A new paradigm for the roles of the genome in ssRNA viruses

Papers of special note have been highlighted as: ▪ of interest ▪▪ of considerable interest

References

• 1  Schneemann A. The structural and functional role of RNA in icosahedral virus assembly. Annu. Rev. Microbiol.60,51–67 (2006).
  Medline CASGoogle Scholar
• 2  Rossmann MG, Johnson JE. Icosahedral RNA virus structure. Annu. Rev. Biochem.58,533–573 (1989).
  Medline CASGoogle Scholar
• 3  Cadena-Nava RD, Comas-Garcia M, Garmann RF et 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).
  Medline CASGoogle Scholar
• 4  Bruinsma RF. Physics of RNA and viral assembly. Eur. Phys. J. E Soft Matter19(3),303–310 (2006).
  Medline CASGoogle Scholar
• 5  Morozov AY, Bruinsma RF, J Rudnick. Assembly of viruses and the pseudo-law of mass action. J. Chem. Phys.131(15),155101 (2009).
  MedlineGoogle Scholar
• 6  Bruinsma RF, WM Gelbart, Reguera D et al. Viral self-assembly as a thermodynamic process. Phys. Rev. Lett.90(24),248101 (2003).
  MedlineGoogle Scholar
• 7  Endres DM, Miyahara M, Moisant P, Zlotnick A. A reaction landscape identifies the intermediates critical for self-assembly of virus capsids and other polyhedral structures. Protein Sci.14(6),1518–1525 (2005).
  Medline CASGoogle Scholar
• 8  Fejer SN, Chakrabarti D, Wales DJ. Emergent complexity from simple anisotropic building blocks: shells, tubes, and spirals. ACS Nano4(1),219–228 (2010).
  Medline CASGoogle Scholar
• 9  Hagan MF, Chandler D. Dynamic pathways for viral capsid assembly. Biophys. J.91(1),42–54 (2006).
  Medline CASGoogle Scholar
• 10  Keef T, Micheletti C, Twarock R. Master equation approach to the assembly of viral capsids. J. Theor. Biol.242(3),713–721 (2006).
  Medline CASGoogle Scholar
• 11  Keef T, Taormina A, Twarock R. Assembly models for Papovaviridae based on tiling theory. Phys. Biol.2(3),175–188 (2005).
  Medline CASGoogle Scholar
• 12  Kumar MS, Schwartz R. A parameter estimation technique for stochastic self-assembly systems and its application to human papillomavirus self-assembly. Phys. Biol.7(4),045005 (2010).
  MedlineGoogle Scholar
• 13  Lee B, Leduc PR, Schwartz R. 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),031911 (2008).
  MedlineGoogle Scholar
• 14  Moisant P, Neeman H, Zlotnick A. Exploring the paths of (virus) assembly. Biophys. J.99(5),1350–1357 (2010).
  Medline CASGoogle Scholar
• 15  Rapaport DC. Self-assembly of polyhedral shells: a molecular dynamics study. Phys. Rev. E Stat. Nonlin. Soft Matter Phys.70(5 Pt 1),051905 (2004).
  Medline CASGoogle Scholar
• 16  Sitharam M, Agbandje-McKenna M. Modeling virus self-assembly pathways: avoiding dynamics using geometric constraint decomposition. J. Comput. Biol.13(6),1232–1265 (2006).
  Medline CASGoogle Scholar
• 17  Sweeney B, Zhang T, Schwartz R. Exploring the parameter space of complex self-assembly through virus capsid models. Biophys. J.94(3),772–783 (2008).
  Medline CASGoogle Scholar
• 18  Zandi R, van der Schoot P, Reguera D et al. Classical nucleation theory of virus capsids. Biophys. J.90(6),1939–1948 (2006).
  Medline CASGoogle Scholar
• 19  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).
  Medline CASGoogle Scholar
• 20  Bancroft JB, Hills GJ, Markham R. 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).
  Medline CASGoogle Scholar
• 21  Bancroft JB, Hiebert E, Bracker CE. The effects of various polyanions on shell formation of some spherical viruses. Virology39(4),924–930 (1969).
