Porcine reproductive and respiratory syndrome virus nonstructural protein 1β modulates host innate immune response by antagonizing IRF3 activation

Journal of Virology

Volumn 84, Issue 3, 2010, Pages 1574-1584

  Beura, Lalit K ^a   Sarkar, Saumendra N ^b   Kwon, Byungjoon ^a   Subramaniam, Sakthivel ^a   Jones, Clinton ^a   Pattnaik, Asit K ^a   Osorio, Fernando A ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; DOUBLE STRANDED RNA; I KAPPA B KINASE EPSILON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; NONSTRUCTURAL PROTEIN 1; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1;

ANTIVIRAL ACTIVITY; ARTERIVIRUS; ARTICLE; BETA CHAIN; CONTROLLED STUDY; GENE EXPRESSION; GENE INDUCTION; GENE TRANSLOCATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; SENDAI VIRUS; VIRUS GENOME;

BASE SEQUENCE; CELL LINE; CELL NUCLEUS; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNITY, INNATE; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; NF-KAPPA B; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; PROMOTER REGIONS, GENETIC; VIRAL NONSTRUCTURAL PROTEINS;

PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SENDAI VIRUS; SUIDAE; SUS;

EID: 73949087536     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01326-09     Document Type: Article

References (59)

1. 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.
2. Allende, R., W. W. Laegreid, G. F. Kutish, J. A. Galeota, R. W. Wills, and F. A. Osorio. 2000. Porcine reproductive and respiratory syndrome virus: description of persistence in individual pigs upon experimental infection. J. Virol. 74:10834-10837.
3. Ansari, I. H., B. Kwon, F. A. Osorio, and A. K. Pattnaik. 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.
4. Bauhofer, O., A. Summerfield, Y. Sakoda, J. D. Tratschin, M. A. Hofmann, and N. Ruggli. 2007. Classical swine fever virus Npro interacts with interferon regulatory factor 3 and induces its proteasomal degradation. J. Virol. 81:3087-3096.
5. Bautista, E. M., K. S. Faaberg, D. Mickelson, and E. D. McGruder. 2002. Functional properties of the predicted helicase of porcine reproductive and respiratory syndrome virus. Virology 298:258-270.
6. Bhoj, V. G., and Z. J. Chen. 2009. Ubiquitylation in innate and adaptive immunity. Nature 458:430-437.
7. Bowie, A. G., and L. Unterholzner. 2008. Viral evasion and subversion of pattern-recognition receptor signalling. Nat. Rev. Immunol. 8:911-922.
8. 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.
9. Cavanagh, D. 1997. Nidovirales: a new order comprising Coronaviridae and Arteriviridae. Arch. Virol. 142:629-633.
10. Costers, S., D. J. Lefebvre, P. L. Delputte, and H. J. Nauwynck. 2008. Porcine reproductive and respiratory syndrome virus modulates apoptosis during replication in alveolar macrophages. Arch. Virol. 153:1453-1465.
11. de Lima, M., B. Kwon, I. H. Ansari, A. K. Pattnaik, E. F. Flores, and F. A. Osorio. 2008. Development of a porcine reproductive and respiratory syndrome virus differentiable (DIVA) strain through deletion of specific immunodominant epitopes. Vaccine 26:3594-3600.
12. den Boon, J. A., K. S. Faaberg, J. J. Meulenberg, A. L. Wassenaar, P. G. Plagemann, A. E. Gorbalenya, and E. J. Snijder. 1995. Processing and evolution of the N-terminal region of the arterivirus replicase ORF1a protein: identification of two papainlike cysteine proteases. J. Virol. 69:4500-4505.
