Viruses as supramolecular self-assemblies: modelling of capsid formation and genome packaging

Viruses are considered the simplest form of live. A virus is basically composed of genomic material surrounded by a protecting capsid. Today, full molecular details of many viruses are known, and several subclasses can be discerned. In this review, we present recent advances made over the past few years obtained from theoretical considerations and model simulations to improve our understanding on two vital aspects of the physics of viruses: viz. viral capsid self-assembly and viral genome packaging. Many processes, such as the self-assembly pathway, genome packing, and ultimately the infection mechanism, differ between viruses containing double-stranded polynucleotides on one hand and single-stranded polynucleotides on the other hand. We believe that these differences to a large degree originate from the different genome flexibilities.

[1]  N. Hud Double-stranded DNA organization in bacteriophage heads: an alternative toroid-based model. , 1995, Biophysical journal.

[2]  Alasdair C Steven,et al.  Encapsidated Conformation of Bacteriophage T7 DNA , 1997, Cell.

[3]  Jianzhong Wu,et al.  Osmotic pressure and packaging structure of caged DNA. , 2008, Biophysical journal.

[4]  W. Gelbart,et al.  Osmotic shock and the strength of viral capsids. , 2003, Biophysical journal.

[5]  David Reguera,et al.  Viral self-assembly as a thermodynamic process. , 2002, Physical review letters.

[6]  V. Belyĭ,et al.  Electrostatic origin of the genome packing in viruses , 2006, Proceedings of the National Academy of Sciences.

[7]  Zhen‐Gang Wang,et al.  Semiflexible polymer confined to a spherical surface. , 2003, Physical review letters.

[8]  Adam Zlotnick,et al.  Theoretical aspects of virus capsid assembly , 2005, Journal of molecular recognition : JMR.

[9]  Stephen C Harvey,et al.  Structural and thermodynamic principles of viral packaging. , 2007, Structure.

[10]  Radu P. Mondescu,et al.  Brownian motion and polymer statistics on certain curved manifolds , 1998, cond-mat/9804050.

[11]  W. Gelbart,et al.  Origin of icosahedral symmetry in viruses. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[12]  R. Bruinsma,et al.  Structural transitions of encapsidated polyelectrolytes , 2008, The European physical journal. E, Soft matter.

[13]  David Reguera,et al.  Classical nucleation theory of virus capsids. , 2006, Biophysical journal.

[14]  R. H. Watson,et al.  Conformation of DNA packaged in bacteriophage T7. Analysis by use of ultraviolet light-induced DNA-capsid cross-linking. , 1992, Journal of molecular biology.

[15]  F. Quiocho,et al.  Architecture of the herpes simplex virus major capsid protein derived from structural bioinformatics. , 2003, Journal of molecular biology.

[16]  P. Linse,et al.  Monte Carlo simulations of flexible polyelectrolytes inside viral capsids with dodecahedral charge distribution. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[17]  S. Harvey,et al.  Investigation of viral DNA packaging using molecular mechanics models. , 2002, Biophysical chemistry.

[18]  Sharon C Glotzer,et al.  Simulation studies of the self-assembly of cone-shaped particles. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[19]  N H Dekker,et al.  Single-molecule measurements of the persistence length of double-stranded RNA. , 2005, Biophysical journal.

[20]  S. Harrison,et al.  DNA arrangement in isometric phage heads , 1977, Nature.

[21]  Liang Tang,et al.  The structure of Pariacoto virus reveals a dodecahedral cage of duplex RNA , 2000, Nature Structural Biology.

[22]  R Twarock,et al.  Master equation approach to the assembly of viral capsids. , 2006, Journal of theoretical biology.

[23]  Sharon C. Glotzer,et al.  A precise packing sequence for self-assembled convex structures , 2007, Proceedings of the National Academy of Sciences.

[24]  J. Skolnick,et al.  Electrostatic Persistence Length of a Wormlike Polyelectrolyte , 1977 .

[25]  J M Yeomans,et al.  Polymer packaging and ejection in viral capsids: shape matters. , 2006, Physical review letters.

[26]  David R Nelson,et al.  Virus shapes and buckling transitions in spherical shells. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[27]  Rob Phillips,et al.  Mechanics of DNA packaging in viruses , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[28]  W. Kegel,et al.  Competing hydrophobic and screened-coulomb interactions in hepatitis B virus capsid assembly. , 2004, Biophysical journal.