  Medline CASGoogle Scholar
• 22  Johnson JM, Willits DA, Young MJ et 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).
  Medline CASGoogle Scholar
• 23  Harrison SC, Olson AJ, Schutt CE et al. Tomato bushy stunt virus at 2.9 A resolution. Nature276(5686),368–373 (1978).▪ Defines the important structural questions relating to quasiequivalent ssRNA virions.
  Medline CASGoogle Scholar
• 24  Ling CM, Hung PP, Overby LR. Independent assembly of Qbeta and MS2 phages in doubly infected Escherichia coli. Virology40(4),920–929 (1970).
  Medline CASGoogle Scholar
• 25  Lodish HF, Zinder ND. Mutants of the bacteriophage f2. 8. Control mechanisms for phage-specific syntheses. J. Mol. Biol.19(2),333–348 (1966).
  Medline CASGoogle Scholar
• 26  Gott JM, Wilhelm LJ, Uhlenbeck OC. RNA binding properties of the coat protein from bacteriophage GA. Nucleic Acids Res.19(23),6499–6503 (1991).
  Medline CASGoogle Scholar
• 27  Qu F, Morris TJ. Encapsidation of turnip crinkle virus is defined by a specific packaging signal and RNA size. J. Virol.71(2),1428–1435 (1997).
  Medline CASGoogle Scholar
• 28  Bunka DH, Lane SW, Lane CL et 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).
  Medline CASGoogle Scholar
• 29  Lane SW, Dennis CA, Lane CL et al. Construction and crystal structure of recombinant STNV capsids. J. Mol. Biol.413(1),41–50 (2011).
  Medline CASGoogle Scholar
• 30  Kim DY, Firth AE, Atasheva S et al. Conservation of a packaging signal and the viral genome RNA packaging mechanism in alphavirus evolution. J. Virol.85(16),8022–8036 (2011).
  Medline CASGoogle Scholar
• 31  Frolova E, Frolov I, Schlesinger S. Packaging signals in alphaviruses. J. Virol.71(1),248–258 (1997).
  Medline CASGoogle Scholar
• 32  Gell C, Sabir T, Westwood J et 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).
  Medline CASGoogle Scholar
• 33  Lago H, Parrott AM, Moss T et 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).
  Medline CASGoogle Scholar
• 34  Carey J, Uhlenbeck OC. Kinetic and thermodynamic characterization of the R17 coat protein–ribonucleic acid interaction. Biochemistry22(11),2610–2615 (1983).
  Medline CASGoogle Scholar
• 35  Carey J, Cameron V, de Haseth PL, Uhlenbeck OC. Sequence-specific interaction of R17 coat protein with its ribonucleic acid binding site. Biochemistry22(11),2601–2610 (1983).
  Medline CASGoogle Scholar
• 36  Stockley PG, Baron AJ, Wild CM et 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).
  Medline CASGoogle Scholar
• 37  Lago H, Fonseca SA, Murray JB et al. Dissecting the key recognition features of the MS2 bacteriophage translational repression complex. Nucleic Acids Res.26(5),1337–1344 (1998).
  Medline CASGoogle Scholar
• 38  Rowsell S, Stonehouse NJ, Convery MA et al. Crystal structures of a series of RNA aptamers complexed to the same protein target. Nat. Struct. Biol.5(11),970–975 (1998).
  Medline CASGoogle Scholar
• 39  Convery MA, Rowsell S, NJ Stonehouse et al. Crystal structure of an RNA aptamer–protein complex at 2.8 A resolution. Nat. Struct. Biol.5(2),133–139 (1998).
  Medline CASGoogle Scholar
• 40  Valegard K, Murray JB, Stockley PG et al. Crystal structure of an RNA bacteriophage coat protein–operator complex. Nature371(6498),623–626 (1994).▪ Reports the high-resolution structure of TR bound to the phage coat protein shell, allowing the essential structural recognition features to be determined.
