Zinc Binding in Pestivirus Npro Is Required for Interferon Regulatory Factor 3 Interaction and Degradation

Journal of Molecular Biology

Volumn 391, Issue 2, 2009, Pages 438-449

  Szymanski, Michal R ^a   Fiebach, Ana R ^b   Tratschin, Jon Duri ^b   Gut, Marco ^b   Ramanujam, V M Sadagopa ^a   Gottipati, Keerthi ^a   Patel, Purvi ^a   Ye, Mengyi ^a   Ruggli, Nicolas ^b   Choi, Kyung H ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b INSTITUTE OF VIROLOGY AND IMMUNOLOGY   (Switzerland)

Author keywords

interferon regulatory factor 3; N terminal protease Npro; pestivirus; proteasomal degradation; zinc binding protein

Indexed keywords

CYSTEINE; INTERFERON REGULATORY FACTOR 3; PROTEINASE; ZINC;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; METAL BINDING; MICROBIAL ACTIVITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PESTIVIRUS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; VIRUS CELL INTERACTION; VIRUS INFECTION;

BOVINE VIRAL DIARRHEA VIRUS 1; CLASSICAL SWINE FEVER VIRUS; PESTIVIRUS;

EID: 67650692248     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.06.040     Document Type: Article

References (53)

1. Randall R.E., and Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 89 (2008) 1-47
2. Weber F., Kochs G., and Haller O. Inverse interference: how viruses fight the interferon system. Viral Immunol. 17 (2004) 498-515
3. Kawai T., and Akira S. Innate immune recognition of viral infection. Nat. Immunol. 7 (2006) 131-137
4. Saitoh T., Tun-Kyi A., Ryo A., Yamamoto M., Finn G., Fujita T., et al. Negative regulation of interferon-regulatory factor 3-dependent innate antiviral response by the prolyl isomerase Pin1. Nat. Immunol. 7 (2006) 598-605
5. Haller O., Kochs G., and Weber F. The interferon response circuit: induction and suppression by pathogenic viruses. Virology 344 (2006) 119-130
6. Haller O., and Weber F. Pathogenic viruses: smart manipulators of the interferon system. Curr. Top. Microbiol. Immunol. 316 (2007) 315-334
7. Graff J.W., Ewen J., Ettayebi K., and Hardy M.E. Zinc-binding domain of rotavirus NSP1 is required for proteasome-dependent degradation of IRF3 and autoregulatory NSP1 stability. J. Gen. Virol. 88 (2007) 613-620
8. pro from a cytopathic bovine viral diarrhea virus. Virology 366 (2007) 277-292
9. pro interacts with interferon regulatory factor 3 and induces its proteasomal degradation. J. Virol. 81 (2007) 3087-3096
10. Hilton L., Moganeradj K., Zhang G., Chen Y.H., Randall R.E., McCauley J.W., and Goodbourn S. The NPro product of bovine viral diarrhea virus inhibits DNA binding by interferon regulatory factor 3 and targets it for proteasomal degradation. J. Virol. 80 (2006) 11723-11732
11. pro product of classical swine fever virus and bovine viral diarrhea virus uses a conserved mechanism to target interferon regulatory factor-3. J. Gen. Virol. 88 (2007) 3002-3006
12. Meyers G., and Thiel H.J. Molecular characterization of pestiviruses. Adv. Virus Res. 47 (1996) 53-118
13. Lindenbach B.D., Thiel H.J., and Rice C.M. Flaviviridae: the viruses and their replication. In: Knipe D.M., and Howley P.M. (Eds). Fields Virology vol. 1 (2007), Lippincott-Raven Publishers, Philadelphia, PA 1101-1152
14. Stark R., Meyers G., Rumenapf T., and Thiel H.J. Processing of pestivirus polyprotein: cleavage site between autoprotease and nucleocapsid protein of classical swine fever virus. J. Virol. 67 (1993) 7088-7095
15. Wiskerchen M., Belzer S.K., and Collett M.S. Pestivirus gene expression: the first protein product of the bovine viral diarrhea virus large open reading frame, p20, possesses proteolytic activity. J. Virol. 65 (1991) 4508-4514
16. Rumenapf T., Stark R., Heimann M., and Thiel H.J. N-terminal protease of pestiviruses: identification of putative catalytic residues by site-directed mutagenesis. J. Virol. 72 (1998) 2544-2547
17. Rawlings N.D., Morton F.R., and Barrett A.J. MEROPS: the peptidase database. Nucleic Acids Res. 34 (2006) D270-272
18. Lai V.C., Zhong W., Skelton A., Ingravallo P., Vassilev V., Donis R.O., et al. Generation and characterization of a hepatitis C virus NS3 protease-dependent bovine viral diarrhea virus. J. Virol. 74 (2000) 6339-6347
19. pro is not required for viral replication in cell culture. J. Virol. 72 (1998) 7681-7684
20. Ruggli N., Tratschin J.D., Schweizer M., McCullough K.C., Hofmann M.A., and Summerfield A. Classical swine fever virus interferes with cellular antiviral defense: evidence for a novel function of N(pro). J. Virol. 77 (2003) 7645-7654
21. pro protein is necessary for alpha/beta interferon antagonism. J. Virol. 80 (2006) 900-911
22. Ruggli N., Bird B.H., Liu L., Bauhofer O., Tratschin J.D., and Hofmann M.A. N(pro) of classical swine fever virus is an antagonist of double-stranded RNA-mediated apoptosis and IFN-alpha/beta induction. Virology 340 (2005) 265-276
23. Schweizer M., and Peterhans E. Noncytopathic bovine viral diarrhea virus inhibits double-stranded RNA-induced apoptosis and interferon synthesis. J. Virol. 75 (2001) 4692-4698
