Mechanisms of Adaptive Immunity to Porcine Reproductive and Respiratory Syndrome Virus
Abstract
:1. Introduction
2. The Targets of Infection
3. Immunosuppression
4. Antibody Response
4.1. Neutralizing Antibody Response
4.2. Non-Neutralizing Antibody Response
5. The B Cell Response
Plasma Cells
6. T Cell Response
7. Natural Killer Cell Response
8. Conclusions
Acknowledgments
Conflicts of Interest
References
- Wensvoort, G.; Terpstra, C.; Pol, J.M.; ter Laak, E.A.; Bloemraad, M.; de Kluyver, E.P.; Kragten, C.; van Buiten, L.; den Besten, A.; Wagenaar, F. Mystery swine disease in The Netherlands: The isolation of Lelystad virus. Vet. Q. 1991, 13, 121–130. [Google Scholar] [CrossRef] [PubMed]
- Terpstra, C.; Wensvoort, G.; Pol, J.M. 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, 131–136. [Google Scholar] [CrossRef] [PubMed]
- Collins, J.E.; Benfield, D.A.; Christianson, W.T.; Harris, L.; Hennings, J.C.; Shaw, D.P.; Goyal, S.M.; McCullough, S.; Morrison, R.B.; Joo, H.S. Isolation of swine infertility and respiratory syndrome virus (isolate ATCC VR-2332) in North America and experimental reproduction of the disease in gnotobiotic pigs. J. Vet. Diagn. Investig. 1992, 4, 117–126. [Google Scholar] [CrossRef] [PubMed]
- Nelsen, C.J.; Murtaugh, M.P.; Faaberg, K.S. Porcine reproductive and respiratory syndrome virus comparison: Divergent evolution on two continents. J. Virol. 1999, 73, 270–280. [Google Scholar] [PubMed]
- Allende, R.; Lewis, T.L.; Lu, Z.; Rock, D.L.; Kutish, G.F.; Ali, A.; Doster, A.R.; Osorio, F.A. North American and European porcine reproductive and respiratory syndrome viruses differ in non-structural protein coding regions. J. Gen. Virol. 1999, 80, 307–315. [Google Scholar] [CrossRef] [PubMed]
- Zimmerman, J.; Benfield, D.; Dee, S.; Murtaugh, M.; Stadejek, T.; Stevenson, G.; Torremorell, M. Porcine reproductive and respiratory syndrome virus (porcine arterivirus). In Diseases of Swine, 10th ed.; John Wiley & Sons Ltd.: West Sussex, UK, 2012. [Google Scholar]
- Kuhn, J.H.; Lauck, M.; Bailey, A.L.; Shchetinin, A.M.; Vishnevskaya, T.V.; Bào, Y.; Ng, T.F.; LeBreton, M.; Schneider, B.S.; Gillis, A.; et al. Reorganization and expansion of the nidoviral family Arteriviridae. Arch. Virol. 2016, 161, 755–768. [Google Scholar] [CrossRef] [PubMed]
- Meulenberg, J.J. PRRSV, the virus. Vet. Res. 2000, 31, 11–21. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Murtaugh, M.P.; Stadejek, T.; Abrahante, J.E.; Lam, T.T.; Leung, F.C. The ever-expanding diversity of porcine reproductive and respiratory syndrome virus. Virus Res. 2010, 154, 18–30. [Google Scholar] [CrossRef] [PubMed]
- Loving, C.L.; Osorio, F.A.; Murtaugh, M.P.; Zuckermann, F.A. Innate and adaptive immunity against porcine reproductive and respiratory syndrome virus. Vet. Immunol. Immunopathol. 2015, 167, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Tian, D.; Zheng, H.; Zhang, R.; Zhuang, J.; Yuan, S. Chimeric porcine reproductive and respiratory syndrome viruses reveal full function of genotype 1 envelope proteins in the backbone of genotype 2. Virology 2011, 412, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Fang, Y.; Snijder, E.J. The PRRSV replicase: Exploring the multifunctionality of an intriguing set of nonstructural proteins. Virus Res. 2010, 154, 61–76. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Meulenberg, J.J.; van Nieuwstadt, A.P.; van Essen-Zandbergen, A.; Bos-de Ruijter, J.N.; Langeveld, J.P.; Meloen, R.H. Localization and fine mapping of antigenic sites on the nucleocapsid protein N of porcine reproductive and respiratory syndrome virus with monoclonal antibodies. Virology 1998, 252, 106–114. [Google Scholar] [CrossRef] [PubMed]
- Brar, M.S.; Shi, M.; Murtaugh, M.P.; Leung, F.C. Evolutionary diversification of type 2 porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 2015, 96, 1570–1580. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Lunney, J.K.; Fang, Y.; Ladinig, A.; Chen, N.; Li, Y.; Rowland, B.; Renukaradhya, G.J. Porcine reproductive and respiratory syndrome virus (PRRSV): Pathogenesis and interaction with the immune system. Annu. Rev. Anim. Biosci. 2016, 4, 129–154. [Google Scholar] [CrossRef] [PubMed]
- Lawson, S.R.; Rossow, K.D.; Collins, J.E.; Benfield, D.A.; Rowland, R.R. Porcine reproductive and respiratory syndrome virus infection of gnotobiotic pigs: Sites of virus replication and co-localization with MAC-387 staining at 21 days post-infection. Virus Res. 1997, 51, 105–113. [Google Scholar] [CrossRef]
