Immune control of PRRS: Lessons to be learned and possible ways forward

Frontiers in Veterinary Science

Volumn 1, Issue OCT, 2014, Pages

  Amadori, Massimo ^a   Razzuoli, Elisabetta ^a,b  

^a ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLA LOMBARDIA E DELL EMILIA ROMAGNA   (Italy)

^b LIGURIA E VALLE D AOSTA   (Italy)

Author keywords

Immunomodulation; Interferon alpha; Pig; PRRSV; Vaccination

Indexed keywords

EID: 84949655937     PISSN: None     EISSN: 22971769     Source Type: Journal    
DOI: 10.3389/fvets.2014.00002     Document Type: Review

References (128)

1. Pastoret PP. Role of vaccination in animal health. Bull Acad Natl Med (2012) 196:589-90
2. Sanchez-Vizcaino JM, Mur L, Martinez-Lopez B. African swine fever: an epidemiological update. Transbound Emerg Dis (2012). doi: 10.1111/j.1865-1682.2011.01293.x
3. Murtaugh MP, Genzow M. Immunological solutions for treatment and prevention of porcine reproductive and respiratory syndrome (PRRS). Vaccine (2011) 29:8192-204. doi:10.1016/j.vaccine.2011.09.013
4. Terpstra C, Wensvoort G, 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) 13:131-6. doi:10.1080/01652176.1991.9694297
5. Darwich L, Diaz I, Mateu E. Certainties, doubts and hypotheses in porcine reproductive and respiratory syndrome virus immunobiology. Virus Res (2010) 154:123-32. doi:10.1016/j.virusres.2010.07.017
6. Zimmerman J, Benfield DA, Murtaugh MP, Osorio F, Stevenson GW, Tottemorell M. Porcine reproductive and respiratory syndrome virus (porcine arterivirus). 9th ed. In: Straw BE, Zimmerman JJ, D'Allaire S, Taylor DJ, editors. Diseases of Swine. Ames, IA: Iowa State University Press (2006). p. 387-417
7. Neumann EJ, Kliebenstein JB, Johnson CD, Mabry JW, Bush EJ, Seitzinger AH, et al. Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States. J Am Vet Med Assoc (2005) 227:385-92. doi:10.2460/javma.2005.227.385
8. Nelsen CJ, Murtaugh MP, Faaberg KS. Porcine reproductive and respiratory syndrome virus comparison: divergent evolution on two continents. J Virol (1999) 73:270-80
9. Dokland T. The structural biology of PRRSV. Virus Res (2010) 154:86-97. doi:10.1016/j.virusres.2010.07.029
10. Shi M, Lam TT, Hon CC, Hui RK, Faaberg KS, Wennblom T, et al. Molecular epidemiology of PRRSV: a phylogenetic perspective. Virus Res (2010) 154:7-17. doi:10.1016/j.virusres.2010.08.014
11. Nodelijk G, Nielen M, De Jong MC, Verheijden JH. A review of porcine reproductive and respiratory syndrome virus in Dutch breeding herds: population dynamics and clinical relevance. Prev Vet Med (2003) 60:37-52. doi:10.1016/S0167-5877(03)00081-3
12. Han K, Seo HW, Park C, Oh Y, Kang I, Chae C. Comparative pathogenesis of type 1 (European genotype) and type 2 (North American genotype) porcine reproductive and respiratory syndrome virus in infected boar. Virol J (2013) 10:156. doi:10.1186/1743-422X-10-156
13. Holtkamp DJ, Polson DD, Torremorell M, Morrison B, Classen DM, Becton L, et al. Terminology for classifying swine herds by porcine reproductive and respiratory syndrome virus status. Tierarztl Prax Ausg G Grosstiere Nutztiere (2011) 39:101-12
14. Corzo CA, Mondaca E, Wayne S, Torremorell M, Dee S, Davies P, et al. Control and elimination of porcine reproductive and respiratory syndrome virus. Virus Res (2010) 154:185-92. doi:10.1016/j.virusres.2010.08.016
15. Dee S, Cano JP, Spronk G, Reicks D, Ruen P, Pitkin A, et al. Evaluation of the long-term effect of air filtration on the occurrence of new PRRSV infections in large breeding herds in swine-dense regions. Viruses (2012) 4:654-62. doi:10.3390/v4050654