13. Feng, W., S. M. Laster, M. Tompkins, T. Brown, J. S. Xu, C. Altier, W. Gomez, D. Benfield, and M. B. McCaw. 2001. In utero infection by porcine reproductive and respiratory syndrome virus is sufficient to increase susceptibility of piglets to challenge by Streptococcus suis type II. J. Virol. 75:4889-4895.
14. Foy, E., K. Li, R. Sumpter, Jr., Y. M. Loo, C. L. Johnson, C. Wang, P. M. Fish, M. Yoneyama, T. Fujita, S. M. Lemon, and M. Gale, Jr. 2005. Control of antiviral defenses through hepatitis C virus disruption of retinoic acidinducible gene-I signaling. Proc. Natl. Acad. Sci. U. S. A. 102:2986-2991.
15. Frias-Staheli, N., N. V. Giannakopoulos, M. Kikkert, S. L. Taylor, A. Bridgen, J. Paragas, J. A. Richt, R. R. Rowland, C. S. Schmaljohn, D. J. Lenschow, E. J. Snijder, A. Garcia-Sastre, and H. W. t. Virgin. 2007. Ovarian tumor domain-containing viral proteases evade ubiquitin- and ISG15-dependent innate immune responses. Cell Host Microbe 2:404-416.
16. Garcia-Sastre, A., and C. A. Biron. 2006. Type 1 interferons and the virushost relationship: a lesson in detente. Science 312:879-882.
17. Genini, S., P. L. Delputte, R. Malinverni, M. Cecere, A. Stella, H. J. Nauwynck, and E. Giuffra. 2008. Genome-wide transcriptional response of primary alveolar macrophages following infection with porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 89:2550-2564.
18. Gil, L. H., I. H. Ansari, V. Vassilev, D. Liang, V. C. Lai, W. Zhong, Z. Hong, E. J. Dubovi, and R. O. Donis. 2006. The amino-terminal domain of bovine viral diarrhea virus Npro protein is necessary for alpha/beta interferon antagonism. J. Virol. 80:900-911.
19. Guo, J., K. L. Peters, and G. C. Sen. 2000. Induction of the human protein P56 by interferon, double-stranded RNA, or virus infection. Virology 267: 209-219.
20. Hartman, A. L., B. H. Bird, J. S. Towner, Z. A. Antoniadou, S. R. Zaki, and S. T. Nichol. 2008. Inhibition of IRF-3 activation by VP35 is critical for the high level of virulence of Ebola virus. J. Virol. 82:2699-2704.
21. Hiscott, J., H. Kwon, and P. Genin. 2001. Hostile takeovers: viral appropriation of the NF-κB pathway. J. Clin. Invest. 107:143-151.
22. Huang, Y. W., Y. Fang, and X. J. Meng. 2009. Identification and characterization of a porcine monocytic cell line supporting porcine reproductive and respiratory syndrome virus (PRRSV) replication and progeny virion production by using an improved DNA-launched PRRSV reverse genetics system. Virus Res. 145:1-8.
23. Jiang, Z., T. W. Mak, G. Sen, and X. Li. 2004. Toll-like receptor 3-mediated activation of NF-κB and IRF3 diverges at Toll-IL-1 receptor domain-containing adapter inducing IFN-beta. Proc. Natl. Acad. Sci. U. S. A. 101:3533-3538.
24. Kato, H., O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K. J. Ishii, O. Yamaguchi, K. Otsu, T. Tsujimura, C. S. Koh, C. Reis e Sousa, Y. Matsuura, T. Fujita, and S. Akira. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101-105.
25. Kim, H. S., J. Kwang, I. J. Yoon, H. S. Joo, and M. L. Frey. 1993. Enhanced replication of porcine reproductive and respiratory syndrome (PRRS) virus in a homogeneous subpopulation of MA-104 cell line. Arch. Virol. 133:477-483.
