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Annual Review of Animal Biosciences

Volume 4, 2016

Porcine Reproductive and Respiratory Syndrome Virus (PRRSV): Pathogenesis and Interaction with the Immune System

Abstract

This review addresses important issues of porcine reproductive and respiratory syndrome virus (PRRSV) infection, immunity, pathogenesis, and control. Worldwide, PRRS is the most economically important infectious disease of pigs. We highlight the latest information on viral genome structure, pathogenic mechanisms, and host immunity, with a special focus on immune factors that modulate PRRSV infections during the acute and chronic/persistent disease phases. We address genetic control of host resistance and probe effects of PRRSV infection on reproductive traits. A major goal is to identify cellular/viral targets and pathways for designing more effective vaccines and therapeutics. Based on progress in viral reverse genetics, host transcriptomics and genomics, and vaccinology and adjuvant technologies, we have identified new areas for PRRS control and prevention. Finally, we highlight the gaps in our knowledge base and the need for advanced molecular and immune tools to stimulate PRRS research and field applications.

Keyword(s): fetal infection, genetic control, host immunity, porcine reproductive and respiratory syndrome, PRRSV, vaccine responses
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/content/journals/10.1146/annurev-animal-022114-111025
2016-02-15
2024-04-26
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Literature Cited

  1. Holtkamp DJ, Kliebenstein JB, Neumann EJ, Zimmerman J, Rotto HF. 1.  et al. 2013. Assessment of the economic impact of porcine reproductive and respiratory syndrome virus on United States pork producers. J. Swine Health Prod. 21:72–84 [Google Scholar]
  2. Snijder EJ, Kikkert M, Fang Y. 2.  2013. Arterivirus molecular biology and pathogenesis. J. Gen. Virol. 94:2141–63 [Google Scholar]
  3. Dokland T. 3.  2010. The structural biology of PRRSV. Virus Res. 154:86–97 [Google Scholar]
  4. Fang Y, Snijder EJ. 4.  2010. The PRRSV replicase: exploring the multifunctionality of an intriguing set of nonstructural proteins. Virus Res. 154:61–76 [Google Scholar]
  5. Fang Y, Treffers EE, Li Y, Tas A, Sun Z. 5.  et al. 2012. Efficient −2 frameshifting by mammalian ribosomes to synthesize an additional arterivirus protein. PNAS 109:E2920–28 [Google Scholar]
  6. Li Y, Treffers EE, Napthine S, Tas A, Zhu L. 6.  et al. 2014. Transactivation of programmed ribosomal frameshifting by a viral protein. PNAS 111:E2172–81 [Google Scholar]
  7. Duan X, Nauwynck HJ, Pensaert MB. 7.  1997. Effects of origin and state of differentiation and activation of monocytes/macrophages on their susceptibility to porcine reproductive and respiratory syndrome virus (PRRSV). Arch. Virol. 142:2483–97 [Google Scholar]
  8. Loving CL, Brockmeier SL, Sacco RE. 8.  2007. Differential type I interferon activation and susceptibility of dendritic cell populations to porcine arterivirus. Immunology 120:217–29 [Google Scholar]
  9. Kim HS, Kwang J, Yoon IJ, Joo HS, Frey ML. 9.  1993. Enhanced replication of porcine reproductive and respiratory syndrome (PRRS) virus in a homogeneous subpopulation of MA-104 cell line. Arch. Virol. 133:477–83 [Google Scholar]
  10. Nauwynck HJ, Duan X, Favoreel HW, Van Oostveldt P, Pensaert MB. 10.  1999. Entry of porcine reproductive and respiratory syndrome virus into porcine alveolar macrophages via receptor-mediated endocytosis. J. Gen. Virol. 80:297–305 [Google Scholar]
  11. Welch SK, Calvert JG. 11.  2010. A brief review of CD163 and its role in PRRSV infection. Virus Res. 154:98–103 [Google Scholar]
  12. Van Breedam W, Van Gorp H, Zhang JQ, Crocker PR, Delputte PL, Nauwynck HJ. 12.  2010. The M/GP(5) glycoprotein complex of porcine reproductive and respiratory syndrome virus binds the sialoadhesin receptor in a sialic acid-dependent manner. PLOS Pathog. 6:e1000730 [Google Scholar]
  13. Prather RS, Rowland RR, Ewen C, Trible B, Kerrigan M. 13.  et al. 2013. An intact sialoadhesin (Sn/SIGLEC1/CD169) is not required for attachment/internalization of the porcine reproductive and respiratory syndrome virus. J. Virol. 87:9538–46 [Google Scholar]
  14. Calvert JG, Slade DE, Shields SL, Jolie R, Mannan RM. 14.  et al. 2007. CD163 expression confers susceptibility to porcine reproductive and respiratory syndrome viruses. J. Virol. 81:7371–79 [Google Scholar]
  15. Das PB, Dinh PX, Ansari IH, de Lima M, Osorio FA, Pattnaik AK. 15.  2010. The minor envelope glycoproteins GP2a and GP4 of porcine reproductive and respiratory syndrome virus interact with the receptor CD163. J. Virol. 84:1731–40 [Google Scholar]
