Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014, Article ID 315470, 9 pages
http://dx.doi.org/10.1155/2014/315470
Review Article

Antagonizing Interferon-Mediated Immune Response by Porcine Reproductive and Respiratory Syndrome Virus

1Laboratory Animal Center, School of Medicine, Xi’an Jiaotong University, Xi’an, Shaanxi 710061, China
2Molecular Virology Laboratory, VA-MD Regional College of Veterinary Medicine and Maryland Pathogen Research Institute, University of Maryland, College Park, MD 20742, USA

Received 9 May 2014; Revised 18 June 2014; Accepted 18 June 2014; Published 3 July 2014

Academic Editor: Anton M. Jetten

Copyright © 2014 Rong Wang and Yan-Jin Zhang. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. J. Holtkamp, J. B. Kliebenstein, E. J. Neumann et al., “Assessment of the economic impact of porcine reproductive and respiratory syndrome virus on United States pork producers,” Journal of Swine Health and Production, vol. 21, no. 2, pp. 72–84, 2013. View at Google Scholar · View at Scopus
  2. E. J. Neumann, J. B. Kliebenstein, C. D. Johnson et al., “Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States,” Journal of the American Veterinary Medical Association, vol. 227, no. 3, pp. 385–392, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. K. S. Faaberg, U. B. R. Balasuriya, M. A. Brinton et al., “Family arteriviridae,” in Virus Taxonomy, Ninth Report of the International Committee on Taxonomy of Viruses, A. M. Q. King, Ed., Elsevier Academic Press, London, UK, 2011. View at Google Scholar
  4. E. J. Snijder, M. Kikkert, and Y. Fang, “Arterivirus molecular biology and pathogenesis,” Journal of General Virology, vol. 94, part 10, pp. 2141–2163, 2013. View at Publisher · View at Google Scholar
  5. G. G. Labarque, H. J. Nauwynck, K. van Reeth, and M. B. Pensaert, “Effect of cellular changes and onset of humoral immunity on the replication of porcine reproductive and respiratory syndrome virus in the lungs of pigs,” Journal of General Virology, vol. 81, no. 5, pp. 1327–1334, 2000. View at Google Scholar · View at Scopus
  6. Z. Xiao, L. Batista, S. Dee, P. Halbur, and M. P. Murtaugh, “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,” Journal of Virology, vol. 78, no. 11, pp. 5923–5933, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. G. Wensvoort, C. Terpstra, J. M. Pol et al., “Mystery swine disease in The Netherlands: the isolation of Lelystad virus.,” Veterinary Quarterly, vol. 13, no. 3, pp. 121–130, 1991. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Pestka, “The interferons: 50 years after their discovery, there is much more to learn,” The Journal of Biological Chemistry, vol. 282, no. 28, pp. 20047–20051, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Pestka, C. D. Krause, and M. R. Walter, “Interferons, interferon-like cytokines, and their receptors,” Immunological Reviews, vol. 202, pp. 8–32, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. G. Uze, G. Schreiber, J. Piehler, and S. Pellegrini, “The receptor of the type I interferon family,” in Interferon: The 50th Anniversary, vol. 316 of Current Topics in Microbiology and Immunology, pp. 71–95, 2007. View at Publisher · View at Google Scholar
  11. V. Fensterl and G. C. Sen, “Interferons and viral infections,” BioFactors, vol. 35, no. 1, pp. 14–20, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. F. P. Siegal, N. Kadowaki, M. Shodell et al., “The nature of the principal type 1 interferon-producing cells in human blood,” Science, vol. 284, no. 5412, pp. 1835–1837, 1999. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Liu, “IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors,” Annual Review of Immunology, vol. 23, pp. 275–306, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Valente, L. Ozmen, F. Novelli et al., “Distribution of interferon-γ receptor in human tissues,” European Journal of Immunology, vol. 22, no. 9, pp. 2403–2412, 1992. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Sun, M. Han, C. Kim, J. G. Calvert, and D. Yoo, “Interplay between interferon-mediated innate immunity and porcine reproductive and respiratory syndrome virus,” Viruses, vol. 4, no. 4, pp. 424–446, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Sang, R. R. R. Rowland, and F. Blecha, “Interaction between innate immunity and porcine reproductive and respiratory syndrome virus,” Animal Health Research Reviews, vol. 12, no. 2, pp. 149–167, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. D. Yoo, C. Song, Y. Sun, Y. Du, O. Kim, and H. Liu, “Modulation of host cell responses and evasion strategies for porcine reproductive and respiratory syndrome virus,” Virus Research, vol. 154, no. 1-2, pp. 48–60, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. F. Heil, P. Ahmad-Nejad, H. Hemmi et al., “The Toll-like receptor 7 (TLR7)-specific stimulus loxoribine uncovers a strong relationship within the TLR7, 8 and 9 subfamily,” European Journal of Immunology, vol. 33, no. 11, pp. 2987–2997, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Kawai and S. Akira, “Innate immune recognition of viral infection,” Nature Immunology, vol. 7, no. 2, pp. 131–137, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Kawai, K. Takahashi, S. Sato et al., “IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction,” Nature Immunology, vol. 6, no. 10, pp. 981–988, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Sang, R. R. R. Rowland, R. A. Hesse, and F. Blecha, “Differential expression and activity of the porcine type I interferon family,” Physiological Genomics, vol. 42, no. 2, pp. 248–258, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. W. Buddaert, K. van Reeth, and M. Pensaert, “In vivo and in vitro interferon (IFN) studies with the porcine reproductive and respiratory syndrome virus (PRRSV),” Advances in Experimental Medicine and Biology, vol. 440, pp. 461–467, 1998. View at Google Scholar · View at Scopus
  23. C. Overend, R. Mitchell, D. He, G. Rompato, M. J. Grubman, and A. E. Garmendia, “Recombinant swine beta interferon protects swine alveolar macrophages and MARC-145 cells from infection with Porcine reproductive and respiratory syndrome virus,” Journal of General Virology, vol. 88, part 3, pp. 925–931, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. S. L. Brockmeier, K. M. Lager, M. J. Grubman et al., “Adenovirus-mediated expression of interferon-α delays viral replication and reduces disease signs in swine challenged with porcine reproductive and respiratory syndrome virus,” Viral Immunology, vol. 22, no. 3, pp. 173–180, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. E. Albina, C. Carrat, and B. Charley, “Interferon-α response to swine arterivirus (PoAV), the porcine reproductive and respiratory syndrome virus,” Journal of Interferon and Cytokine Research, vol. 18, no. 7, pp. 485–490, 1998. View at Publisher · View at Google Scholar · View at Scopus
  26. G. Calzada-Nova, W. Schnitzlein, R. Husmann, and F. A. Zuckermann, “Characterization of the cytokine and maturation responses of pure populations of porcine plasmacytoid dendritic cells to porcine viruses and toll-like receptor agonists,” Veterinary Immunology and Immunopathology, vol. 135, no. 1-2, pp. 20–33, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. G. Calzada-Nova, W. M. Schnitzlein, R. J. Husmann, and F. A. Zuckermann, “North American porcine reproductive and respiratory syndrome viruses inhibit type I interferon production by plasmacytoid dendritic cells,” Journal of Virology, vol. 85, no. 6, pp. 2703–2713, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. C. L. Loving, S. L. Brockmeier, and R. E. Sacco, “Differential type I interferon activation and susceptibility of dendritic cell populations to porcine arterivirus,” Immunology, vol. 120, no. 2, pp. 217–229, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. L. C. Miller, W. W. Laegreid, J. L. Bono, C. G. Chitko-McKown, and J. M. Fox, “Interferon type I response in porcine reproductive and respiratory syndrome virus-infected MARC-145 cells,” Archives of Virology, vol. 149, no. 12, pp. 2453–2463, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. O. Kim, Y. Sun, F. W. Lai, C. Song, and D. Yoo, “Modulation of type I interferon induction by porcine reproductive and respiratory syndrome virus and degradation of CREB-binding protein by non-structural protein 1 in MARC-145 and HeLa cells,” Virology, vol. 402, no. 2, pp. 315–326, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. L. K. Beura, S. N. Sarkar, B. Kwon et al., “Porcine reproductive and respiratory syndrome virus nonstructural protein 1β modulates host innate immune response by antagonizing IRF3 activation,” Journal of Virology, vol. 84, no. 3, pp. 1574–1584, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. Z. Chen, S. Lawson, Z. Sun et al., “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, vol. 398, no. 1, pp. 