North American porcine reproductive and respiratory syndrome viruses inhibit type I interferon production by plasmacytoid dendritic cells

Journal of Virology

Volumn 85, Issue 6, 2011, Pages 2703-2713

  Calzada Nova, Gabriela ^a   Schnitzlein, William M ^a   Husmann, Robert J ^a   Zuckermann, Federico A ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 2; INTERLEUKIN 6; OLIGODEOXYNUCLEOTIDE; OLIGODEOXYNUCLEOTIDE D19; STAT1 PROTEIN; TOLL LIKE RECEPTOR 9 AGONIST; TOLL LIKE RECEPTOR AGONIST; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ACIDIFICATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIVIRUS; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION; IMMUNOSUPPRESSIVE TREATMENT; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TRANSMISSABLE GASTROENTERITIS VIRUS; VIRUS VIABILITY;

ANIMALS; DENDRITIC CELLS; DOWN-REGULATION; GENE EXPRESSION; INTERFERON REGULATORY FACTOR-7; INTERFERON TYPE I; NORTH AMERICA; OLIGODEOXYRIBONUCLEOTIDES; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; RNA, MESSENGER; SWINE; TRANSMISSIBLE GASTROENTERITIS VIRUS;

PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUS; TRANSMISSIBLE GASTROENTERITIS VIRUS;

EID: 79952435739     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01616-10     Document Type: Article

References (76)