[29]  A. Zlotnick,et al.  Weak protein-protein interactions are sufficient to drive assembly of hepatitis B virus capsids. , 2002, Biochemistry.

[30]  T S Baker,et al.  The structure of isometric capsids of bacteriophage T4. , 2001, Virology.

[31]  S. Harvey,et al.  Packaging of DNA by bacteriophage epsilon15: structure, forces, and thermodynamics. , 2007, Structure.

[32]  A. Evilevitch,et al.  Measuring the Force Ejecting DNA from Phage , 2004 .

[33]  Klaus Schulten,et al.  Stability and dynamics of virus capsids described by coarse-grained modeling. , 2006, Structure.

[34]  R. Twarock,et al.  Assembly models for Papovaviridae based on tiling theory , 2005, Physical biology.

[35]  William M. Gelbart,et al.  DNA packaging and ejection forces in bacteriophage , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[36]  A. Slosar,et al.  On the connected-charges Thomson problem , 2006, Europhysics Letters (EPL).

[37]  T S Baker,et al.  Reconstruction of the three-dimensional structure of simian virus 40 and visualization of the chromatin core. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[38]  A. McPherson Micelle formation and crystallization as paradigms for virus assembly. , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[39]  P. Linse,et al.  Packaging of a flexible polyelectrolyte inside a viral capsid: effect of salt concentration and salt valence. , 2007, The journal of physical chemistry. B.

[40]  Davide Marenduzzo,et al.  Thermodynamics of DNA packaging inside a viral capsid: the role of DNA intrinsic thickness. , 2003, Journal of molecular biology.

[41]  R Twarock,et al.  A tiling approach to virus capsid assembly explaining a structural puzzle in virology. , 2004, Journal of theoretical biology.

[42]  S. Harvey,et al.  DNA organization and thermodynamics during viral packing. , 2007, Biophysical journal.

[43]  C. Brooks,et al.  Deciphering the kinetic mechanism of spontaneous self-assembly of icosahedral capsids. , 2007, Nano letters (Print).

[44]  R. Metzler,et al.  Helical packaging of semiflexible polymers in bacteriophages , 2004, European Biophysics Journal.

[45]  John E. Johnson,et al.  Virus Particle Explorer (VIPER), a Website for Virus Capsid Structures and Their Computational Analyses , 2001, Journal of Virology.

[46]  W. Gelbart,et al.  Continuum theory of retroviral capsids. , 2006, Physical review letters.

[47]  Carlos Bustamante,et al.  Supplemental data for : The Bacteriophage ø 29 Portal Motor can Package DNA Against a Large Internal Force , 2001 .

[48]  J. King,et al.  The structural organization of DNA packaged within the heads of T4 wild-type, isometric and giant bacteriophages , 1978, Cell.

[49]  Kenneth H Downing,et al.  Three-dimensional architecture of the bacteriophage phi29 packaged genome and elucidation of its packaging process. , 2008, Virology.

[50]  W. R. Wikoff,et al.  Imaging RNA and dynamic protein segments with low-resolution virus crystallography: experimental design, data processing and implications of electron density maps. , 1998, Journal of molecular biology.

[51]  Michael G Rossmann,et al.  Molecular architecture of the prolate head of bacteriophage T4. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Kinetics of viral self-assembly: role of the single-stranded RNA antenna. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[53]  Javier Arsuaga,et al.  DNA knots reveal a chiral organization of DNA in phage capsids. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[54]  S. Harvey,et al.  The conformation of double-stranded DNA inside bacteriophages depends on capsid size and shape. , 2007, Journal of structural biology.

[55]  Martin Phillips,et al.  Measurements of DNA lengths remaining in a viral capsid after osmotically suppressed partial ejection. , 2005, Biophysical journal.

[56]  M. Vázquez,et al.  Knotting probability of DNA molecules confined in restricted volumes: DNA knotting in phage capsids , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[57]  D. Chandler,et al.  Dynamic pathways for viral capsid assembly. , 2005, Biophysical journal.

[58]  G. S. Manning A procedure for extracting persistence lengths from light-scattering data on intermediate molecular weight DNA , 1981 .

[59]  R. Consigli,et al.  Use of the baculovirus system to assemble polyomavirus capsid-like particles with different polyomavirus structural proteins: analysis of the recombinant assembled capsid-like particles. , 1999, The Journal of general virology.

