulations in pigs infected with porcine reproductive and respiratory syndrome (PRRS) virus. Vet. Immunol. Immunopathol. 1996, 50:19-27.
123. Silva-Campa E., Cordoba L., Fraile L., Flores-Mendoza L., Montoya M., Hernandez J. European genotype of porcine reproductive and respiratory syndrome (PRRSV) infects monocyte-derived dendritic cells but does not induce Treg cells. Virology 2010, 396:264-271.
124. Silva-Campa E., Flores-Mendoza L., Resendiz M., Pinelli-Saavedra A., Mata-Haro V., Mwangi W., Hernandez J. Induction of T helper 3 regulatory cells by dendritic cells infected with porcine reproductive and respiratory syndrome virus. Virology 2009, 387:373-379.
125. Silva-Campa E., Mata-Haro V., Mateu E., Hernandez J. Porcine reproductive and respiratory syndrome virus induces CD4+ CD8+ CD25+ Foxp3+ regulatory T cells (Tregs). Virology 2012, 430:73-80.
126. Snijder E.J., Meulenberg J.M. Arteriviruses in Fields Virology 2001, vol. 1:1205-1220. Publ. by Lippincott Williams & Wilkins, Philadelphia. 4th ed.
127. Spilman M.S., Welbon C., Nelson E., Dokland T. Cryo-electron tomography of porcine reproductive and respiratory syndrome virus: organization of the nucleocapsid. J. Gen. Virol. 2009, 90:527-535.
128. Sun Y., Han M., Kim C., Calvert J.G., Yoo D. Interplay between interferon-mediated innate immunity and porcine reproductive and respiratory syndrome virus. Viruses 2012, 4:424-446.
129. Swiecki M., Colonna M. Unraveling the functions of plasmacytoid dendritic cells during viral infections, autoimmunity, and tolerance. Immunol. Rev. 2010, 234:142-162.
130. Takeuchi O., Akira S. Innate immunity to virus infection. Immunol. Rev. 2009, 227:75-86.
131. 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.
132. Tingstedt J.E., Nielsen J. Cellular immune responses in the lungs of pigs infected in utero with PRRSV: an immunohistochemical study. Viral Immunol. 2004, 17:558-564.
133. Torremorell M., Moore C., Christianson W.T. Establishment of a herd negative for porcine reproductive and respiratory syndrome virus (PRRSV) from PRRSV-positive sources. J. Swine Health Prod. 2002, 10:153-160.
134. Tough D.F. Type I interferon as a link between innate and adaptive immunity through dendritic cell stimulation. Leukemia Lymphoma 2004, 45:257-264.
135. Trible B.R., Popescu L.N., Monday N., Calvert J.G., Rowland R.R. A single amino Acid deletion in the matrix protein of porcine reproductive and respiratory syndrome virus confers resistance to a polyclonal Swine antibody with broadly neutralizing activity. J. Virol. 2015, 89:6515-6520.
136. Trus I., Bonckaert C., van der Meulen K., Nauwynck H.J. Efficacy of an attenuated European subtype 1 porcine reproductive and respiratory syndrome virus (PRRSV) vaccine in pigs upon challenge with the East European subtype 3 PRRSV strain Lena. Vaccine 2014, 32:2995-3003.
137. 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.
138. Van Reeth K., Labarque G., Nauwynck H., Pensaert M. Differential production of proinflammatory cytokines in the pig lung during different respiratory virus infections: correlations with pathogenicity. Res. Vet. Sci. 1999, 67:47-52.
139. van Reeth K., Nauwynck H. Proinflammatory cytokines and viral respiratory disease in pigs. Vet. Res. 2000, 31:187-213.
140. 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.
141. Vashisht K., Erlandson K.R., Firkins L.D., Zuckermann F.A., Goldberg T.L. Evaluation of contact exposure as a method for acclimatizing growing pigs to porcine reproductive and respiratory syndrome virus. J. Am. Vet. Med. Assoc. 2008, 232:1530-1535.
142. 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, 85:5555-5564.
143. Wang C.C., Chen J.R., Tseng Y.C., Hsu C.H., Hung Y.F., Chen S.W., Chen C.M., Khoo K.H., Cheng T.J., Cheng Y.S., Jan J.T., Wu C.Y., Ma C., Wong C.H. Glycans on influenza hemagglutinin affect receptor binding and immune response. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:18137-18142.
144. Wang R., Xiao Y., Opriessnig T., Ding Y., Yu Y., Nan Y., Ma Z., Halbur P.G., Zhang Y.J. Enhancing neutralizing antibody production by an interferon-inducing porcine reproductive and respiratory syndrome virus strain. Vaccine 2013, 31:5537-5543.
145. Wang X., Christopher-Hennings J. Post-transcriptional control of type I interferon induction by porcine reproductive and respiratory syndrome virus in its natural host cells. Viruses 2012, 4:725-733.
146. Wang X., Li J., Jiang P., Li Y., Zeshan B., Cao J., Wang X. GM-CSF fused with GP3 and GP5 of porcine reproductive and respiratory syndrome virus increased the immune responses and protective efficacy against virulent PRRSV challenge. Virus Res. 2009, 143:24-32.
147. Wang Y.X., Zhou Y.J., Li G.X., Zhang S.R., Jiang Y.F., Xu A.T., Yu H., Wang M.M., Yan L.P., Tong G.Z. Identification of immunodominant T-cell epitopes in membrane protein of highly pathogenic porcine reproductive and respiratory syndrome virus. Virus Res. 2011, 158:108-115.