  Medline CASGoogle Scholar
• 41  Valegard K, Murray JB, Stonehouse NJ et 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).
  Medline CASGoogle Scholar
• 42  Grahn E, Moss T, Helgstrand C et al. Structural basis of pyrimidine specificity in the MS2 RNA hairpin–coat-protein complex. RNA7(11),1616–1627 (2001).
  Medline CASGoogle Scholar
• 43  Grahn E, Stonehouse NJ, Adams CJ et 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).
  Medline CASGoogle Scholar
• 44  Grahn E, Stonehouse NJ, Murray JB et al. Crystallographic studies of RNA hairpins in complexes with recombinant MS2 capsids: implications for binding requirements. RNA5(1),131–138 (1999).
  Medline CASGoogle Scholar
• 45  Helgstrand C, Grahn E, Moss T et 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).
  Medline CASGoogle Scholar
• 46  Horn WT, Convery MA, Stonehouse NJ et 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. RNA10(11),1776–1782 (2004).
  Medline CASGoogle Scholar
• 47  Horn WT, Tars K, Grahn E et al. Structural basis of RNA binding discrimination between bacteriophages Qbeta and MS2. Structure14(3),487–495 (2006).
  Medline CASGoogle Scholar
• 48  Plevka P, Kazaks A, Voronkova T et 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).
  Medline CASGoogle Scholar
• 49  Tars K, Fridborg K, Bundule M et al. The three-dimensional structure of bacteriophage PP7 from Pseudomonas aeruginosa at 3.7-A resolution. Virology272(2),331–337 (2000).
  Medline CASGoogle Scholar
• 50  Golmohammadi R, Fridborg K, Bundule M et al. The crystal structure of bacteriophage Q beta at 3.5 A resolution. Structure4(5),543–554 (1996).
  Medline CASGoogle Scholar
• 51  Golmohammadi R, Valegard K, Fridborg K et al. The refined structure of bacteriophage MS2 at 2.8 A resolution. J. Mol. Biol.234(3),620–639 (1993).
  Medline CASGoogle Scholar
• 52  Liljas L, Fridborg K, Valegard K et al. Crystal structure of bacteriophage fr capsids at 3.5 A resolution. J. Mol. Biol.244(3),279–290 (1994).
  Medline CASGoogle Scholar
• 53  Beckett D, Uhlenbeck OC. Ribonucleoprotein complexes of R17 coat protein and a translational operator analog. J. Mol. Biol.204(4),927–938 (1988).
  Medline CASGoogle Scholar
• 54  Beckett D, Wu HN, Uhlenbeck OC. Roles of operator and non-operator RNA sequences in bacteriophage R17 capsid assembly. J. Mol. Biol.204(4),939–947 (1988).
  Medline CASGoogle Scholar
• 55  Dykeman EC, Stockley PG, Twarock R. 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).
  Google Scholar
• 56  Stockley PG, Rolfsson O, Thompson GS et 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).▪▪ Identifies the mechanistic basis of quasiequivalent conformational switching during the assembly of MS2.
  Medline CASGoogle Scholar
• 57  Morton VL, Dykeman EC, Stonehouse NJ et al. The impact of viral RNA on assembly pathway selection. J. Mol. Biol.401(2),298–308 (2010).
  Medline CASGoogle Scholar
• 58  Morton VL, Stockley PG, Stonehouse NJ et al. Insights into virus capsid assembly from non-covalent mass spectrometry. Mass Spectrom. Rev.27(6),575–595 (2008).
  MedlineGoogle Scholar
• 59  Caspar DL, A Klug. Physical principles in the construction of regular viruses. Cold Spring Harb. Symp. Quant. Biol.27,1–24 (1962).
  Medline CASGoogle Scholar
• 60  Dykeman EC, Grayson NE, Toropova K et al. Simple rules for efficient assembly predict the layout of a packaged viral RNA. J. Mol. Biol.408(3),399–407 (2011).▪▪ Reveals the first structure of an ssRNA virus showing asymmetric distribution of the RNA along the fivefold axis, and suggested that this is a direct consequence of the dimer switching model requiring the RNA to take a defined (Hamiltonian) path along the inner protein shell.