87–97, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. H. Li, Z. Zheng, P. Zhou et al., “The cysteine protease domain of porcine reproductive and respiratory syndrome virus non-structural protein 2 antagonizes interferon regulatory factor 3 activation,” Journal of General Virology, vol. 91, no. 12, pp. 2947–2958, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Sagong and C. Lee, “Porcine reproductive and respiratory syndrome virus nucleocapsid protein modulates interferon-β production by inhibiting IRF3 activation in immortalized porcine alveolar macrophages,” Archives of Virology, vol. 156, no. 12, pp. 2187–2195, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. Z. Sun, Z. Chen, S. R. Lawson, and Y. Fang, “The cysteine protease domain of porcine reproductive and respiratory syndrome virus nonstructural protein 2 possesses deubiquitinating and interferon antagonism functions,” Journal of Virology, vol. 84, no. 15, pp. 7832–7846, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. X. Shi, L. Wang, X. Li et al., “Endoribonuclease activities of porcine reproductive and respiratory syndrome virus nsp11 was essential for nsp11 to inhibit IFN-β induction,” Molecular Immunology, vol. 48, no. 12-13, pp. 1568–1572, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. X. Tian, G. Lu, F. Gao et al., “Structure and cleavage specificity of the chymotrypsin-like serine protease (3CLSP/nsp4) of Porcine Reproductive and Respiratory Syndrome Virus (PRRSV),” Journal of Molecular Biology, vol. 392, no. 4, pp. 977–993, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. R. Luo, S. Xiao, Y. Jiang et al., “Porcine reproductive and respiratory syndrome virus (PRRSV) suppresses interferon-β production by interfering with the RIG-I signaling pathway,” Molecular Immunology, vol. 45, no. 10, pp. 2839–2846, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. X. Shi, L. Wang, Y. Zhi et al., “Porcine reproductive and respiratory syndrome virus (PRRSV) could be sensed by professional beta interferon-producing system and had mechanisms to inhibit this action in MARC-145 cells,” Virus Research, vol. 153, no. 1, pp. 151–156, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Song, P. Krell, and D. Yoo, “Nonstructural protein 1-alpha subunit-based inhibition of NF-κB activation and suppression of interferon-β production by porcine reproductive and respiratory syndrome virus,” Virology, vol. 407, no. 2, pp. 268–280, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. X. Shi, J. Chen, G. Xing et al., “Amino acid at position 176 was essential for porcine reproductive and respiratory syndrome virus (PRRSV) non-structural protein 1α (nsp1α) as an inhibitor to the induction of IFN-β,” Cellular Immunology, vol. 280, no. 2, pp. 125–131, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. Li, L. Zhu, S. R. Lawson, and Y. Fang, “Targeted mutations in a highly conserved motif of the nsp1β protein impair the interferon antagonizing activity of porcine reproductive and respiratory syndrome virus,” Journal of General Virology, vol. 94, no. 9, pp. 1972–1983, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. D. D. Nedialkova, R. Ulferts, E. van den Born et al., “Biochemical characterization of arterivirus nonstructural protein 11 reveals the nidovirus-wide conservation of a replicative endoribonuclease,” Journal of Virology, vol. 83, no. 11, pp. 5671–5682, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Lee, S. K. Schommer, and S. B. Kleiboeker, “Porcine reproductive and respiratory syndrome virus field isolates differ in in vitro interferon phenotypes,” Veterinary Immunology and Immunopathology, vol. 102, no. 3, pp. 217–231, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Zhang, X. Guo, E. Nelson, J. Christopher-Hennings, and X. Wang, “Porcine reproductive and respiratory syndrome virus activates the transcription of interferon alpha/beta (IFN-α/β) in monocyte-derived dendritic cells (Mo-DC),” Veterinary Microbiology, vol. 159, no. 3-4, pp. 494–498, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Baumann, E. Mateu, M. P. Murtaugh, and A. Summerfield, “Impact of genotype 1 and 2 of porcine reproductive and respiratory syndrome viruses on interferon-α responses by plasmacytoid dendritic cells,” Veterinary Research, vol. 44, no. 1, article 33, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Nan, R. Wang, M. Shen, K. S. Faaberg, S. K. Samal, and Y. Zhang, “Induction of type I interferons by a novel porcine reproductive and respiratory syndrome virus isolate,” Virology, vol. 432, no. 2, pp. 261–270, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Wang, Y. Xiao, T. Opriessnig et al., “Enhancing neutralizing antibody production by an interferon-inducing porcine reproductive and respiratory syndrome virus strain,” Vaccine, vol. 31, no. 47, pp. 5537–5543, 2013. View at Publisher · View at Google Scholar