16. Van Reeth K. Pathogenesis and clinical aspects of a respiratory porcine reproductive and respiratory syndrome virus infection. Vet Microbiol (1997) 55:223-30. doi:10.1016/S0378-1135(96)01331-4
17. van Gucht S, van Reeth K, Pensaert M. Interaction between porcine reproductive-respiratory syndrome virus and bacterial endotoxin in the lungs of pigs: potentiation of cytokine production and respiratory disease. J Clin Microbiol (2003) 41:960-6. doi:10.1128/JCM.41.3.960-966.2003
18. Zhang K, Hou Q, Zhong Z, Li X, Chen H, Li W, et al. Porcine reproductive and respiratory syndrome virus activates inflammasomes of porcine alveolar macrophages via its small envelope protein E. Virology (2013) 442:156-62. doi:10.1016/j.virol.2013.04.007
19. Brambilla G, Civitareale C, Ballerini A, Fiori M, Amadori M, Archetti LI, et al. Response to oxidative stress as a welfare parameter in swine. Redox Rep (2002) 7:159-63. doi:10.1179/135100002125000406
20. Grimble RF. Dietary lipids and the inflammatory response. Proc Nutr Soc (1998) 57:535-42. doi:10.1079/PNS19980078
21. Zhiping W, Malmberg P, Larsson BM, Larsson K, Larsson L, Saraf A. Exposure to bacteria in swine-house dust and acute inflammatory reactions in humans. Am J Respir Crit Care Med (1996) 154:1261-6. doi:10.1164/ajrccm.154.5.8912733
22. Stadejek T, Oleksiewicz MB, Potapchuk D, Podgorska K. Porcine reproductive and respiratory syndrome virus strains of exceptional diversity in Eastern Europe support the definition of new genetic subtypes. J Gen Virol (2006) 87(Pt 7):1835-41. doi:10.1099/vir.0.81782-0
23. Petry DB, Holl JW, Weber JS, Doster AR, Osorio FA, Johnson RK. Biological responses to porcine respiratory and reproductive syndrome virus in pigs of two genetic populations. J Anim Sci (2005) 83:1494-502
24. Reiner G, Willems H, Pesch S, Ohlinger VF. Variation in resistance to the porcine reproductive and respiratory syndrome virus (PRRSV) in pietrain and miniature pigs. J Anim Breed Genet (2010) 127:100-6. doi:10.1111/j.1439-0388.2009.00818.x
25. Lewis CR, Ait-Ali T, Clapperton M, Archibald AL, Bishop S. Genetic perspectives on host responses to porcine reproductive and respiratory syndrome (PRRS). Viral Immunol (2007) 20:343-58. doi:10.1089/vim.2007.0024
26. Ait-Ali T, Wilson AD, Carre W, Westcott DG, Frossard JP, Mellencamp MA, et al. Host inhibits replication of European porcine reproductive and respiratory syndrome virus in macrophages by altering differential regulation of type-I interferon transcriptional response. Immunogenetics (2011) 63:437-48. doi:10.1007/s00251-011-0518-8
27. Klinge KL, Vaughn EM, Roof MB, Bautista EM, Murtaugh MP. Age-dependent resistance to porcine reproductive and respiratory syndrome virus replication in swine. Virol J (2009) 6:177. doi:10.1186/1743-422X-6-177
28. Karniychuk UU, Nauwynck HJ. Pathogenesis and prevention of placental and transplacental porcine reproductive and respiratory syndrome virus infection. Vet Res (2013) 44:95. doi:10.1186/1297-9716-44-95
29. Halbur PG. Update on abortion storms and sow mortality. J Swine Health Prod (1997) 5:73-7
30. Lv J, Zhang J, Sun Z, Liu W, Yuan S. An infectious cDNA clone of a highly pathogenic porcine reproductive and respiratory syndrome virus variant associated with porcine high fever syndrome. J Gen Virol (2008) 89(Pt 9):2075-9. doi:10.1099/vir.0.2008/001529-0
31. Karniychuk UU, Geldhof M, Vanhee M, Van Doorsselaere J, Saveleva TA, Nauwynck HJ. Pathogenesis and antigenic characterization of a new East European subtype 3 porcine reproductive and respiratory syndrome virus isolate. BMC Vet Res (2010) 6:30. doi:10.1186/1746-6148-6-30
