Bovine viral diarrhea virus core is an intrinsically disordered protein that binds RNA

Journal of Virology

Volumn 82, Issue 3, 2008, Pages 1294-1304

  Murray, Catherine L ^a   Marcotrigiano, Joseph ^a,b   Rice, Charles M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CORE PROTEIN; GLYCOPROTEIN E1; GLYCOPROTEIN E2; LIPID; POLYPEPTIDE; RNA; VIRUS RNA;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BOVINE DIARRHEA VIRUS; CONTROLLED STUDY; GENE SEQUENCE; HEPATITIS C VIRUS; MORPHOGENESIS; NONHUMAN; PESTIVIRUS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PURIFICATION; PROTEIN RNA BINDING; RNA BINDING; SEQUENCE ANALYSIS; VIRION; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS CORE; VIRUS PARTICLE;

AMINO ACID SEQUENCE; DIARRHEA VIRUSES, BOVINE VIRAL; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; RNA, VIRAL; RNA-BINDING PROTEINS; VIRAL CORE PROTEINS; VIRUS ASSEMBLY;

ANIMALIA; BOVINE VIRAL DIARRHEA VIRUS 1; HEPATITIS C VIRUS; MIRIDAE; PESTIVIRUS;

EID: 38349088979     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01815-07     Document Type: Article

References (55)

