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Review

A New Paradigm for the Roles of the Genome in ssRNA Viruses

, &
Pages 531-543 | Published online: 31 May 2013

References

  • Schneemann A . The structural and functional role of RNA in icosahedral virus assembly. Annu. Rev. Microbiol.60 , 51–67 (2006).
  • Rossmann MG , JohnsonJE. Icosahedral RNA virus structure. Annu. Rev. Biochem.58 , 533–573 (1989).
  • Cadena-Nava RD , Comas-GarciaM, GarmannRFet al. Self-assembly of viral capsid protein and RNA molecules of different sizes: requirement for a specific high protein/RNA mass ratio. J. Virol. 86(6) , 3318–3326 (2012).
  • Bruinsma RF . Physics of RNA and viral assembly. Eur. Phys. J. E Soft Matter19(3) , 303–310 (2006).
  • Morozov AY , BruinsmaRF, J Rudnick. Assembly of viruses and the pseudo-law of mass action. J. Chem. Phys.131(15) , 155-101 (2009).
  • Bruinsma RF Gelbart WM Reguera D et al. Viral self-assembly as a thermodynamic process. Phys. Rev. Lett.90(24) , 248-101 (2003).
  • Endres DM , MiyaharaM, MoisantP, ZlotnickA. A reaction landscape identifies the intermediates critical for self-assembly of virus capsids and other polyhedral structures. Protein Sci.14(6) , 1518–1525 (2005).
  • Fejer SN , ChakrabartiD, WalesDJ. Emergent complexity from simple anisotropic building blocks: shells, tubes, and spirals. ACS Nano4(1) , 219–228 (2010).
  • Hagan MF , ChandlerD. Dynamic pathways for viral capsid assembly. Biophys. J.91(1) , 42–54 (2006).
  • Keef T , MichelettiC, TwarockR. Master equation approach to the assembly of viral capsids. J. Theor. Biol.242(3) , 713–721 (2006).
  • Keef T , TaorminaA, TwarockR. Assembly models for Papovaviridae based on tiling theory. Phys. Biol.2(3) , 175–188 (2005).
  • Kumar MS , SchwartzR. A parameter estimation technique for stochastic self-assembly systems and its application to human papillomavirus self-assembly. Phys. Biol.7(4) , 045005 (2010).
  • Lee B , LeducPR, SchwartzR. Stochastic off-lattice modeling of molecular self-assembly in crowded environments by Green‘s function reaction dynamics. Phys. Rev. E Stat. Nonlin. Soft Matter Phys.78(3 Pt 1) , 031-911 (2008).
  • Moisant P , NeemanH, ZlotnickA. Exploring the paths of (virus) assembly. Biophys. J.99(5) , 1350–1357 (2010).
  • Rapaport DC . Self-assembly of polyhedral shells: a molecular dynamics study. Phys. Rev. E Stat. Nonlin. Soft Matter Phys.70(5 Pt 1) , 051-905 (2004).
  • Sitharam M , Agbandje-McKennaM. Modeling virus self-assembly pathways: avoiding dynamics using geometric constraint decomposition. J. Comput. Biol.13(6) , 1232–1265 (2006).
  • Sweeney B , ZhangT, SchwartzR. Exploring the parameter space of complex self-assembly through virus capsid models. Biophys. J.94(3) , 772–783 (2008).
  • Zandi R van der Schoot Reguera D et al. Classical nucleation theory of virus capsids. Biophys. J.90(6) , 1939–1948 (2006).
  • Zlotnick A . To build a virus capsid. An equilibrium model of the self assembly of polyhedral protein complexes. J. Mol. Biol.241(1) , 59–67 (1994).
  • Bancroft JB , HillsGJ, MarkhamR. A study of the self-assembly process in a small spherical virus. Formation of organized structures from protein subunits in vitro. Virology31(2) , 354–379 (1967).
  • Bancroft JB , HiebertE, BrackerCE. The effects of various polyanions on shell formation of some spherical viruses. Virology39(4) , 924–930 (1969).
  • Johnson JM , WillitsDA, YoungMJet al. Interaction with capsid protein alters RNA structure and the pathway for in vitro assembly of cowpea chlorotic mottle virus. J. Mol. Biol. 335(2) , 455–464 (2004).
  • Harrison SC , OlsonAJ, SchuttCEet al. Tomato bushy stunt virus at 2.9 A resolution. Nature 276(5686) , 368–373 (1978).
  • Ling CM , HungPP, OverbyLR. Independent assembly of Qbeta and MS2 phages in doubly infected Escherichia coli. Virology40(4) , 920–929 (1970).
  • Lodish HF , ZinderND. Mutants of the bacteriophage f2. 8. Control mechanisms for phage-specific syntheses. J. Mol. Biol.19(2) , 333–348 (1966).