32. Qiao S, Feng L, Bao D, Guo J, Wan B, Xiao Z, et al. Porcine reproductive and respiratory syndrome virus and bacterial endotoxin act in synergy to amplify the inflammatory response of infected macrophages. Vet Microbiol (2011) 149:213-20. doi:10.1016/j.vetmic.2010.11.006
33. Frossard JP, Fearnley C, Naidu B, Errington J, Westcott DG, Drew TW. Porcine reproductive and respiratory syndrome virus: antigenic and molecular diversity of British isolates and implications for diagnosis. Vet Microbiol (2012) 158:308-15. doi:10.1016/j.vetmic.2012.03.004
34. Xiao Z, Batista L, Dee S, Halbur P, Murtaugh MP. 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) 78:5923-33. doi:10.1128/JVI.78.11.5923-5933.2004
35. Basta S, Carrasco CP, Knoetig SM, Rigden RC, Gerber H, Summerfield A, et al. Porcine alveolar macrophages: poor accessory or effective suppressor cells for T-lymphocytes. Vet Immunol Immunopathol (2000) 77:177-90. doi:10.1016/S0165-2427(00)00237-3
36. Thanawongnuwech R, Brown GB, Halbur PG, Roth JA, Royer RL, Thacker BJ. Pathogenesis of porcine reproductive and respiratory syndrome virus-induced increase in susceptibility to Streptococcus suis infection. Vet Pathol (2000) 37:143-52. doi:10.1354/vp.37-2-143
37. Mateu E, Diaz I. The challenge of PRRS immunology. Vet J (2008) 177:345-51. doi:10.1016/j.tvjl.2007.05.022
38. Dotti S, Guadagnini G, Salvini F, Razzuoli E, Ferrari M, Alborali GL, et al. Time-course of antibody and cell-mediated immune responses to porcine reproductive and respiratory syndrome virus under field conditions. Res Vet Sci (2013) 94:510-7. doi:10.1016/j.rvsc.2012.12.003
39. Wesley RD, Lager KM, Kehrli ME Jr. Infection with Porcine reproductive and respiratory syndrome virus stimulates an early gamma interferon response in the serum of pigs. Can J Vet Res (2006) 70:176-82
40. Razzuoli E, Dotti S, Villa R, Martinelli N, Ferrari M, Amadori M. Early immune response to infection by attenuated and non-attenuated, type I PRRS virus strains. Proceedings 4th European Veterinary Immunology Workshop. Edinburgh: (2012). 23 p
41. Yoo D, Song C, Sun Y, Du Y, Kim O, Liu HC. Modulation of host cell responses and evasion strategies for porcine reproductive and respiratory syndrome virus. Virus Res (2010) 154:48-60. doi:10.1016/j.virusres.2010.07.019
42. Sang Y, Rowland RR, Blecha F. Interaction between innate immunity and porcine reproductive and respiratory syndrome virus. Anim Health Res Rev (2011) 12:149-67. doi:10.1017/S1466252311000144
43. Silva-Campa E, Flores-Mendoza L, Resendiz M, Pinelli-Saavedra A, Mata-Haro V, Mwangi W, et al. Induction of T helper 3 regulatory cells by dendritic cells infected with porcine reproductive and respiratory syndrome virus. Virology (2009) 387:373-9. doi:10.1016/j.virol.2009.02.033
44. Gimeno M, Darwich L, Diaz I, de la Torre E, Pujols J, Martin M, et al. Cytokine profiles and phenotype regulation of antigen presenting cells by genotype-I porcine reproductive and respiratory syndrome virus isolates. Vet Res (2011) 42:9. doi:10.1186/1297-9716-42-9
45. Thanawongnuwech R, Young TF, Thacker BJ, Thacker EL. Differential production of proinflammatory cytokines: in vitro PRRSV and Mycoplasma hyopneumoniae co-infection model. Vet Immunol Immunopathol (2001) 79:115-27. doi:10.1016/S0165-2427(01)00243-4
46. Welch SK, Calvert JG. A brief review of CD163 and its role in PRRSV infection. Virus Res (2010) 154:98-103. doi:10.1016/j.virusres.2010.07.018
47. Han Z, Liu Y, Wang G, He Y, Hu S, Li Y, et al. Comparative analysis of immune responses in pigs to high and low pathogenic porcine reproductive and respiratory syndrome viruses isolated in China. Transbound Emerg Dis (2013). doi:10.1111/tbed.12190