  Medline CASGoogle Scholar
• 61  Dykeman EC, Stockley PG, Twarock R. Dynamic allostery controls coat protein conformer switching during MS2 phage assembly. J. Mol. Biol.395(5),916–923 (2010).▪ Shows that RNA allostery occurs via effects on protein dynamics and is not sequence specific.
  Medline CASGoogle Scholar
• 62  Dykeman EC, Twarock R. 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),031908 (2010).
  MedlineGoogle Scholar
• 63  Morton VL, Burkitt W, O’Connor G et 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).
  Medline CASGoogle Scholar
• 64  Basnak G, Morton VL, Rolfsson O et al. Viral genomic single-stranded RNA directs the pathway toward a T=3 capsid. J. Mol. Biol.395(5),924–936 (2010).
  Medline CASGoogle Scholar
• 65  Rolfsson O, Toropova K, Ranson NA et 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).
  Medline CASGoogle Scholar
• 66  Elsawy KM, Caves LS, Twarock R. 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).
  Medline CASGoogle Scholar
• 67  Valegard K, Liljas L, Fridborg K et al. The three-dimensional structure of the bacterial virus MS2. Nature345(6270),36–41 (1990).
  Medline CASGoogle Scholar
• 68  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).
  Medline CASGoogle Scholar
• 69  van den Worm SH, Koning RI, Warmenhoven HJ et al. Cryo electron microscopy reconstructions of the Leviviridae unveil the densest icosahedral RNA packing possible. J. Mol. Biol.363(4),858–865 (2006).
  Medline CASGoogle Scholar
• 70  Toropova K, Basnak G, Twarock R et al. The three-dimensional structure of genomic RNA in bacteriophage MS2: implications for assembly. J. Mol. Biol.375(3),824–836 (2008).
  Medline CASGoogle Scholar
• 71  Hamilton WR. An account of the Icosian calculus. Proc. R. Ir. Acad.6,415–416 (1858).
  Google Scholar
• 72  Knapman TW, VL Morton, NJ Stonehouse et al. Determining the topology of virus assembly intermediates using ion mobility spectrometry-mass spectrometry. Rapid Commun. Mass Spectrom.24(20),3033–3042 (2010).
  Medline CASGoogle Scholar
• 73  Borodavka A, Tuma R, Stockley PG. Evidence that viral RNAs have evolved for efficient, two-stage packaging. Proc. Natl. Acad. Sci. USA109,15769–15774 (2012).
  Medline CASGoogle Scholar
• 74  Borodavka A, Tuma R, Stockley PG. A two-stage mechanism of viral RNA compaction revealed by single molecule fluorescence. RNA Biol.10,1–9 (2013).▪▪ Demonstrates using single-molecule fluorescence assays that RNA encapsidation in vitro is specific at low concentrations.
  MedlineGoogle Scholar
• 75  Groeneveld H. Secondary Structure of Bacteriophage MS2 RNA: Translational Control by Kinetics of RNA Folding. PhD Thesis, University of Leiden, Leiden, The Netherlands (1997).
  Google Scholar
• 76  Olsthoorn RCL. Structure and Evolution of RNA Phages. PhD Thesis, University of Leiden, Leiden, The Netherlands (1996).
  Google Scholar
• 77  Krahn PM, O’Callaghan RJ, Paranchych W. Stages in phage R17 infection. VI. Injection of A protein and RNA into the host cell. Virology47(3),628–637 (1972).
  Medline CASGoogle Scholar
• 78  Shiba T, Suzuki Y. Localization of A protein in the RNA–A protein complex of RNA phage MS2. Biochim. Biophys. Acta654(2),249–255 (1981).
  Medline CASGoogle Scholar
• 79  Schwartz R, Garcea RL, Berger B. “Local rules” theory applied to polyomavirus polymorphic capsid assemblies. Virology268(2),461–470 (2000).
