The vOTU domain of highly-pathogenic porcine reproductive and respiratory syndrome virus displays a differential substrate preference

Virology

Volumn 454-455, Issue 1, 2014, Pages 247-253

  Deaton, Michelle K ^a   Spear, Allyn ^b   Faaberg, Kay S ^b   Pegan, Scott D ^c  

^a UNIVERSITY OF DENVER   (United States)

^b NATIONAL ANIMAL DISEASE CENTER   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

ISG15; Nsp2; PLP2; PRRSV; Ubiquitin; VOTU

Indexed keywords

NONSTRUCTURAL PROTEIN 2; TUMOR PROTEIN; UBIQUITIN;

ARTERIVIRUS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SUBSTRATE; IMMUNE RESPONSE; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; ISG15 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; REGULATORY MECHANISM; UBIQUITINATION; VIRUS GENE; VIRUS STRAIN; VIRUS VIRULENCE;

ISG15; NSP2; PLP2; PRRSV; UBIQUITIN; VOTU;

ANIMALS; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUBSTRATE SPECIFICITY; SWINE; UBIQUITIN-SPECIFIC PROTEASES; VIRAL NONSTRUCTURAL PROTEINS; VIRULENCE FACTORS;

EID: 84896028719     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.02.026     Document Type: Article

References (54)