48. Morgan SB, Graham SP, Salguero FJ, Sanchez Cordon PJ, Mokhtar H, Rebel JM, et al. Increased pathogenicity of European porcine reproductive and respiratory syndrome virus is associated with enhanced adaptive responses and viral clearance. Vet Microbiol (2013) 163:13-22. doi:10.1016/j.vetmic.2012.11.024
49. Ladinig A, Lunney J, Ashley C, Harding J. Exploring cytokine profiles of pregnant gilts infected with porcine reproductive and respiratory syndrome virus. Proceedings 10th International Veterinary Immunology Symposium. Milan: (2013). 163 p
50. Baumann A, Mateu E, Murtaugh MP, 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. doi:10.1186/1297-9716-44-33
51. Lauw FN, Pajkrt D, Hack CE, Kurimoto M, van Deventer SJ, van der Poll T. Proinflammatory effects of IL-10 during human endotoxemia. J Immunol (2000) 165:2783-9. doi:10.4049/jimmunol.165.5.2783
52. Murtaugh MP, Xiao Z, Zuckermann F. Immunological responses of swine to porcine reproductive and respiratory syndrome virus infection. Viral Immunol (2002) 15:533-47. doi:10.1089/088282402320914485
53. Yoon KJ, Wu LL, Zimmerman JJ, Platt KB. Field isolates of porcine reproductive and respiratory syndrome virus (PRRSV) vary in their susceptibility to antibody dependent enhancement (ADE) of infection. Vet Microbiol (1997) 55:277-87. doi:10.1016/S0378-1135(96)01338-7
54. Yang Q, Zhang Y, Chen J, Zhou Y, Li N, Qin Y, et al. Ligation of porcine Fc gamma receptor I inhibits levels of antiviral cytokine in response to PRRSV infection in vitro. Virus Res (2013) 173:421-5. doi:10.1016/j.virusres.2013.02.005
55. Yu Y, Cai X, Wang G, Kong N, Liu Y, Xiao Y, et al. Anti-idiotypic antibodies reduce efficacy of the attenuated vaccine against highly pathogenic PRRSV challenge. BMC Vet Res (2014) 10:39. doi:10.1186/1746-6148-10-39
56. Costers S, Lefebvre DJ, Goddeeris B, Delputte PL, Nauwynck HJ. Functional impairment of PRRSV-specific peripheral CD3+CD8high cells. Vet Res (2009) 40:46. doi:10.1051/vetres/2009029
57. Costers S, Delputte PL, Nauwynck HJ. Porcine reproductive and respiratory syndrome virus-infected alveolar macrophages contain no detectable levels of viral proteins in their plasma membrane and are protected against antibody-dependent, complement-mediated cell lysis. J Gen Virol (2006) 87(Pt 8):2341-51. doi:10.1099/vir.0.81808-0
58. Brockmeier SL, Lager KM, Grubman MJ, Brough DE, Ettyreddy D, Sacco RE, et al. 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) 22:173-80. doi:10.1089/vim.2008.0075
59. Loving CL, Brockmeier SL, Vincent AL, Lager KM, Sacco RE. Differences in clinical disease and immune response of pigs challenged with a high-dose versus low-dose inoculum of porcine reproductive and respiratory syndrome virus. Viral Immunol (2008) 21:315-25. doi:10.1089/vim.2008.0038
60. Meier WA, Galeota J, Osorio FA, Husmann RJ, Schnitzlein WM, Zuckermann FA. Gradual development of the interferon-gamma response of swine to porcine reproductive and respiratory syndrome virus infection or vaccination. Virology (2003) 309:18-31. doi:10.1016/S0042-6822(03)00009-6
61. Lopez OJ, Osorio FA. Role of neutralizing antibodies in PRRSV protective immunity. Vet Immunol Immunopathol (2004) 102:155-63. doi:10.1016/j.vetimm.2004.09.005
62. Osorio FA, Galeota JA, Nelson E, Brodersen B, Doster A, Wills R, et al. 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. doi:10.1006/viro.2002.1612
63. Lopez OJ, Oliveira MF, Garcia EA, Kwon BJ, Doster A, 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) 14:269-75. doi:10.1128/CVI.00304-06
64. Diaz I, Gimeno M, Darwich L, Navarro N, Kuzemtseva L, Lopez S, et al. Characterization of homologous and heterologous adaptive immune responses in porcine reproductive and respiratory syndrome virus infection. Vet Res (2012) 43:30. doi:10.1186/1297-9716-43-30