  49. A. Takaoka and H. Yanai, “Interferon signalling network in innate defence,” Cellular Microbiology, vol. 8, no. 6, pp. 907–922, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. J. M. Gonzalez-Navajas, J. Lee, M. David, and E. Raz, “Immunomodulatory functions of type I interferons,” Nature Reviews Immunology, vol. 12, no. 2, pp. 125–135, 2012. View at Google Scholar
  51. J. E. Darnell Jr., I. M. Kerr, and G. R. Stark, “Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins,” Science, vol. 264, no. 5164, pp. 1415–1421, 1994. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Schindler and J. E. Darnell Jr., “Transcriptional responses to polypeptide ligands: the JAK-STAT pathway,” Annual Review of Biochemistry, vol. 64, pp. 621–651, 1995. View at Publisher · View at Google Scholar · View at Scopus
  53. G. R. Stark, I. M. Kerr, B. R. Williams, R. H. Silverman, and R. D. Schreiber, “How cells respond to interferons,” Annual Review of Biochemistry, vol. 67, pp. 227–264, 1998. View at Google Scholar
  54. D. Patel, Y. Nan, M. Shen, K. Ritthipichai, X. Zhu, and Y. Zhang, “Porcine reproductive and respiratory syndrome virus inhibits type I interferon signaling by blocking STAT1/STAT2 nuclear translocation,” Journal of Virology, vol. 84, no. 21, pp. 11045–11055, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. R. Wang, Y. Nan, Y. Yu, Z. Yang, and Y. Zhang, “Variable interference with interferon signal transduction by different strains of porcine reproductive and respiratory syndrome virus,” Veterinary Microbiology, vol. 166, no. 3-4, pp. 493–503, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. R. Wang, Y. Nan, Y. Yu, and Y. Zhang, “Porcine reproductive and respiratory syndrome virus Nsp1β inhibits interferon-activated JAK/STAT signal transduction by inducing karyopherin-α1 degradation,” Journal of Virology, vol. 87, no. 9, pp. 5219–5228, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. E. C. Borden, G. C. Sen, G. Uze et al., “Interferons at age 50: past, current and future impact on biomedicine,” Nature Reviews Drug Discovery, vol. 6, no. 12, pp. 975–990, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. Z. Sun, R. Ransburgh, E. J. Snijder, and Y. Fang, “Nonstructural protein 2 of porcine reproductive and respiratory syndrome virus inhibits the antiviral function of interferon-stimulated gene 15,” Journal of Virology, vol. 86, no. 7, pp. 3839–3850, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Recht, E. C. Borden, and E. Knight Jr., “A human 15-kDa IFN-induced protein induces the secretion of IFN-γ,” The Journal of Immunology, vol. 147, no. 8, pp. 2617–2623, 1991. View at Google Scholar · View at Scopus
  60. D. J. Lenschow, C. Lai, N. Frias-Staheli et al., “IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 4, pp. 1371–1376, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. M. J. Clemens and A. Elia, “The double-stranded RNA-dependent protein kinase PKR: structure and function,” Journal of Interferon and Cytokine Research, vol. 17, no. 9, pp. 503–524, 1997. View at Publisher · View at Google Scholar · View at Scopus
  62. R. R. R. Rowland, B. Robinson, J. Stefanick et al., “Inhibition of porcine reproductive and respiratory syndrome virus by interferon-gamma and recovery of virus replication with 2-aminopurine,” Archives of Virology, vol. 146, no. 3, pp. 539–555, 2001. View at Publisher · View at Google Scholar · View at Scopus
  63. D. He, C. Overend, J. Ambrogio, R. J. Maganti, M. J. Grubman, and A. E. Garmendia, “Marked differences between MARC-145 cells and swine alveolar macrophages in IFNβ-induced activation of antiviral state against PRRSV,” Veterinary Immunology and Immunopathology, vol. 139, no. 1, pp. 57–60, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. B. Guo, K. M. Lager, J. N. Henningson et al., “Experimental infection of United States swine with a Chinese highly pathogenic strain of porcine reproductive and respiratory syndrome virus,” Virology, vol. 435, no. 2, pp. 372–384, 2013. View at Publisher · View at Google Scholar · View at Scopus