1. Albina, E. 1997. Epidemiology of porcine reproductive and respiratory syndrome (PRRS): an overview. Vet. Microbiol. 55:309-316.
2. Albina, E., C. Carrat, and B. Charley. 1998. Interferon-alpha response to swine arterivirus (PoAV), the porcine reproductive and respiratory syndrome virus. J. Interferon Cytokine Res. 18:485-490. (Pubitemid 28363575)
3. Albina, E., L. Piriou, E. Hutet, R. Cariolet, and R. L'Hospitalier. 1998. Immune responses in pigs infected with porcine reproductive and respiratory syndrome virus (PRRSV). Vet. Immunol. Immunopathol. 61:49-66.
4. Allende, R., et al. 2000. Porcine reproductive and respiratory syndrome virus: description of persistence in individual pigs upon experimental infection. J. Virol. 74:10834-10837.
5. Baudoux, P., C. Carrat, L. Besnardeau, B. Charley, and H. Laude. 1998. Coronavirus pseudoparticles formed with recombinant M and E proteins induce alpha interferon synthesis by leukocytes. J. Virol. 72:8636-8643. (Pubitemid 28471802)
6. Beignon, A. S., et al. 2005. Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J. Clin. Invest. 115:3265-3275.
7. Buddaert, W., K. Van Reeth, and M. Pensaert. 1998. In vivo and in vitro interferon (IFN) studies with the porcine reproductive and respiratory syndrome virus (PRRSV). Adv. Exp. Med. Biol. 440:461-467.
8. Calzada-Nova, G., W. Schnitzlein, R. Husmann, and F. A. Zuckermann. 2010. Characterization of the cytokine and maturation responses of pure populations of porcine plasmacytoid dendritic cells to porcine viruses and Toll-like receptor agonists. Vet. Immunol. Immunopathol. 135:20-33.
9. Cao, W., and L. Bover. 2010. Signaling and ligand interaction of ILT7: receptor-mediated regulatory mechanisms for plasmacytoid dendritic cells. Immunol. Rev. 234:163-176.
10. Cao, W., et al. 2007. BDCA2/FcεRIγ complex signals through a novel BCR-like pathway in human plasmacytoid dendritic cells. PLoS Biol. 5:e248.
11. Cella, M., F. Facchetti, A. Lanzavecchia, and M. Colonna. 2000. Plasmacytoid dendritic cells activated by influenza virus and CD40L drive a potent TH1 polarization. Nat. Immunol. 1:305-310.
12. Colina, R., et al. 2008. Translational control of the innate immune response through IRF-7. Nature 452:323-328. (Pubitemid 351430792)
13. Colonna, M., G. Trinchieri, and Y. J. Liu. 2004. Plasmacytoid dendritic cells in immunity. Nat. Immunol. 5:1219-1226.
14. Dai, J., N. J. Megjugorac, S. B. Amrute, and P. Fitzgerald-Bocarsly. 2004. Regulation of IFN regulatory factor-7 and IFN-alpha production by enveloped virus and lipopolysaccharide in human plasmacytoid dendritic cells. J. Immunol. 173:1535-1548. (Pubitemid 38971583)
15. Duan, X., H. J. Nauwynck, and M. B. Pensaert. 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. 142:2483-2497.
16. Dzionek, A., et al. 2001. BDCA-2, a novel plasmacytoid dendritic cell-specific type II C-type lectin, mediates antigen capture and is a potent inhibitor of interferon alpha/beta induction. J. Exp. Med. 194:1823-1834.
17. Fanning, S. L., et al. 2006. Receptor cross-linking on human plasmacytoid dendritic cells leads to the regulation of IFN-alpha production. J. Immunol. 177:5829-5839. (Pubitemid 44628796)
18. Feldman, S. B., et al. 1994. Viral induction of low frequency interferon-alpha producing cells. Virology 204:1-7. (Pubitemid 24305312)
19. Fitzgerald-Bocarsly, P., J. Dai, and S. Singh. 2008. Plasmacytoid dendritic cells and type I IFN: 50 years of convergent history. Cytokine Growth Factor Rev. 19:3-19.
20. Fonteneau, J. F., et al. 2004. Human immunodeficiency virus type 1 activates plasmacytoid dendritic cells and concomitantly induces the bystander maturation of myeloid dendritic cells. J. Virol. 78:5223-5232.
21. Genini, S., et al. 2008. Genome-wide transcriptional response of primary alveolar macrophages following infection with porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 89:2550-2564.
22. George, T. C., et al. 2006. Quantitative measurement of nuclear translocation events using similarity analysis of multispectral cellular images obtained in flow. J. Immunol. Methods 311:117-129.
23. Gerosa, F., et al. 2005. The reciprocal interaction of NK cells with plasmacytoid or myeloid dendritic cells profoundly affects innate resistance functions. J. Immunol. 174:727-734. (Pubitemid 40094266)
24. Gilliet, M., W. Cao, and Y. J. Liu. 2008. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat. Rev. Immunol. 8:594-606.
25. Goldberg, T. L., E. C. Hahn, R. M. Weigel, and G. Scherba. 2000. Genetic, geographical and temporal variation of porcine reproductive and respiratory syndrome virus in Illinois. J. Gen. Virol. 81:171-179.