  16. Tian D, Wei Z, Zevenhoven-Dobbe JC, Liu R, Tong G. 16.  et al. 2012. Arterivirus minor envelope proteins are a major determinant of viral tropism in cell culture. J. Virol. 86:3701–12 [Google Scholar]
  17. Wills RW, Zimmerman JJ, Yoon KJ, Swenson SL, McGinley MJ. 17.  et al. 1997. Porcine reproductive and respiratory syndrome virus: a persistent infection. Vet. Microbiol. 55:231–40 [Google Scholar]
  18. Allende R, Laegreid WW, Kutish GF, Galeota JA, Wills RW, Osorio FA. 18.  2000. Porcine reproductive and respiratory syndrome virus: description of persistence in individual pigs upon experimental infection. J. Virol. 74:10834–37 [Google Scholar]
  19. Rowland RRR, Lawson S, Rossow K, Benfield DA. 19.  2003. Lymphoid tissue tropism of porcine reproductive and respiratory syndrome virus replication during persistent infection of pigs originally exposed to virus in utero. Vet. Microbiol. 96:219–35 [Google Scholar]
  20. Christopher-Hennings J, Nelson EA, Althouse GC, Lunney J. 20.  2008. Comparative antiviral and proviral factors in semen and vaccines for preventing viral dissemination from the male reproductive tract and semen. Anim. Health Res. Rev. 9:59–69 [Google Scholar]
  21. Wills RW, Doster AR, Galeota JA, Sur JH, Osorio FA. 21.  2003. Duration of infection and proportion of pigs persistently infected with porcine reproductive and respiratory syndrome virus. J. Clin. Microbiol. 41:58–62 [Google Scholar]
  22. Keffaber KK. 22.  1989. Reproductive failure of unknown etiology. Am. Assoc. Swine Pract. Newsl. 1:1–9 [Google Scholar]
  23. Wensvoort G, Terpstra C, Pol JM, ter Laak EA, Bloemraad M. 23.  et al. 1991. Mystery swine disease in The Netherlands: the isolation of Lelystad virus. Vet. Q. 13:121–30 [Google Scholar]
  24. Allende R, Lewis TL, Lu Z, Rock DL, Kutish GF. 24.  et al. 1999. North American and European porcine reproductive and respiratory syndrome viruses differ in non-structural protein coding regions. J. Gen. Virol. 80:307–15 [Google Scholar]
  25. Nelsen CJ, Murtaugh MP, Faaberg KS. 25.  1999. Porcine reproductive and respiratory syndrome virus comparison: divergent evolution on two continents. J. Virol. 73:270–80 [Google Scholar]
  26. Plagemann PG. 26.  2003. Porcine reproductive and respiratory syndrome virus: origin hypothesis. Emerg. Infect. Dis. 9:903–8 [Google Scholar]
  27. Mengeling WL, Lager KM, Vorwald AC. 27.  1998. Clinical consequences of exposing pregnant gilts to strains of porcine reproductive and respiratory syndrome (PRRS) virus isolated from field cases of “atypical” PRRS. Am. J. Vet. Res. 59:1540–44 [Google Scholar]
  28. Han J, Wang Y, Faaberg KS. 28.  2006. Complete genome analysis of RFLP 184 isolates of porcine reproductive and respiratory syndrome virus. Virus Res. 122:175–82 [Google Scholar]
  29. Tian K, Yu X, Zhao T, Feng Y, Cao Z. 29.  et al. 2007. Emergence of fatal PRRSV variants: unparalleled outbreaks of atypical PRRS in China and molecular dissection of the unique hallmark. PLOS ONE 2e526
  30. Karniychuk UU, Geldhof M, Vanhee M, Van Doorsselaere J, Saveleva TA, Nauwynck HJ. 30.  2010. Pathogenesis and antigenic characterization of a new East European subtype 3 porcine reproductive and respiratory syndrome virus isolate. BMC Vet. Res. 6:30 [Google Scholar]
  31. Han M, Yoo D. 31.  2014. Engineering the PRRS virus genome: updates and perspectives. Vet. Microbiol. 174:279–95 [Google Scholar]
  32. Brockmeier SL, Halbur PG, Thacker EL. 32.  2002. Porcine respiratory disease complex. Polymicrobial Diseases KA Brogden, JM Guthmiller 231–58 Washington, DC: ASM Press [Google Scholar]
  33. Thacker EL, Halbur PG, Ross RF, Thanawongnuwech R, Thacker BJ. 33.  1999. Mycoplasma hyopneumoniae potentiation of porcine reproductive and respiratory syndrome virus-induced pneumonia. J. Clin. Microbiol. 37:620–27 [Google Scholar]
  34. Brockmeier SL, Palmer MV, Bolin SR. 34.  2000. Effects of intranasal inoculation of porcine reproductive and respiratory syndrome virus, Bordetella bronchiseptica, or a combination of both organisms in pigs. Am. J. Vet. Res. 61:892–99 [Google Scholar]
  35. Allan GM, McNeilly F, Kennedy S, Meehan B, Ellis J, Krakowka S. 35.  2000. Immunostimulation, PCV-2 and PMWS. Vet. Rec. 147:170–71 [Google Scholar]
  36. Van Reeth K, Nauwynck H, Pensaert M. 36.  1996. Dual infections of feeder pigs with porcine reproductive and respiratory syndrome virus followed by porcine respiratory coronavirus or swine influenza virus: a clinical and virological study. Vet. Microbiol. 48:325–35 [Google Scholar]
