Structure of a VP1-VP3 complex suggests how birnaviruses package the VP1 polymerase

Journal of Virology

Volumn 87, Issue 6, 2013, Pages 3229-3236

  Bahar, Mohammad W ^a   Sarin, L Peter ^b,e   Graham, Stephen C ^a,d   Pang, Jances ^a   Bamford, Dennis H ^b   Stuart, David I ^a,c   Grimes, Jonathan M ^a,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF HELSINKI   (Finland)

^c DIAMOND LIGHT SOURCE LTD   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; MULTIPROTEIN COMPLEX; PROTEIN VP1; PROTEIN VP2; PROTEIN VP3; RNA DIRECTED RNA POLYMERASE; VIRUS RNA;

ARTICLE; BIRNAVIRIDAE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; INFECTIOUS PANCREATIC NECROSIS VIRUS; NONHUMAN; PISCICULTURE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; SALMON; VIRUS CAPSID; VIRUS GENOME; VIRUS MORPHOGENESIS;

CRYSTALLOGRAPHY, X-RAY; INFECTIOUS PANCREATIC NECROSIS VIRUS; PROTEIN BINDING; PROTEIN CONFORMATION; RNA REPLICASE; VIRAL STRUCTURAL PROTEINS;

EID: 84874731746     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02939-12     Document Type: Article

References (50)