26. Kroese, M. V., J. C. Zevenhoven-Dobbe, J. N. Bos-de Ruijter, B. P. Peeters, J. J. Meulenberg, L. A. Cornelissen, and E. J. Snijder. 2008. The nsp1alpha and nsp1 papain-like autoproteinases are essential for porcine reproductive and respiratory syndrome virus RNA synthesis. J. Gen. Virol. 89:494-499.
27. Kwon, B., I. H. Ansari, A. K. Pattnaik, and F. A. Osorio. 2008. Identification of virulence determinants of porcine reproductive and respiratory syndrome virus through construction of chimeric clones. Virology 380:371-378.
28. Lee, S. M., and S. B. Kleiboeker. 2005. Porcine arterivirus activates the NF-κB pathway through IκB degradation. Virology 342:47-59.
29. 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.
30. Loo, Y. M., J. Fornek, N. Crochet, G. Bajwa, O. Perwitasari, L. Martinez-Sobrido, S. Akira, M. A. Gill, A. Garcia-Sastre, M. G. Katze, and M. Gale, Jr. 2008. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol. 82:335-345.
31. Lopez, O. J., and F. A. Osorio. 2004. Role of neutralizing antibodies in PRRSV protective immunity. Vet. Immunol. Immunopathol. 102:155-163.
32. 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.
33. Lu, L. L., M. Puri, C. M. Horvath, and G. C. Sen. 2008. Select paramyxoviral V proteins inhibit IRF3 activation by acting as alternative substrates for inhibitor of κB kinase epsilon (IKKe)/TBK1. J. Biol. Chem. 283:14269-14276.
34. Mateu, E., and I. Diaz. 2008. The challenge of PRRS immunology. Vet. J. 177:345-351.
35. Meier, W. A., J. Galeota, F. A. Osorio, R. J. Husmann, W. M. Schnitzlein, and F. A. Zuckermann. 2003. Gradual development of the interferon-gamma response of swine to porcine reproductive and respiratory syndrome virus infection or vaccination. Virology 309:18-31.
36. 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.
37. Miller, L. C., K. M. Lager, and M. E. Kehrli, Jr. 2009. Role of Toll-like receptors in activation of porcine alveolar macrophages by porcine reproductive and respiratory syndrome virus. Clin. Vaccine Immunol. 16:360-365.
38. Neumann, E. J., J. B. Kliebenstein, C. D. Johnson, J. W. Mabry, E. J. Bush, A. H. Seitzinger, A. L. Green, and J. J. Zimmerman. 2005. Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States. J. Am. Vet. Med. Assoc. 227:385-392.
39. Ostrowski, M., J. A. Galeota, A. M. Jar, K. B. Platt, F. A. Osorio, and O. J. Lopez. 2002. Identification of neutralizing and nonneutralizing epitopes in the porcine reproductive and respiratory syndrome virus GP5 ectodomain. J. Virol. 76:4241-4250.
40. Overend, C., R. Mitchell, D. He, G. Rompato, M. J. Grubman, and A. E. Garmendia. 2007. Recombinant swine beta interferon protects swine alveolar macrophages and MARC-145 cells from infection with porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 88:925-931.
41. Posthuma, C. C., K. W. Pedersen, Z. Lu, R. G. Joosten, N. Roos, J. C. Zevenhoven-Dobbe, and E. J. Snijder. 2008. Formation of the arterivirus replication/transcription complex: a key role for nonstructural protein 3 in the remodeling of intracellular membranes. J. Virol. 82:4480-4491.
42. Richt, J. A., P. Lekcharoensuk, K. M. Lager, A. L. Vincent, C. M. Loiacono, B. H. Janke, W. H. Wu, K. J. Yoon, R. J. Webby, A. Solorzano, and A. Garcia-Sastre. 2006. Vaccination of pigs against swine influenza viruses by using an NS1-truncated modified live-virus vaccine. J. Virol. 80:11009-11018.