[60]  R. Bruinsma,et al.  Monte Carlo simulations of polyelectrolytes inside viral capsids. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[61]  P. Stockley,et al.  Multiple presentation of foreign peptides on the surface of an RNA-free spherical bacteriophage capsid. , 1993, The Journal of general virology.

[62]  Russell Schwartz,et al.  Simulation study of the contribution of oligomer/oligomer binding to capsid assembly kinetics. , 2006, Biophysical journal.

[63]  M. Muthukumar,et al.  Langevin dynamics simulations of genome packing in bacteriophage. , 2006, Biophysical journal.

[64]  J. Rudnick,et al.  Icosahedral packing of RNA viral genomes. , 2003, Physical review letters.

[65]  G. S. Manning The persistence length of DNA is reached from the persistence length of its null isomer through an internal electrostatic stretching force. , 2006, Biophysical journal.

[66]  R. Bruinsma,et al.  Electrostatics and the assembly of an RNA virus. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[67]  Sherwood R. Casjens,et al.  DNA packaging by the double-stranded DNA bacteriophages , 1980, Cell.

[68]  S. Glotzer Some Assembly Required , 2004, Science.

[69]  David Reguera,et al.  Mechanical properties of viral capsids. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[70]  D L Caspar,et al.  Movement and self-control in protein assemblies. Quasi-equivalence revisited. , 1980, Biophysical journal.

[71]  E. Katzav,et al.  A statistical approach to close packing of elastic rods and to DNA packaging in viral capsids , 2006, Proceedings of the National Academy of Sciences.

[72]  Henk Koerten,et al.  Visualization by cryo-electron microscopy of genomic RNA that binds to the protein capsid inside bacteriophage MS2. , 2003, Journal of molecular biology.

[73]  Stephen C Harvey,et al.  Packaging double‐helical DNA into viral capsids , 2004, Biopolymers.

[74]  T. Odijk Polyelectrolytes near the rod limit , 1977 .

[75]  D. Porschke Structure and dynamics of double helices in solution: modes of DNA bending. , 1986, Journal of biomolecular structure & dynamics.

[76]  Peter L. Freddolino,et al.  Molecular dynamics simulations of the complete satellite tobacco mosaic virus. , 2006, Structure.

[77]  S. Larson,et al.  Crystallization of Brome mosaic virus and T = 1 Brome mosaic virus particles following a structural transition. , 2001, Virology.

[78]  B. Trus,et al.  Assembly of the Herpes Simplex Virus Procapsid from Purified Components and Identification of Small Complexes Containing the Major Capsid and Scaffolding Proteins , 1999, Journal of Virology.

[79]  R. Bruinsma Physics of RNA and viral assembly , 2006, The European physical journal. E, Soft matter.

[80]  John E. Johnson,et al.  Supramolecular self-assembly: molecular dynamics modeling of polyhedral shell formation , 1999 .

[81]  Zhen‐Gang Wang,et al.  DNA packaging in bacteriophage: is twist important? , 2005, Biophysical journal.

[82]  Michelle D. Wang,et al.  Stretching DNA with optical tweezers. , 1997, Biophysical journal.

[83]  William M Gelbart,et al.  Forces and pressures in DNA packaging and release from viral capsids. , 2003, Biophysical journal.

[84]  A. Klug,et al.  Physical principles in the construction of regular viruses. , 1962, Cold Spring Harbor symposia on quantitative biology.

[85]  J. Harpst,et al.  Effects of Na+ on the persistence length and excluded volume of T7 bacteriophage DNA , 1991, Biopolymers.

[86]  D. Rapaport,et al.  Self-assembly of polyhedral shells: a molecular dynamics study. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[87]  T. Odijk,et al.  Hexagonally packed DNA within bacteriophage T7 stabilized by curvature stress. , 1998, Biophysical journal.

[88]  Rob Phillips,et al.  Forces during bacteriophage DNA packaging and ejection. , 2004, Biophysical journal.

[89]  W. Gelbart,et al.  Packaging of a polymer by a viral capsid: the interplay between polymer length and capsid size. , 2008, Biophysical journal.

[90]  Derek N. Fuller,et al.  Ionic effects on viral DNA packaging and portal motor function in bacteriophage φ29 , 2007, Proceedings of the National Academy of Sciences.