Viral Genomic Single-Stranded RNA Directs the Pathway Toward a T = 3 Capsid

Journal of Molecular Biology

Volumn 395, Issue 5, 2010, Pages 924-936

  Basnak, Gabriella ^a   Morton, Victoria L ^a   Rolfsson, Óttar ^a   Stonehouse, Nicola J ^a   Ashcroft, Alison E ^a   Stockley, Peter G ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

mass spectrometry; RNA protein interaction; virus assembly

Indexed keywords

APTAMER; COAT PROTEIN; GENOMIC RNA; SINGLE STRANDED RNA; VIRUS DNA;

ARTICLE; CONCENTRATION (PARAMETERS); CONFORMATIONAL TRANSITION; DNA PACKAGING; ELECTROSPRAY MASS SPECTROMETRY; GEL FILTRATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; MOLECULAR MECHANICS; MS2 VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; RNA SEQUENCE; VIRAL GENETICS; VIRUS CAPSID; WILD TYPE;

ENTEROBACTERIA PHAGE T3; MIRIDAE; RNA VIRUSES;

EID: 73649091047     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.11.018     Document Type: Article

References (44)

1. Harrison S.C., Olson A.J., Schutt C.E., Winkler F.K., and Bricogne G. Tomato bushy stunt virus at 2.9 Å resolution. Nature 276 (1978) 368-373
2. Sorger P.K., Stockley P.G., and Harrison S.C. Structure and assembly of turnip crinkle virus: II. Mechanism of reassembly in vitro. J. Mol. Biol. 191 (1986) 639-658
3. Caspar D.L., and Klug A. Physical principles in the construction of regular viruses. Cold Spring Harbor Symp. Quant. Biol. 27 (1962) 1-24
4. Golmohammadi R., Valegard K., Fridborg K., and Liljas L. The refined structure of bacteriophage MS2 at 2.8 Å resolution. J. Mol. Biol. 234 (1993) 620-639
5. Valegard K., Liljas L., Fridborg K., and Unge T. The three-dimensional structure of the bacterial virus MS2. Nature 345 (1990) 36-41
6. Stockley P.G., Rolfsson O., Thompson G.S., Basnak G., Francese S., Stonehouse N.J., et al. A simple, RNA-mediated allosteric switch controls the pathway to formation of a T = 3 viral capsid. J. Mol. Biol. 369 (2007) 541-552
7. Carey J., and Uhlenbeck O.C. Kinetic and thermodynamic characterization of the R17 coat protein-ribonucleic acid interaction. Biochemistry 22 (1983) 2610-2615
8. Lago H., Parrott A.M., Moss T., Stonehouse N.J., and Stockley P.G. Probing the kinetics of formation of the bacteriophage MS2 translational operator complex: identification of a protein conformer unable to bind RNA. J. Mol. Biol. 305 (2001) 1131-1144
9. Stockley P.G., Stonehouse N.J., and Valegard K. Molecular mechanism of RNA phage morphogenesis. Int. J. Biochem. 26 (1994) 1249-1260
10. Talbot S.J., Goodman S., Bates S.R., Fishwick C.W., and Stockley P.G. Use of synthetic oligoribonucleotides to probe RNA-protein interactions in the MS2 translational operator complex. Nucleic Acids Res. 18 (1990) 3521-3528
11. Valegard K., Murray J.B., Stockley P.G., Stonehouse N.J., and Liljas L. Crystal structure of an RNA bacteriophage coat protein-operator complex. Nature 371 (1994) 623-626
12. Valegard K., Murray J.B., Stonehouse N.J., van den Worm S., Stockley P.G., and Liljas L. The three-dimensional structures of two complexes between recombinant MS2 capsids and RNA operator fragments reveal sequence-specific protein-RNA interactions. J. Mol. Biol. 270 (1997) 724-738
13. Witherell G.W., Gott J.M., and Uhlenbeck O.C. Specific interaction between RNA phage coat proteins and RNA. Prog. Nucleic Acid Res. Mol. Biol. 40 (1991) 185-220
14. Beckett D., and Uhlenbeck O.C. Ribonucleoprotein complexes of R17 coat protein and a translational operator analog. J. Mol. Biol. 204 (1988) 927-938
15. Beckett D., Wu H.N., and Uhlenbeck O.C. Roles of operator and non-operator RNA sequences in bacteriophage R17 capsid assembly. J. Mol. Biol. 204 (1988) 939-947
16. Fiers W., Contreras R., Duerinck F., Haegeman G., Iserentant D., Merregaert J., et al. Complete nucleotide sequence of bacteriophage MS2 RNA: primary and secondary structure of the replicase gene. Nature 260 (1976) 500-507
17. Koning R., van den Worm S., Plaisier J.R., van Duin J., Pieter Abrahams J., and Koerten H. Visualization by cryo-electron microscopy of genomic RNA that binds to the protein capsid inside bacteriophage MS2. J. Mol. Biol. 332 (2003) 415-422
18. Toropova K., Basnak G., Twarock R., Stockley P.G., and Ranson N.A. The three-dimensional structure of genomic RNA in bacteriophage MS2: implications for assembly. J. Mol. Biol. 375 (2008) 824-836
19. van den Worm S.H., Koning R.I., Warmenhoven H.J., Koerten H.K., and van Duin J. Cryo electron microscopy reconstructions of the Leviviridae unveil the densest icosahedral RNA packing possible. J. Mol. Biol. 363 (2006) 858-865