- Duan, X.; Nauwynck, H.J.; Pensaert, M.B. Virus quantification and identification of cellular targets in the lungs and lymphoid tissues of pigs at different time intervals after inoculation with porcine reproductive and respiratory syndrome virus (PRRSV). Vet. Microbiol. 1997, 56, 9–19. [Google Scholar] [CrossRef]
- Kim, H.S.; Kwang, J.; Yoon, I.J.; Joo, H.S.; Frey, M.L. Enhanced replication of porcine reproductive and respiratory syndrome (PRRS) virus in a homogeneous subpopulation of MA-104 cell line. Arch. Virol. 1993, 133, 477–483. [Google Scholar] [CrossRef] [PubMed]
- Park, J.Y.; Kim, H.S.; Seo, S.H. Characterization of interaction between porcine reproductive and respiratory syndrome virus and porcine dendritic cells. J. Microbiol. Biotechnol. 2008, 18, 1709–1716. [Google Scholar] [PubMed]
- Whitworth, K.M.; Rowland, R.R.; Ewen, C.L.; Trible, B.R.; Kerrigan, M.A.; Cino-Ozuna, A.G.; Samuel, M.S.; Lightner, J.E.; McLaren, D.G.; Mileham, A.J.; et al. Gene-edited pigs are protected from porcine reproductive and respiratory syndrome virus. Nat. Biotechnol. 2016, 34, 20–22. [Google Scholar] [CrossRef] [PubMed]
- Prather, R.S.; Whitworth, K.M.; Schommer, S.K.; Wells, K.D. Genetic engineering alveolar macrophages for host resistance to PRRSV. Vet. Microbiol. 2017. [Google Scholar] [CrossRef] [PubMed]
- Gao, L.; Guo, X.K.; Wang, L.; Zhang, Q.; Li, N.; Chen, X.X.; Wang, Y.; Feng, W.H. MicroRNA 181 suppresses porcine reproductive and respiratory syndrome virus (PRRSV) infection by targeting PRRSV receptor CD163. J. Virol. 2013, 87, 8808–8812. [Google Scholar] [CrossRef] [PubMed]
- Hume, D.A. Macrophages as APC and the dendritic cell myth. J. Immunol. 2008, 181, 5829–5835. [Google Scholar] [CrossRef] [PubMed]
- Batista, F.D.; Harwood, N.E. The who, how and where of antigen presentation to B cells. Nat. Rev. Immunol. 2009, 9, 15–27. [Google Scholar] [CrossRef] [PubMed]
- Katz, D.H.; Unanue, E.R. Critical role of determinant presentation in the induction of specific responses in immunocompetent lymphocytes. J. Exp. Med. 1973, 137, 967–990. [Google Scholar] [CrossRef] [PubMed]
- Podinovskaia, M.; Lee, W.; Caldwell, S.; Russell, D.G. Infection of macrophages with Mycobacterium tuberculosis induces global modifications to phagosomal function. Cell. Microbiol. 2013, 15, 843–859. [Google Scholar] [CrossRef] [PubMed]
- Kalam, H.; Fontana, M.F.; Kumar, D. Alternate splicing of transcripts shape macrophage response to Mycobacterium tuberculosis infection. PLoS Pathog. 2017, 13, e1006236. [Google Scholar] [CrossRef] [PubMed]
- Abbas, W.; Tariq, M.; Iqbal, M.; Kumar, A.; Herbein, G. Eradication of HIV-1 from the macrophage reservoir: An uncertain goal? Viruses 2015, 7, 1578–1598. [Google Scholar] [CrossRef] [PubMed]
- Koppensteiner, H.; Brack-Werner, R.; Schindler, M. Macrophages and their relevance in human immunodeficiency virus type I infection. Retrovirology 2012, 9, 82. [Google Scholar] [CrossRef] [PubMed]
- Koppensteiner, H.; Banning, C.; Schneider, C.; Hohenberg, H.; Schindler, M. Macrophage internal HIV-1 is protected from neutralizing antibodies. J. Virol. 2012, 86, 2826–2836. [Google Scholar] [CrossRef] [PubMed]
- Moradin, N.; Descoteaux, A. Leishmania promastigotes: Building a safe niche within macrophages. Front. Cell. Infect. Microbiol. 2012, 2, 121. [Google Scholar] [CrossRef] [PubMed]
- Matheoud, D.; Moradin, N.; Bellemare-Pelletier, A.; Shio, M.T.; Hong, W.J.; Olivier, M.; Gagnon, E.; Desjardins, M.; Descoteaux, A. Leishmania evades host immunity by inhibiting antigen cross-presentation through direct cleavage of the SNARE VAMP8. Cell Host Microbe 2013, 14, 15–25. [Google Scholar] [CrossRef] [PubMed]
- Ghosh, J.; Bose, M.; Roy, S.; Bhattacharyya, S.N. Leishmania donovani targets Dicer1 to downregulate miR-122, lower serum cholesterol, and facilitate murine liver infection. Cell Host Microbe 2013, 13, 277–288. [Google Scholar] [CrossRef] [PubMed]
- Lam, G.Y.; Czuczman, M.A.; Higgins, D.E.; Brumell, J.H. Interactions of Listeria monocytogenes with the autophagy system of host cells. Adv. Immunol. 2012, 113, 7–18. [Google Scholar] [PubMed]
- Lee, J.W.; Lee, E.J. Regulation and function of the Salmonella MgtC virulence protein. J. Microbiol. 2015, 53, 667–672. [Google Scholar] [CrossRef] [PubMed]
- Laksono, B.M.; de Vries, R.D.; McQuaid, S.; Duprex, W.P.; de Swart, R.L. Measles virus host invasion and pathogenesis. Viruses 2016, 8, 210. [Google Scholar] [CrossRef] [PubMed]
- Yang, L.; Zhang, Y.J. Antagonizing cytokine-mediated JAK-STAT signaling by porcine reproductive and respiratory syndrome virus. Vet. Microbiol. 2016. [Google Scholar] [CrossRef] [PubMed]
