Biogenesis of non-structural protein 1 (nsp1) and nsp1-mediated type I interferon modulation in arteriviruses

Virology

Volumn 458-459, Issue 1, 2014, Pages 136-150

  Han, Mingyuan ^a   Kim, Chi Yong ^a   Rowland, Raymond R R ^b   Fang, Ying ^b   Kim, Daewoo ^a   Yoo, Dongwan ^a  

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

^b KANSAS STATE UNIVERSITY   (United States)

Author keywords

Arteriviridae; CBP degradation; EAV; IFN antagonism; LDV; Nsp1; PRRSV; SHFV

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 3; NONSTRUCTURAL PROTEIN 1; PAPAIN;

ALPHA CHAIN; ARTERIVIRUS; ARTICLE; BETA CHAIN; BIOGENESIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE RESPONSE; EQUINE VIRAL ARTERITIS VIRUS; GAMMA SUBUNIT; IMMUNE EVASION; IMMUNOMODULATION; LACTIC DEHYDROGENASE TOGAVIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SENSITIVITY ANALYSIS; SEQUENCE ANALYSIS; VIRUS INACTIVATION;

ARTERIVIRIDAE; CBP DEGRADATION; EAV; IFN ANTAGONISM; LDV; NSP1; PRRSV; SHFV;

ANIMALS; ARTERIVIRIDAE; CELL LINE; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, VIRAL; HUMANS; INTERFERON TYPE I; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84900001822     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.04.028     Document Type: Article

References (52)