1. Rodriguez Saint-Jean S, Borrego JJ, Perez-Prieto SI. 2003. Infectious pancreatic necrosis virus: biology, pathogenesis, and diagnostic methods. Adv. Virus Res. 62:113-165.
2. Jackwood DJ, Saif YM, Hughes JH. 1982. Characteristics and serologic studies of two serotypes of infectious bursal disease virus in turkeys. Avian Dis. 26:871-882.
3. Dobos P, Hill BJ, Hallett R, Kells DT, Becht H, Teninges D. 1979. Biophysical and biochemical characterization of five animal viruses with bisegmented double-stranded RNA genomes. J. Virol. 32:593-605.
4. Coulibaly F, Chevalier C, Gutsche I, Pous J, Navaza J, Bressanelli S, Delmas B, Rey FA. 2005. The birnavirus crystal structure reveals structural relationships among icosahedral viruses. Cell 120:761-772.
5. Dobos P. 1993. In vitro guanylylation of infectious pancreatic necrosis virus polypeptide VP1. Virology 193:403-413.
6. Calvert JG, Nagy E, Soler M, Dobos P. 1991. Characterization of the VPg-dsRNA linkage of infectious pancreatic necrosis virus. J. Gen. Virol. 72(Pt 10):2563-2567.
7. Muller H, Nitschke R. 1987. The two segments of the infectious bursal disease virus genome are circularized by a 90,000-Da protein. Virology 159:174-177.
8. Gorbalenya AE, Pringle FM, Zeddam JL, Luke BT, Cameron CE, Kalmakoff J, Hanzlik TN, Gordon KH, Ward VK. 2002. The palm subdomain-based active site is internally permuted in viral RNAdependent RNA polymerases of an ancient lineage. J. Mol. Biol. 324: 47-62.
9. Graham SC, Sarin LP, Bahar MW, Myers RA, Stuart DI, Bamford DH, Grimes JM. 2011. The N-terminus of the RNA polymerase from infectious pancreatic necrosis virus is the determinant of genome attachment. PLoS Pathog. 7:e1002085. doi:10.1371/journal.ppat.1002085.
10. Pan J, Vakharia VN, Tao YJ. 2007. The structure of a birnavirus polymerase reveals a distinct active site topology. Proc. Natl. Acad. Sci. U. S. A. 104:7385-7390.
11. Lee J, Feldman AR, Delmas B, Paetzel M. 2007. Crystal structure of the VP4 protease from infectious pancreatic necrosis virus reveals the acylenzyme complex for an intermolecular self-cleavage reaction. J. Biol. Chem. 282:24928-24937.
12. Birghan C, Mundt E, Gorbalenya AE. 2000. A non-canonical lon proteinase lacking the ATPase domain employs the ser-Lys catalytic dyad to exercise broad control over the life cycle of a double-stranded RNA virus. EMBO J. 19:114-123.
13. Duncan R, Nagy E, Krell PJ, Dobos P. 1987. Synthesis of the infectious pancreatic necrosis virus polyprotein, detection of a virus-encoded protease, and fine structure mapping of genome segment A coding regions. J. Virol. 61:3655-3664.
14. Da Costa B, Chevalier C, Henry C, Huet JC, Petit S, Lepault J, Boot H, Delmas B. 2002. The capsid of infectious bursal disease virus contains several small peptides arising from the maturation process of pVP2. J. Virol. 76:2393-2402.
15. Sanchez AB, Rodriguez JF. 1999. Proteolytic processing in infectious bursal disease virus: identification of the polyprotein cleavage sites by site-directed mutagenesis. Virology 262:190-199.
16. Caston JR, Martinez-Torrecuadrada JL, Maraver A, Lombardo E, Rodriguez JF, Casal JI, Carrascosa JL. 2001. C terminus of infectious bursal disease virus major capsid protein VP2 is involved in definition of the T number for capsid assembly. J. Virol. 75:10815-10828.
17. Bottcher B, Kiselev NA, Stel'Mashchuk VY, Perevozchikova NA, Borisov AV, Crowther RA. 1997. Three-dimensional structure of infectious bursal disease virus determined by electron cryomicroscopy. J. Virol. 71: 325-330.
18. Ona A, Luque D, Abaitua F, Maraver A, Caston JR, Rodriguez JF. 2004. The C-terminal domain of the pVP2 precursor is essential for the interaction between VP2 and VP3, the capsid polypeptides of infectious bursal disease virus. Virology 322:135-142.
19. Chevalier C, Lepault J, Da Costa B, Delmas B. 2004. The last C-terminal residue of VP3, glutamic acid 257, controls capsid assembly of infectious bursal disease virus. J. Virol. 78:3296-3303.
20. Maraver A, Ona A, Abaitua F, Gonzalez D, Clemente R, Ruiz-Diaz JA, Caston JR, Pazos F, Rodriguez JF. 2003. The oligomerization domain of VP3, the scaffolding protein of infectious bursal disease virus, plays a critical role in capsid assembly. J. Virol. 77:6438-6449.
21. Kochan G, Gonzalez D, Rodriguez JF. 2003. Characterization of the RNA-binding activity of VP3, a major structural protein of infectious bursal disease virus. Arch. Virol. 148:723-744.
22. Hjalmarsson A, Carlemalm E, Everitt E. 1999. Infectious pancreatic necrosis virus: identification of a VP3-containing ribonucleoprotein core structure and evidence for O-linked glycosylation of the capsid protein VP2. J. Virol. 73:3484-3490.