  37. Solano GI, Segalés J, Collins JE, Molitor TW, Pijoan C. 37.  1997. Porcine reproductive and respiratory syndrome virus (PRRSv) interaction with Haemophilus parasuis. Vet. Microbiol. 55:247–57 [Google Scholar]
  38. Yoon IJ, Joo HS, Goyal SM, Molitor TW. 38.  1994. A modified serum neutralization test for the detection of antibody to porcine reproductive and respiratory syndrome virus in swine sera. J. Vet. Diagn. Investig. 6:289–92 [Google Scholar]
  39. Loving CL, Osorio FA, Murtaugh MP, Zuckermann FA. 39.  2015. Innate and adaptive immunity against PRRSV. Vet. Immunol. Immunopathol. 167:1–14 [Google Scholar]
  40. Lopez OJ, Oliveira MF, Garcia EA, Kwon BJ, Doster A, Osorio FA. 40.  2007. Protection against porcine reproductive and respiratory syndrome virus (PRRSV) infection through passive transfer of PRRSV-neutralizing antibodies is dose dependent. Clin. Vaccine Immunol. 14:269–75 [Google Scholar]
  41. Lopez OJ, Osorio FA. 41.  2004. Role of neutralizing antibodies in PRRSV protective immunity. Vet. Immunol. Immunopathol. 102:155–63 [Google Scholar]
  42. de Lima M, Pattnaik AK, Flores EF, Osorio FA. 42.  2006. 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 353:410–21 [Google Scholar]
  43. Oleksiewicz MB, Botner A, Toft P, Normann P, Storgaard T. 43.  2001. 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. 75:3277–90 [Google Scholar]
  44. Osorio FA, Galeota JA, Nelson E, Brodersen B, Doster A. 44.  et al. 2002. 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 302:9–20 [Google Scholar]
  45. Ansari IH, Kwon B, Osorio FA, Pattnaik AK. 45.  2006. 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. 80:3994–4004 [Google Scholar]
  46. Ostrowski M, Galeota JA, Jar AM, Platt KB, Osorio FA, Lopez OJ. 46.  2002. Identification of neutralizing and nonneutralizing epitopes in the porcine reproductive and respiratory syndrome virus GP5 ectodomain. J. Virol. 76:4241–50 [Google Scholar]
  47. Cancel-Tirado SM, Evans RB, Yoon KJ. 47.  2004. Monoclonal antibody analysis of porcine reproductive and respiratory syndrome virus epitopes associated with antibody-dependent enhancement and neutralization of virus infection. Vet. Immunol. Immunopathol. 102:249–62 [Google Scholar]
  48. Sang Y, Rowland RR, Blecha F. 48.  2011. Interaction between innate immunity and porcine reproductive and respiratory syndrome virus. Anim. Health Res. Rev. 12:149–67 [Google Scholar]
  49. Butler JE, Lager KM, Golde W, Faaberg KS, Sinkora M. 49.  et al. 2014. Porcine reproductive and respiratory syndrome (PRRS): an immune dysregulatory pandemic. Immunol. Res. 59:81–108 [Google Scholar]
  50. Vu HL, Kwon B, Yoon KJ, Laegreid WW, Pattnaik AK, Osorio FA. 50.  2011. Immune evasion of porcine reproductive and respiratory syndrome virus through glycan shielding involves both glycoprotein 5 as well as glycoprotein 3. J. Virol. 85:5555–64 [Google Scholar]
  51. Zhou L, Ni YY, Pineyro P, Sanford BJ, Cossaboom CM. 51.  et al. 2012. 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 434:96–109 [Google Scholar]
  52. Robinson SR, Li J, Nelson EA, Murtaugh MP. 52.  2015. Broadly neutralizing antibodies against the rapidly evolving porcine reproductive and respiratory syndrome virus. Virus Res. 203:56–65 [Google Scholar]
  53. Lee JA, Kwon B, Osorio FA, Pattnaik AK, Lee NH. 53.  et al. 2014. Protective humoral immune response induced by an inactivated porcine reproductive and respiratory syndrome virus expressing the hypo-glycosylated glycoprotein 5. Vaccine 32:3617–22 [Google Scholar]
  54. Trible BR, Popescu LN, Monday N, Calvert JG, Rowland RR. 54.  2015. 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. 89:6515–20 [Google Scholar]
  55. Koyama S, Ishii KJ, Coban C, Akira S. 55.  2008. Innate immune response to viral infection. Cytokine 43:336–41 [Google Scholar]
  56. Gerner W, Kaser T, Saalmüller A. 56.  2009. Porcine T lymphocytes and NK cells—an update. Dev. Comp. Immunol. 33:310–20 [Google Scholar]
  57. Van Reeth K, Labarque G, Nauwynck H, Pensaert M. 57.  1999. Differential production of proinflammatory cytokines in the pig lung during different respiratory virus infections: correlations with pathogenicity. Res. Vet. Sci. 67:47–52 [Google Scholar]
  58. Albina E, Carrat C, Charley B. 58.  1998. Interferon-α response to swine arterivirus (PoAV), the porcine reproductive and respiratory syndrome virus. J. Interf. Cytokine Res. 18:485–90 [Google Scholar]
  59. Renukaradhya GJ, Alekseev K, Jung K, Fang Y, Saif LJ. 59.  2010. Porcine reproductive and respiratory syndrome virus-induced immunosuppression exacerbates the inflammatory response to porcine respiratory coronavirus in pigs. Viral. Immunol. 23:457–66 [Google Scholar]