1. Akutsu M., Ye Y., Virdee S., Chin J.W., Komander D. Molecular basis for ubiquitin and ISG15 cross-reactivity in viral ovarian tumor domains. Proc. Natl. Acad. Sci. USA 2011, 108:2228-2233.
2. Alkalay I., Yaron A., Hatzubai A., Orian A., Ciechanover A., Ben-Neriah Y. Stimulation-dependent I kappa B alpha phosphorylation marks the NF-kappa B inhibitor for degradation via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA 1995, 92:10599-10603.
3. An T.Q., Tian Z.J., Zhou Y.J., Xiao Y., Peng J.M., Chen J., Jiang Y.F., Hao X.F., Tong G.Z. Comparative genomic analysis of five pairs of virulent parental/attenuated vaccine strains of PRRSV. Vet. Microbiol. 2011, 149:104-112.
4. 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.
5. Brockmeier S.L., Loving C.L., Vorwald A.C., Kehrli M.E., Baker R.B., Nicholson T.L., Lager K.M., Miller L.C., Faaberg K.S. Genomic sequence and virulence comparison of four Type 2 porcine reproductive and respiratory syndrome virus strains. Virus Res. 2012, 169:212-221.
6. Capodagli G.C., Deaton M.K., Baker E.A., Lumpkin R.J., Pegan S.D. Diversity of ubiquitin and ISG15 Specificity among nairoviruses[U+05F3] viral ovarian tumor domain proteases. J. Virol. 2013, 87:3815-3827.
7. Capodagli G.C., McKercher M.A., Baker E.A., Masters E.M., Brunzelle J.S., Pegan S.D. Structural analysis of a viral ovarian tumor domain protease from the Crimean-Congo hemorrhagic fever virus in complex with covalently bonded ubiquitin. J. Virol. 2011, 85:3621-3630.
8. Charerntantanakul W., Platt R., Roth J.A. Effects of porcine reproductive and respiratory syndrome virus-infected antigen-presenting cells on T cell activation and antiviral cytokine production. Viral Immunol. 2006, 19:646-661.
9. Chen Z., Hagler J., Palombella V.J., Melandri F., Scherer D., Ballard D., Maniatis T. Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev. 1995, 9:1586-1597.
10. den Boon J.A., Faaberg K.S., Meulenberg J.J., Wassenaar A.L., Plagemann P.G., Gorbalenya A.E., Snijder E.J. Processing and evolution of the N-terminal region of the arterivirus replicase ORF1a protein: identification of two papainlike cysteine proteases. J. Virol. 1995, 69:4500-4505.
11. Ellingson J.S., Wang Y., Layton S., Ciacci-Zanella J., Roof M.B., Faaberg K.S. Vaccine efficacy of porcine reproductive and respiratory syndrome virus chimeras. Vaccine 2010, 28:2679-2686.
12. 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:E2920-2928.
13. Frias-Staheli N., Giannakopoulos N.V., Kikkert M., Taylor S.L., Bridgen A., Paragas J., Richt J.A., Rowland R.R., Schmaljohn C.S., Lenschow D.J., Snijder E.J., Garcia-Sastre A., Virgin H.W.t. Ovarian tumor domain-containing viral proteases evade ubiquitin- and ISG15-dependent innate immune responses. Cell Host Microbe 2007, 2:404-416.
14. Guo B., Lager K.M., Henningson J.N., Miller L.C., Schlink S.N., Kappes M.A., Kehrli M.E., Brockmeier S.L., Nicholson T.L., Yang H.C., Faaberg K.S. Experimental infection of United States swine with a Chinese highly pathogenic strain of porcine reproductive and respiratory syndrome virus. Virology 2013, 435:372-384.
15. Guo B., Lager K.M., Schlink S.N., Kehrli M.E., Brockmeier S.L., Miller L.C., Swenson S.L., Faaberg K.S. Chinese and Vietnamese strains of HP-PRRSV cause different pathogenic outcomes in United States high health swine. Virology 2013, 446:238-250.
16. Han J., Rutherford M.S., Faaberg K.S. The porcine reproductive and respiratory syndrome virus nsp2 cysteine protease domain possesses both trans- and cis-cleavage activities. J. Virol. 2009, 83:9449-9463.
17. Han J., Wang Y., Faaberg K.S. Complete genome analysis of RFLP 184 isolates of porcine reproductive and respiratory syndrome virus. Virus Res. 2006, 122:175-182.
18. Han M., Du Y., Song C., Yoo D. 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 nsp1alpha subunit. Virus Res. 2013, 172:54-65.
19. Han W., Wu J.J., Deng X.Y., Cao Z., Yu X.L., Wang C.B., Zhao T.Z., Chen N.H., Hu H.H., Bin W., Hou L.L., Wang L.L., Tian K.G., Zhang Z.Q. Molecular mutations associated with the in vitro passage of virulent porcine reproductive and respiratory syndrome virus. Virus Genes 2009, 38:276-284.
20. Huang J., Zhao S., Zhu M., Wu Z., Yu M. Sequence and expression analyses of porcine ISG15 and ISG43 genes. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 2009, 153:301-309.
21. Jiang X., Kinch L.N., Brautigam C.A., Chen X., Du F., Grishin N.V., Chen Z.J. Ubiquitin-induced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response. Immunity 2012, 36:959-973.
22. 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.
23. Komander D., Clague M.J., Urbe S. Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 2009, 10:550-563.
24. Kulathu Y., Komander D. Atypical ubiquitylation - the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat. Rev. Mol. Cell Biol. 2012, 13:508-523.
25. Kwon B., Ansari I.H., Pattnaik A.K., Osorio F.A. Identification of virulence determinants of porcine reproductive and respiratory syndrome virus through construction of chimeric clones. Virology 2008, 380:371-378.
26. 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. 2010, 91:2947-2958.
27. Li Y., Wang X., Bo K., Tang B., Yang B., Jiang W., Jiang P. Emergence of a highly pathogenic porcine reproductive and respiratory syndrome virus in the Mid-Eastern region of China. Vet. J. 2007, 174:577-584.