23. Tacken MG, Peeters BP, Thomas AA, Rottier PJ, Boot HJ. 2002. Infectious bursal disease virus capsid protein VP3 interacts both with VP1, the RNA-dependent RNA polymerase, and with viral double-stranded RNA. J. Virol. 76:11301-11311.
24. Pedersen T, Skjesol A, Jorgensen JB. 2007. VP3, a structural protein of infectious pancreatic necrosis virus, interacts with RNA-dependent RNA polymerase VP1 and with double-stranded RNA. J. Virol. 81:6652-6663.
25. Casanas A, Navarro A, Ferrer-Orta C, Gonzalez D, Rodriguez JF, Verdaguer N. 2008. Structural insights into the multifunctional protein VP3 of birnaviruses. Structure 16:29-37.
26. Garriga D, Navarro A, Querol-Audi J, Abaitua F, Rodriguez JF, Verdaguer N. 2007. Activation mechanism of a noncanonical RNAdependent RNA polymerase. Proc. Natl. Acad. Sci. U. S. A. 104:20540-20545.
27. Berrow NS, Alderton D, Owens RJ. 2009. The precise engineering of expression vectors using high-throughput In-Fusion PCR cloning. Methods Mol. Biol. 498:75-90.
28. Rossi AM, Taylor CW. 2011. Analysis of protein-ligand interactions by fluorescence polarization. Nat. Protoc. 6:365-387.
29. Walter TS, Diprose JM, Mayo CJ, Siebold C, Pickford MG, Carter L, Sutton GC, Berrow NS, Brown J, Berry IM, Stewart-Jones GB, Grimes JM, Stammers DK, Esnouf RM, Jones EY, Owens RJ, Stuart DI, Harlos K. 2005. A procedure for setting up high-throughput nanolitre crystallization experiments. Crystallization workflow for initial screening, automated storage, imaging and optimization. Acta Crystallogr. D Biol. Crystallogr. 61:651-657.
30. Kabsch W. 1993. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26:795-800.
31. Evans P. 2006. Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62:72-82.
32. Winter G. 2010. xia2: an expert system for macromolecular crystallography data reduction. J. Appl. Crystallogr. 43:186-190.
33. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J. Appl. Crystallogr. 40: 658-674.
34. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66:486-501.
35. Blanc E, Roversi P, Vonrhein C, Flensburg C, Lea SM, Bricogne G. 2004. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D Biol. Crystallogr. 60:2210-2221.
36. Smart O, Brandl M, Flensburg C, Keller P, Paciorek W, Vonrhein C, Womack T, Bricogne G. 2008. Refinement with local structure similarity restraints (LSSR) enables exploitation of information from related structures and facilitates use of NCS. Abstr. Annu. Meet. Am. Crystallogr. Assoc., abstr TP139, p 117.
37. Bricogne G, Blanc E, Brandl M, Flensburg C, Keller P, Paciorek P, Roversi P, Sharff A, Smart O, Vonrhein C, Womack T. 2011. BUSTER version 2.11.1. Global Phasing Ltd., Cambridge, United Kingdom.
38. Chen VB, Arendall WB, III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66:12-21.
39. DeLano WL. 2008. The PyMOL molecular graphics system. DeLano Scientific LLC, Palo Alto, CA. http://www.pymol.org.
40. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
41. Gouet P, Robert X, Courcelle E. 2003. ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res. 31:3320-3323.
42. Stuart DI, Levine M, Muirhead H, Stammers DK. 1979. Crystal structure of cat muscle pyruvate kinase at a resolution of 2.6 A. J. Mol. Biol. 134:109-142.
43. Krissinel E, Henrick K. 2007. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372:774-797.
44. Tina KG, Bhadra R, Srinivasan N. 2007. PIC: Protein Interactions Calculator. Nucleic Acids Res. 35:W473-W476.
45. Wright S, Poranen MM, Bamford DH, Stuart DI, Grimes JM. 2012. Noncatalytic ions direct the RNA-dependentRNApolymerase of bacterial double-stranded RNA virus 6 from de novo initiation to elongation. J. Virol. 86:2837-2849.
46. Pagratis N, Revel HR. 1990. Detection of bacteriophage phi 6 minusstrand RNA and novel mRNA isoconformers synthesized in vivo and in vitro, by strand-separating agarose gels. Virology 177:273-280.
47. Sambrook J, Russell D. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. Dobos P. 1995. Protein-primed RNA synthesis in vitro by the virionassociated RNA polymerase of infectious pancreatic necrosis virus. Virology 208:19-25.
49. Trask SD, McDonald SM, Patton JT. 2012. Structural insights into the coupling of virion assembly and rotavirus replication. Nat. Rev. Microbiol. 10:165-177.
50. Luque D, Rivas G, Alfonso C, Carrascosa JL, Rodriguez JF, Caston JR. 2009. Infectious bursal disease virus is an icosahedral polyploid dsRNA virus. Proc. Natl. Acad. Sci. U. S. A. 106:2148-2152.