  • Gott JM , WilhelmLJ, UhlenbeckOC. RNA binding properties of the coat protein from bacteriophage GA. Nucleic Acids Res.19(23) , 6499–6503 (1991).
  • Qu F , MorrisTJ. Encapsidation of turnip crinkle virus is defined by a specific packaging signal and RNA size. J. Virol.71(2) , 1428–1435 (1997).
  • Bunka DH , LaneSW, LaneCLet al. Degenerate RNA packaging signals in the genome of satellite tobacco necrosis virus: implications for the assembly of a T=1 capsid. J. Mol. Biol. 413(1) , 51–65 (2011).
  • Lane SW , DennisCA, LaneCLet al. Construction and crystal structure of recombinant STNV capsids. J. Mol. Biol. 413(1) , 41–50 (2011).
  • Kim DY , FirthAE, AtashevaSet al. Conservation of a packaging signal and the viral genome RNA packaging mechanism in alphavirus evolution. J. Virol. 85(16) , 8022–8036 (2011).
  • Frolova E , FrolovI, SchlesingerS. Packaging signals in alphaviruses. J. Virol.71(1) , 248–258 (1997).
  • Gell C , SabirT, WestwoodJet al. Single-molecule fluorescence resonance energy transfer assays reveal heterogeneous folding ensembles in a simple RNA stem-loop. J. Mol. Biol. 384(1) , 264–278 (2008).
  • Lago H , ParrottAM, MossTet al. 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(5) , 1131–1144 (2001).
  • Carey J , UhlenbeckOC. Kinetic and thermodynamic characterization of the R17 coat protein–ribonucleic acid interaction. Biochemistry22(11) , 2610–2615 (1983).
  • Carey J , CameronV, de Haseth PL, Uhlenbeck OC. Sequence-specific interaction of R17 coat protein with its ribonucleic acid binding site. Biochemistry22(11) , 2601–2610 (1983).
  • Stockley PG , BaronAJ, WildCMet al. Dissecting the molecular details of prokaryotic transcriptional control by surface plasmon resonance: the methionine and arginine repressor proteins. Biosens. Bioelectron. 13(6) , 637–650 (1998).
  • Lago H , FonsecaSA, MurrayJBet al. Dissecting the key recognition features of the MS2 bacteriophage translational repression complex. Nucleic Acids Res. 26(5) , 1337–1344 (1998).
  • Rowsell S , StonehouseNJ, ConveryMAet al. Crystal structures of a series of RNA aptamers complexed to the same protein target. Nat. Struct. Biol. 5(11) , 970–975 (1998).
  • Convery MA , RowsellS, StonehouseNJet al. Crystal structure of an RNA aptamer–protein complex at 2.8 A resolution. Nat. Struct. Biol.5(2) , 133–139 (1998).
  • Valegard K , MurrayJB, StockleyPGet al. Crystal structure of an RNA bacteriophage coat protein–operator complex. Nature 371(6498) , 623–626 (1994).
  • Valegard K , MurrayJB, StonehouseNJet al. 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(5) , 724–738 (1997).
  • Grahn E , MossT, HelgstrandCet al. Structural basis of pyrimidine specificity in the MS2 RNA hairpin–coat-protein complex. RNA 7(11) , 1616–1627 (2001).
  • Grahn E , StonehouseNJ, AdamsCJet al. Deletion of a single hydrogen bonding atom from the MS2 RNA operator leads to dramatic rearrangements at the RNA–coat protein interface. Nucleic Acids Res. 28(23) , 4611–4616 (2000).
  • Grahn E , StonehouseNJ, MurrayJBet al. Crystallographic studies of RNA hairpins in complexes with recombinant MS2 capsids: implications for binding requirements. RNA 5(1) , 131–138 (1999).
  • Helgstrand C , GrahnE, MossTet al. Investigating the structural basis of purine specificity in the structures of MS2 coat protein RNA translational operator hairpins. Nucleic Acids Res. 30(12) , 2678–2685 (2002).
  • Horn WT , ConveryMA, StonehouseNJet al. The crystal structure of a high affinity RNA stem-loop complexed with the bacteriophage MS2 capsid: further challenges in the modeling of ligand–RNA interactions. RNA 10(11) , 1776–1782 (2004).
  • Horn WT , TarsK, GrahnEet al. Structural basis of RNA binding discrimination between bacteriophages Qbeta and MS2. Structure 14(3) , 487–495 (2006).
  • Plevka P , KazaksA, VoronkovaTet al. The structure of bacteriophage phiCb5 reveals a role of the RNA genome and metal ions in particle stability and assembly. J. Mol. Biol. 391(3) , 635–647 (2009).
  • Tars K , FridborgK, BunduleMet al. The three-dimensional structure of bacteriophage PP7 from Pseudomonas aeruginosa at 3.7-A resolution. Virology 272(2) , 331–337 (2000).
