Encapsulation of a polymer by an icosahedral virus

Physical Biology

Volumn 7, Issue 4, 2010, Pages

  Elrad, Oren M ^a   Hagan, Michael F ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MIRIDAE; RNA VIRUSES;

BIOPOLYMER; NUCLEIC ACID;

ARTICLE; CHEMICAL STRUCTURE; METABOLISM; PHYSIOLOGY; RNA VIRUS; VIRUS REPLICATION;

BIOPOLYMERS; MODELS, MOLECULAR; NUCLEIC ACIDS; RNA VIRUSES; VIRUS REPLICATION;

EID: 79551478383     PISSN: 14783967     EISSN: 14783975     Source Type: Journal    
DOI: 10.1088/1478-3975/7/4/045003     Document Type: Article

References (107)

1. Gupta B, Levchenko T S and Torchilin V P 2005 Intracellular delivery of large molecules and small particles by cell-penetrating proteins and peptides Adv. Drug Deliv. Rev. 57 637-51
2. Garcea R L and Gissmann L 2004 Virus-like particles as vaccines and vessels for the delivery of small molecules Curr. Opin. Biotechnol. 15 513-7
3. Dietz G P H and Bahr M 2004 Delivery of bioactive molecules into the cell: the Trojan horse approach Mol. Cell. Neurosci. 27 85-131
4. Soto C M, Blum A S, Vora G J, Lebedev N, Meador C E, Won A P, Chatterji A, Johnson J E and Ratna B R 2006 Fluorescent signal amplification of carbocyanine dyes using engineered viral nanoparticles J. Am. Chem. Soc. 128 5184-9
5. Sapsford K E, Soto C M, Blum A S, Chatterji A, Lin T W, Johnson J E, Ligler F S and Ratna B R 2006 A cowpea mosaic virus nanoscaffold for multiplexed antibody conjugation: application as an immunoassay tracer Biosens. Bioelectron. 21 1668-73
6. Boldogkoi Z, Sik A, Denes A, Reichart A, Toldi J, Gerendai I, Kovacs K J and Palkovits M 2004 Novel tracing paradigms-genetically engineered herpesviruses as tools for mapping functional circuits within the CNS: present status and future prospects Prog. Neurobiol. 72 417-45
7. Dragnea B, Chen C, Kwak E S, Stein B and Kao C C 2003 Gold nanoparticles as spectroscopic enhancers for in vitro studies on single viruses J. Am. Chem. Soc. 125 6374-5
8. Hiebert E, Bancroft J E and Bracker C E 1968 Assembly in vitro of some small spherical viruses hybrid viruses and other nucleoproteins Virology 34 492-509
9. Bancroft J B, Hiebert E and Bracker C E 1969 Effects of various polyanions on shell formation of some spherical viruses Virology 39 924-30
10. Dixit S K, Goicochea N L, Daniel M C, Murali A, Bronstein L, De M, Stein B, Rotello V M, Kao C C and Dragnea B 2006 Quantum dot encapsulation in viral capsids Nano Lett. 6 1993-9
11. Loo L, Guenther R H, Basnayake V R, Lommel S A and Franzen S 2006 Controlled encapsidation of gold nanoparticles by a viral protein shell J. Am. Chem. Soc. 128 4502-3
12. Goicochea N L, Mrinmoy DE, Rotello V M, Mukhopadhyay S and Dragnea B 2007 Core-like particles of an enveloped animal virus can self-assemble efficiently on artificial templates Nano Lett. 7 2281-90
13. Huang Xinlei et al 2007 Self-assembled virus-like particles with magnetic cores Nano Lett. 7 2407-16
14. Loo LiNa, Guenther R H, Lommel S A and Franzen S 2007 Encapsidation of nanoparticies by Red Clover Necrotic Mosaic Virus J. Am. Chem. Soc. 129 11111-7
15. Sikkema F D, Comellas-Aragones M, Fokkink R G, Verduin B J M, Cornelissen J J L M and Nolte R J M 2007 Monodisperse polymer-virus hybrid nanoparticles Org. Biomol. Chem. 5 54-7
16. Sun J et al 2007 Core-controlled polymorphism in virus-like particles Proc. Natl Acad. Sci. USA 104 1354-9
17. Yufang Hu, Zandi R, Anavitarte A, Knobler C M and Gelbart W M 2008 Packaging of a polymer by a viral capsid: the interplay between polymer length and capsid size Biophys. J. 94 1428-36
18. Comellas-Aragones M, De La Escosura A, Dirks A (Ton) J, van der Ham A, Fuste-Cune A, Cornelissen J J L M and Nolte R J M 2009 Controlled integration of polymers into viral capsids Biomacromolecules 10 3141-7
19. Crist R M, Datta S A K, Stephen A G, Soheilian F, Mirro J, Fisher R J, Nagashima K and Rein A 2009 Assembly properties of human immunodeficiency virus type 1 Gag-leucine zipper chimeras: implications for retrovirus assembly J. Virol. 83 2216-25