- Yang, L.; Wang, R.; Ma, Z.; Xiao, Y.; Nan, Y.; Wang, Y.; Lin, S.; Zhang, Y.J. Porcine reproductive and respiratory syndrome virus antagonizes JAK/STAT3 signaling via Nsp5 by inducing STAT3 degradation. J. Virol. 2016, 91, e02087–e02116. [Google Scholar]
- Huang, C.; Zhang, Q.; Guo, X.K.; Yu, Z.B.; Xu, A.T.; Tang, J.; Feng, W.H. Porcine reproductive and respiratory syndrome virus nonstructural protein 4 antagonizes beta interferon expression by targeting the NF-κB essential modulator. J. Virol. 2014, 88, 10934–10945. [Google Scholar] [CrossRef] [PubMed]
- Beura, L.K.; Sarkar, S.N.; Kwon, B.; Subramaniam, S.; Jones, C.; Pattnaik, A.K.; Osorio, F.A. Porcine reproductive and respiratory syndrome virus nonstructural protein 1b modulates host innate immune response by antagonizing IRF3 activation. J. Virol. 2010, 84, 1574–1584. [Google Scholar] [CrossRef] [PubMed]
- Sun, Z.; Li, Y.; Ransburgh, R.; Snijder, E.J.; Fang, Y. Nonstructural protein 2 of porcine reproductive and respiratory syndrome virus inhibits the antiviral function of interferon-stimulated gene 15. J. Virol. 2012, 86, 3839–3850. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.; Ke, H.; Han, M.; Chen, N.; Fang, W.; Yoo, D. Nonstructural protein 11 of porcine reproductive and respiratory syndrome virus suppresses both MAVS and RIG-I expression as one of the mechanisms to antagonize type I interferon production. PLoS ONE 2016, 11, e0168314. [Google Scholar] [CrossRef] [PubMed]
- 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, 485–490. [Google Scholar] [CrossRef] [PubMed]
- Badaoui, B.; Tuggle, C.K.; Hu, Z.; Reecy, J.M.; Ait-Ali, T.; Anselmo, A.; Botti, S. Pig immune response to general stimulus and to porcine reproductive and respiratory syndrome virus infection: A meta-analysis approach. BMC Genom. 2013, 14, 220. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Guo, R.; Katz, B.B.; Tomich, J.M.; Gallagher, T.; Fang, Y. Porcine reproductive and respiratory syndrome virus utilizes nanotubes for intercellular spread. J. Virol. 2016, 90, 5163–5175. [Google Scholar] [CrossRef] [PubMed]
- Cafruny, W.A.; Duman, R.G.; Wong, G.H.; Said, S.; Ward-Demo, P.; Rowland, R.R.; Nelson, E.A. Porcine reproductive and respiratory syndrome virus (PRRSV) infection spreads by cell-to-cell transfer in cultured MARC-145 cells, is dependent on an intact cytoskeleton, and is suppressed by drug-targeting of cell permissiveness to virus infection. Virol. J. 2006, 3, 90. [Google Scholar] [CrossRef] [PubMed]
- Corthésy, B.; Benureau, Y.; Perrier, C.; Fourgeux, C.; Parez, N.; Greenberg, H.; Schwartz-Cornil, I. Rotavirus anti-VP6 secretory immunoglobulin A contributes to protection via intracellular neutralization but not via immune exclusion. J. Virol. 2006, 80, 10692–10699. [Google Scholar] [CrossRef] [PubMed]
- Bai, Y.; Ye, L.; Tesar, D.B.; Song, H.; Zhao, D.; Björkman, P.J.; Roopenian, D.C.; Zhu, X. Intracellular neutralization of viral infection in polarized epithelial cells by neonatal Fc receptor (FcRn)-mediated IgG transport. Proc. Natl. Acad. Sci. USA 2011, 108, 18406–18411. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Zhou, L.; Ge, X.; Guo, X.; Han, J.; Yang, H. The Chinese highly pathogenic porcine reproductive and respiratory syndrome virus infection suppresses Th17 cells response in vivo. Vet. Microbiol. 2016, 189, 75–85. [Google Scholar] [CrossRef] [PubMed]
- Amarilla, S.P.; Gómez-Laguna, J.; Carrasco, L.; Rodríguez-Gómez, I.M.; Caridad Y Ocerín, J.M.; Graham, S.P.; Frossard, J.P.; Steinbach, F.; Salguero, F.J. Thymic depletion of lymphocytes is associated with the virulence of PRRSV-1 strains. Vet. Microbiol. 2016, 188, 47–58. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Wang, G.; Liu, Y.; Tu, Y.; He, Y.; Wang, Z.; Han, Z.; Li, L.; Li, A.; Tao, Y.; et al. Identification of apoptotic cells in the thymus of piglets infected with highly pathogenic porcine reproductive and respiratory syndrome virus. Virus Res. 2014, 189, 29–33. [Google Scholar] [CrossRef] [PubMed]
- Cao, J.; Grauwet, K.; Vermeulen, B.; Devriendt, B.; Jiang, P.; Favoreel, H.; Nauwynck, H. Suppression of NK cell-mediated cytotoxicity against PRRSV-infected porcine alveolar macrophages in vitro. Vet. Microbiol. 2013, 164, 261–269. [Google Scholar] [CrossRef] [PubMed]
- Sinkora, M.; Butler, J.E.; Lager, K.M.; Potockova, H.; Sinkorova, J. The comparative profile of lymphoid cells and the T and B cell spectratype of germ-free piglets infected with viruses SIV, PRRSV or PCV2. Vet. Res. 2014, 45, 91. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Pandiyan, P.; Zheng, L.; Lenardo, M.J. The molecular mechanisms of regulatory T cell immunosuppression. Front. Immunol. 2011, 2, 60. [Google Scholar] [CrossRef] [PubMed]