1. Agapov, E. V., C. L. Murray, I. Frolov, L. Qu, T. M. Myers, and C. M. Rice. 2004. Uncleaved NS2-3 is required for production of infectious bovine viral diarrhea virus. J. Virol. 78:2414-2425.
2. Beckman, M. T., and K. Kirkegaard. 1998. Site size of cooperative single-stranded RNA binding by poliovirus RNA-dependent RNA polymerase. J. Biol. Chem. 273:6724-6730.
3. Bick, M. J., G. Gao, S. P. Goff, C. M. Rice, and M. R. MacDonald. 2003. Expression of the zinc-finger antiviral protein inhibits alphavirus replication. J. Virol. 77:11555-11562.
4. Boulant, S., C. Vanbelle, C. Ebel, F. Penin, and J. P. Lavergne. 2005. Hepatitis C virus core protein is a dimeric alpha-helical protein exhibiting membrane protein features. J. Virol. 79:11353-11365.
5. Cheng, R. H., R. J. Kuhn, N. H. Olson, M. G. Rossmann, H. K. Choi, T. J. Smith, and T. S. Baker. 1995. Nucleocapsid and glycoprotein organization in an enveloped virus. Cell 80:621-630.
6. Choi, H.-K., L. Tong, W. Minor, P. Dumas, U. Boege, M. G. Rossman, and G. Wengler. 1991. Structure of Sindbis virus core protein reveals a chymotrypsin-like serine proteinase and the organization of the virion. Nature 354:37-43.
7. Chromy, L. R., J. M. Pipas, and R. L. Garcea. 2003. Chaperone-mediated in vitro assembly of Polyomavirus capsids. Proc. Natl. Acad. Sci. USA 100: 10477-10482.
8. Cohen, S. S., and M. L. Greenberg. 1981. Spermidine, an intrinsic component of turnip yellow mosaic virus. Proc. Natl. Acad. Sci. USA 78:5470-5474.
9. Dokland, T., M. Walsh, J. M. Mackenzie, A. A. Khromykh, K. H. Ee, and S. Wang. 2004. West Nile virus core protein; tetramer structure and ribbon formation. Structure 12:1157-1163.
10. Dunker, A. K., C. J. Brown, J. D. Lawson, L. M. Iakoucheva, and Z. Obradovic. 2002. Intrinsic disorder and protein function. Biochemistry 41:6573-6582.
11. 2-terminal domain of the Semliki Forest virus capsid protein. J. Virol. 69:1556-1563.
12. Frolov, I., and S. Schlesinger. 1994. Translation of Sindbis virus mRNA: effects of sequences downstream of the initiating codon. J. Virol. 68:8111-8117.
13. Geigenmuller-Gnirke, U., H. Nitschko, and S. Schlesinger. 1993. Deletion analysis of the capsid protein of Sindbis virus: identification of the RNA binding region. J. Virol. 67:1620-1626.
14. Harada, T., N. Tautz, and H. J. Thiel. 2000. E2-p7 region of the bovine viral diarrhea virus polyprotein: processing and functional studies. J. Virol. 74:9498-9506.
15. Heimann, M., G. Roman-Sosa, B. Martoglio, H. J. Thiel, and T. Rumenapf. 2006. Core protein of pestiviruses is processed at the C terminus by signal peptide peptidase. J. Virol. 80:1915-1921.
16. Hong, E. M., R. Perera, and R. J. Kuhn. 2006. Alphavirus capsid protein helix I controls a checkpoint in nucleocapsid core assembly. J. Virol. 80:8848-8855.
17. Jensen, K. B., K. Musunuru, H. A. Lewis, S. K. Burley, and R. B. Darnell. 2000. The tetranucleotide UCAY directs the specific recognition of RNA by the Nova K-homology 3 domain. Proc. Natl. Acad. Sci. USA 97:5740-5745.
18. Jones, C. T., L. Ma, J. W. Burgner, T. D. Groesch, C. B. Post, and R. J. Kuhn. 2003. Flavivirus capsid is a dimeric alpha-helical protein. J. Virol. 77:7143-7149.
19. Kelly, S. M., T. J. Jess, and N. C. Price. 2005. How to study proteins by circular dichroism. Biochim. Biophys. Acta 1751:119-139.
20. Khromykh, A. A., and E. G. Westaway. 1996. RNA binding properties of core protein of the flavivirus Kunjin. Arch. Virol. 141:685-699.
21. Kiermayr, S., R. M. Roller, C. W. Mandl, P. Messner, and F. X. Heinz. 2004. Isolation of capsid protein dimers from the tick-borne encephalitis flavivirus and in vitro assembly of capsid-like particles. J. Virol. 78:8078-8084.
22. Kofler, R. M., F. X. Heinz, and C. W. Mandl. 2002. Capsid protein C of tick-borne encephalitis virus tolerates large internal deletions and is a favorable target for attenuation of virulence. J. Virol. 76:3534-3543.
23. Kuhn, R. J., W. Zhang, M. G. Rossmann, S. V. Pletnev, J. Corver, E. Lenches, C. T. Jones, S. Mukhopadhyay, P. R. Chipman, E. G. Strauss, T. S. Baker, and J. H. Strauss. 2002. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108:717-725.
24. Kunkel, M., M. Lorinczi, R. Rijnbrand, S. M. Lemon, and S. J. Watowich. 2001. Self-assembly of nucleocapsid-like particles from recombinant hepatitis C virus core protein. J. Virol. 75:2119-2129.
25. Kunkel, M., and S. J. Watowich. 2004. Biophysical characterization of hepatitis C virus core protein: implications for interactions within the virus and host. FEBS Lett. 557:174-180.
26. 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.
27. Li, X., P. Romero, M. Rani, A. K. Dunker, and Z. Obradovic. 1999. Predicting protein disorder for N-, C-, and internal regions. Genome Inform. Ser. Workshop Genome Inform. 10:30-40.