20. Chang C B, Knobler C M, Gelbart W M and Mason T G 2008 Curvature dependence of viral protein structures on encapsidated nanoemulsion droplets ACS Nano. 2 281-6
21. Freddolino P L, Arkhipov A S, and Larson S B, McPherson A and Schulten K 2006 Molecular dynamics simulations of the complete satellite tobacco mosaic virus Structure 14 437-49
22. Rapaport D C 2004 Self-assembly of polyhedral shells: a molecular dynamics study Phys. Rev. E. 70 051905
23. Nguyen H D, Reddy V S and Brooks C L 2007 Deciphering the kinetic mechanism of spontaneous self-assembly of icosahedral capsids Nano Lett. 7 338-44
24. Fox J M, Johnson J E and Young M J 1994 RNA/protein interactions in icosahedral virus assembly Semin. Virol. 5 51-60
25. Valegard K, Murray J B, Stonehouse N J, van den Worm S, Stockley P G and Liljas L 1997 The three-dimensional structures of two complexes between recombinant MS2 capsids and RNA operator fragments reveal sequence-specific protein-RNA interactions J. Mol. Biol. 270 724-38
26. Johnson K N, Tang L, Johnson J E and Ball L A 2004 Heterologous RNA encapsidated in Pariacoto virus-like particles forms a dodecahedral cage similar to genomic RNA in wild-type virions J. Virol. 78 11371-8
27. Tihova M, Dryden K A, Le T V L, Harvey S C, Johnson J E, Yeager M and Schneemann A 2004 Nodavirus coat protein imposes dodecahedral RNA structure independent of nucleotide sequence and length J. Virol. 78 2897-905
28. Krol M A, Olson N H, Tate J, Johnson J E, Baker T S and Ahlquist P 1999 RNA-controlled polymorphism in the in vivo assembly of 180-subunit and 120-subunit virions from a single capsid protein Proc. Natl Acad. Sci. USA 96 13650-5
29. Stockley P G, Rolfsson O, Thompson G S, Basnak G, Francese S, Stonehouse N J, Homans S W and Ashcroft A E 2007 A simple, RNA-mediated allosteric switch controls the pathway to formation of a t=3 viral capsid J. Mol. Biol. 369 541-52
30. Toropova K, Basnak G, Twarock R, Stockley P G and Ranson N A 2008 The three-dimensional structure of genomic RNA in bacteriophage MS2: implications for assembly J. Mol. Biol. 375 824-36
31. Larson S B, Lucas R W and McPherson A 2005 Crystallographic structure of the T = 1 particle of brome mosaic virus J. Mol. Biol. 346 815-31
32. Lucas R W, Larson S B and McPherson A 2002 The crystallographic structure of brome mosaic virus J. Mol. Biol. 317 95-108
33. Valegard K, Murray J B, Stockley P G, Stonehouse N J and Liljas L 1994 Crystal structure of a bacteriophage RNA coat protein operator complex Nature 371 623-6
34. van den Worm S H E, Stonehouse N J, Valegard K, Murray J B, Walton C, Fridborg K, Stockley P G and Liljas L 1998 Crystal structures of MS2 coat protein mutants in complex with wild-type RNA operator fragments Nucleic Acids Res. 26 1345-51
35. Grahn E et al 2001 Structural basis of pyrimidine specificity in the MS2 RNA hairpin-coat-protein complex RNA Soc. 7 1616-27
36. Helgstrand C, Grahn E, Moss T, Stonehouse N J, Tars K, Stockley P G and Liljas L 2002 Investigating the structural basis of purine specificity in the structures of MS2 coat protein RNA translational operator hairpins Nucleic Acids Res. 30 2678-85
37. Schneemann A 2006 The structural and functional role of RNA in icosahedral virus assembly Annu. Rev. Microbiol. 60 51-67
38. Zlotnick A, Cheng N, Stahl S J, Conway J F, Steven A C and Wingfield P T 1997 Localization of the C terminus of the assembly domain of hepatitis B virus capsid protein: implications for morphogenesis and organization of encapsidated RNA Proc. Natl Acad. Sci. USA 94 9556-61
39. Conway J F and Steven A C 1999 Methods for reconstructing density maps of 'single' particles from cryoelectron micrographs to subnanometer resolution J. Struct. Biol. 128 106-18
40. Devkota B, Petrov A S, Lemieux S, Boz M B, Tang L, Schneemann A, Johnson J E and Harvey S C 2009 Structural and electrostatic characterization of pariacoto virus: implications for viral assembly Biopolymers 91 530-8