  60. Klinge KL, Vaughn EM, Roof MB, Bautista EM, Murtaugh MP. 60.  2009. Age-dependent resistance to Porcine reproductive and respiratory syndrome virus replication in swine. Virol. J. 6:177 [Google Scholar]
  61. Mann JFS, Acevedo R, del Campo J, Pérez O, Ferro VA. 61.  2009. Delivery systems: A vaccine strategy for overcoming mucosal tolerance?. Expert Rev. Vaccines 8:103–12 [Google Scholar]
  62. Murtaugh MP, Xiao Z, Zuckermann F. 62.  2002. Immunological responses of swine to porcine reproductive and respiratory syndrome virus infection. Viral Immunol. 15:533–47 [Google Scholar]
  63. Dwivedi V, Manickam C, Patterson R, Dodson K, Murtaugh M. 63.  et al. 2011. Cross-protective immunity to porcine reproductive and respiratory syndrome virus by intranasal delivery of a live virus vaccine with a potent adjuvant. Vaccine 29:4058–66 [Google Scholar]
  64. Dwivedi V, Manickam C, Binjawadagi B, Linhares D, Murtaugh MP, Renukaradhya GJ. 64.  2012. Evaluation of immune responses to porcine reproductive and respiratory syndrome virus in pigs during early stage of infection under farm conditions. Virol. J. 9:45 [Google Scholar]
  65. Dwivedi V, Manickam C, Patterson R, Dodson K, Weeman M, Renukaradhya GJ. 65.  2011. 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 29:4067–76 [Google Scholar]
  66. Nguyen KB, Salazar-Mather TP, Dalod MY, Van Deusen JB, Wei XQ. 66.  et al. 2002. Coordinated and distinct roles for IFN-αβ, IL-12, and IL-15 regulation of NK cell responses to viral infection. J. Immunol. 169:4279–87 [Google Scholar]
  67. Lee CK, Rao DT, Gertner R, Gimeno R, Frey AB, Levy DE. 67.  2000. Distinct requirements for IFNs and STAT1 in NK cell function. J. Immunol. 165:3571–77 [Google Scholar]
  68. Lunney JK, Fritz ER, Reecy JM, Kuhar D, Prucnal E. 68.  et al. 2010. Interleukin-8, interleukin-1β and interferon-γ levels are linked to PRRS virus clearance. Viral Immunol. 23:127–34 [Google Scholar]
  69. Chen Z, Lawson S, Sun Z, Zhou X, Guan X. 69.  et al. 2010. 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 398:87–97 [Google Scholar]
  70. Delputte PL, Van Breedam W, Barbe F, Van Reeth K, Nauwynck HJ. 70.  2007. IFN-α treatment enhances porcine arterivirus infection of monocytes via upregulation of the porcine arterivirus receptor sialoadhesin. J. Interf. Cytokine Res. 27:757–66 [Google Scholar]
  71. Murtaugh MP, Johnson CR, Xiao Z, Scamurra RW, Zhou Y. 71.  2009. Species specialization in cytokine biology: Is interleukin-4 central to the TH1-TH2 paradigm in swine?. Dev. Comp. Immunol. 33:344–52 [Google Scholar]
  72. Zhou Y, Lin G, Baarsch MJ, Scamurra RJ, Murtaugh MP. 72.  1994. Interleukin-4 suppresses inflammatory cytokine gene transcription in porcine macrophages. J. Leukoc. Biol. 56:507–13 [Google Scholar]
  73. Weesendorp E, Morgan S, Stockhofe-Zurwieden N, Popma-De Graaf DJ, Graham SP, Rebel JM. 73.  2013. Comparative analysis of immune responses following experimental infection of pigs with European porcine reproductive and respiratory syndrome virus strains of differing virulence. Vet. Microbiol. 163:1–12 [Google Scholar]
  74. Weesendorp E, Rebel JMJ, Popma-De Graaf DJ, Fijten HPD, Stockhofe-Zurwieden N. 74.  2014. Lung pathogenicity of European genotype 3 strain porcine reproductive and respiratory syndrome virus (PRRSV) differs from that of subtype 1 strains. Vet. Microbiol. 174:1–2127–38 [Google Scholar]
  75. Amarilla SP, Gómez-Laguna J, Carrasco L, Rodríguez-Gómez IM, Caridad Y. 75.  et al. 2015. A comparative study of the local cytokine response in the lungs of pigs experimentally infected with different PRRSV-1 strains: upregulation of IL-1α in highly pathogenic strain induced lesions. Vet. Immunol. Immunopathol. 164:137–47 [Google Scholar]
  76. Gómez-Laguna J, Salguero FJ, Pallarés FJ, Carrasco L. 76.  2013. Immunopathogenesis of porcine reproductive and respiratory syndrome in the respiratory tract of pigs. Vet. J. 195:148–55 [Google Scholar]
  77. Xiao Z, Batista L, Dee S, Halbur P, Murtaugh MP. 77.  2004. 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. 78:5923–33 [Google Scholar]
  78. Ferrari L, Martelli P, Saleri R, De Angelis E, Cavalli V. 78.  et al. 2013. 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. 151:193–206 [Google Scholar]
  79. Costers S, Lefebvre DJ, Goddeeris B, Delputte PL, Nauwynck HJ. 79.  2009. Functional impairment of PRRSV-specific peripheral CD3+CD8high cells. Vet. Res. 40:46 [Google Scholar]
  80. Johnsen CK, Botner A, Kamstrup S, Lind P, Nielsen J. 80.  2002. Cytokine mRNA profiles in bronchoalveolar cells of piglets experimentally infected in utero with porcine reproductive and respiratory syndrome virus: association of sustained expression of IFN-γ and IL-10 after viral clearance. Viral. Immunol. 15:549–56 [Google Scholar]