65. Zuckermann FA, Garcia EA, Luque ID, Christopher-Hennings J, Doster A, Brito M, et al. 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. doi:10.1016/j.vetmic.2007.02.009
66. Kimman TG, Cornelissen LA, Moormann RJ, Rebel JM, Stockhofe-Zurwieden N. Challenges for porcine reproductive and respiratory syndrome virus (PRRSV) vaccinology. Vaccine (2009) 27:3704-18. doi:10.1016/j.vaccine.2009.04.022
67. Ferrari L, Martelli P, Saleri R, De Angelis E, Cavalli V, Bresaola M, et al. 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. doi:10.1016/j.vetimm.2012.11.006
68. Onyekaba CO, Harty JT, Even C, Hu BG, Plagemann PG. Persistent infection of mice by lactate dehydrogenase-elevating virus: effects of immunosuppression on virus replication and antiviral immune responses. Virus Res (1989) 14:297-315. doi:10.1016/0168-1702(89)90023-3
69. Rowland RR, Even C, Anderson GW, Chen Z, Hu B, Plagemann PG. Neonatal infection of mice with lactate dehydrogenase-elevating virus results in suppression of humoral antiviral immune response but does not alter the course of viraemia or the polyclonal activation of B cells and immune complex formation. J Gen Virol (1994) 75(Pt 5):1071-81. doi:10.1099/0022-1317-75-5-1071
70. Diaz I, Ganges L, Galindo-Cardiel I, Tarradas J, Alvarez B, Lorca-Oro C, et al. Immunization with DNA vaccines containing porcine reproductive and respiratory syndrome virus open reading frames 5, 6, and 7 may be related to the exacerbation of clinical disease after an experimental challenge. Viral Immunol (2013) 26:93-101. doi:10.1089/vim.2012.0041
71. Labarque GG, Nauwynck HJ, Van Reeth K, 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(Pt 5):1327-34
72. Nauwynck HJ, Van Gorp H, Vanhee M, Karniychuk U, Geldhof M, Cao A, et al. Micro-dissecting the pathogenesis and immune response of PRRSV infection paves the way for more efficient PRRSV vaccines. Transbound Emerg Dis (2012). doi:10.1111/j.1865-1682.2011.01292.x
73. Saalmuller A, Hirt W, Maurer S, Weiland E. Discrimination between two subsets of porcine CD8+ cytolytic T lymphocytes by the expression of CD5 antigen. Immunology (1994) 81:578-83
74. Mair KH, Essler SE, Patzl M, Storset AK, Saalmuller A, Gerner W. NKp46 expression discriminates porcine NK cells with different functional properties. Eur J Immunol (2012) 42:1261-71. doi:10.1002/eji.201141989
75. Amadori M, Cristiano A, Ferrari M. Constitutive expression of interferons in swine leukocytes. Res Vet Sci (2010) 88:64-71. doi:10.1016/j.rvsc.2009.05.011
76. Horowitz A, Stegmann KA, Riley EM. Activation of natural killer cells during microbial infections. Front Immunol (2011) 2:88. doi:10.3389/fimmu.2011.00088
77. Dwivedi V, Manickam C, Binjawadagi B, Linhares D, Murtaugh MP, Renukaradhya GJ. 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. doi:10.1186/1743-422X-9-45
78. Mair KH, Sedlak C, Kaser T, Pasternak A, Levast B, Gerner W, et al. The porcine innate immune system: an update. Dev Comp Immunol (2014) 45:321-43. doi:10.1016/j.dci.2014.03.022
79. Martelli P, Gozio S, Ferrari L, Rosina S, De Angelis E, Quintavalla C, et al. 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) 27:3788-99. doi:10.1016/j.vaccine.2009.03.028
80. Borghetti P, Saleri R, Ferrari L, Morganti M, De Angelis E, Franceschi V, et al. Cytokine expression, glucocorticoid and growth hormone changes after porcine reproductive and respiratory syndrome virus (PRRSV-1) infection in vaccinated and unvaccinated naturally exposed pigs. Comp Immunol Microbiol Infect Dis (2011) 34:143-55. doi:10.1016/j.cimid.2010.06.004
