Identification of viral genes associated with the interferon-inducing phenotype of a synthetic porcine reproductive and respiratory syndrome virus strain

Virology

Volumn 499, Issue , 2016, Pages 313-321

  Sun, Haiyan ^a   Pattnaik, Asit K ^a   Osorio, Fernando A ^a   Vu, Hiep L X ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Innate immunity; PRRSV; Reverse genetics; Synthetic virus

Indexed keywords

ALPHA INTERFERON; MESSENGER RNA; NONSTRUCTURAL PROTEIN 1ALPHA; NONSTRUCTURAL PROTEIN 1BETA; NONSTRUCTURAL PROTEIN 2; UNCLASSIFIED DRUG; VIRAL PROTEIN; BETA INTERFERON; SYNTHETIC DNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE IDENTIFICATION; IN VITRO STUDY; INTERFERON INDUCTION; LUNG ALVEOLUS MACROPHAGE; NONHUMAN; PHENOTYPE; PIG; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENDAI VIRUS; VIRUS GENE; VIRUS GENOME; ANIMAL; CELL LINE; CHEMISTRY; GENETICS; METABOLISM; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; SYNTHESIS; VIROLOGY;

ANIMALS; CELL LINE; GENES, SYNTHETIC; GENOME, VIRAL; INTERFERON-BETA; PHENOTYPE; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SWINE; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84991434350     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2016.09.018     Document Type: Article

References (51)