148. Wee G.J., Cao M.J., Liu W., Kwang J. Efficacy of porcine reproductive and respiratory syndrome virus vaccine and porcine interleukin-12. Vet. Therap.: Res. Appl. Vet. Med. 2001, 2:112-119.
149. Weesendorp E., Stockhofe-Zurwieden N., Popma-De Graaf D.J., Fijten H., Rebel J.M. Phenotypic modulation and cytokine profiles of antigen presenting cells by European subtype 1 and 3 porcine reproductive and respiratory syndrome virus strains in vitro and in vivo. Vet. Microbiol. 2013, 167:638-650.
150. 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, 422:307-312.
151. Wei Z., Lin T., Sun L., Li Y., Wang X., Gao F., Liu R., Chen C., Tong G., Yuan S. N-linked glycosylation of GP5 of porcine reproductive and respiratory syndrome virus is critically important for virus replication in vivo. J. Virol. 2013, 86:9941-9951.
152. Wei Z., Tian D., Sun L., Lin T., Gao F., Liu R., Tong G., Yuan S. Influence of N-linked glycosylation of minor proteins of porcine reproductive and respiratory syndrome virus on infectious virus recovery and receptor interaction. Virology 2013, 429:1-11.
153. Weiland E., Wieczorek-Krohmer M., Kohl D., Conzelmann K.K., 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.
154. Wills R.W., Zimmerman J.J., Yoon K.J., Swenson S.L., McGinley M.J., Hill H.T., Platt K.B., Christopher-Hennings J., Nelson E.A. Porcine reproductive and respiratory syndrome virus: a persistent infection. Vet. Microbiol. 1997, 55:231-240.
155. 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.
156. Wongyanin P., Buranapraditkun S., Chokeshai-Usaha K., Thanawonguwech R., Suradhat S. Induction of inducible CD4+ CD25+ Foxp3+ regulatory T lymphocytes by porcine reproductive and respiratory syndrome virus (PRRSV). Vet. Immunol. Immunopathol. 2010, 133:170-182.
157. 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.
158. Xiao S., Jia J., Mo D., Wang Q., Qin L., He Z., Zhao X., Huang Y., Li A., Yu J., Niu Y., Liu X., Chen Y. Understanding PRRSV infection in porcine lung based on genome-wide transcriptome response identified by deep sequencing. PLoS ONE 2010, 5:e11377.
159. Xiao S., Wang Q., Jia J., Cong P., Mo D., Yu X., Qin L., Li A., Niu Y., Zhu K., Wang X., Liu X., Chen Y. Proteome changes of lungs artificially infected with H-PRRSV and N-PRRSV by two-dimensional fluorescence difference gel electrophoresis. Virol. J. 2010, 7:107.
160. Xiao Z., Batista L., Dee S., Halbur P., Murtaugh M.P. The level of virus-specific T-cell and macrophage recruitment in porcine reproductive and respiratory syndrome virus infection in pigs is independent of virus load. J. Virol. 2004, 78:5923-5933.
161. Xiao Z., Trincado C.A., Murtaugh M.P. Beta-glucan enhancement of T cell IFNgamma response in swine. Vet. Immunol. Immunopathol. 2004, 102:315-320.
162. Xu X.G., Wang Z.S., Zhang Q., Li Z.C., Ding L., Li W., Wu H.Y., Chang C.D., Lee L.H., Tong D.W., Liu H.J. Baculovirus as a PRRSV and PCV2 bivalent vaccine vector: baculovirus virions displaying simultaneously GP5 glycoprotein of PRRSV and capsid protein of PCV2. J. Virol. Methods 2012, 179:359-366.
163. Yang L., Frey M.L., Yoon K.J., Zimmerman J.J., Platt K.B. 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.
164. Yoon I.J., Joo H.S., Goyal S.M., Molitor T.W. 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.
165. 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, 9:51-63.
166. 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 (ADE) of infection. Vet. Microbiol. 1997, 55:277-287.
167. Zhang H., Guo X., Nelson E., Christopher-Hennings J., Wang X. Porcine reproductive and respiratory syndrome virus activates the transcription of interferon alpha/beta (IFN-alpha/beta) in monocyte-derived dendritic cells (Mo-DC). Vet. Microbiol. 2012, 159:494-498.
168. Zheng Q., Chen D., Li P., Bi Z., Cao R., Zhou B., Chen P. Co-expressing GP5 and M proteins under different promoters in recombinant modified vaccinia virus ankara (rMVA)-based vaccine vector enhanced the humoral and cellular immune responses of porcine reproductive and respiratory syndrome virus (PRRSV). Virus Genes 2007, 35:585-595.
169. Zhou J.X., Xue J.D., Yu T., Zhang J.B., Liu Y., Jiang N., Li Y.L., Hu R.L. Immune responses in pigs induced by recombinant canine adenovirus 2 expressing the glycoprotein 5 of porcine reproductive and respiratory syndrome virus. Vet. Res. Commun. 2010, 34:371-380.
170. Zhou L., Ni Y.Y., Pineyro 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 2012, 434:96-109.
171. Zuckermann F.A. Extrathymic CD4/CD8 double positive T cells. Vet. Immunol. Immunopathol. 1999, 72:55-66.
172. 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.
173. Zuckermann F.A., Husmann R.J. Functional and phenotypic analysis of porcine peripheral blood CD4/CD8 double-positive T cells. Immunology 1996, 87:500-512.