- Sakaguchi, S.; Takahashi, T.; Nishizuka, Y. Study on cellular events in post-thymectomy autoimmune oophoritis in mice. II. Requirement of Lyt-1 cells in normal female mice for the prevention of oophoritis. J. Exp. Med. 1982, 156, 1577–1586. [Google Scholar] [CrossRef] [PubMed]
- Sakaguchi, S.; Toda, M.; Asano, M.; Itoh, M.; Morse, S.S.; Sakaguchi, N. T cell-mediated maintenance of natural self-tolerance: Its breakdown as a possible cause of various autoimmune diseases. J. Autoimmun. 1996, 9, 211–220. [Google Scholar] [CrossRef] [PubMed]
- Silva-Campa, E.; Flores-Mendoza, L.; Reséndiz, M.; Pinelli-Saavedra, A.; Mata-Haro, V.; Mwangi, W.; Hernández, J. Induction of T helper 3 regulatory cells by dendritic cells infected with porcine reproductive and respiratory syndrome virus. Virology 2009, 387, 373–379. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Rodríguez-Gómez, I.M.; Käser, T.; Gómez-Laguna, J.; Lamp, B.; Sinn, L.; Rümenapf, T.; Carrasco, L.; Saalmüller, A.; Gerner, W. PRRSV-infected monocyte-derived dendritic cells express high levels of SLA-DR and CD80/86 but do not stimulate PRRSV-naïve regulatory T cells to proliferate. Vet. Res. 2015, 46, 54. [Google Scholar] [CrossRef] [PubMed]
- Silva-Campa, E.; Cordoba, L.; Fraile, L.; Flores-Mendoza, L.; Montoya, M.; Hernández, 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. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Suradhat, S.; Thanawongnuwech, R. Upregulation of interleukin-10 gene expression in the leukocytes of pigs infected with porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 2003, 84, 2755–2760. [Google Scholar] [CrossRef] [PubMed]
- García-Nicolás, O.; Quereda, J.J.; Gómez-Laguna, J.; Salguero, F.J.; Carrasco, L.; Ramis, G.; Pallarés, F.J. Cytokines transcript levels in lung and lymphoid organs during genotype 1 porcine reproductive and respiratory syndrome virus (PRRSV) infection. Vet. Immunol. Immunopathol. 2014, 160, 26–40. [Google Scholar] [CrossRef] [PubMed]
- Gómez-Laguna, J.; Salguero, F.J.; De Marco, M.F.; Pallarés, F.J.; Bernabé, 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-CD8high. Viral. Immunol. 2009, 22, 261–271. [Google Scholar] [CrossRef] [PubMed]
- Zeman, D. Concurrent respiratory infections in 221 cases of PRRS virus pneumonia. J. Swine Health Prod. 1996, 4, 143–145. [Google Scholar]
- Halbur, P. “PRRS Plus”—PRRSV Infection in Combination with Other Agents; National Pork Board: Des Moines, IA, USA, 2003; pp. 19–24. [Google Scholar]
- Sinha, A.; Shen, H.G.; Schalk, S.; Beach, N.M.; Huang, Y.W.; Meng, X.J.; Halbur, P.G.; Opriessnig, T. Porcine reproductive and respiratory syndrome virus (PRRSV) influences infection dynamics of porcine circovirus type 2 (PCV2) subtypes PCV2a and PCV2b by prolonging PCV2 viremia and shedding. Vet. Microbiol. 2011, 152, 235–246. [Google Scholar] [CrossRef] [PubMed]
- Dobrescu, I.; Levast, B.; Lai, K.; Delgado-Ortega, M.; Walker, S.; Banman, S.; Townsend, H.; Simon, G.; Zhou, Y.; Gerdts, V.; et al. 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. [Google Scholar] [CrossRef] [PubMed]
- Jamieson, A.M.; Pasman, L.; Yu, S.; Gamradt, P.; Homer, R.J.; Decker, T.; Medzhitov, R. Role of tissue protection in lethal respiratory viral-bacterial coinfection. Science 2013, 340, 1230–1234. [Google Scholar] [CrossRef] [PubMed]
- Johnson, W.; Roof, M.; Vaughn, E.; Christopher-Hennings, J.; Johnson, C.R.; Murtaugh, M.P. Pathogenic and humoral immune responses to porcine reproductive and respiratory syndrome virus (PRRSV) are related to viral load in acute infection. Vet. Immunol. Immunopathol. 2004, 102, 233–247. [Google Scholar] [CrossRef] [PubMed]
- Butler, J.E.; Lager, K.M.; Golde, W.; Faaberg, K.S.; Sinkora, M.; Loving, C.; Zhang, Y.I. Porcine reproductive and respiratory syndrome (PRRS): An immune dysregulatory pandemic. Immunol. Res. 2014, 59, 81–108. [Google Scholar] [CrossRef] [PubMed]
- 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.; et al. 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. 2009, 16, 628–635. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- De Bruin, M.G.; Samsom, J.N.; Voermans, J.J.; van Rooij, E.M.; De Visser, Y.E.; Bianchi, A.T. Effects of a porcine reproductive and respiratory syndrome virus infection on the development of the immune response against pseudorabies virus. Vet. Immunol. Immunopathol. 2000, 76, 125–135. [Google Scholar] [CrossRef]
- Burton, D.R. Antibodies, viruses and vaccines. Nat. Rev. Immunol. 2002, 2, 706–713. [Google Scholar] [CrossRef] [PubMed]