1. Albina, E., Epidemiology of porcine reproductive and respiratory syndrome (PRRS): an overview. Vet. Microbiol. 55 (1997), 309–316.
2. Albina, E., Carrat, C., Charley, B., Interferon-alpha response to swine arterivirus (PoAV), the porcine reproductive and respiratory syndrome virus. J. Interferon Cytokine Res. 18 (1998), 485–490.
3. 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 1beta modulates host innate immune response by antagonizing IRF3 activation. J. Virol. 84 (2010), 1574–1584.
4. Beura, L.K., Subramaniam, S., Vu, H.L., Kwon, B., Pattnaik, A.K., Osorio, F.A., Identification of amino acid residues important for anti-IFN activity of porcine reproductive and respiratory syndrome virus non-structural protein 1. Virology 433 (2012), 431–439.
5. 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. 440 (1998), 461–467.
6. Calzada-Nova, G., Schnitzlein, W.M., Husmann, R.J., Zuckermann, F.A., North American porcine reproductive and respiratory syndrome viruses inhibit type I interferon production by plasmacytoid dendritic cells. J. Virol. 85 (2011), 2703–2713.
7. Cavanagh, D., Nidovirales: a new order comprising Coronaviridae and Arteriviridae. Arch. Virol. 142 (1997), 629–633.
8. Chen, Z., Li, M., He, Q., Du, J., Zhou, L., Ge, X., Guo, X., Yang, H., The amino acid at residue 155 in nonstructural protein 4 of porcine reproductive and respiratory syndrome virus contributes to its inhibitory effect for interferon-beta transcription in vitro. Virus Res. 189C (2014), 226–234.
9. Conzelmann, K.K., Visser, N., Van Woensel, P., Thiel, H.J., Molecular characterization of porcine reproductive and respiratory syndrome virus, a member of the arterivirus group. Virology 193 (1993), 329–339.
10. Das, S.C., Nayak, D., Zhou, Y., Pattnaik, A.K., Visualization of intracellular transport of vesicular stomatitis virus nucleocapsids in living cells. J. Virol. 80 (2006), 6368–6377.
11. Fang, Y., Snijder, E.J., The PRRSV replicase: exploring the multifunctionality of an intriguing set of nonstructural proteins. Virus Res. 154 (2010), 61–76.
12. Garcia-Nicolas, O., Quereda, J.J., Gomez-Laguna, J., Salguero, F.J., Carrasco, L., Ramis, G., Pallares, F.J., Cytokines transcript levels in lung and lymphoid organs during genotype 1 Porcine Reproductive and Respiratory Syndrome Virus (PRRSV) infection. Vet. Immunol. Immunopathol. 160 (2014), 26–40.
13. Gonzalez-Navajas, J.M., Lee, J., David, M., Raz, E., Immunomodulatory functions of type I interferons. Nat. Rev. Immunol. 12 (2012), 125–135.
14. Han, M.Y., Yoo, D.W., Modulation of innate immune signaling by nonstructural protein 1 (nsp1) in the family Arteriviridae. Virus Res. 194 (2014), 100–109.
15. Holtkamp DJ, K.J., Neumann, E.J., et al. Assessment of the economic impact of porcine reproductive and respiratory syndrome virus on United States pork producers. J. Swine Health Prod. 21 (2013), 72–84.
16. 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-kappaB essential modulator. J. Virol. 88 (2014), 10934–10945.
17. Ito, Y., Hosaka, Y., Component(s) of Sendai virus that can induce interferon in mouse spleen cells. Infect. Immun. 39 (1983), 1019–1023.
18. 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. 92 (2011), 1107–1116.
19. 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. 133 (1993), 477–483.
20. Kim, O., Sun, Y., Lai, F.W., Song, C., Yoo, D., 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 402 (2010), 315–326.
21. Kimman, T.G., Cornelissen, L.A., Moormann, R.J., Rebel, J.M., Stockhofe-Zurwieden, N., Challenges for porcine reproductive and respiratory syndrome virus (PRRSV) vaccinology. Vaccine 27 (2009), 3704–3718.
22. Li, H., Zheng, Z., Zhou, P., Zhang, B., Shi, Z., Hu, Q., Wang, H., The cysteine protease domain of porcine reproductive and respiratory syndrome virus non-structural protein 2 antagonizes interferon regulatory factor 3 activation. J. Gen. Virol. 91 (2010), 2947–2958.
23. Li, Y., Shyu, D.L., Shang, P., Bai, J., Ouyang, K., Dhakal, S., Hiremath, J., Binjawadagi, B., Renukaradhya, G.J., Fang, Y., Mutations in a highly conserved motif of nsp1beta protein attenuate the innate immune suppression function of porcine reproductive and respiratory syndrome virus. J. Virol. 90 (2016), 3584–3599.
24. Li, Y., Tas, A., Snijder, E.J., Fang, Y., Identification of porcine reproductive and respiratory syndrome virus ORF1a-encoded non-structural proteins in virus-infected cells. J. Gen. Virol. 93 (2012), 829–839.
25. Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25 (2001), 402–408.
26. Lopez, O.J., Osorio, F.A., Role of neutralizing antibodies in PRRSV protective immunity. Vet. Immunol. Immunopathol. 102 (2004), 155–163.
27. Mengeling, W.L., Lager, K.M., Vorwald, A.C., Alveolar macrophages as a diagnostic sample for detecting natural infection of pigs with porcine reproductive and respiratory syndrome virus. J. Vet. Diagn. Investig. 8 (1996), 238–240.
28. Miller, L.C., Laegreid, W.W., Bono, J.L., Chitko-McKown, C.G., Fox, J.M., Interferon type I response in porcine reproductive and respiratory syndrome virus-infected MARC-145 cells. Arch. Virol. 149 (2004), 2453–2463.