  81. Díaz I, Darwich L, Pappaterra G, Pujols J, Mateu E. 81.  2005. Immune responses of pigs after experimental infection with a European strain of Porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 86:1943–51 [Google Scholar]
  82. Suradhat S, Thanawongnuwech R, Poovorawan Y. 82.  2003. Upregulation of IL-10 gene expression in porcine peripheral blood mononuclear cells by porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 84:453–59 [Google Scholar]
  83. Wongyanin P, Buranapraditkul S, Yoo D, Thanawongnuwech R, Roth JA, Suradhat S. 83.  2012. Role of porcine reproductive and respiratory syndrome virus nucleocapsid protein in induction of interleukin-10 and regulatory T-lymphocytes (Treg). J. Gen. Virol. 93:1236–46 [Google Scholar]
  84. Cecere TE, Todd SM, LeRoith T. 84.  2012. Regulatory T cells in arterivirus and coronavirus infections: Do they protect against disease or enhance it?. Viruses 4:833–46 [Google Scholar]
  85. Vahlenkamp TW, Tompkins MB, Tompkins WA. 85.  2005. The role of CD4+CD25+ regulatory T cells in viral infections. Vet. Immunol. Immunopathol. 108:219–25 [Google Scholar]
  86. Silva-Campa E, Mata-Haro V, Mateu E, Hernández J. 86.  2012. Porcine reproductive and respiratory syndrome virus induces CD4+CD8+CD25+Foxp3+ regulatory T cells (Tregs). Virology 430:73–80 [Google Scholar]
  87. Wongyanin P, Buranapraditkun S, Chokeshai-Usaha K, Thanawonguwech R, Suradhat S. 87.  2010. Induction of inducible CD4+CD25+Foxp3+ regulatory T lymphocytes by porcine reproductive and respiratory syndrome virus (PRRSV). Vet. Immunol. Immunopathol. 133:170–82 [Google Scholar]
  88. Wang G, He Y, Tu Y, Liu Y, Zhou EM. 88.  et al. 2014. Comparative analysis of apoptotic changes in peripheral immune organs and lungs following experimental infection of piglets with highly pathogenic and classical porcine reproductive and respiratory syndrome virus. Virol. J. 11:2 [Google Scholar]
  89. Lunney JK, Chen H. 89.  2010. Genetic control of porcine reproductive and respiratory syndrome virus responses. Virus Res. 154:161–69 [Google Scholar]
  90. Sun Y, Han M, Kim C, Calvert JG, Yoo D. 90.  2012. Interplay between interferon-mediated innate immunity and porcine reproductive and respiratory syndrome virus. Viruses 4:424–46 [Google Scholar]
  91. García-Nicolás O, Rosales RS, Pallarés FJ, Risco D, Quereda JJ. 91.  et al. 2015. Comparative analysis of cytokine transcript profiles within mediastinal lymph node compartments of pigs after infection with porcine reproductive and respiratory syndrome genotype 1 strains differing in pathogenicity. Vet. Res. 46:34 [Google Scholar]
  92. Chen X, Quan R, Guo X, Gao L, Shi J, Feng WH. 92.  2014. Up-regulation of pro-inflammatory factors by HP-PRRSV infection in microglia: implications for HP-PRRSV neuropathogenesis. Vet. Microbiol. 170:48–57 [Google Scholar]
  93. Badaoui B, Tuggle CK, Hu Z, Reecy JM, Ait-Ali T. 93.  et al. 2013. Pig immune response to general stimulus and to porcine reproductive and respiratory syndrome virus infection: a meta-analysis approach. BMC Genom. 14:220 [Google Scholar]
  94. Cao L, Xu Z, Fang L, Zhong Y, Chen Q. 94.  et al. 2013. MiR-125b reduces porcine reproductive and respiratory syndrome virus replication by negatively regulating the NF-κB pathway. PLOS ONE 8:e55838 [Google Scholar]
  95. Gao L, Guo XK, Wang L, Zhang Q, Li N. 95.  et al. 2013. MicroRNA 181 suppresses porcine reproductive and respiratory syndrome virus (PRRSV) infection by targeting PRRSV receptor CD163. J. Virol. 87:8808–12 [Google Scholar]
  96. Zhang Q, Guo XK, Gao L, Huang C, Li N. 96.  et al. 2014. MicroRNA-23 inhibits PRRSV replication by directly targeting PRRSV RNA and possibly by upregulating type I interferons. Virology 450–51:182–95 [Google Scholar]
  97. Xiao S, Wang X, Ni H, Li N, Zhang A. 97.  et al. 2015. MicroRNA miR-24-3p promotes porcine reproductive and respiratory syndrome virus replication through suppression of heme oxygenase-1 expression. J. Virol. 89:4494–503 [Google Scholar]
  98. Cong P, Xiao S, Chen Y, Wang L, Gao J. 98.  et al. 2014. Integrated miRNA and mRNA transcriptomes of porcine alveolar macrophages (PAM cells) identifies strain-specific miRNA molecular signatures associated with H-PRRSV and N-PRRSV infection. Mol. Biol. Rep. 41:5863–75 [Google Scholar]
  99. Wysocki M, Chen H, Steibel JP, Kuhar D, Petry D. 99.  et al. 2012. Identifying putative candidate genes and pathways involved in immune responses to porcine reproductive and respiratory syndrome virus (PRRSV) infection. Anim. Genet. 43:328–32 [Google Scholar]