  • Golmohammadi R , FridborgK, BunduleMet al. The crystal structure of bacteriophage Q beta at 3.5 A resolution. Structure 4(5) , 543–554 (1996).
  • Golmohammadi R , ValegardK, FridborgKet al. The refined structure of bacteriophage MS2 at 2.8 A resolution. J. Mol. Biol. 234(3) , 620–639 (1993).
  • Liljas L , FridborgK, ValegardKet al. Crystal structure of bacteriophage fr capsids at 3.5 A resolution. J. Mol. Biol. 244(3) , 279–290 (1994).
  • Beckett D , UhlenbeckOC. Ribonucleoprotein complexes of R17 coat protein and a translational operator analog. J. Mol. Biol.204(4) , 927–938 (1988).
  • Beckett D , WuHN, UhlenbeckOC. Roles of operator and non-operator RNA sequences in bacteriophage R17 capsid assembly. J. Mol. Biol.204(4) , 939–947 (1988).
  • Dykeman EC , StockleyPG, TwarockR. Packaging signals in two single-stranded RNA viruses imply a conserved assembly mechanism and geometry of the packaged genome. J. Mol. Biol. (2013) (In press).
  • Stockley PG , RolfssonO, ThompsonGSet al. A simple, RNA-mediated allosteric switch controls the pathway to formation of a T=3 viral capsid. J. Mol. Biol. 369(2) , 541–552 (2007).
  • Morton VL , DykemanEC, StonehouseNJet al. The impact of viral RNA on assembly pathway selection. J. Mol. Biol. 401(2) , 298–308 (2010).
  • Morton VL , StockleyPG, StonehouseNJet al. Insights into virus capsid assembly from non-covalent mass spectrometry. Mass Spectrom. Rev. 27(6) , 575–595 (2008).
  • Caspar DL , A Klug. Physical principles in the construction of regular viruses. Cold Spring Harb. Symp. Quant. Biol.27 , 1–24 (1962).
  • Dykeman EC , GraysonNE, ToropovaKet al. Simple rules for efficient assembly predict the layout of a packaged viral RNA. J. Mol. Biol. 408(3) , 399–407 (2011).
  • Dykeman EC , StockleyPG, TwarockR. Dynamic allostery controls coat protein conformer switching during MS2 phage assembly. J. Mol. Biol.395(5) , 916–923 (2010).
  • Dykeman EC , TwarockR. All-atom normal-mode analysis reveals an RNA-induced allostery in a bacteriophage coat protein. Phys. Rev. E Stat. Nonlin. Soft Matter Phys.81(3 Pt 1) , 031-908 (2010).
  • Morton VL , BurkittW, O‘ConnorGet al. RNA-induced conformational changes in a viral coat protein studied by hydrogen/deuterium exchange mass spectrometry. Phys. Chem. Chem. Phys. 12(41) , 13468–13475 (2010).
  • Basnak G , MortonVL, RolfssonOet al. Viral genomic single-stranded RNA directs the pathway toward a T=3 capsid. J. Mol. Biol. 395(5) , 924–936 (2010).
  • Rolfsson O , ToropovaK, RansonNAet al. Mutually-induced conformational switching of RNA and coat protein underpins efficient assembly of a viral capsid. J. Mol. Biol. 401(2) , 309–322 (2010).
  • Elsawy KM , CavesLS, TwarockR. The impact of viral RNA on the association rates of capsid protein assembly: bacteriophage MS2 as a case study. J. Mol. Biol.400(4) , 935–947 (2010).
  • Valegard K , LiljasL, FridborgKet al. The three-dimensional structure of the bacterial virus MS2. Nature 345(6270) , 36–41 (1990).
  • Koning R van den Worm S Plaisier JR et al. Visualization by cryo-electron microscopy of genomic RNA that binds to the protein capsid inside bacteriophage MS2. J. Mol. Biol.332(2) , 415–422 (2003).
  • van den Worm SH , KoningRI, WarmenhovenHJet al. Cryo electron microscopy reconstructions of the Leviviridae unveil the densest icosahedral RNA packing possible. J. Mol. Biol. 363(4) , 858–865 (2006).
  • Toropova K , BasnakG, TwarockRet al. The three-dimensional structure of genomic RNA in bacteriophage MS2: implications for assembly. J. Mol. Biol. 375(3) , 824–836 (2008).
  • Hamilton WR . An account of the Icosian calculus. Proc. R. Ir. Acad.6 , 415–416 (1858).
  • Knapman TW Morton VL Stonehouse NJ et al. Determining the topology of virus assembly intermediates using ion mobility spectrometry-mass spectrometry. Rapid Commun. Mass Spectrom.24(20) , 3033–3042 (2010).