28. 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, 5th ed., vol. 1. Lippincott-Raven Publishers, Philadelphia, PA.
29. Linger, B. R., L. Kunovska, R. J. Kuhn, and B. L. Golden. 2004. Sindbis virus nucleocapsid assembly: RNA folding promotes capsid protein dimerization. RNA 10:128-138.
30. Ma, L., C. T. Jones, T. D. Groesch, R. J. Kuhn, and C. B. Post. 2004. Solution structure of dengue virus capsid protein reveals another fold. Proc. Natl. Acad. Sci. USA 101:3414-3419.
31. Matsumoto, M., S. B. Hwang, K.-S. Jeng, N. Zhu, and M. M. C. Lai. 1996. Homotypic interaction and multimerization of hepatitis C virus core protein. Virology 218:43-51.
32. Moennig, V., and P. G. Plagemann. 1992. The pestiviruses. Adv. Virus Res. 41:53-98.
33. Mukhopadhyay, S., B. S. Kim, P. R. Chipman, M. G. Rossmann, and R. J. Kuhn. 2003. Structure of West Nile virus. Science 302:248.
34. Mukhopadhyay, S., R. J. Kuhn, and M. G. Rossmann. 2005. A structural perspective of the flavivirus life cycle. Nat. Rev. Microbiol. 3:13-22.
35. Mukhopadhyay, S., W. Zhang, S. Gabler, P. R. Chipman, E. G. Strauss, J. H. Strauss, T. S. Baker, R. J. Kuhn, and M. G. Rossmann. 2006. Mapping the structure and function of the E1 and E2 glycoproteins in alphaviruses. Structure 14:63-73.
36. Owen, K. E., and R. J. Kuhn. 1996. Identification of a region in the Sindbis virus nucleocapsid protein that is involved in specificity of RNA encapsidation. J. Virol. 70:2757-2763.
37. Patkar, C. G., C. T. Jones, Y. H. Chang, R. Warrier, and R. J. Kuhn. 2007. Functional requirements of the yellow fever virus capsid protein. J. Virol. 81:6471-6481.
38. Perera, R., K. E. Owen, T. L. Tellinghuisen, A. E. Gorbalenya, and R. J. Kuhn. 2001. Alphavirus nucleocapsid protein contains a putative coiled coil alpha-helix important for core assembly. J. Virol. 75:1-10.
39. Rice, C. M., J. R. Bell, M. W. Hunkapiller, E. G. Strauss, and J. H. Strauss. 1982. Isolation and characterization of the hydrophobic COOH-terminal domains of the Sindbis virion glycoproteins. J. Mol. Biol. 154:355-378.
40. Rice, C. M., and J. H. Strauss. 1982. Association of Sindbis virion glycoproteins and their precursors. J. Mol. Biol. 154:325-348.
41. Romero, P., Z. Obradovic, and K. Dunker. 1997. Sequence data analysis for long disordered region prediction in the calcineurin family. Genome Inform. Ser. Workshop Genome Inform. 8:110-124.
42. Romero, P., Z. Obradovic, X. Li, E. C. Garner, C. J. Brown, and A. K. Dunker. 2001. Sequence complexity of disordered protein. Proteins 42:38-48.
43. Rost, B., and C. Sander. 1993. Prediction of protein secondary structure at better than 70% accuracy. J. Mol. Biol. 232:584-599.
44. Rouille, Y., F. Helle, D. Delgrange, P. Roingeard, C. Voisset, E. Blanchard, S. Belouzard, J. McKeating, A. H. Patel, G. Maertens, T. Wakita, C. Wychowski, and J. Dubuisson. 2006. Subcellular localization of hepatitis C virus structural proteins in a cell culture system that efficiently replicates the virus. J. Virol. 80:2832-2841.
45. Rümenapf, T., G. Unger, J. H. Strauss, and H.-J. Thiel. 1993. Processing of the envelope glycoproteins of pestiviruses. J. Virol. 67:3288-3294.
46. Santolini, E., G. Migliaccio, and N. La Monica. 1994. Biosynthesis and biochemical properties of the hepatitis C virus core protein. J. Virol. 68:3631-3641.
47. Sheppard, S. L., A. T. Burness, and S. M. Boyle. 1980. Polyamines in cncephalomyocarditis virus. J. Virol. 34:266-267.
48. Stark, R., G. Meyers, T. Rümenapf, and H.-J. Thiel. 1993. Processing of pestivirus polyprotein: cleavage site between autoprotease and nucleocapsid protein of classical swine fever virus. J. Virol. 67:7088-7095.
49. 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.
50. Tompa, P. 2005. The interplay between structure and function in intrinsically unstructured proteins. FEBS Lett. 579:3346-3354.
51. Uversky, V. N. 2002. What does it mean to be natively unfolded? Eur. J. Biochem. 269:2-12.
52. Weiss, B., U. Geigenmuller-Gnirke, and S. Schlesinger. 1994. Interactions between Sindbis virus RNAs and a 68 amino acid derivative of the viral capsid protein further defines the capsid binding site. Nucleic Acids Res. 22:780-786.
53. Zhang, W., S. Mukhopadhyay, S. V. Pletnev, T. S. Baker, R. J. Kuhn, and M. G. Rossmann. 2002. Placement of the structural proteins in Sindbis virus. J. Virol. 76:11645-11658.
54. Zhang, Y., J. Corver, P. R. Chipman, W. Zhang, S. V. Pletnev, D. Sedlak, T. S. Baker, J. H. Strauss, R. J. Kuhn, and M. G. Rossmann. 2003. Structures of immature flavivirus particles. EMBO J. 22:2604-2613.
55. Zhang, Y., V. A. Kostyuchenko, and M. G. Rossmann. 2007. Structural analysis of viral nucleocapsids by subtraction of partial projections. J. Struct. Biol. 157:356-364.