26. Guzylack-Piriou, L., F. Bergamin, M. Gerber, K. C. McCullough, and A. Summerfield. 2006. Plasmacytoid dendritic cell activation by foot-and-mouth disease virus requires immune complexes. Eur. J. Immunol. 36:1674-1683.
27. Harms, P. A., et al. 2001. Experimental reproduction of severe disease in CD/CD pigs concurrently infected with type 2 porcine circovirus and porcine reproductive and respiratory syndrome virus. Vet. Pathol. 38:528-539.
28. Honda, K., et al. 2005. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434:772-777. (Pubitemid 44739521)
29. Horter, D. C., et al. 2002. Characterization of the carrier state in porcine reproductive and respiratory syndrome virus infection. Vet. Microbiol. 86:213-228.
30. Ito, T., et al. 2007. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J. Exp. Med. 204:105-115.
31. Izaguirre, A., et al. 2003. Comparative analysis of IRF and IFN-alpha expression in human plasmacytoid and monocyte-derived dendritic cells. J. Leukoc. Biol. 74:1125-1138.
32. Jego, G., et al. 2003. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity 19:225-234. (Pubitemid 37011337)
33. Kamstrup, S., D. Verthelyi, and D. M. Klinman. 2001. Response of porcine peripheral blood mononuclear cells to CpG-containing oligodeoxynucleotides. Vet. Microbiol. 78:353-362.
34. Katz, J. B., A. L. Shafer, K. A. Eernisse, J. G. Landgraf, and E. A. Nelson. 1995. Antigenic differences between European and American isolates of porcine reproductive and respiratory syndrome virus (PRRSV) are encoded by the carboxyterminal portion of viral open reading frame 3. Vet. Microbiol. 44:65-76.
35. Kawai, T., et al. 2004. Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat. Immunol. 5:1061-1068.
36. high T cells. Viral Immunol. 16:395-406.
37. Latz, E., et al. 2004. TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat. Immunol. 5:190-198.
38. Laude, H., J. Gelfi, L. Lavenant, and B. Charley. 1992. Single amino acid changes in the viral glycoprotein M affect induction of alpha interferon by the coronavirus transmissible gastroenteritis virus. J. Virol. 66:743-749.
39. Lee, C., and D. Yoo. 2006. The small envelope protein of porcine reproductive and respiratory syndrome virus possesses ion channel protein-like properties. Virology 355:30-43. (Pubitemid 44585054)
40. Lee, S. M., S. K. Schommer, and S. B. Kleiboeker. 2004. Porcine reproductive and respiratory syndrome virus field isolates differ in in vitro interferon phenotypes. Vet. Immunol. Immunopathol. 102:217-231.
41. -ΔΔCT method. Methods 25:402-408.
42. Loemba, H. D., S. Mounir, H. Mardassi, D. Archambault, and S. Dea. 1996. Kinetics of humoral immune response to the major structural proteins of the porcine reproductive and respiratory syndrome virus. Arch. Virol. 141:751-761.
43. Loving, C. L., S. L. Brockmeier, and R. E. Sacco. 2007. Differential type I interferon activation and susceptibility of dendritic cell populations to porcine arterivirus. Immunology 120:217-229.
44. Martinelli, E., et al. 2007. HIV-1 gp120 inhibits TLR9-mediated activation and IFN-α secretion in plasmacytoid dendritic cells. Proc. Natl. Acad. Sci. U. S. A. 104:3396-3401.
45. McKenna, K., A. S. Beignon, and N. Bhardwaj. 2005. Plasmacytoid dendritic cells: linking innate and adaptive immunity. J. Virol. 79:17-27. (Pubitemid 39648359)
46. Meier, W. A., et al. 2003. Gradual development of the interferon-gamma response of swine to porcine reproductive and respiratory syndrome virus infection or vaccination. Virology 309:18-31. (Pubitemid 36511403)
47. Mengeling, W. L., K. M. Lager, A. C. Vorwald, and K. J. Koehler. 2003. Strain specificity of the immune response of pigs following vaccination with various strains of porcine reproductive and respiratory syndrome virus. Vet. Microbiol. 93:13-24.
48. Miller, L. C., W. W. Laegreid, J. L. Bono, C. G. Chitko-McKown, and J. M. Fox. 2004. Interferon type I response in porcine reproductive and respiratory syndrome virus-infected MARC-145 cells. Arch. Virol. 149:2453-2463.
49. Misinzo, G. M., P. L. Delputte, and H. J. Nauwynck. 2008. Involvement of proteases in porcine reproductive and respiratory syndrome virus uncoating upon internalization in primary macrophages. Vet. Res. 39:55.
50. Nauwynck, H. J., X. Duan, H. W. Favoreel, P. Van Oostveldt, and M. B. Pensaert. 1999. Entry of porcine reproductive and respiratory syndrome virus into porcine alveolar macrophages via receptor-mediated endocytosis. J. Gen. Virol. 80:297-305.
51. Nelson, E. A., J. Christopher-Hennings, and D. A. Benfield. 1994. Serum immune responses to the proteins of porcine reproductive and respiratory syndrome (PRRS) virus. J. Vet. Diagn. Invest. 6:410-415.