41. Siber A and Podgornik R 2008 Nonspecific interactions in spontaneous assembly of empty versus functional single-stranded RNA viruses Phys. Rev. E 78 051915
42. Tao H, Zhang R and Shklovskii B I 2008 Electrostatic theory of viral self-assembly: a toy model Physica A 387 3059
43. Forrey C and Muthukumar M 2009 Electrostatics of capsid-induced viral RNA organization J. Chem. Phys.131
44. Harvey S C, Petrov A S, Devkota B and Boz M B 2009 Viral assembly: a molecular modeling perspective Phys. Chem. Chem. Phys. 11 10553-64
45. Belyi V A and Muthukumar M 2006 Electrostatic origin of the genome packing in viruses Proc. Natl Acad. Sci. USA 103 17174-8
46. Angelescu D G, Bruinsma R and Linse P 2006 Monte Carlo simulations of polyelectrolytes inside viral capsids Phys. Rev. E 73 041921
47. van der Schoot P and Bruinsma R 2005 Electrostatics and the assembly of an RNA virus Phys. Rev. E 71 061928
48. Zhang D Q, Konecny R, Baker N A and McCammon J A 2004 Electrostatic interaction between RNA and protein capsid in cowpea chlorotic mottle virus simulated by a coarse-grain RNA model and a Monte Carlo approach Biopolymers 75 325-37
49. Lee S and Nguyen T T 2008 Radial distribution of RNA genomes packaged inside spherical viruses Phys. Rev. Lett. 100 198102
50. Angelescu D G, Linse P, Nguyen T T and Bruinsma R F 2008 Structural transitions of encapsidated polyelectrolytes Eur. Phys. J. E 25 323-34
51. Jiang T, Wang Z G and Wu J Z 2009 Electrostatic regulation of genome packaging in human hepatitis b virus Biophys. J. 96 3065-73
52. Lorenzen K, Olia A S, Uetrecht C, Cingolani G and Heck A J R 2008 Determination of stoichiometry and conformational changes in the first step of the P22 tail assembly J. Mol. Biol. 379 385-96
53. Uetrecht C, Versluis C, Watts N R, Roos W H, Wuite G J L, Wingfield P T, Steven A C and Heck A J R 2008 High-resolution mass spectrometry of viral assemblies: molecular composition and stability of dimorphic hepatitis B virus capsids Proc. Natl Acad. Sci. USA 105 9216-20
54. Basnak G, Morton V L, Rolfsson O, Stonehouse N J, Ashcroft A E and Stockley P G 2010 Viral genomic single-stranded RNA directs the pathway toward a t = 3 capsid J. Mol. Biol. 395 924-36
55. Dykeman E C, Stockley P G and Twarock R 2010 Dynamic allostery controls coat protein conformer switching during MS2 phage assembly J. Mol. Biol. 395 916-23
56. Bancroft J B 1970 Adv. Virus Res. 16 99-134
57. Adolph K W and Butler P J G 1974 Studies on assembly of a spherical plant virus. 1. States of aggregation of isolated protein J. Mol. Biol. 88 327-88
58. Lavelle L, Gingery M, Phillips M, Gelbart W M, Knobler C M, Cadena-Nava R D, Vega-Acosta J R, Pinedo Torres L A and Ruiz-Garcia J 2009 Phase diagram of self-assembled viral capsid protein polymorphs J. Phys. Chem. B 113 3813-9
59. Rudnick J and Bruinsma R 2005 Icosahedral packing of RNA viral genomes Phys. Rev. Lett. 94 038101
60. Tao Hu and Shklovskii B I 2007 Kinetics of viral self-assembly: role of the single-stranded RNA antenna Phys. Rev. E 75 051901
61. Kivenson A and Hagan M F 2010 Mechanisms of viral capsid assembly around a polymer J. Biophys. 99 619-28
62. McPherson A 2005 Micelle formation and crystallization as paradigms for virus assembly Bioessays 27 447-58
63. Hagan M F 2008 Controlling viral capsid assembly with templating Phys. Rev. E 77 051904
64. Zlotnick A 2005 Theoretical aspects of virus capsid assembly J. Mol. Recognit. 18 479-90
65. Schwartz R, Shor P W, Prevelige P E and Berger B 1998 Local rules simulation of the kinetics of virus capsid self-assembly Biophys. J. 75 2626-36
66. Hagan M F and Chandler D 2006 Dynamic pathways for viral capsid assembly Biophys. J. 91 42-54
67. Hicks S D and Henley C L 2006 Irreversible growth model for virus capsid assembly Phys. Rev. E 74 031912