81. Lopez Fuertes L, Domenech N, Alvarez B, Ezquerra A, Dominguez J, Castro JM, et al. Analysis of cellular immune response in pigs recovered from porcine respiratory and reproductive syndrome infection. Virus Res (1999) 64:33-42. doi:10.1016/S0168-1702(99)00073-8
82. Batista L, Pijoan C, Dee S, Olin M, Molitor T, Joo HS, et al. Virological and immunological responses to porcine reproductive and respiratory syndrome virus in a large population of gilts. Can J Vet Res (2004) 68:267-73
83. Stadejek T, Jablonski A, Chabros K, Skrzypiec E, Pejsak Z. Analysis of circulation of porcine reproductive and respiratory syndrome virus in 22 polish pig farms: implications for diagnosis and control. Proceedings EuroPRRS2011 'Understanding and combating PRRS in Europe'. Novi Sad: (2011). p. 25-6
84. Knetter SM, Tuggle CK, Wannemuehler MJ, Ramer-Tait AE. Organic barn dust extract exposure impairs porcine macrophage function in vitro: implications for respiratory health. Vet Immunol Immunopathol (2014) 157:20-30. doi:10.1016/j.vetimm.2013.10.019
85. Meng XJ. Heterogeneity of porcine reproductive and respiratory syndrome virus: implications for current vaccine efficacy and future vaccine development. Vet Microbiol (2000) 74:309-29. doi:10.1016/S0378-1135(00)00196-6
86. Nodelijk G, de Jong MC, van Leengoed LA, Wensvoort G, Pol JM, Steverink PJ, et al. A quantitative assessment of the effectiveness of PRRSV vaccination in pigs under experimental conditions. Vaccine (2001) 19:3636-44. doi:10.1016/S0264-410X(01)00099-8
87. Scortti M, Prieto C, Alvarez E, Simarro I, Castro JM. Failure of an inactivated vaccine against porcine reproductive and respiratory syndrome to protect gilts against a heterologous challenge with PRRSV. Vet Rec (2007) 161:809-13
88. Plana-Duran J, Bastons M, Urniza A, Vayreda M, Vila X, Mane H. Efficacy of an inactivated vaccine for prevention of reproductive failure induced by porcine reproductive and respiratory syndrome virus. Vet Microbiol (1997) 55:361-70. doi:10.1016/S0378-1135(96)01317-X
89. Papatsiros VG, Alexopoulos C, Kritas SK, Koptopoulos G, Nauwynck HJ, Pensaert MB, et al. Long-term administration of a commercial porcine reproductive and respiratory syndrome virus (PRRSV)-inactivated vaccine in PRRSV-endemically infected sows. J Vet Med B Infect Dis Vet Public Health (2006) 53:266-72. doi:10.1111/j.1439-0450.2006.00965.x
90. Madsen KG, Hansen CM, Madsen ES, Strandbygaard B, Botner A, Sorensen KJ. Sequence analysis of porcine reproductive and respiratory syndrome virus of the American type collected from Danish swine herds. Arch Virol (1998) 143:1683-700. doi:10.1007/s007050050409
91. Diaz 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 (2006) 351:249-59. doi:10.1016/j.virol.2006.03.046
92. de Lima M, Kwon B, Ansari IH, Pattnaik AK, Flores EF, Osorio FA. Development of a porcine reproductive and respiratory syndrome virus differentiable (DIVA) strain through deletion of specific immunodominant epitopes. Vaccine (2008) 26:3594-600. doi:10.1016/j.vaccine.2008.04.078
93. Fang Y, Rowland RR, Roof M, Lunney JK, Christopher-Hennings J, Nelson EA. 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 (2006) 80:11447-55. doi:10.1128/JVI.01032-06
94. Prieto C, Alvarez E, Martinez-Lobo FJ, Simarro I, Castro JM. Similarity of European porcine reproductive and respiratory syndrome virus strains to vaccine strain is not necessarily predictive of the degree of protective immunity conferred. Vet J (2008) 175:356-63. doi:10.1016/j.tvjl.2007.01.021
95. Roca M, Gimeno M, Bruguera S, Segales J, Diaz I, Galindo-Cardiel IJ, et al. 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) 193:92-6. doi:10.1016/j.tvjl.2011.11.019