1. Albina E., Carrat C., Charley B. Interferon-alpha response to swine arterivirus (PoAV), the porcine reproductive and respiratory syndrome virus. J. Interferon Cytokin. Res. 1998, 18:485-490.
2. 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.
3. Anderson G.W., Rowland R.R.R., Palmer G.A., Even C., Plagemann P.G.W. Lactate dehydrogenase-elevating virus-replication persists in liver, spleen, lymph-node, and testis tissues and results in accumulation of viral-RNA in germinal-centers, concomitant with polyclonal activation of B-cells. J. Virol. 1995, 69:5177-5185.
4. Baccala R., Hoebe K., Kono D.H., Beutler B., Theofilopoulos A.N. TLR-dependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity. Nat. Med. 2007, 13:543-551.
5. 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. 2010, 84:1574-1584.
6. 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 2012, 433:431-439.
7. Chelbi-Alix M.K., Pelicano L., Quignon F., Koken M.H., Venturini L., Stadler M., Pavlovic J., Degos L., de The H. Induction of the PML protein by interferons in normal and APL cells. Leukemia 1995, 9:2027-2033.
8. Chen Z., Lawson S., Sun Z., Zhou X., Guan X., Christopher-Hennings J., Nelson E.A., Fang Y. 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 2010, 398:87-97.
9. Dalton K.P., Rose J.K. Vesicular stomatitis virus glycoprotein containing the entire green fluorescent protein on its cytoplasmic domain is incorporated efficiently into virus particles. Virology 2001, 279:414-421.
10. den Boon J.A., Snijder E.J., Chirnside E.D., Devries A.A.F., Horzinek M.C., Spaan W.J.M. Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily. J. Virol. 1991, 65:2910-2920.
11. Dyck J.A., Maul G.G., Miller W.H., Chen J.D., Kakizuka A., Evans R.M. A novel macromolecular structure is a target of the promyelocyte-retinoic acid receptor oncoprotein. Cell 1994, 76:333-343.
12. Ehrhardt C., Kardinal C., Wurzer W.J., Wolff T., von Eichel-Streiber C., Pleschka S., Planz O., Ludwig S. Rac1 and PAK1 are upstream of IKK-epsilon and TBK-1 in the viral activation of interferon regulatory factor-3. FEBS Lett. 2004, 567:230-238.
13. Fang Y., Snijder E.J. The PRRSV replicase: exploring the multifunctionality of an intriguing set of nonstructural proteins. Virus Res. 2010, 154:61-76.
14. Fang Y., Treffers E.E., Li Y., Tas A., Sun Z., van der Meer Y., de Ru A.H., van Veelen P.A., Atkins J.F., Snijder E.J., Firth A.E. Efficient-2 frameshifting by mammalian ribosomes to synthesize an additional arterivirus protein. Proc. Natl. Acad. Sci. USA 2012, 109:E2920-E2928.
15. Firth A.E., Zevenhoven-Dobbe J.C., Wills N.M., Go Y.Y., Balasuriya U.B.R., Atkins J.F., Snijder E.J., Posthuma C.C. Discovery of a small arterivirus gene that overlaps the GP5 coding sequence and is important for virus production. J. Gen. Virol. 2011, 92:1097-1106.
16. Godeny E.K., de Vries A.A., Wang X.C., Smith S.L., de Groot R.J. Identification of the leader-body junctions for the viral subgenomic mRNAs and organization of the simian hemorrhagic fever virus genome: evidence for gene duplication during arterivirus evolution. J. Virol. 1998, 72:862-867.
17. Han M.Y., Du Y.J., Song C., Yoo D.W. Degradation of CREB-binding protein and modulation of type I interferon induction by the zinc finger motif of the porcine reproductive and respiratory syndrome virus nsp1 alpha subunit. Virus Res. 2013, 172:54-65.
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. 2011, 92:1107-1116.
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. 1993, 133:477-483.
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 2010, 402:315-326.
21. Kroese M.V., Zevenhoven-Dobbe J.C., Bos-de Ruijter J.N., Peeters B.P., Meulenberg J.J., Cornelissen L.A., Snijder E.J. The nsp1alpha and nsp1 papain-like autoproteinases are essential for porcine reproductive and respiratory syndrome virus RNA synthesis. J. Gen. Virol. 2008, 89:494-499.
22. Lauck M., Hyeroba D., Tumukunde A., Weny G., Lank S.M., Chapman C.A., O'Connor D.H., Friedrich T.C., Goldberg T.L. Novel, divergent simian hemorrhagic fever viruses in a wild Ugandan red colobus monkey discovered using direct pyrosequencing. PloS One 2011, 6:e19056.
23. Lauck M., Sibley S.D., Hyeroba D., Tumukunde A., Weny G., Chapman C.A., Ting N., Switzer W.M., Kuhn J.H., Friedrich T.C., O'Connor D.H., Goldberg T.L. Exceptional simian hemorrhagic fever virus diversity in a wild African primate community. J. Virol. 2013, 87:688-691.
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. 2012, 93:829-839.
25. Li Y., Zhu L., Lawson S.R., Fang Y. Targeted mutations in a highly conserved motif of the nsp1beta protein impair the interferon antagonizing activity of porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 2013, 94:1972-1983.