  100. Schroyen M, Steibel JP, Koltes JE, Choi I, Eisley C. 100.  et al. 2015. Whole blood microarray analysis of pigs showing extreme phenotypes after a porcine reproductive and respiratory syndrome virus infection. BMC Genom. 16:516 [Google Scholar]
  101. Groenen MAM, Archibald AL, Uenishi H, Tuggle CK, Takeuchi Y. 101.  et al. 2012. Pig genomes provide insight into porcine demography and evolution. Nature 491:393–98 [Google Scholar]
  102. Dawson HD, Loveland JE, Pascal G, Gilbert JJG, Uenishi H. 102.  et al. 2013. Structural and functional annotation of the porcine immunome. BMC Genomics 14:332 [Google Scholar]
  103. Vincent AL, Thacker BJ, Halbur PG, Rothschild MF, Thacker EL. 103.  2005. In vitro susceptibility of macrophages to porcine reproductive and respiratory syndrome virus varies between genetically diverse lines of pigs. Viral Immunol. 18:506–12 [Google Scholar]
  104. Carlson DF, Tan W, Hackett PB, Fahrenkrug SC. 104.  2013. Editing livestock genomes with site-specific nucleases. Reprod. Fertil. Dev. 26:74–82 [Google Scholar]
  105. Lunney JK, Steibel JP, Reecy JM, Fritz E, Rothschild M. 105.  et al. 2011. Probing genetic control of swine responses to PRRSV infection: current progress of the PRRS Host Genetics Consortium. BMC Proc. 5:Suppl. 4S30 [Google Scholar]
  106. Rowland RR, Lunney J, Dekkers J. 106.  2012. Control of porcine reproductive and respiratory syndrome (PRRS) through genetic improvements in disease resistance and tolerance. Front. Genet. 3:260 [Google Scholar]
  107. Boddicker N, Waide EH, Rowland RR, Lunney JK, Garrick DJ. 107.  et al. 2012. Evidence for a major QTL associated with host response to porcine reproductive and respiratory syndrome virus challenge. J. Anim. Sci. 90:1733–46 [Google Scholar]
  108. Boddicker NJ, Garrick DJ, Rowland RR, Lunney JK, Reecy JM, Dekkers JC. 108.  2014. Validation and further characterization of a major quantitative trait locus associated with host response to experimental infection with porcine reproductive and respiratory syndrome virus. Anim. Genet. 45:48–58 [Google Scholar]
  109. Boddicker NJ, Bjorkquist A, Rowland RR, Lunney JK, Reecy JM, Dekkers JC. 109.  2014. Genome-wide association and genomic prediction for host response to porcine reproductive and respiratory syndrome virus infection. Genet. Sel. Evol. 46:18 [Google Scholar]
  110. Koltes JE, Fritz-Waters E, Eisley CJ, Choi I, Bao H. 110.  et al. 2015. Identification of a putative quantitative trait nucleotide in guanylate binding protein 5 for host response to PRRS virus infection. BMC Genom. 16:412 [Google Scholar]
  111. Lunney JK, Ho C-S, Wysocki M, Smith DM. 111.  2009. Molecular genetics of the swine major histocompatibility complex, the SLA complex. Dev. Comp. Immunol. 33:362–74 [Google Scholar]
  112. Mellencamp MA, Galina-Pantoja L, Gladney CD, Torremorell M. 112.  2008. Improving pig health through genomics: a view from the industry. Dev. Biol. 132:35–41 [Google Scholar]
  113. Prieto C, Sánchez R, Martín-Rillo S, Suárez P, Simarro I. 113.  et al. 1996. Exposure of gilts in early gestation to porcine reproductive and respiratory syndrome virus. Vet. Rec. 138:536–39 [Google Scholar]
  114. Prieto C, Suárez P, Simarro I, García C, Fernández A, Castro JM. 114.  1997. Transplacental infection following exposure of gilts to porcine reproductive and respiratory syndrome virus at the onset of gestation. Vet. Microbiol. 57:301–11 [Google Scholar]
  115. Christianson WT, Choi CS, Collins JE, Molitor TW, Morrison RB, Joo HS. 115.  1993. Pathogenesis of porcine reproductive and respiratory syndrome virus infection in mid-gestation sows and fetuses. Can. J. Vet. Res. 57:262–68 [Google Scholar]
  116. Kranker S, Nielsen J, Bille-Hansen V, Botner A. 116.  1998. Experimental inoculation of swine at various stages of gestation with a Danish isolate of porcine reproductive and respiratory syndrome virus (PRRSV). Vet. Microbiol. 61:21–31 [Google Scholar]
  117. Ladinig A, Detmer SE, Clarke K, Ashley C, Rowland RR. 117.  et al. 2015. Pathogenicity of three type 2 porcine reproductive and respiratory syndrome virus strains in experimentally inoculated pregnant gilts. Virus Res. 203:24–35 [Google Scholar]
  118. Park BK, Yoon IJ, Joo HS. 118.  1996. Pathogenesis of plaque variants of porcine reproductive and respiratory syndrome virus in pregnant sows. Am. J. Vet. Res. 57:320–23 [Google Scholar]
  119. Mengeling WL, Lager KM, Vorwald AC. 119.  1994. Temporal characterization of transplacental infection of porcine fetuses with porcine reproductive and respiratory syndrome virus. Am. J. Vet. Res. 55:1391–98 [Google Scholar]