  Medline CASGoogle Scholar
• 80  Schwartz R, Shor PW, Prevelige PE Jr et al. Local rules simulation of the kinetics of virus capsid self-assembly. Biophys. J.75(6),2626–2636 (1998).
  Medline CASGoogle Scholar
• 81  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).
  MedlineGoogle Scholar
• 82  Toropova K, Stockley PG, Ranson NA. Visualising a viral RNA genome poised for release from its receptor complex. J. Mol. Biol.408(3),408–419 (2011).▪▪ Describes the first structure of an ssRNA virus showing asymmetric distribution of the RNA along the fivefold axis, and suggests that this is a direct consequence of the dimer switching model requiring the RNA to take a defined (Hamiltonian) path along the inner protein shell.
  Medline CASGoogle Scholar
• 83  Dent KC, Thompson R, Barker AM et al. The asymmetric structure of an icosahedral virus bound to its receptor suggests a mechanism for genome release. Structure (2013) (In press).
  Google Scholar
• 84  Nicastro D, Schwartz C, Pierson J et al. The molecular architecture of axonemes revealed by cryoelectron tomography. Science313(5789),944–948 (2006).
  Medline CASGoogle Scholar
• 85  Zhang X, Xiang Y, Dunigan DD et al. Three-dimensional structure and function of the Paramecium bursaria chlorella virus capsid. Proc. Natl. Acad. Sci. USA108,14837–14842 (2011).
  Medline CASGoogle Scholar
• 86  Xiao C, Kuznetzov YG, Sun S et al. Structural studies of the giant mimivirus. PLoS Biol.7,e92 (2009).
  Medline CASGoogle Scholar
• 87  van der Schoot P, Bruinsma R. Electrostatics and the assembly of an RNA virus. Phys. Rev. E Stat. Nonlin. Soft Matter Phys.71(6 Pt 1),061928 (2005).
  MedlineGoogle Scholar
• 88  Kivenson A, Hagan MF. Mechanisms of capsid assembly around a polymer. Biophys. J.99(2),619–628 (2010).
  Medline CASGoogle Scholar
• 89  Hagan MF. A theory for viral capsid assembly around electrostatic cores. J. Chem. Phys.130(11),114902 (2009).
  MedlineGoogle Scholar
• 90  Dykeman EC, Stockley PG, Twarock R. Building a viral capsid in the presence of genomic RNA. Phys. Rev. E Stat. Nonlin. Soft Matter Phys.87(2),022717 (2013).▪▪ Demonstrates the impact of packaging signals on capsid assembly efficiency in a model system.
  MedlineGoogle Scholar
• 91  Ford RJ, Barker AM, Bakker SE et 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).
  Medline CASGoogle Scholar
• 92  Hogle JM, Maeda A, Harrison SC. 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).
  Medline CASGoogle Scholar
• 93  Sorger PK, Stockley PG, Harrison SC. Structure and assembly of turnip crinkle virus. II. Mechanism of reassembly in vitro. J. Mol. Biol.191(4),639–658 (1986).
  Medline CASGoogle Scholar
• 94  Xing L, Li TC, Mayazaki N et al. Structure of hepatitis E virion-sized particle reveals an RNA-dependent viral assembly pathway. J. Biol. Chem.285(43),33175–33183 (2010).
  Medline CASGoogle Scholar
• 95  Jones TA, Liljas L. Structure of satellite tobacco necrosis virus after crystallographic refinement at 2.5 A resolution. J. Mol. Biol.177(4),735–767 (1984).
  Medline CASGoogle Scholar
• 96  Bakker SE, Ford RJ, Barker AM et al. Isolation of an asymmetric RNA uncoating intermediate for a single-stranded RNA plant virus. J. Mol. Biol.417(1–2),65–78 (2012).
  Medline CASGoogle Scholar
• 97  Zhang R, Hryc CF, Cong Y et al. 4.4 A cryo-EM structure of an enveloped alphavirus Venezuelan equine encephalitis virus. EMBO J.30(18),3854–3863 (2011).
  Medline CASGoogle Scholar