20. Convery M.A., Rowsell S., Stonehouse N.J., Ellington A.D., Hirao I., Murray J.B., et al. Crystal structure of an RNA aptamer-protein complex at 2.8 Å resolution. Nat. Struct. Biol. 5 (1998) 133-139
21. Hirao I., Spingola M., Peabody D., and Ellington A.D. The limits of specificity: an experimental analysis with RNA aptamers to MS2 coat protein variants. Mol. Diversity 4 (1998) 75-89
22. Rowsell S., Stonehouse N.J., Convery M.A., Adams C.J., Ellington A.D., Hirao I., et al. Crystal structures of a series of RNA aptamers complexed to the same protein target. Nat. Struct. Biol. 5 (1998) 970-975
23. Horn W.T., Tars K., Grahn E., Helgstrand C., Baron A.J., Lago H., et al. Structural basis of RNA binding discrimination between bacteriophages Qbeta and MS2. Structure 14 (2006) 487-495
24. Ling C.M., Hung P.P., and Overby L.R. Independent assembly of Qbeta and MS2 phages in doubly infected Escherichia coli. Virology 40 (1970) 920-929
25. Murray J.B., Collier A.K., and Arnold J.R. A general purification procedure for chemically synthesized oligoribonucleotides. Anal. Biochem. 218 (1994) 177-184
26. Zuker M. Mfold Web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31 (2003) 3406-3415
27. Parrott A.M., Lago H., Adams C.J., Ashcroft A.E., Stonehouse N.J., and Stockley P.G. RNA aptamers for the MS2 bacteriophage coat protein and the wild-type RNA operator have similar solution behaviour. Nucleic Acids Res. 28 (2000) 489-497
28. Rolfsson O., Toropova K., Morton V.L., Francese S., Basnak G., Thompson G.S., et al. RNA packing specificity and folding during assembly of the bacteriophage MS2. Comput. Math. Methods Med. 9 (2008) 339-349
29. Hohn T. Role of RNA in the assembly process of bacteriophage fr. J. Mol. Biol. 43 (1969) 191-200
30. van den Worm S.H., Stonehouse N.J., Valegard K., Murray J.B., Walton C., Fridborg K., et al. Crystal structures of MS2 coat protein mutants in complex with wild-type RNA operator fragments. Nucleic Acids Res. 26 (1998) 1345-1351
31. Du Z., Yu J., Ulyanov N.B., Andino R., and James T.L. Solution structure of a consensus stem-loop D RNA domain that plays important roles in regulating translation and replication in enteroviruses and rhinoviruses. Biochemistry 43 (2004) 11959-11972
32. Zimmern D. The nucleotide sequence at the origin for assembly on tobacco mosaic virus RNA. Cell 11 (1977) 463-482
33. Qu F., and Morris T.J. Encapsidation of turnip crinkle virus is defined by a specific packaging signal and RNA size. J. Virol. 71 (1997) 1428-1435
34. Stoker K., Koperzwarthoff E.C., Bol J.F., and Jaspars E.M.J. Localization of a high-affinity binding site for coat protein on the 3′-terminal part of RNA-4 of alfalfa mosaic virus. FEBS Lett. 121 (1980) 123-126
35. Sun J., DuFort C., Daniel M.C., Murali A., Chen C., Gopinath K., et al. Core-controlled polymorphism in virus-like particles. Proc. Natl Acad. Sci. USA 104 (2007) 1354-1359
36. Aniagyei S.E., Kennedy C.J., Stein B., Willits D.A., Douglas T., Young M.J., et al. Synergistic effects of mutations and nanoparticles templating in the self-assembly of cowpea chlorotic mottle virus capsids. Nano Lett. 9 (2008) 393-398
37. Dykeman E.C., Stockley P.G., and Twarock R. Dynamic allostery controls coat protein conformer switching during MS2 phage assembly. J. Mol. Biol. 395 (2009) 916-923
38. Stockley P.G., Ashcroft A.E., Francese S., Thompson G.S., Ranson N.A., Smith A.M., et al. Dissecting the fine details of assembly of a T = 3 phage capsid. Comput. Math. Methods Med. 6 (2005) 119-125
39. Shiba T., and Suzuki Y. Localization of A protein in the RNA-A protein complex of RNA phage MS2. Biochim. Biophys. Acta 654 (1981) 249-255
40. Kern D., and Zuiderweg E.R. The role of dynamics in allosteric regulation. Curr. Opin. Struct. Biol. 13 (2003) 748-757
41. Mastico R.A., Talbot S.J., and Stockley P.G. Multiple presentation of foreign peptides on the surface of an RNA-free spherical bacteriophage capsid. J. Gen. Virol. 74 Pt. 4 (1993) 541-548
42. Sugiyama T., and Nakada D. Control of translation of MS2 RNA cistrons by MS2 coat protein. Proc. Natl. Acad. Sci. USA 57 (1967) 1744-1750
43. Schuck P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys. J. 78 (2000) 1606-1619
44. Enger M.D., Stubbs E.A., Mitra S., and Kaesberg P. Biophysical characteristics of the RNA-containing bacterial virus R17. Proc. Natl Acad. Sci. USA 49 (1963) 857-860