  120. Terpstra C, Wensvoort G, Pol JMA. 120.  1991. Experimental reproduction of porcine epidemic abortion and respiratory syndrome (mystery swine disease) by infection with Lelystad virus: Koch's postulates fulfilled. Vet. Q. 13:131–36 [Google Scholar]
  121. Cheon DS, Chae C. 121.  2000. Comparison of virus isolation, reverse transcription-polymerase chain reaction, immunohistochemistry, and in situ hybridization for the detection of porcine reproductive and respiratory syndrome virus from naturally aborted fetuses and stillborn piglets. J. Vet. Diagn. Investig. 12:582–87 [Google Scholar]
  122. Ladinig A, Gerner W, Saalmüller A, Lunney JK, Ashley C, Harding JCS. 122.  2014a. Changes in leukocyte subsets of pregnant gilts experimentally infected with porcine reproductive and respiratory syndrome virus and relationships with viral load and fetal outcome. Vet. Res. 45:128 [Google Scholar]
  123. Lowe JE, Husmann R, Firkins LD, Zuckermann FA, Goldberg TL. 123.  2005. 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. 226:1707–11 [Google Scholar]
  124. Ladinig A, Lunney JK, Souza C, Ashley C, Plastow G, Harding J. 124.  2014b. Cytokine profiles in pregnant gilts experimentally infected with porcine reproductive and respiratory syndrome virus and relationships with viral load and fetal outcome. Vet. Res. 45:113 [Google Scholar]
  125. Rowland RR. 125.  2010. The interaction between PRRSV and the late gestation pig fetus. Virus Res. 154:114–22 [Google Scholar]
  126. Serao NV, Matika O, Kemp RA, Harding JC, Bishop SC. 126.  et al. 2014. Genetic analysis of reproductive traits and antibody response in a PRRS outbreak herd. J. Anim. Sci. 92:2905–21 [Google Scholar]
  127. Ladinig A, Ashley C, Detmer SE, Wilkinson JM, Lunney JK. 127.  et al. 2015. Maternal and fetal predictors of fetal viral load and death in third trimester, type 2 porcine reproductive and respiratory syndrome virus infected pregnant gilts. Vet. Res. 46:107 [Google Scholar]
  128. Karniychuk UU, Nauwynck HJ. 128.  2013. Pathogenesis and prevention of placental and transplacental porcine reproductive and respiratory syndrome virus infection. Vet. Res. 44:195 [Google Scholar]
  129. Karniychuk UU, Saha D, Geldhof M, Vanhee M, Cornillie P. 129.  et al. 2011. Porcine reproductive and respiratory syndrome virus (PRRSV) causes apoptosis during its replication in fetal implantation sites. Microb. Pathol. 51:194–202 [Google Scholar]
  130. Karniychuk UU, Saha D, Vanhee M, Geldhof M, Cornillie P. 130.  et al. 2012. Impact of a novel inactivated PRRS virus vaccine on virus replication and virus-induced pathology in fetal implantation sites and fetuses upon challenge. Theriogenology 78:1527–37 [Google Scholar]
  131. Karniychuk UU, Nauwynck HJ. 131.  2009. Quantitative changes of sialoadhesin and CD163 positive macrophages in the implantation sites and organs of porcine embryos/fetuses during gestation. Placenta 30:497–500 [Google Scholar]
  132. Karniychuk UU, De Spiegelaere W, Nauwynck HJ. 132.  2013. Porcine reproductive and respiratory syndrome virus infection is associated with an increased number of Sn-positive and CD8-positive cells in the maternal-fetal interface. Virus Res. 176:285–91 [Google Scholar]
  133. Basu S, Eriksson M, Pioli PA, Conejo-Garcia J, Mselle TF. 133.  et al. 2009. Human uterine NK cells interact with uterine macrophages via NKG2D upon stimulation with PAMPs. Am. J. Reprod. Immunol. 61:52–61 [Google Scholar]
  134. Croy BA, van den Heuvel MJ, Borzychowski AM, Tayade C. 134.  2006. Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol. Rev. 214:161–85 [Google Scholar]
  135. Dimova T, Mihaylova A, Spassova P, Georgieva R. 135.  2008. Superficial implantation in pigs is associated with decreased numbers and redistribution of endometrial NK-cell populations. Am. J. Reprod. Immunol. 59:359–69 [Google Scholar]
  136. Engelhardt H, Croy BA, King GJ. 136.  2002. Evaluation of natural killer cell recruitment to embryonic attachment sites during early porcine pregnancy. Biol. Reprod. 66:1185–92 [Google Scholar]
  137. Cheon DS, Chae C. 137.  2001. Distribution of porcine reproductive and respiratory syndrome virus in stillborn and liveborn piglets from experimentally infected sows. J. Comp. Pathol. 124:231–37 [Google Scholar]
  138. Han K, Seo HW, Oh Y, Kang I, Park C. 138.  et al. 2013. Pathogenesis of Korean type 1 (European genotype) porcine reproductive and respiratory syndrome virus in experimentally infected pregnant gilts. J. Comp. Pathol. 148:396–404 [Google Scholar]
  139. Rossow KD, Laube KL, Goyal SM, Collins JE. 139.  1996. Fetal microscopic lesions in porcine reproductive and respiratory syndrome virus-induced abortion. Vet. Pathol. 33:95–99 [Google Scholar]