52. Osawa, Y., et al. 2006. Collaborative action of NF-κB and p38 MAPK is involved in CpG DNA-induced IFN-alpha and chemokine production in human plasmacytoid dendritic cells. J. Immunol. 177:4841-4852. (Pubitemid 44469820)
53. Paquette, R. L., et al. 1998. Interferon-alpha and granulocyte-macrophage colony-stimulating factor differentiate peripheral blood monocytes into potent antigen-presenting cells. J. Leukoc. Biol. 64:358-367.
54. Pfaller, C. K., and K. Conzelmann. 2008. Measles virus V protein is a decoy substrate for IκB kinase α and prevents Toll-like receptor 7/9-mediated interferon induction. J. Virol. 82:12365-12373.
55. Poeck, H., et al. 2004. Plasmacytoid dendritic cells, antigen, and CpG-C license human B cells for plasma cell differentiation and immunoglobulin production in the absence of T-cell help. Blood 103:3058-3064. (Pubitemid 38451681)
56. Poole, B., and S. Ohkuma. 1981. Effect of weak bases on the intralysosomal pH in mouse peritoneal macrophages. J. Cell Biol. 90:665-669. (Pubitemid 12254922)
57. Proietti, E., et al. 2002. Type I IFN as a natural adjuvant for a protective immune response: lessons from the influenza vaccine model. J. Immunol. 169:375-383. (Pubitemid 34686158)
58. Randall, R. E., and S. Goodbourn. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 89:1-47.
59. Rock, J., et al. 2007. CD303 (BDCA-2) signals in plasmacytoid dendritic cells via a BCR-like signalosome involving Syk, Slp65 and PLCγ2. Eur. J. Immunol. 37:3564-3575.
60. Rutz, M., et al. 2004. Toll-like receptor 9 binds single-stranded CpG-DNA in a sequence- and pH-dependent manner. Eur. J. Immunol. 34:2541-2550.
61. Sanjuan, M. A., et al. 2006. CpG-induced tyrosine phosphorylation occurs via a TLR9-independent mechanism and is required for cytokine secretion. J. Cell Biol. 172:1057-1068.
62. Schlender, J., et al. 2005. Inhibition of toll-like receptor 7- and 9-mediated alpha/beta interferon production in human plasmacytoid dendritic cells by respiratory syncytial virus and measles virus. J. Virol. 79:5507-5515. (Pubitemid 40548219)
63. Seeds, R. E., S. Gordon, and J. L. Miller. 2006. Receptors and ligands involved in viral induction of type I interferon production by plasmacytoid dendritic cells. Immunobiology 211:525-535.
64. Swiecki, M., and M. Colonna. 2010. Unraveling the functions of plasmacytoid dendritic cells during viral infections, autoimmunity, and tolerance. Immunol. Rev. 234:142-162.
65. Takaoka, A., et al. 2005. Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 434:243-249. (Pubitemid 40388058)
66. Takauji, R., et al. 2002. CpG-DNA-induced IFN-alpha production involves p38 MAPK-dependent STAT1 phosphorylation in human plasmacytoid dendritic cell precursors. J. Leukoc. Biol. 72:1011-1019.
67. Truong, H. M., et al. 2004. A highly pathogenic porcine reproductive and respiratory syndrome virus generated from an infectious cDNA clone retains the in vivo virulence and transmissibility properties of the parental virus. Virology 325:308-319. (Pubitemid 38902796)
68. Van Gorp, H., W. Van Breedam, P. L. Delputte, and H. J. Nauwynck. 2009. The porcine reproductive and respiratory syndrome virus requires trafficking through CD163-positive early endosomes, but not late endosomes, for productive infection. Arch. Virol. 154:1939-1943.
69. Van Reeth, K., G. Labarque, H. Nauwynck, and M. Pensaert. 1999. Differential production of proinflammatory cytokines in the pig lung during different respiratory virus infections: correlations with pathogenicity. Res. Vet. Sci. 67:47-52.
70. Vincent, I. E., et al. 2007. Silencing of natural interferon producing cell activation by porcine circovirus type 2 DNA. Immunology 120:47-56.
71. Vincent, I. E., et al. 2005. Subset-dependent modulation of dendritic cell activity by circovirus type 2. Immunology 115:388-398. (Pubitemid 40903077)
72. Weslow-Schmidt, J. L., et al. 2007. Type I interferon inhibition and dendritic cell activation during gammaherpesvirus respiratory infection. J. Virol. 81:9778-9789. (Pubitemid 350067682)
73. Xiao, Z., L. Batista, S. Dee, P. Halbur, and M. P. Murtaugh. 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. 78:5923-5933.
74. Xu, Y., et al. 2009. HBsAg inhibits TLR9-mediated activation and IFN-alpha production in plasmacytoid dendritic cells. Mol. Immunol. 46:2640-2646.
75. Yoo, D., S. W. Welch, C. Lee, and J. G. Calvert. 2004. Infectious cDNA clones of porcine reproductive and respiratory syndrome virus and their potential as vaccine vectors. Vet. Immunol. Immunopathol. 102:143-154.
76. Yoon, K. J., et al. 1995. Characterization of the humoral immune response to porcine reproductive and respiratory syndrome (PRRS) virus infection. J. Vet. Diagn. Invest. 7:305-312.