  • Borodavka A , TumaR, StockleyPG. Evidence that viral RNAs have evolved for efficient, two-stage packaging. Proc. Natl. Acad. Sci. USA109 , 15769–15774 (2012).
  • Borodavka A , TumaR, StockleyPG. A two-stage mechanism of viral RNA compaction revealed by single molecule fluorescence. RNA Biol.10 , 1–9 (2013).
  • Groeneveld H . Secondary Structure of Bacteriophage MS2 RNA: Translational Control by Kinetics of RNA Folding. PhD Thesis, University of Leiden, Leiden, The Netherlands (1997).
  • Olsthoorn RCL . Structure and Evolution of RNA Phages. PhD Thesis, University of Leiden, Leiden, The Netherlands (1996).
  • Krahn PM , O‘CallaghanRJ, ParanchychW. Stages in phage R17 infection. VI. Injection of A protein and RNA into the host cell. Virology47(3) , 628–637 (1972).
  • Shiba T , SuzukiY. Localization of A protein in the RNA–A protein complex of RNA phage MS2. Biochim. Biophys. Acta654(2) , 249–255 (1981).
  • Schwartz R , GarceaRL, BergerB. “Local rules” theory applied to polyomavirus polymorphic capsid assemblies. Virology268(2) , 461–470 (2000).
  • Schwartz R , ShorPW, PreveligePEet al. Jr Local rules simulation of the kinetics of virus capsid self-assembly. Biophys. J.75(6) , 2626–2636 (1998).
  • Brinton CC Jr, Gemski P Jr, Carnahan J. A new type of bacterial pilus genetically controlled by the fertility factor of E. Coli K 12 and its role in chromosome transfer. Proc. Natl Acad. Sci. USA52 , 776–783 (1964).
  • Toropova K , StockleyPG, RansonNA. Visualising a viral RNA genome poised for release from its receptor complex. J. Mol. Biol.408(3) , 408–419 (2011).
  • Dent KC , ThompsonR, BarkerAMet al. The asymmetric structure of an icosahedral virus bound to its receptor suggests a mechanism for genome release. Structure (2013) (In press).
  • Nicastro D , SchwartzC, PiersonJet al. The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313(5789) , 944–948 (2006).
  • Zhang X , XiangY, DuniganDDet al. Three-dimensional structure and function of the Paramecium bursaria chlorella virus capsid. Proc. Natl. Acad. Sci. USA 108 , 14837–14842 (2011).
  • Xiao C , KuznetzovYG, SunSet al. Structural studies of the giant mimivirus. PLoS Biol. 7 , e92 (2009).
  • van der Schoot P , BruinsmaR. Electrostatics and the assembly of an RNA virus. Phys. Rev. E Stat. Nonlin. Soft Matter Phys.71(6 Pt 1) , 061-928 (2005).
  • Kivenson A , HaganMF. Mechanisms of capsid assembly around a polymer. Biophys. J.99(2) , 619–628 (2010).
  • Hagan MF . A theory for viral capsid assembly around electrostatic cores. J. Chem. Phys.130(11) , 114902 (2009).
  • Dykeman EC , StockleyPG, TwarockR. Building a viral capsid in the presence of genomic RNA. Phys. Rev. E Stat. Nonlin. Soft Matter Phys.87(2) , 022717 (2013).
  • Ford RJ , BarkerAM, BakkerSEet al. Sequence-specific, RNA–protein interactions overcome electrostatic barriers preventing assembly of satellite tobacco necrosis virus coat protein. J. Mol. Biol. 425 , 1050–1064 (2013).
  • Hogle JM , MaedaA, HarrisonSC. Structure and assembly of turnip crinkle virus. I. x-ray crystallographic structure analysis at 3.2 A resolution. J. Mol. Biol.191(4) , 625–638 (1986).
  • Sorger PK , StockleyPG, HarrisonSC. Structure and assembly of turnip crinkle virus. II. Mechanism of reassembly in vitro. J. Mol. Biol.191(4) , 639–658 (1986).
  • Xing L , LiTC, MayazakiNet al. Structure of hepatitis E virion-sized particle reveals an RNA-dependent viral assembly pathway. J. Biol. Chem. 285(43) , 33175–33183 (2010).
  • Jones TA , LiljasL. Structure of satellite tobacco necrosis virus after crystallographic refinement at 2.5 A resolution. J. Mol. Biol.177(4) , 735–767 (1984).
  • Bakker SE , FordRJ, BarkerAMet al. Isolation of an asymmetric RNA uncoating intermediate for a single-stranded RNA plant virus. J. Mol. Biol. 417(1–2) , 65–78 (2012).
  • Zhang R , HrycCF, CongYet al. 4.4 A cryo-EM structure of an enveloped alphavirus Venezuelan equine encephalitis virus. EMBO J. 30(18) , 3854–3863 (2011).

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