29. Murtaugh, M.P., Xiao, Z., Zuckermann, F., Immunological responses of swine to porcine reproductive and respiratory syndrome virus infection. Viral Immunol. 15 (2002), 533–547.
30. Music, N., Gagnon, C.A., The role of porcine reproductive and respiratory syndrome (PRRS) virus structural and non-structural proteins in virus pathogenesis. Anim. Health Res. Rev. 11 (2010), 135–163.
31. Nan, Y., Wang, R., Shen, M., Faaberg, K.S., Samal, S.K., Zhang, Y.J., Induction of type I interferons by a novel porcine reproductive and respiratory syndrome virus isolate. Virology 432 (2012), 261–270.
32. Patel, D., Nan, Y., Shen, M., Ritthipichai, K., Zhu, X., Zhang, Y.J., Porcine reproductive and respiratory syndrome virus inhibits type I interferon signaling by blocking STAT1/STAT2 nuclear translocation. J. Virol. 84 (2010), 11045–11055.
33. Rossow, K.D., Porcine reproductive and respiratory syndrome. Vet. Pathol. 35 (1998), 1–20.
34. Sagong, M., Lee, C., Porcine reproductive and respiratory syndrome virus nucleocapsid protein modulates interferon-beta production by inhibiting IRF3 activation in immortalized porcine alveolar macrophages. Arch. Virol. 156 (2011), 2187–2195.
35. Shi, M., Lam, T.T., Hon, C.C., Murtaugh, M.P., Davies, P.R., Hui, R.K., Li, J., Wong, L.T., Yip, C.W., Jiang, J.W., Leung, F.C., Phylogeny-based evolutionary, demographical, and geographical dissection of North American type 2 porcine reproductive and respiratory syndrome viruses. J. Virol. 84 (2010), 8700–8711.
36. Snijder, E.J., Wassenaar, A.L., Spaan, W.J., Proteolytic processing of the replicase ORFla protein of equine arteritis virus. J. Virol. 68 (1994), 5755–5764.
37. Song, C., Krell, P., Yoo, D., Nonstructural protein 1alpha subunit-based inhibition of NF-kappaB activation and suppression of interferon-beta production by porcine reproductive and respiratory syndrome virus. Virology 407 (2010), 268–280.
38. Strahle, L., Garcin, D., Kolakofsky, D., Sendai virus defective-interfering genomes and the activation of interferon-beta. Virology 351 (2006), 101–111.
39. Subramaniam, S., Beura, L.K., Kwon, B., Pattnaik, A.K., Osorio, F.A., Amino acid residues in the non-structural protein 1 of porcine reproductive and respiratory syndrome virus involved in down-regulation of TNF-alpha expression in vitro and attenuation in vivo. Virology 432 (2012), 241–249.
40. Subramaniam, S., Kwon, B., Beura, L.K., Kuszynski, C.A., Pattnaik, A.K., Osorio, F.A., Porcine reproductive and respiratory syndrome virus non-structural protein 1 suppresses tumor necrosis factor-alpha promoter activation by inhibiting NF-kappaB and Sp1. Virology 406 (2010), 270–279.
41. Sun, Y., Li, D., Giri, S., Prasanth, S.G., Yoo, D., Differential host cell gene expression and regulation of cell cycle progression by nonstructural protein 11 of porcine reproductive and respiratory syndrome virus. Biomed. Res. Int., 2014, 2014, 430508.
42. Sun, Z., Chen, Z., Lawson, S.R., Fang, Y., The cysteine protease domain of porcine reproductive and respiratory syndrome virus nonstructural protein 2 possesses deubiquitinating and interferon antagonism functions. J. Virol. 84 (2010), 7832–7846.
43. Tian, K., Yu, X., Zhao, T., Feng, Y., Cao, Z., Wang, C., Hu, Y., Chen, X., Hu, D., Tian, X., Liu, D., Zhang, S., Deng, X., Ding, Y., Yang, L., Zhang, Y., Xiao, H., Qiao, M., Wang, B., Hou, L., Wang, X., Yang, X., Kang, L., Sun, M., Jin, P., Wang, S., Kitamura, Y., Yan, J., Gao, G.F., Emergence of fatal PRRSV variants: unparalleled outbreaks of atypical PRRS in China and molecular dissection of the unique hallmark. PLoS One, 2, 2007, e526.
44. Truong, H.M., Lu, Z., Kutish, G.F., Galeota, J., Osorio, F.A., Pattnaik, A.K., 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 (2004), 308–319.
45. van Dinten, L.C., Wassenaar, A.L., Gorbalenya, A.E., Spaan, W.J., J., S.E, Processing of the equine arteritis virus replicase ORF1b protein- identification of cleavage products containing the putative viral polymerase and helicase domains. J. Virol. 70 (1996), 6625–6633.
46. Vu, H.L., Kwon, B., de Lima, M., Pattnaik, A.K., Osorio, F.A., Characterization of a serologic marker candidate for development of a live-attenuated DIVA vaccine against porcine reproductive and respiratory syndrome virus. Vaccine 31 (2013), 4330–4337.
47. 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. 85 (2011), 5555–5564.
48. Vu, H.L., Ma, F., Laegreid, W.W., Pattnaik, A.K., Steffen, D., Doster, A.R., Osorio, F.A., A synthetic porcine reproductive and respiratory syndrome virus strain confers unprecedented levels of heterologous protection. J. Virol. 89 (2015), 12070–12083.
49. Wang, R., Nan, Y., Yu, Y., Yang, Z., Zhang, Y.J., Variable interference with interferon signal transduction by different strains of porcine reproductive and respiratory syndrome virus. Vet. Microbiol. 166 (2013), 493–503.
50. Wang, R., Xiao, Y., Opriessnig, T., Ding, Y., Yu, Y., Nan, Y., Ma, Z., Halbur, P.G., Zhang, Y.J., Enhancing neutralizing antibody production by an interferon-inducing porcine reproductive and respiratory syndrome virus strain. Vaccine 31 (2013), 5537–5543.
51. Wang, R., Zhang, Y.J., Antagonizing interferon-mediated immune response by porcine reproductive and respiratory syndrome virus. Biomed. Res. Int., 2014, 2014, 315470.