96. Dotti S, Villa R, Sossi E, Guadagnini G, Salvini F, Ferrari M, et al. Comparative evaluation of PRRS virus infection in vaccinated and naive pigs. Res Vet Sci (2011) 90:218-25. doi:10.1016/j.rvsc.2010.06.011
97. Li X, Qiu L, Yang Z, Dang R, Wang X. Emergency vaccination alleviates highly pathogenic porcine reproductive and respiratory syndrome virus infection after contact exposure. BMC Vet Res (2013) 9:26. doi:10.1186/1746-6148-9-26
98. Cano JP, Dee SA, Murtaugh MP, Trincado CA, Pijoan CB. Effect of vaccination with a modified-live porcine reproductive and respiratory syndrome virus vaccine on dynamics of homologous viral infection in pigs. Am J Vet Res (2007) 68:565-71. doi:10.2460/ajvr.68.5.565
99. Cano JP, Dee SA, Murtaugh MP, Pijoan C. Impact of a modified-live porcine reproductive and respiratory syndrome virus vaccine intervention on a population of pigs infected with a heterologous isolate. Vaccine (2007) 25:4382-91. doi:10.1016/j.vaccine.2007.03.031
100. Dee SA. Using vaccination and unidirectional pig flow to control PRRSV transmission. J Swine Health Prod (1998) 6:21-5
101. Hu J, Zhang C. Porcine reproductive and respiratory syndrome virus vaccines: current status and strategies to a universal vaccine. Transbound Emerg Dis (2013). doi:10.1111/tbed.12016
102. Thanawongnuwech R, Suradhat S. Taming PRRSV: revisiting the control strategies and vaccine design. Virus Res (2010) 154:133-40. doi:10.1016/j.virusres.2010.09.003
103. Dwivedi V, Manickam C, Patterson R, Dodson K, Murtaugh M, Torrelles JB, et al. Cross-protective immunity to porcine reproductive and respiratory syndrome virus by intranasal delivery of a live virus vaccine with a potent adjuvant. Vaccine (2011) 29:4058-66. doi:10.1016/j.vaccine.2011.03.006
104. Dwivedi V, Manickam C, Patterson R, Dodson K, Weeman M, Renukaradhya GJ. Intranasal delivery of whole cell lysate of Mycobacterium tuberculosis induces protective immune responses to a modified live porcine reproductive and respiratory syndrome virus vaccine in pigs. Vaccine (2011) 29:4067-76. doi:10.1016/j.vaccine.2011.03.005
105. Manickam C, Dwivedi V, Miller J, Papenfuss T, Renukaradhya GJ. Mycobacterium tuberculosis whole cell lysate enhances proliferation of CD8 positive lymphocytes and nitric oxide secretion in the lungs of live porcine respiratory and reproductive syndrome virus vaccinated pigs. Viral Immunol (2013) 26:102-8. doi:10.1089/vim.2012.0065
106. Dwivedi V, Manickam C, Binjawadagi B, Renukaradhya GJ. PLGA nanoparticle entrapped killed porcine reproductive and respiratory syndrome virus vaccine helps in viral clearance in pigs. Vet Microbiol (2013) 166:47-58. doi:10.1016/j.vetmic.2013.04.029
107. Delrue I, Delputte PL, Nauwynck HJ. Assessing the functionality of viral entry-associated domains of porcine reproductive and respiratory syndrome virus during inactivation procedures, a potential tool to optimize inactivated vaccines. Vet Res (2009) 40:62. doi:10.1051/vetres/2009047
108. Vanhee M, Delputte PL, Delrue I, Geldhof MF, Nauwynck HJ. Development of an experimental inactivated PRRSV vaccine that induces virus-neutralizing antibodies. Vet Res (2009) 40:63. doi:10.1051/vetres/2009046
109. Zhang L, Bai J, Liu J, Wang X, Li Y, Jiang P. Toll-like receptor ligands enhance the protective effects of vaccination against porcine reproductive and respiratory syndrome virus in swine. Vet Microbiol (2013) 164:253-60. doi:10.1016/j.vetmic.2013.02.016
110. Huang YW, Meng XJ. Novel strategies and approaches to develop the next generation of vaccines against porcine reproductive and respiratory syndrome virus (PRRSV). Virus Res (2010) 154:141-9. doi:10.1016/j.virusres.2010.07.020