- Plotkin, S.A. Correlates of protection induced by vaccination. Clin. Vaccine Immunol. 2010, 17, 1055–1065. [Google Scholar] [CrossRef] [PubMed]
- 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. Investig. 1994, 6, 289–292. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Galliher-Beckley, A.; Pappan, L.; Trible, B.; Kerrigan, M.; Beck, A.; Hesse, R.; Blecha, F.; Nietfeld, J.C.; Rowland, R.R.; et al. 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. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Correas, I.; Osorio, F.A.; Steffen, D.; Pattnaik, A.K.; Vu, H.L. Cross reactivity of immune responses to porcine reproductive and respiratory syndrome virus infection. Vaccine 2017, 35, 782–788. [Google Scholar] [CrossRef] [PubMed]
- Bilodeau, R.; Archambault, D.; Vézina, S.A.; Sauvageau, R.; Fournier, M.; Dea, S. Persistence of porcine reproductive and respiratory syndrome virus infection in a swine operation. Can. J. Vet. Res. 1994, 58, 291–298. [Google Scholar] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Lopez, O.J.; Oliveira, M.F.; Garcia, E.A.; Kwon, B.J.; Doster, A.; Osorio, F.A. Protection against porcine reproductive and respiratory syndrome virus (PRRSV) infection through passive transfer of PRRSV-neutralizing antibodies is dose dependent. Clin. Vaccine Immunol. 2007, 14, 269–275. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Choi, K.; Park, C.; Jeong, J.; Chae, C. Comparison of protection provided by type 1 and type 2 porcine reproductive and respiratory syndrome field viruses against homologous and heterologous challenge. Vet. Microbiol. 2016, 191, 72–81. [Google Scholar] [CrossRef] [PubMed]
- Wang, G.; Yu, Y.; Zhang, C.; Tu, Y.; Tong, J.; Liu, Y.; Chang, Y.; Jiang, C.; Wang, S.; Zhou, E.M.; et al. Immune responses to modified live virus vaccines developed from classical or highly pathogenic PRRSV following challenge with a highly pathogenic PRRSV strain. Dev. Comp. Immunol. 2016, 62, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Lager, K.M.; Mengeling, W.L.; Brockmeier, S.L. Evaluation of protective immunity in gilts inoculated with the NADC-8 isolate of porcine reproductive and respiratory syndrome virus (PRRSV) and challenge-exposed with an antigenically distinct PRRSV isolate. Am. J. Vet. Res. 1999, 60, 1022–1027. [Google Scholar] [PubMed]
- Opriessnig, T.; Pallares, F.; Nilubol, D.; Vincent, A.; Thacker, E.; Vaughn, E.; Roof, M.; Halbur, P. Genomic homology of ORF 5 gene sequence between modified live vaccine virus and porcine reproductive and respiratory syndrome virus challenge isolates is not predictive of vaccine efficacy. J. Swine Health Prod. 2005, 13, 246–253. [Google Scholar]
- Dea, S.; Gagnon, C.A.; Mardassi, H.; Milane, G. Antigenic variability among North American and European strains of porcine reproductive and respiratory syndrome virus as defined by monoclonal antibodies to the matrix protein. J. Clin. Microbiol. 1996, 34, 1488–1493. [Google Scholar] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Schimpl, A.; Wecker, E. Stimulation of IgG antibody response in vitro by T cell-replacing factor. J. Exp. Med. 1973, 137, 547–552. [Google Scholar] [CrossRef] [PubMed]
- Singer, A.; Hodes, R.J. Mechanisms of T cell-B cell interaction. Annu. Rev. Immunol. 1983, 1, 211–241. [Google Scholar] [CrossRef] [PubMed]
- Islam, Z.U.; Bishop, S.C.; Savill, N.J.; Rowland, R.R.; Lunney, J.K.; Trible, B.; Doeschl-Wilson, A.B. Quantitative analysis of porcine reproductive and respiratory syndrome (PRRS) viremia profiles from experimental infection: A statistical modelling approach. PLoS ONE 2013, 8, e83567. [Google Scholar] [CrossRef] [PubMed]
- Molina, R.M.; Cha, S.H.; Chittick, W.; Lawson, S.; Murtaugh, M.P.; Nelson, E.A.; Christopher-Hennings, J.; Yoon, K.J.; Evans, R.; Rowland, R.R.; et al. Immune response against porcine reproductive and respiratory syndrome virus during acute and chronic infection. Vet. Immunol. Immunopathol. 2008, 126, 283–292. [Google Scholar] [CrossRef] [PubMed]
- Mateu, E.; Diaz, I. The challenge of PRRS immunology. Vet. J. 2008, 177, 345–351. [Google Scholar] [CrossRef] [PubMed]
- 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. Investig. 1994, 6, 410–415. [Google Scholar] [CrossRef] [PubMed]
- Dosenovic, P.; von Boehmer, L.; Escolano, A.; Jardine, J.; Freund, N.T.; Gitlin, A.D.; McGuire, A.T.; Kulp, D.W.; Oliveira, T.; Scharf, L.; et al. Immunization for HIV-1 broadly neutralizing antibodies in human Ig knockin mice. Cell 2015, 161, 1505–1515. [Google Scholar] [CrossRef] [PubMed]