  140. Frydas IS, Verbeeck M, Cao J, Nauwynck HJ. 140.  2013. Replication characteristics of porcine reproductive and respiratory syndrome virus (PRRSV) European subtype 1 (Lelystad) and subtype 3 (Lena) strains in nasal mucosa and cells of the monocytic lineage: indications for the use of new receptors of PRRSV (Lena). Vet. Res. 44:173 [Google Scholar]
  141. Butler JE, Sinkora M, Wertz N, Holtmeier W, Lemke CD. 141.  2006. Development of the neonatal B and T cell repertoire in swine: implications for comparative and veterinary immunology. Vet. Res. 37:417–41 [Google Scholar]
  142. Li Y, Wang G, Liu Y, Tu Y, He Y. 142.  et al. 2014. Identification of apoptotic cells in the thymus of piglets infected with highly pathogenic porcine reproductive and respiratory syndrome virus. Virus Res. 189:29–33 [Google Scholar]
  143. Nielsen J, Botner A, Tingstedt JE, Aasted B, Johnsen CK. 143.  et al. 2003. 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. 93:135–51 [Google Scholar]
  144. Aasted B, Bach P, Nielsen J, Lind P. 144.  2002. Cytokine profiles in peripheral blood mononuclear cells and lymph node cells from piglets infected in utero with porcine reproductive and respiratory syndrome virus. Clin. Diag. Lab. Immunol. 9:1229–34 [Google Scholar]
  145. Ladinig A, Wilkinson J, Ashley C, Detmer SE, Lunney JK. 145.  et al. 2014. Variation in fetal outcome, viral load and ORF5 sequence mutations in a large scale study of phenotypic responses to late gestation exposure to type 2 porcine reproductive and respiratory syndrome virus. PLOS ONE 9:e96104 [Google Scholar]
  146. Lager KM, Halbur PG. 146.  1996. Gross and microscopic lesions in porcine fetuses infected with porcine reproductive and respiratory syndrome virus. J. Vet. Diagn. Investig. 8:275–82 [Google Scholar]
  147. Nielsen J, Ronsholt L, Sorensen KJ. 147.  1991. Experimental in utero infection of pig foetuses with porcine parvovirus (PPV). Vet. Microbiol. 28:1–11 [Google Scholar]
  148. Pensaert MB, Sanchez RE Jr, Ladekjaer-Mikkelsen AS, Allan GM, Nauwynck HJ. 148.  2004. Viremia and effect of fetal infection with porcine viruses with special reference to porcine circovirus 2 infection. Vet. Microbiol. 98:175–83 [Google Scholar]
  149. Renukaradhya GJ, Meng XJ, Calvert JG, Roof M, Lager KM. 149.  2015. Inactivated and subunit vaccines against porcine reproductive and respiratory syndrome: Current status and future direction. Vaccine 33:3065–72 [Google Scholar]
  150. Mair KH, Koinig H, Gerner W, Höhne A, Bretthauer J. 150.  et al. 2015. Carbopol improves the early cellular immune responses induced by the modified-life vaccine Ingelvac PRRS® MLV. Vet. Microbiol. 176:352–57 [Google Scholar]
  151. Murthy AM, Ni Y, Meng X, Zhang C. 151.  2015. Production and evaluation of virus-like particles displaying immunogenic epitopes of porcine reproductive and respiratory syndrome virus (PRRSV). Int. J. Mol. Sci. 16:8382–96 [Google Scholar]
  152. Wang R, Xiao Y, Opriessnig T, Ding Y, Yu Y. 152.  et al. 2013. Enhancing neutralizing antibody production by an interferon-inducing porcine reproductive and respiratory syndrome virus strain. Vaccine 31:5537–43 [Google Scholar]
  153. Renukaradhya GJ, Meng XJ, Calvert JG, Roof M, Lager KM. 153.  2015. Live porcine reproductive and respiratory syndrome virus vaccines: Current status and future direction. Vaccine 33:4069–80 [Google Scholar]
  154. Wang YX, Zhou YJ, Li GX, Zhang SR, Jiang YF. 154.  et al. 2011. Identification of immunodominant T-cell epitopes in membrane protein of highly pathogenic porcine reproductive and respiratory syndrome virus. Virus Res. 158:108–15 [Google Scholar]
  155. Burgara-Estrella A, Díaz I, Rodríguez-Gómez IM, Essler SE, Hernández J, Mateu E. 155.  2013. Predicted peptides from non-structural proteins of porcine reproductive and respiratory syndrome virus are able to induce IFN-γ and IL-10. Viruses 5:663–77 [Google Scholar]
  156. Hu J, Zhang C. 156.  2014. Porcine reproductive and respiratory syndrome virus vaccines: current status and strategies to a universal vaccine. Transbound. Emerg. Dis. 61:109–20 [Google Scholar]
/content/journals/10.1146/annurev-animal-022114-111025
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Porcine Reproductive and Respiratory Syndrome Virus (PRRSV): Pathogenesis and Interaction with the Immune System
Annual Review of Animal Biosciences 4, 129 (2016); https://doi.org/10.1146/annurev-animal-022114-111025
/content/journals/10.1146/annurev-animal-022114-111025
/content/journals/10.1146/annurev-animal-022114-111025
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