43. Ruggli, N., A. Summerfield, A. R. Fiebach, L. Guzylack-Piriou, O. Bauhofer, C. G. Lamm, S. Waltersperger, K. Matsuno, L. Liu, M. Gerber, K. H. Choi, M. A. Hofmann, Y. Sakoda, and J. D. Tratschin. 2009. Classical swine fever virus can remain virulent after specific elimination of the interferon regulatory factor 3-degrading function of Npro. J. Virol. 83:817-829.
44. Saira, K., Y. Zhou, and C. Jones. 2007. The infected cell protein 0 encoded by bovine herpesvirus 1 (bICP0) induces degradation of interferon response factor 3 and, consequently, inhibits beta interferon promoter activity. J. Virol. 81:3077-3086.
45. Sarkar, S. N., K. L. Peters, C. P. Elco, S. Sakamoto, S. Pal, and G. C. Sen. 2004. Novel roles of TLR3 tyrosine phosphorylation and PI3 kinase in double-stranded RNA signaling. Nat. Struct. Mol. Biol. 11:1060-1067.
46. Sarkar, S. N., and G. C. Sen. 2004. Novel functions of proteins encoded by viral stress-inducible genes. Pharmacol. Ther. 103:245-259.
47. Shaw, M. L., W. B. Cardenas, D. Zamarin, P. Palese, and C. F. Basler. 2005. Nuclear localization of the Nipah virus W protein allows for inhibition of both virus- and Toll-like receptor 3-triggered signaling pathways. J. Virol. 79:6078-6088.
48. Sizemore, N., N. Lerner, N. Dombrowski, H. Sakurai, and G. R. Stark. 2002. Distinct roles of the IκB kinase alpha and beta subunits in liberating nuclear factor κB (NF-κB) from IκB and in phosphorylating the p65 subunit of NF-κB. J. Biol. Chem. 277:3863-3869.
49. Snijder, E. J., and J. J. Meulenberg. 1998. The molecular biology of arteriviruses. J. Gen. Virol. 79(Pt. 5):961-979.
50. Steel, J., A. C. Lowen, L. Pena, M. Angel, A. Solorzano, R. Albrecht, D. R. Perez, A. Garcia-Sastre, and P. Palese. 2009. Live attenuated influenza viruses containing NS1 truncations as vaccine candidates against H5N1 highly pathogenic avian influenza. J. Virol. 83:1742-1753.
51. Stordeur, P., L. F. Poulin, L. Craciun, L. Zhou, L. Schandene, A. de Lavareille, S. Goriely, and M. Goldman. 2002. Cytokine mRNA quantification by real-time PCR. J. Immunol. Methods 259:55-64.
52. Sumpter, R., Jr., Y. M. Loo, E. Foy, K. Li, M. Yoneyama, T. Fujita, S. M. Lemon, and M. Gale, Jr. 2005. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J. Virol. 79:2689-2699.
53. Tenoever, B. R., S. L. Ng, M. A. Chua, S. M. McWhirter, A. Garcia-Sastre, and T. Maniatis. 2007. Multiple functions of the IKK-related kinase IKKε in interferon-mediated antiviral immunity. Science 315:1274-1278.
54. Tijms, M. A., D. D. Nedialkova, J. C. Zevenhoven-Dobbe, A. E. Gorbalenya, and E. J. Snijder. 2007. Arterivirus subgenomic mRNA synthesis and virion biogenesis depend on the multifunctional nsp1 autoprotease. J. Virol. 81: 10496-10505.
55. Tijms, M. A., L. C. van Dinten, A. E. Gorbalenya, and E. J. Snijder. 2001. A zinc finger-containing papain-like protease couples subgenomic mRNA synthesis to genome translation in a positive-stranded RNA virus. Proc. Natl. Acad. Sci. U. S. A. 98:1889-1894.
56. Truong, H. M., Z. Lu, G. F. Kutish, J. Galeota, F. A. Osorio, and A. K. Pattnaik. 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.
57. 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.
58. Weaver, B. K., K. P. Kumar, and N. C. Reich. 1998. Interferon regulatory factor 3 and CREB-binding protein/p300 are subunits of double-stranded RNA-activated transcription factor DRAF1. Mol. Cell. Biol. 18:1359-1368.
59. 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.