Mutation of cysteine 171 of pestivirus Erns RNase prevents homodimer formation and leads to attenuation of classical swine fever virus

Journal of Virology

Volumn 83, Issue 10, 2009, Pages 4823-4834

  Tews, Birke Andrea ^a,b   Schürmann, Eva Maria ^a   Meyers, Gregor ^a  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^b INSTITUT PASTEUR DE LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; HOMODIMER; NEUTRALIZING ANTIBODY; PROTEIN E RNS; RIBONUCLEASE; UNCLASSIFIED DRUG; VIRUS PROTEIN; E(RNS) PROTEIN, CLASSIC SWINE FEVER VIRUS; INTERFERON; MEMBRANE PROTEIN; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ARTICLE; CODON; DIMERIZATION; DISULFIDE BOND; ENZYME ACTIVITY; GEL ELECTROPHORESIS; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PESTIVIRUS; PRECIPITATION; PRIORITY JOURNAL; PROTEIN GEL BLOT ANALYSIS; SWINE; TISSUE CULTURE; VIRION; VIRUS ATTENUATION; VIRUS MUTANT; VIRUS VIRULENCE; ANIMAL; BLOOD; CELL LINE; GENETICS; IMMUNOLOGY; METABOLISM; PATHOGENICITY; PLASMID; PROTEIN MULTIMERIZATION; SWINE DISEASE; VIROLOGY;

ANIMALIA; CLASSICAL SWINE FEVER VIRUS; PESTIVIRUS; SUIDAE;

ANIMALS; ANTIBODIES, VIRAL; CELL LINE; CLASSICAL SWINE FEVER; CLASSICAL SWINE FEVER VIRUS; CYSTEINE; INTERFERON TYPE I; MEMBRANE GLYCOPROTEINS; MUTATION; PLASMIDS; PROTEIN MULTIMERIZATION; RIBONUCLEASES; SWINE; VIRAL ENVELOPE PROTEINS;

EID: 65349124093     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01710-08     Document Type: Article

References (62)