26. Meulenberg J.J.M., Hulst M.M., Demeijer E.J., Moonen P.L.J.M., Denbesten A., Dekluyver E.P., Wensvoort G., Moormann R.J.M. Lelystad virus, the causative agent of porcine epidemic abortion and respiratory syndrome (Pears), is related to LDV and EAV. Virology 1993, 192:62-72.
27. Nedialkova D.D., Gorbalenya A.E., Snijder E.J. Arterivirus nsp1 modulates the accumulation of minus-strand templates to control the relative abundance of viral mRNAs. Plos Pathog. 2010, 6.
28. 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.
29. Patel D., Nan Y.C., Shen M.Y., Ritthipichai K., Zhu X.P., Zhang Y.J. Porcine reproductive and respiratory syndrome virus inhibits type I interferon signaling by blocking STAT1/STAT2 nuclear translocation. J. Virol. 2010, 84:11045-11055.
30. Plagemann P.G.W., Rowland R.R.R., Even C., Faaberg K.S. Lactate dehydrogenase-elevating virus - an ideal persistent virus. Springer Semin. Immunol. 1995, 17:167-186.
31. Ren J., Liu T., Pang L., Li K., Garofalo R.P., Casola A., Bao X. A novel mechanism for the inhibition of interferon regulatory factor-3-dependent gene expression by human respiratory syncytial virus NS1 protein. J. Gen. Virol. 2011, 92:2153-2159.
32. Sadler A.J., Williams B.R.G. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 2008, 8:559-568.
33. Samuel C.E. Antiviral actions of interferons. Clin. Microbiol. Rev. 2001, 14:778-809.
34. Sen N., Sommer M., Che X., White K., Ruyechan W.T., Arvin A.M. Varicella-zoster virus immediate-early protein 62 blocks interferon regulatory factor 3 (IRF3) phosphorylation at key serine residues: a novel mechanism of IRF3 inhibition among herpesviruses. J. Virol. 2010, 84:9240-9253.
35. Snijder E.J., Kikkert M., Fang Y. Arterivirus molecular biology and pathogenesis. J. Gen. Virol. 2013, 94:2141-2163.
36. Snijder E.J., Meulenberg J.J.M. The molecular biology of arteriviruses. J. Gen. Virol. 1998, 79:961-979.
37. Snijder E.J., van Tol H., Pedersen K.W., Raamsman M.J.B., de Vries A.A.F. Identification of a novel structural protein of arteriviruses. J. Virol. 1999, 73:6335-6345.
38. Snijder E.J., Wassenaar A.L., Spaan W.J. The 5' end of the equine arteritis virus replicase gene encodes a papainlike cysteine protease. J. Virol. 1992, 66:7040-7048.
39. 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 2010, 407:268-280.
40. Sun Y., Han M.Y., Kim C., Calvert J.G., Yoo D. Interplay between interferon-mediated innate immunity and porcine reproductive and respiratory syndrome virus. Viruses 2012, 4:424-446.
41. Sun Y.N., Xue F., Guo Y., Ma M., Hao N., Zhang X.J.C., Lou Z.Y., Li X.M., Rao Z.H. Crystal structure of porcine reproductive and respiratory syndrome virus leader protease nsp1 alpha. J. Virol. 2009, 83:10931-10940.
42. Tijms M.A., van der Meer Y., Snijder E.J. Nuclear localization of non-structural protein 1 and nucleocapsid protein of equine arteritis virus. J. Gen. Virol. 2002, 83:795-800.
43. Tijms M.A., van Dinten L.C., Gorbalenya A.E., Snijder E.J. A zinc finger-containing papain-like protease couples subgenomic mRNA synthesis to genome translation in a positive-stranded RNA virus. Proc. Natl. Acad. Sci. USA 2001, 98:1889-1894.
44. Van Hemert M.J., Snijder E.J. Nidoviruses, the Arterivirus Replicase 2007, 83-101. (Chapter 6).
45. Wang R., Nan Y.C., Yu Y., Zhang Y.J. Porcine reproductive and respiratory syndrome virus nsp1 beta inhibits interferon-activated JAK/STAT signal transduction by inducing karyopherin-alpha 1 degradation. J. Virol. 2013, 87:5219-5228.
46. Wootton S., Yoo D., Rogan D. Full-length sequence of a Canadian porcine reproductive and respiratory syndrome virus (PRRSV) isolate. Arch. Virol. 2000, 145:2297-2323.
47. Xiao J.H., Davidson I., Matthes H., Garnier J.M., Chambon P. Cloning, expression, and transcriptional properties of the human enhancer factor TEF-1. Cell 1991, 65:551-568.
48. Xue F., Sun Y.N., Yan L.M., Zhao C., Chen J., Bartlam M., Li X.M., Lou Z.Y., Rao Z.H. The crystal structure of porcine reproductive and respiratory syndrome virus nonstructural protein nsp1-beta reveals a novel metal-dependent nuclease. J. Virol. 2010, 84:6461-6471.
49. Yoo D., Song C., Sun Y., Du Y., Kim O., Liu H.C. Modulation of host cell responses and evasion strategies for porcine reproductive and respiratory syndrome virus. Virus Res. 2010, 154:48-60.
50. Zhou H.X., Perlman S. Mouse hepatitis virus does not induce beta interferon synthesis and does not inhibit its induction by double-stranded RNA. J. Virol. 2007, 81:568-574.
51. Zhu H., Zheng C., Xing J., Wang S., Li S., Lin R., Mossman K.L. Varicella-zoster virus immediate-early protein ORF61 abrogates the IRF3-mediated innate immune response through degradation of activated IRF3. J. Virol. 2011, 85:11079-11089.
52. Ziebuhr J., Snijder E.J., Gorbalenya A.E. Virus-encoded proteinases and proteolytic processing in the Nidovirales. J. Gen. Virol. 2000, 81:853-879.