- Sanders, R.W.; van Gils, M.J.; Derking, R.; Sok, D.; Ketas, T.J.; Burger, J.A.; Ozorowski, G.; Cupo, A.; Simonich, C.; Goo, L.; et al. HIV-1 vaccines. HIV-1 neutralizing antibodies induced by native-like envelope trimers. Science 2015, 349, 156–161. [Google Scholar] [CrossRef] [PubMed]
- Jardine, J.G.; Kulp, D.W.; Havenar-Daughton, C.; Sarkar, A.; Briney, B.; Sok, D.; Sesterhenn, F.; Ereño-Orbea, J.; Kalyuzhniy, O.; Deresa, I.; et al. HIV-1 broadly neutralizing antibody precursor B cells revealed by germline-targeting immunogen. Science 2016, 351, 1458–1463. [Google Scholar] [CrossRef] [PubMed]
- Bonsignori, M.; Hwang, K.K.; Chen, X.; Tsao, C.Y.; Morris, L.; Gray, E.; Marshall, D.J.; Crump, J.A.; Kapiga, S.H.; Sam, N.E.; et al. Analysis of a clonal lineage of HIV-1 envelope V2/V3 conformational epitope-specific broadly neutralizing antibodies and their inferred unmutated common ancestors. J. Virol. 2011, 85, 9998–10009. [Google Scholar] [CrossRef] [PubMed]
- Bonsignori, M.; Zhou, T.; Sheng, Z.; Chen, L.; Gao, F.; Joyce, M.G.; Ozorowski, G.; Chuang, G.Y.; Schramm, C.A.; Wiehe, K.; et al. Maturation pathway from germline to broad HIV-1 neutralizer of a CD4-mimic antibody. Cell 2016, 165, 449–463. [Google Scholar] [CrossRef] [PubMed]
- MacLeod, D.T.; Choi, N.M.; Briney, B.; Garces, F.; Ver, L.S.; Landais, E.; Murrell, B.; Wrin, T.; Kilembe, W.; Liang, C.H.; et al. Early antibody lineage diversification and independent limb maturation lead to broad HIV-1 neutralization targeting the Env high-mannose patch. Immunity 2016, 44, 1215–1226. [Google Scholar] [CrossRef] [PubMed]
- Scheid, J.F.; Mouquet, H.; Feldhahn, N.; Seaman, M.S.; Velinzon, K.; Pietzsch, J.; Ott, R.G.; Anthony, R.M.; Zebroski, H.; Hurley, A.; et al. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 2009, 458, 636–640. [Google Scholar] [CrossRef] [PubMed]
- Jardine, J.; Julien, J.P.; Menis, S.; Ota, T.; Kalyuzhniy, O.; McGuire, A.; Sok, D.; Huang, P.S.; MacPherson, S.; Jones, M.; et al. Rational HIV immunogen design to target specific germline B cell receptors. Science 2013, 340, 711–716. [Google Scholar] [CrossRef] [PubMed]
- Escolano, A.; Dosenovic, P.; Nussenzweig, M.C. Progress toward active or passive HIV-1 vaccination. J. Exp. Med. 2017, 214, 3–16. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Sang, Y.; Rowland, R.R.; Blecha, F. Interaction between innate immunity and porcine reproductive and respiratory syndrome virus. Anim. Health Res. Rev. 2011, 12, 149–167. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Costers, S.; Lefebvre, D.J.; Van Doorsselaere, J.; Vanhee, M.; Delputte, P.L.; Nauwynck, H.J. GP4 of porcine reproductive and respiratory syndrome virus contains a neutralizing epitope that is susceptible to immunoselection in vitro. Arch. Virol. 2010, 155, 371–378. [Google Scholar] [CrossRef] [PubMed]
- Zhou, L.; Ni, Y.Y.; Piñeyro, P.; Sanford, B.J.; Cossaboom, C.M.; Dryman, B.A.; Huang, Y.W.; Cao, D.J.; Meng, X.J. DNA shuffling of the GP3 genes of porcine reproductive and respiratory syndrome virus (PRRSV) produces a chimeric virus with an improved cross-neutralizing ability against a heterologous PRRSV strain. Virology 2012, 434, 96–109. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Burkard, C.; Lillico, S.G.; Reid, E.; Jackson, B.; Mileham, A.J.; Ait-Ali, T.; Whitelaw, C.B.; Archibald, A.L. Precision engineering for PRRSV resistance in pigs: Macrophages from genome edited pigs lacking CD163 SRCR5 domain are fully resistant to both PRRSV genotypes while maintaining biological function. PLoS Pathog. 2017, 13, e1006206. [Google Scholar] [CrossRef] [PubMed]
- Van Breedam, W.; Delputte, P.L.; Van Gorp, H.; Misinzo, G.; Vanderheijden, N.; Duan, X.; Nauwynck, H.J. Porcine reproductive and respiratory syndrome virus entry into the porcine macrophage. J. Gen. Virol. 2010, 91, 1659–1667. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Von Bredow, B.; Arias, J.F.; Heyer, L.N.; Moldt, B.; Le, K.; Robinson, J.E.; Zolla-Pazner, S.; Burton, D.R.; Evans, D.T. Comparison of antibody-dependent cell-mediated cytotoxicity and virus neutralization by HIV-1 Env-specific monoclonal antibodies. J. Virol. 2016, 90, 6127–6139. [Google Scholar] [CrossRef] [PubMed]
- Ackerman, M.E.; Alter, G. Opportunities to exploit non-neutralizing HIV-specific antibody activity. Curr. HIV Res. 2013, 11, 365–377. [Google Scholar] [CrossRef] [PubMed]
- Long, L.; Jia, M.; Fan, X.; Liang, H.; Wang, J.; Zhu, L.; Xie, Z.; Shen, T. Non-neutralizing epitopes induce robust HCV-specific antibody-dependent CD56+ NK cell responses in chronic HCV-infected patients. Clin. Exp. Immunol. 2017, 189, 92–102. [Google Scholar] [CrossRef] [PubMed]