28. Mielech, A.M., Chen, Y., Mesecar, A.D., Baker, S.C., Nidovirus papain-like proteases: Multifunctional enzymes with protease, deubiquitinating and deISGylating activities. Virus Res., in press.
29. Ni Y.Y., Opriessnig T., Zhou L., Cao D., Huang Y.W., Halbur P.G., Meng X.J. Attenuation of porcine reproductive and respiratory syndrome virus by molecular breeding of virus envelope genes from genetically divergent strains. J. Virol. 2013, 87:304-313.
30. Nielsen H.S., Oleksiewicz M.B., Forsberg R., Stadejek T., Botner A., Storgaard T. Reversion of a live porcine reproductive and respiratory syndrome virus vaccine investigated by parallel mutations. J. Gen. Virol. 2001, 82:1263-1272.
31. Oshiumi H., Miyashita M., Matsumoto M., Seya T. A distinct role of riplet-mediated K63-linked polyubiquitination of the RIG-I repressor domain in human antiviral innate immune responses. PLoS Pathog. 2013, 9:e1003533.
32. Sang, Y., Rowland, R.R., Blecha, F., 2011. Porcine type I interferons: polymorphic sequences and activity against PRRSV. BMC proceedings 5 Suppl 4, S8.
33. Shi M., Lam T.T., Hon C.C., Hui R.K., Faaberg K.S., Wennblom T., Murtaugh M.P., Stadejek T., Leung F.C. Molecular epidemiology of PRRSV: a phylogenetic perspective. Virus Res. 2010, 154:7-17.
34. Shi Y., Hu Z., Xiong Z., Zhou Y., Jin X., Gu C., Hu X., Cheng G., Song N., Zhang W. Analysis of molecular variation of porcine reproductive and respiratory syndrome virus in Central China from 2006 to 2012. Arch. Virol. 2013, 158:717-721.
35. Snijder E.J., Wassenaar A.L., Spaan W.J., Gorbalenya A.E. The arterivirus Nsp2 protease. An unusual cysteine protease with primary structure similarities to both papain-like and chymotrypsin-like proteases. J. Biol. Chem. 1995, 270:16671-16676.
36. 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.
37. Storgaard T., Oleksiewicz M., Botner A. Examination of the selective pressures on a live PRRS vaccine virus. Arch. Virol. 1999, 144:2389-2401.
38. Sun Y., Han M., 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.
39. 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. 2010, 84:7832-7846.
40. Sun Z., Li Y., Ransburgh R., Snijder E.J., Fang Y. Nonstructural protein 2 of porcine reproductive and respiratory syndrome virus inhibits the antiviral function of interferon-stimulated gene 15. J. Virol. 2012, 86:3839-3850.
41. Tokunaga F., Sakata S., Saeki Y., Satomi Y., Kirisako T., Kamei K., Nakagawa T., Kato M., Murata S., Yamaoka S., Yamamoto M., Akira S., Takao T., Tanaka K., Iwai K. Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat. Cell Biol. 2009, 11:123-132.
42. van Hemert M.J., Snijder E.J. The Arterivirus Replicase 2008, 83-101. The Nidoviruses. ASM Press, Washington, DC. T. Stanley Perlman (Ed.).
43. van Kasteren P.B., Bailey-Elkin B.A., James T.W., Ninaber D.K., Beugeling C., Khajehpour M., Snijder E.J., Mark B.L., Kikkert M. Deubiquitinase function of arterivirus papain-like protease 2 suppresses the innate immune response in infected host cells. Proc. Natl. Acad. Sci. USA 2013, 110:E838-847.
44. van Kasteren P.B., Beugeling C., Ninaber D.K., Frias-Staheli N., van Boheemen S., Garcia-Sastre A., Snijder E.J., Kikkert M. Arterivirus and nairovirus ovarian tumor domain-containing Deubiquitinases target activated RIG-I to control innate immune signaling. J. Virol. 2012, 86:773-785.
45. Wang Y., Liang Y., Han J., Burkhart K.M., Vaughn E.M., Roof M.B., Faaberg K.S. Attenuation of porcine reproductive and respiratory syndrome virus strain MN184 using chimeric construction with vaccine sequence. Virology 2008, 371:418-429.
46. Wills R.W., Zimmerman J.J., Yoon K.J., Swenson S.L., Hoffman L.J., McGinley M.J., Hill H.T., Platt K.B. Porcine reproductive and respiratory syndrome virus: routes of excretion. Vet. Microbiol. 1997, 57:69-81.
47. Wu J., Li J., Tian F., Ren S., Yu M., Chen J., Lan Z., Zhang X., Yoo D., Wang J. Genetic variation and pathogenicity of highly virulent porcine reproductive and respiratory syndrome virus emerging in China. Arch. Virol. 2009, 154:1589-1597.
48. 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.
49. Yu X., Chen N., Wang L., Wu J., Zhou Z., Ni J., Li X., Zhai X., Shi J., Tian K. New genomic characteristics of highly pathogenic porcine reproductive and respiratory syndrome viruses do not lead to significant changes in pathogenicity. Vet. Microbiol. 2012, 158:291-299.
50. Yuan S., Mickelson D., Murtaugh M.P., Faaberg K.S. Complete genome comparison of porcine reproductive and respiratory syndrome virus parental and attenuated strains. Virus Res. 2001, 74:99-110.
51. Zeng W., Sun L., Jiang X., Chen X., Hou F., Adhikari A., Xu M., Chen Z.J. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 2010, 141:315-330.
52. Zhao C., Collins M.N., Hsiang T.Y., Krug R.M. Interferon-induced ISG15 pathway: an ongoing virus-host battle. Trends Microbiol. 2013, 21:181-186.
53. Zhou L., Chen S., Zhang J., Zeng J., Guo X., Ge X., Zhang D., Yang H. Molecular variation analysis of porcine reproductive and respiratory syndrome virus in China. Virus Res. 2009, 145:97-105.
54. Ziebuhr J., Snijder E.J., Gorbalenya A.E. Virus-encoded proteinases and proteolytic processing in the Nidovirales. J. Gen. Virol. 2000, 81:853-879.