24. pro. J. Virol. 83 (2009) 817-829
25. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215 (1990) 403-410
26. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
27. Tellinghuisen T.L., Marcotrigiano J., Gorbalenya A.E., and Rice C.M. The NS5A protein of hepatitis C virus is a zinc metalloprotein. J. Biol. Chem. 279 (2004) 48576-48587
28. Tellinghuisen T.L., Marcotrigiano J., and Rice C.M. Structure of the zinc-binding domain of an essential component of the hepatitis C virus replicase. Nature 435 (2005) 374-379
29. Ettema T.J., Huynen M.A., de Vos W.M., and van der Oost J. TRASH: a novel metal-binding domain predicted to be involved in heavy-metal sensing, trafficking and resistance. Trends Biochem. Sci. 28 (2003) 170-173
30. Cuff J.A., Clamp M.E., Siddiqui A.S., Finlay M., and Barton G.J. JPred: a consensus secondary structure prediction server. Bioinformatics 14 (1998) 892-893
31. Prilusky J., Felder C.E., Zeev-Ben-Mordehai T., Rydberg E.H., Man O., Beckmann J.S., et al. FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics 21 (2005) 3435-3438
32. Linding R., Jensen L.J., Diella F., Bork P., Gibson T.J., and Russell R.B. Protein disorder prediction: implications for structural proteomics. Structure 11 (2003) 1453-1459
33. Kalab M. Factors affecting the Ellman determination of sulfhydryl groups in skimmilk powder and gels. J. Dairy Sci. 53 (1969) 711-718
34. Alberts I.L., Nadassy K., and Wodak S.J. Analysis of zinc binding sites in protein crystal structures. Protein Sci. 7 (1998) 1700-1716
35. Maret W. Zinc and sulfur: a critical biological partnership. Biochemistry 43 (2004) 3301-3309
36. Matulis D., Kranz J.K., Salemme F.R., and Todd M.J. Thermodynamic stability of carbonic anhydrase: measurements of binding affinity and stoichiometry using ThermoFluor. Biochemistry 44 (2005) 5258-5266
37. Pantoliano M.W., Petrella E.C., Kwasnoski J.D., Lobanov V.S., Myslik J., Graf E., et al. High-density miniaturized thermal shift assays as a general strategy for drug discovery. J. Biomol. Screening 6 (2001) 429-440
38. Gao G., and Luo H. The ubiquitin-proteasome pathway in viral infections. Can. J. Physiol. Pharmacol. 84 (2006) 5-14
39. Iqbal M., Poole E., Goodbourn S., and McCauley J.W. Role for bovine viral diarrhea virus Erns glycoprotein in the control of activation of beta interferon by double-stranded RNA. J. Virol. 78 (2004) 136-145
40. Magkouras I., Matzener P., Rumenapf T., Peterhans E., and Schweizer M. RNase-dependent inhibition of extracellular, but not intracellular, dsRNA-induced interferon synthesis by Erns of pestiviruses. J. Gen. Virol. 89 (2008) 2501-2506
41. Matzener P., Magkouras I., Rumenapf T., Peterhans E., and Schweizer M. The viral RNase E(rns) prevents IFN type-I triggering by pestiviral single- and double-stranded RNAs. Virus Res. 140 (2009) 15-23
42. Barro M., and Patton J.T. Rotavirus nonstructural protein 1 subverts innate immune response by inducing degradation of IFN regulatory factor 3. Proc. Natl Acad. Sci. USA 102 (2005) 4114-4119
43. Graff J.W., Mitzel D.N., Weisend C.M., Flenniken M.L., and Hardy M.E. Interferon regulatory factor 3 is a cellular partner of rotavirus NSP1. J. Virol. 76 (2002) 9545-9550
44. Saira K., Zhou Y., and Jones C. 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 (2007) 3077-3086
45. McGuffin L.J., Bryson K., and Jones D.T. The PSIPRED protein structure prediction server. Bioinformatics 16 (2000) 404-405
46. Ruggli N., Tratschin J.D., Mittelholzer C., and Hofmann M.A. Nucleotide sequence of classical swine fever virus strain Alfort/187 and transcription of infectious RNA from stably cloned full-length cDNA. J. Virol. 70 (1996) 3478-3487
47. Collett M.S., Larson R., Belzer S.K., and Retzel E. Proteins encoded by bovine viral diarrhea virus: the genomic organization of a pestivirus. Virology 165 (1988) 200-208
48. Moser C., Stettler P., Tratschin J.D., and Hofmann M.A. Cytopathogenic and noncytopathogenic RNA replicons of classical swine fever virus. J. Virol. 73 (1999) 7787-7794
49. Alcock N.W. A hydrogen peroxide digestion system for tissue trace metal analysis. Biol. Trace Elem. Res. 13 (1987) 363-370
50. Wills N.K., Sadagopa Ramanujam V.M., Kalariya N., Lewis J.R., and van Kuijk F.J. Copper and zinc distribution in the human retina: relationship to cadmium accumulation, age, and gender. Exp. Eye Res. 87 (2008) 80-88
51. Ramanujam V.M., Yokoi K., Egger N.G., Dayal H.H., Alcock N.W., and Sandstead H.H. Polyatomics in zinc isotope ratio analysis of plasma samples by inductively coupled plasma-mass spectrometry and applicability of nonextracted samples for zinc kinetics. Biol. Trace Elem. Res. 68 (1999) 143-158
52. Pace C.N., Vajdos F., Fee L., Grimsley G., and Gray T. How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4 (1995) 2411-2423
53. Kosmidou A., Ahl R., Thiel H.J., and Weiland E. Differentiation of classical swine fever virus (CSFV) strains using monoclonal antibodies against structural glycoproteins. Vet. Microbiol. 47 (1995) 111-118