1. 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. (Pubitemid 46456618)
2. Brackenbury, L. S., B. V. Carr, and B. Charleston. 2003. Aspects of the innate and adaptive immune responses to acute infections with BVDV. Vet. Microbiol. 96:337-344. (Pubitemid 37346274)
3. Ciglic, M. I., P. J. Jackson, S. A. Raillard, M. Haugg, T. M. Jermann, J. G. Opitz, N. Trabesinger-Ruf, and S. A. Benner. 1998. Origin of dimeric structure in the ribonuclease superfamily. Biochemistry 37:4008-4022.
4. Cocquerel, L., C. Wychowski, F. Minner, F. Penin, and J. Dubuisson. 2000. Charged residues in the transmembrane domains of hepatitis C virus glycoproteins play a major role in the processing, subcellular localization, and assembly of these envelope proteins. J. Virol. 74:3623-3633.
5. Colett, M. S., R. Larson, C. Gold, D. Strick, D. K. Anderson, and A. F. Purchio. 1988. Molecular cloning and nucleotide sequence of the pestivirus bovine viral diarrhea virus. Virology 165:191-199.
6. Corapi, W. V., R. O. Donis, and E. J. Dubovi. 1990. Characterization of a panel of monoclonal antibodies and their use in the study of the antigenic diversity of bovine viral diarrhea virus. Am. J. Vet. Res. 51:1388-1394.
7. Deleersnyder, V., A. Pillez, C. Wychowski, K. Blight, J. Xu, Y. S. Hahn, C. M. Rice, and J. Dubuisson. 1997. Formation of native hepatitis C virus glycoprotein complexes. J. Virol. 71:697-704. (Pubitemid 26412343)
8. Devereux, J., P. Haeberli, and O. A. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387-395.
9. Doceul, V., B. Charleston, H. Crooke, E. Reid, P. P. Powell, and J. Seago. 2008. The Npro product of classical swine fever virus interacts with IκBα, the NF-κB inhibitor. J. Gen. Virol. 89:1881-1889.
10. Fetzer, C., B. A. Tews, and G. Meyers. 2005. The carboxy-terminal sequence of the pestivirus glycoprotein E(rns) represents an unusual type of membrane anchor. J. Virol. 79:11901-11913. (Pubitemid 41279307)
11. Fray, M. D., G. E. Mann, and B. Charleston. 2001. Validation of an Mx/CAT reporter gene assay for the quantification of bovine type-I interferon. J. Immunol. Methods 249:235-244. (Pubitemid 32171975)
12. Fricke, J., C. Voss, M. Thumm, and G. Meyers. 2004. Processing of a pestivirus protein by a cellular protease specific for light chain 3 of microtubule- associated proteins. J. Virol. 78:5900-5912. (Pubitemid 38661678)
13. 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. (Pubitemid 43062902)
14. Hausmann, Y., G. Roman-Sosa, H. J. Thiel, and T. Rümenapf. 2004. Classical swine fever virus glycoprotein E rns is an endoribonuclease with an unusual base specificity. J. Virol. 78:5507-5512. (Pubitemid 38581501)
15. Heinz, F. X., M. S. Collett, R. H. Purcell, E. A. Gould, C. R. Howard, M. Houghton, J. M. Moormann, C. M. Rice, and H.-J. Thiel. 2000. Family Flaviviridae, p. 859-878. In M. H. V. van Regenmortel, C. M. Fauquet, D. H. L. Bishop, E. B. Carstens, M. K. Estes, S. M. Lemon, J. Maniloff, M. A. Mayo, D. J. McGeoch, C. R. Pringle, and R. B. Wickner (ed.), Virus taxonomy: classification and nomenclature of viruses. Seventh report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, CA.
16. Hilton, L., K. Moganeradj, G. Zhang, Y. H. Chen, R. E. Randall, J. W. McCauley, and S. Goodbourn. 2006. The NPro product of bovine viral diarrhea virus inhibits DNA binding by interferon regulatory factor 3 and targets it for proteasomal degradation. J. Virol. 80:11723-11732.
17. Horiuchi, H., K. Yanai, M. Takagi, K. Yano, E. Wakabayashi, A. Sanda, S. Mine, K. Ohgi, and M. Irie. 1988. Primary structure of a base non-specific ribonuclease from Rhizopus niveus. J. Biochem. (Tokyo) 103:408-418.
18. Hulst, M. M., G. Himes, E. Newbigin, and R. J. M. Moormann. 1994. Glycoprotein E2 of classical swine fever virus: expression in insect cells and identification as a ribonuclease. Virology 200:558-565.
19. Hulst, M. M., H. G. van Gennip, and R. J. Moormann. 2000. Passage of classical swine fever virus in cultured swine kidney cells selects virus variants that bind to heparan sulfate due to a single amino acid change in envelope protein E(rns). J. Virol. 74:9553-9561.
20. Hulst, M. M., H. G. van Gennip, A. C. Vlot, E. Schooten, A. J. de Smit, and R. J. Moormann. 2001. Interaction of classical swine fever virus with membrane-associated heparan sulfate: role for virus replication in vivo and virulence. J. Virol. 75:9585-9595.