- Wong, S.S.; Duan, S.; DeBeauchamp, J.; Zanin, M.; Kercher, L.; Sonnberg, S.; Fabrizio, T.; Jeevan, T.; Crumpton, J.C.; Oshansky, C.; et al. The immune correlates of protection for an avian influenza H5N1 vaccine in the ferret model using oil-in-water adjuvants. Sci. Rep. 2017, 7, 44727. [Google Scholar] [CrossRef] [PubMed]
- Costers, S.; Delputte, P.L.; Nauwynck, H.J. 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, 2341–2351. [Google Scholar] [CrossRef] [PubMed]
- Rahe, M.; Murtaugh, M. Effector mechanisms of humoral immunity to porcine reproductive and respiratory syndrome virus. Vet. Immunol. Immunopathol. 2017, 186, 13–17. [Google Scholar] [CrossRef] [PubMed]
- Lamontagne, L.; Page, C.; Larochelle, R.; Longtin, D.; Magar, R. Polyclonal activation of B cells occurs in lymphoid organs from porcine reproductive and respiratory syndrome virus (PRRSV)-infected pigs. Vet. Immunol. Immunopathol. 2001, 82, 165–182. [Google Scholar] [CrossRef]
- Lemke, C.D.; Haynes, J.S.; Spaete, R.; Adolphson, D.; Vorwald, A.; Lager, K.; Butler, J.E. Lymphoid hyperplasia resulting in immune dysregulation is caused by porcine reproductive and respiratory syndrome virus infection in neonatal pigs. J. Immunol. 2004, 172, 1916–1925. [Google Scholar] [CrossRef] [PubMed]
- Butler, J.E.; Wertz, N.; Weber, P.; Lager, K.M. Porcine reproductive and respiratory syndrome virus subverts repertoire development by proliferation of germline-encoded B cells of all isotypes bearing hydrophobic heavy chain CDR3. J. Immunol. 2008, 180, 2347–2356. [Google Scholar] [CrossRef] [PubMed]
- Plagemann, P.G.; Rowland, R.R.; Cafruny, W.A. Polyclonal hypergammaglobulinemia and formation of hydrophobic immune complexes in porcine reproductive and respiratory syndrome virus-infected and uninfected pigs. Viral. Immunol. 2005, 18, 138–147. [Google Scholar] [CrossRef] [PubMed]
- Sun, X.; Wertz, N.; Lager, K.M.; Butler, J.E. Antibody repertoire development in fetal and neonatal piglets. XV. Porcine circovirus type 2 infection differentially affects serum IgG levels and antibodies to ORF2 in piglets free from other environmental factors. Vaccine 2012, 31, 141–148. [Google Scholar] [CrossRef] [PubMed]
- Butler, J.E.; Sun, J.; Weber, P.; Ford, S.P.; Rehakova, Z.; Sinkora, J.; Lager, K. Antibody repertoire development in fetal and neonatal piglets. IV. Switch recombination, primarily in fetal thymus, occurs independent of environmental antigen and is only weakly associated with repertoire diversification. J. Immunol. 2001, 167, 3239–3249. [Google Scholar] [CrossRef] [PubMed]
- Beura, L.K.; Hamilton, S.E.; Bi, K.; Schenkel, J.M.; Odumade, O.A.; Casey, K.A.; Thompson, E.A.; Fraser, K.A.; Rosato, P.C.; Filali-Mouhim, A.; et al. Normalizing the environment recapitulates adult human immune traits in laboratory mice. Nature 2016, 532, 512–516. [Google Scholar] [CrossRef] [PubMed]
- Graham, D.M. Dirty mice might make better models. Lab. Anim. 2016, 45, 198. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, R.; Gray, D. Immunological memory and protective immunity: Understanding their relation. Science 1996, 272, 54–60. [Google Scholar] [CrossRef] [PubMed]
- Taylor, J.J.; Jenkins, M.K.; Pape, K.A. Heterogeneity in the differentiation and function of memory B cells. Trends Immunol. 2012, 33, 590–597. [Google Scholar] [CrossRef] [PubMed]
- Rahe, M.C.; Murtaugh, M.P. Interleukin-21 drives proliferation and differentiation of porcine memory B cells into antibody secreting cells. PLoS ONE 2017, 12, e0171171. [Google Scholar] [CrossRef] [PubMed]
- Slifka, M.K.; Antia, R.; Whitmire, J.K.; Ahmed, R. Humoral immunity due to long-lived plasma cells. Immunity 1998, 8, 363–372. [Google Scholar] [CrossRef]
- Radbruch, A.; Muehlinghaus, G.; Luger, E.O.; Inamine, A.; Smith, K.G.; Dörner, T.; Hiepe, F. Competence and competition: The challenge of becoming a long-lived plasma cell. Nat. Rev. Immunol. 2006, 6, 741–750. [Google Scholar] [CrossRef] [PubMed]
- McMillan, R.; Longmire, R.L.; Yelenosky, R.; Lang, J.E.; Heath, V.; Craddock, C.G. Immunoglobulin synthesis by human lymphoid tissues: Normal bone marrow as a major site of IgG production. J. Immunol. 1972, 109, 1386–1394. [Google Scholar] [PubMed]
- Benner, R.; Meima, F.; van der Meulen, G.M.; van Muiswinkel, W.B. Antibody formation in mouse bone marrow. I. Evidence for the development of plaque-forming cells in situ. Immunology 1974, 26, 247–255. [Google Scholar] [PubMed]
- Slifka, M.K.; Matloubian, M.; Ahmed, R. Bone marrow is a major site of long-term antibody production after acute viral infection. J. Virol. 1995, 69, 1895–1902. [Google Scholar] [PubMed]