111. Cruz JL, Zuniga S, Becares M, Sola I, Ceriani JE, Juanola S, et al. Vectored vaccines to protect against PRRSV. Virus Res (2010) 154:150-60. doi:10.1016/j.virusres.2010.06.017
112. Charerntantanakul W. Adjuvants for porcine reproductive and respiratory syndrome virus vaccines. Vet Immunol Immunopathol (2009) 129:1-13. doi:10.1016/j.vetimm.2008.12.018
113. Fachinger V, Bischoff R, Jedidia SB, Saalmuller A, Elbers K. The effect of vaccination against porcine circovirus type 2 in pigs suffering from porcine respiratory disease complex. Vaccine (2008) 26:1488-99. doi:10.1016/j.vaccine.2007.11.053
114. Kixmoller M, Ritzmann M, Eddicks M, Saalmuller A, Elbers K, Fachinger V. Reduction of PMWS-associated clinical signs and co-infections by vaccination against PCV2. Vaccine (2008) 26:3443-51. doi:10.1016/j.vaccine.2008.04.032
115. Tico G, Segales J, Martinez J. The blurred border between porcine circovirus type 2-systemic disease and porcine respiratory disease complex. Vet Microbiol (2013) 163:242-7. doi:10.1016/j.vetmic.2013.01.001
116. Carter QL, Curiel RE. Interleukin-12 (IL-12) ameliorates the effects of porcine respiratory and reproductive syndrome virus (PRRSV) infection. Vet Immunol Immunopathol (2005) 107:105-18. doi:10.1016/j.vetimm.2005.04.003
117. Albina E, Carrat C, Charley B. Interferon-alpha response to swine arterivirus (PoAV), the porcine reproductive and respiratory syndrome virus. J Interferon Cytokine Res (1998) 18:485-90. doi:10.1089/jir.1998.18.485
118. Bautista EM, Molitor TW. IFN gamma inhibits porcine reproductive and respiratory syndrome virus replication in macrophages. Arch Virol (1999) 144:1191-200. doi:10.1007/s007050050578
119. Cummins JM, Krakowka GS, Thompson CG. Systemic effects of interferons after oral administration in animals and humans. Am J Vet Res (2005) 66:164-76. doi:10.2460/ajvr.2005.66.164
120. Begni B, Amadori M, Ritelli M, Podavini D. Effects of IFN-alpha on the inflammatory response of swine leukocytes to bacterial endotoxin. J Interferon Cytokine Res (2005) 25:202-8. doi:10.1089/jir.2005.25.202
121. Tompkins WA. Immunomodulation and therapeutic effects of the oral use of interferon-alpha: mechanism of action. J Interferon Cytokine Res (1999) 19:817-28. doi:10.1089/107999099313325
122. Amadori M. The role of IFN-alpha as homeostatic agent in the inflammatory response: a balance between danger and response? J Interferon Cytokine Res (2007) 27:181-9. doi:10.1089/jir.2006.0110
123. Pedretti E, Passeri B, Amadori M, Isola P, Di Pede P, Telera A, et al. Low-dose interferon-alpha treatment for feline immunodeficiency virus infection. Vet ImmunolImmunopathol (2006) 109:245-54. doi:10.1016/j.vetimm.2005.08.020
124. Delputte PL, Van Breedam W, Barbe F, Van Reeth K, Nauwynck HJ. IFN-alpha treatment enhances porcine arterivirus infection of monocytes via upregulation of the porcine arterivirus receptor sialoadhesin. J Interferon Cytokine Res (2007) 27:757-66. doi:10.1089/jir.2007.0001
125. Razzuoli E, Villa R, Amadori M. IPEC-J2 cells as reporter system of the anti-inflammatory control actions of interferon-alpha. J Interferon Cytokine Res (2013) 33:597-605. doi:10.1089/jir.2012.0127
126. Anderson P, Phillips K, Stoecklin G, Kedersha N. Post-transcriptional regulation of proinflammatory proteins. J Leukoc Biol (2004) 76:42-7. doi:10.1189/jlb.1103536
127. Delgado-Ortega M, Marc D, Dupont J, Trapp S, Berri M, Meurens F. SOCS proteins in infectious diseases of mammals. Vet Immunol Immunopathol (2013) 151:1-19. doi:10.1016/j.vetimm.2012.11.008
128. Lemke G, Rothlin CV. Immunobiology of the TAM receptors. Nat Rev Immunol (2008) 8:327-36. doi:10.1038/nri2303