21. Iqbal, M., E. Poole, S. Goodbourn, and J. W. McCauley. 2004. Role for bovine viral diarrhea virus Erns glycoprotein in the control of activation of beta interferon by double-stranded RNA. J. Virol. 78:136-145. (Pubitemid 37549726)
22. Kim, J. S., J. Soucek, J. Matousek, and R. T. Raines. 1995. Mechanism of ribonuclease cytotoxicity. J. Biol. Chem. 270:31097-31102. (Pubitemid 26012196)
23. Kim, J. S., J. Soucek, J. Matousek, and R. T. Raines. 1995. Structural basis for the biological activities of bovine seminal ribonuclease. J. Biol. Chem. 270:10525-10530.
24. König, M., T. Lengsfeld, T. Pauly, R. Stark, and H.-J. Thiel. 1995. Classical swine fever virus: independent induction of protective immunity by two structural glycoproteins. J. Virol. 69:6479-6486.
25. Lackner, T., A. Muller, A. Pankraz, P. Becher, H. J. Thiel, A. E. Gorbalenya, and N. Tautz. 2004. Temporal modulation of an autoprotease is crucial for replication and pathogenicity of an RNA virus. J. Virol. 78:10765-10775. (Pubitemid 39258401)
26. Langedijk, J. P., P. A. van Veelen, W. M. Schaaper, A. H. de Ru, R. H. Meloen, and M. M. Hulst. 2002. A structural model of pestivirus E(rns) based on disulfide bond connectivity and homology modeling reveals an extremely rare vicinal disulfide. J. Virol. 76:10383-10392.
27. La Rocca, S. A., R. J. Herbert, H. Crooke, T. W. Drew, T. E. Wileman, and P. P. Powell. 2005. Loss of interferon regulatory factor 3 in cells infected with classical swine fever virus involves the N-terminal protease, Npro. J. Virol. 79:7239-7247. (Pubitemid 40677353)
28. Lee, J. E., and R. T. Raines. 2005. Cytotoxicity of bovine seminal ribonuclease: monomer versus dimer. Biochemistry 44:15760-15767.
29. Lindenbach, B. D., and C. M. Rice. 2001. Flaviviridae: the viruses and their replication, p. 991-1042. In D. M. Knipe and P. M. Howley (ed.), Fields virology, vol.1. Lippincott-Raven Publishers, Philadelphia, PA.
30. Lindenbach, B. D., H.-J. Thiel, and C. M. Rice. 2007. Flaviviridae: the viruses and their replication, p. 1101-1152. In D. M. Knipe and P. M. Howley (ed.), Fields virology, vol.1. Lippincott-Raven Publishers, Philadelphia, PA.
31. Magkouras, I., P. Matzener, T. Rumenapf, E. Peterhans, and M. Schweizer. 2008. RNase-dependent inhibition of extracellular, but not intracellular, dsRNA-induced interferon synthesis by Erns of pestiviruses. J. Gen. Virol. 89:2501-2506.
32. Meyer, C., M. Von Freyburg, K. Elbers, and G. Meyers. 2002. Recovery of virulent and RNase-negative attenuated type 2 bovine viral diarrhea viruses from infectious cDNA clones. J. Virol. 76:8494-8503.
33. Meyers, G., A. Ege, C. Fetzer, F. M. von, K. Elbers, V. Carr, H. Prentice, B. Charleston, and E. M. Schürmann. 2007. Bovine viral diarrhea virus: prevention of persistent fetal infection by a combination of two mutations affecting the Erns RNase and the Npro protease. J. Virol. 81:3327-3338.
34. Meyers, G., T. Rümenapf, and H.-J. Thiel. 1989. Molecular cloning and nucleotide sequence of the genome of hog cholera virus. Virology 171:555-567.
35. Meyers, G., A. Saalmüller, and M. Büttner. 1999. Mutations abrogating the RNase activity in glycoprotein E(rns) of the pestivirus classical swine fever virus lead to virus attenuation. J. Virol. 73:10224-10235.
36. Meyers, G., N. Tautz, P. Becher, H.-J. Thiel, and B. Kümmerer. 1996. Recovery of cytopathogenic and noncytopathogenic bovine viral diarrhea viruses from cDNA constructs. J. Virol. 70:8606-8613. (Pubitemid 26378440)
37. Meyers, G., H.-J. Thiel, and T. Rümenapf. 1996. Classical swine fever virus: recovery of infectious viruses from cDNA constructs and generation of recombinant cytopathogenic defective interfering particles. J. Virol. 70:1588-1595.
38. Mittelholzer, C., C. Moser, J. D. Tratschin, and M. A. Hofmann. 2000. Analysis of classical swine fever virus replication kinetics allows differentiation of highly virulent from avirulent strains. Vet. Microbiol. 74:293-308. (Pubitemid 30265534)
39. Moennig, V., and P. G. W. Plagemann. 1992. The pestiviruses. Adv. Virus Res. 41:53-98.
40. Niepmann, M., and J. Zheng. 2006. Discontinuous native protein gel electrophoresis. Electrophoresis 27:3949-3951.
41. Op De Beeck, A., R. Montserret, S. Duvet, L. Cocquerel, R. Cacan, B. Barberot, M. M. Le, F. Penin, and J. Dubuisson. 2000. The transmembrane domains of hepatitis C virus envelope glycoproteins E1 and E2 play a major role in heterodimerization. J. Biol. Chem. 275:31428-31437.