- Curtis, J.; Bourne, F.J. Half-lives of immunoglobulins IgG, IgA and IgM in the serum of new-born pigs. Immunology 1973, 24, 147–155. [Google Scholar] [PubMed]
- Polo, J.; Campbell, J.M.; Crenshaw, J.; Rodríguez, C.; Pujol, N.; Navarro, N.; Pujols, J. Half-life of porcine antibodies absorbed from a colostrum supplement containing porcine immunoglobulins. J. Anim. Sci. 2012, 90 (Suppl. 4), 308–310. [Google Scholar] [CrossRef] [PubMed]
- Fontanella, E.; Ma, Z.; Zhang, Y.; de Castro, A.M.; Shen, H.; Halbur, P.G.; Opriessnig, T. An interferon inducing porcine reproductive and respiratory syndrome virus vaccine candidate elicits protection against challenge with the heterologous virulent type 2 strain VR-2385 in pigs. Vaccine 2017, 35, 125–131. [Google Scholar] [CrossRef] [PubMed]
- Batista, L.; Pijoan, C.; Dee, S.; Olin, M.; Molitor, T.; Joo, H.S.; Xiao, Z.; Murtaugh, M. Virological and immunological responses to porcine reproductive and respiratory syndrome virus in a large population of gilts. Can. J. Vet. Res. 2004, 68, 267–273. [Google Scholar] [PubMed]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Wei, S.; Liu, L.; Shan, F.; Zhao, Y.; Shen, G. The role of porcine reproductive and respiratory syndrome virus infection in immune phenotype and Th1/Th2 balance of dendritic cells. Dev. Comp. Immunol. 2016, 65, 245–252. [Google Scholar] [CrossRef] [PubMed]
- Murtaugh, M.P.; Johnson, C.R.; Xiao, Z.; Scamurra, R.W.; Zhou, Y. Species specialization in cytokine biology: Is interleukin-4 central to the TH1–TH2 paradigm in swine? Dev. Comp. Immunol. 2009, 33, 344–352. [Google Scholar] [CrossRef] [PubMed]
- Liang, S.C.; Tan, X.Y.; Luxenberg, D.P.; Karim, R.; Dunussi-Joannopoulos, K.; Collins, M.; Fouser, L.A. Interleukin (IL)-22 and Il-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J. Exp. Med. 2006, 203, 2271–2279. [Google Scholar] [CrossRef] [PubMed]
- Kudva, A.; Scheller, E.V.; Robinson, K.M.; Crowe, C.R.; Choi, S.M.; Slight, S.R.; Khader, S.A.; Dubin, P.J.; Enelow, R.I.; Kolls, J.K.; et al. Influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice. J. Immunol. 2011, 186, 1666–1674. [Google Scholar] [CrossRef] [PubMed]
- Pilon, C.; Levast, B.; Meurens, F.; Le Vern, Y.; Kerboeuf, D.; Salmon, H.; Velge-Roussel, F.; Lebranchu, Y.; Baron, C. CD40 engagement strongly induces CD25 expression on porcine dendritic cells and polarizes the T cell immune response toward Th1. Mol. Immunol. 2009, 46, 437–447. [Google Scholar] [CrossRef] [PubMed]
- Shekhar, S.; Yang, X. Natural killer cells in host defense against veterinary pathogens. Vet. Immunol. Immunopathol. 2015, 168, 30–34. [Google Scholar] [CrossRef] [PubMed]
- Wesley, R.D.; Lager, K.M.; Kehrli, M.E. 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, 176–182. [Google Scholar] [PubMed]
- Choi, C.; Cho, W.S.; Kim, B.; Chae, C. Expression of interferon-gamma and tumour necrosis factor-alpha in pigs experimentally infected with porcine reproductive and respiratory syndrome virus (PRRSV). J. Comp. Pathol. 2002, 127, 106–113. [Google Scholar] [CrossRef] [PubMed]
- Thanawongnuwech, R.; Rungsipipat, A.; Disatian, S.; Saiyasombat, R.; Napakanaporn, S.; Halbur, P.G. Immunohistochemical staining of IFN-γ positive cells in porcine reproductive and respiratory syndrome virus-infected lungs. Vet. Immunol. Immunopathol. 2003, 91, 73–77. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Renukaradhya, G.J.; Alekseev, K.; Jung, K.; Fang, Y.; Saif, L.J. Porcine reproductive and respiratory syndrome virus-induced immunosuppression exacerbates the inflammatory response to porcine respiratory coronavirus in pigs. Viral. Immunol. 2010, 23, 457–466. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Manickam, C.; Dwivedi, V.; Patterson, R.; Papenfuss, T.; Renukaradhya, G.J. Porcine reproductive and respiratory syndrome virus induces pronounced immune modulatory responses at mucosal tissues in the parental vaccine strain VR2332 infected pigs. Vet. Microbiol. 2013, 162, 68–77. [Google Scholar] [CrossRef] [PubMed]
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Rahe, M.C.; Murtaugh, M.P. Mechanisms of Adaptive Immunity to Porcine Reproductive and Respiratory Syndrome Virus. Viruses 2017, 9, 148. https://doi.org/10.3390/v9060148
Rahe MC, Murtaugh MP. Mechanisms of Adaptive Immunity to Porcine Reproductive and Respiratory Syndrome Virus. Viruses. 2017; 9(6):148. https://doi.org/10.3390/v9060148
Chicago/Turabian StyleRahe, Michael C., and Michael P. Murtaugh. 2017. "Mechanisms of Adaptive Immunity to Porcine Reproductive and Respiratory Syndrome Virus" Viruses 9, no. 6: 148. https://doi.org/10.3390/v9060148