42. Reimann, I., I. Semmler, and M. Beer. 2007. Packaged replicons of bovine viral diarrhea virus are capable of inducing a protective immune response. Virology 366:377-386.
43. Rüggli, N., B. H. Bird, L. Liu, O. Bauhofer, J. D. Tratschin, and M. A. Hofmann. 2005. N(pro) of classical swine fever virus is an antagonist of double-stranded RNA-mediated apoptosis and IFN-alpha/beta induction. Virology 340:265-276.
44. Rüggli, N., J. D. Tratschin, M. Schweizer, K. C. McCullough, M. A. Hofmann, and A. Summerfield. 2003. Classical swine fever virus interferes with cellular antiviral defense: evidence for a novel function of N(pro). J. Virol. 77:7645-7654.
45. Rümenapf, T., R. Stark, M. Heimann, and H. J. Thiel. 1998. N-terminal protease of pestiviruses: identification of putative catalytic residues by site-directed mutagenesis. J. Virol. 72:2544-2547.
46. Rümenapf, T., G. Unger, J. H. Strauss, and H.-J. Thiel. 1993. Processing of the envelope glycoproteins of pestiviruses. J. Virol. 67:3288-3295. (Pubitemid 23143701)
47. Sainz, I. F., L. G. Holinka, Z. Lu, G. R. Risatti, and M. V. Borca. 2008. Removal of a N-linked glycosylation site of classical swine fever virus strain Brescia Erns glycoprotein affects virulence in swine. Virology 370:122-129.
48. Schägger, H., and G. V. Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379. (Pubitemid 18004907)
49. Schneider, R., G. Unger, R. Stark, E. Schneider-Scherzer, and H.-J. Thiel. 1993. Identification of a structural glycoprotein of an RNA virus as a ribonuclease. Science 261:1169-1171.
50. Seago, J., L. Hilton, E. Reid, V. Doceul, J. Jeyatheesan, K. Moganeradj, J. McCauley, B. Charleston, and S. Goodbourn. 2007. The Npro product of classical swine fever virus and bovine viral diarrhea virus uses a conserved mechanism to target interferon regulatory factor-3. J. Gen. Virol. 88:3002-3006. (Pubitemid 350131237)
51. Tews, B. A., and G. Meyers. 2007. The pestivirus glycoprotein Erns is anchored in plane in the membrane via an amphipathic helix. J. Biol. Chem. 282:32730-32741. (Pubitemid 350159277)
52. Thiel, H.-J., P. G. W. Plagemann, and V. Moennig. 1996. Pestiviruses, p. 1059-1073. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, vol.1. Lippincott-Raven Publishers, Philadelphia, PA.
53. Thiel, H.-J., R. Stark, E. Weiland, T. Rümenapf, and G. Meyers. 1991. Hog cholera virus: molecular composition of virions from a pestivirus. J. Virol. 65:4705-4712.
54. Tratschin, J. D., C. Moser, N. Rüggli, and M. A. Hofmann. 1998. Classical swine fever virus leader proteinase Npro is not required for viral replication in cell culture. J. Virol. 72:7681-7684. (Pubitemid 28377910)
55. van Gennip, H. G., A. T. Hesselink, R. J. Moormann, and M. M. Hulst. 2005. Dimerization of glycoprotein E(rns) of classical swine fever virus is not essential for viral replication and infection. Arch. Virol. 150:2271-2286. (Pubitemid 41456025)
56. van Gennip, H. G., A. C. Vlot, M. M. Hulst, A. J. de Smit, and R. J. Moormann. 2004. Determinants of virulence of classical swine fever virus strain Brescia. J. Virol. 78:8812-8823. (Pubitemid 39025146)
57. Von Freyburg, M., A. Ege, A. Saalmüller, and G. Meyers. 2004. Comparison of the effects of RNase-negative and wild-type classical swine fever virus on peripheral blood cells of infected pigs. J. Gen. Virol. 85:1899-1908. (Pubitemid 39023269)
58. Weiland, E., R. Stark, B. Haas, T. Rümenapf, G. Meyers, and H.-J. Thiel. 1990. Pestivirus glycoprotein which induces neutralizing antibodies forms part of a disulfide linked heterodimer. J. Virol. 64:3563-3569. (Pubitemid 20227177)
59. Weiland, F., E. Weiland, G. Unger, A. Saalmüller, and H. J. Thiel. 1999. Localization of pestiviral envelope proteins E(rns) and E2 at the cell surface and on isolated particles. J. Gen. Virol. 80:1157-1165. (Pubitemid 29213803)
60. Widjojoatmodjo, M. N., H. G. van Gennip, A. Bouma, P. A. van Rijn, and R. J. Moormann. 2000. Classical swine fever virus E(rns) deletion mutants: trans-complementation and potential use as nontransmissible, modified, live-attenuated marker vaccines. J. Virol. 74:2973-2980.
61. Windisch, J. M., R. Schneider, R. Stark, E. Weiland, G. Meyers, and H.-J. Thiel. 1996. RNase of classical swine fever virus: biochemical characterization and inhibition by virus-neutralizing monoclonal antibodies. J. Virol. 70:352-358.
62. Wyatt, L. S., B. Moss, and S. Rozenblatt. 1995. Replication-deficient vaccinia virus encoding bacteriophage T7 RNA polymerase for transient gene expression in mammalian cells. Virology 210:202-205.