68. Wilber A W, Doye J P K, Louis A A, Noya E G, Miller M A and Wong P 2007 Reversible self-assembly of patchy particles into monodisperse icosahedral clusters J. Chem. Phys.127
69. Nguyen H D, Reddy V S and Brooks C L 2009 Invariant polymorphism in virus capsid assembly J. Am. Chem. Soc. 131 2606-14
70. Johnston I G, Louis A A and Doye J P K 2010 Modelling the self-assembly of virus capsids J Phys.: Condens. Matter 22 104101
71. Wilber A W, Doye J P K, Louis A A, Noya E G, Miller M A and Wong P 2007 Reversible self-assembly of patchy particles into monodisperse icosahedral clusters J. Chem. Phys. 127 085106
72. Zlotnick A 1994 To build a virus capsid-an equilibrium-model of the self-assembly of polyhedral protein complexes J. Mol. Biol. 241 59-67
73. Endres D and Zlotnick A 2002 Model-based analysis of assembly kinetics for virus capsids or other spherical polymers Biophys. J. 83 1217-30
74. Endres D, Miyahara M, Moisant P and Zlotnick A 2005 A reaction landscape identifies the intermediates critical for self-assembly of virus capsids and other polyhedral structures Protein Sci. 14 1518-25
75. Rapaport D C, Johnson J E and Skolnick J 1999 Supramolecular self-assembly: molecular dynamics modeling of polyhedral shell formation Comput. Phys. Commun. 122 231-5
76. Rapaport D C 2008 arXiv:0803.0115v2
77. Chen C, Daniel M C, Quinkert Z T, De M, Stein B, Bowman V D, Chipman P R, Rotello V M, Kao C C and Dragnea B 2006 Nanoparticle-templated assembly of viral protein cages Nano Lett. 6 611-5
78. Yoffe A M, Prinsen P, Gopal A, Knobler C M, Gelbart W M and Ben-Shaul A 2008 Predicting the sizes of large RNA molecules Proc. Natl Acad. Sci. USA 105 16153-8
79. Mannige R V and Brooks C L III 2008 Tilable nature of virus capsids and the role of topological constraints in natural capsid design Phys. Rev. E 77
80. Hariharan R, Biver C, Mays J and Russel W B 1998 Ionic strength and curvature effects in flat and highly curved polyelectrolyte brushes Macromolecules 31 7506-13
81. Humphrey W, Dalke A and Schulten K 1996 VMD: visual molecular dynamics J. Mol. Graph. 14 33-8
82. Reddy V S, Natarajan P, Okerberg B, Li K, Damodaran K V, Morton R T, Brooks C and Johnson J E 2001 Virus particle explorer (viper), a website for virus capsid structures and their computational analyses J. Virol. 75 11943-7
83. Branka A C and Heyes D M 1999 Algorithms for Brownian dynamics computer simulations: multivariable case Phys. Rev. E 60 2381-7
84. Heyes D M and Branka A C 2000 More efficient Brownian dynamics algorithms Mol. Phys. 98 1949-60
85. De La Torre J G and Carrasco B 2002 Hydrodynamic properties of rigid macromolecules composed of ellipsoidal and cylindrical subunits Biopolymers 63 163-7
86. Zandi R and van der Schoot P 2009 Size regulation of ss-RNA viruses Biophys. J. 96 9-20
87. Hagan M F 2009 A theory for viral capsid assembly around electrostatic cores J. Chem. Phys. 130 114902
88. Kumar S K, Szleifer I and Panagiotopoulos A Z 1991 Determination of the chemical potentials of polymeric systems from Monte-Carlo simulations Phys. Rev. Lett. 66 2935-8
89. Frenkel D and Smit B 2002 Understanding Molecular Simulation: From Algorithms to Applications 2nd edn (London: Academic)
90. Chandler D 1987 Introduction to Modern Statistical Mechanics 1st edn (Oxford: Oxford University Press)
91. Ceres P and Zlotnick A 2002 Weak protein-protein interactions are sufficient to drive assembly of hepatitis B virus capsids Biochemistry 41 11525-31
92. Kegel W K and van der Schoot P 2004 Competing hydrophobic and screened-coulomb interactions in hepatitis B virus capsid assembly Biophys. J. 86 3905-13
93. Erickson HP and Pantaloni D 1981 The role of subunit entropy in cooperative assembly-nucleation of microtubules and other two-dimensional polymers Biophys. J. 34 293-309
94. Ben-Tal N, Honig B, Bagdassarian C K and Ben-Shaul A 2000 Association entropy in adsorption processes Biophys. J. 79 1180-7
95. Parent K N, Zlotnick A and Teschke C M 2006 Quantitative analysis of multi-component spherical virus assembly: scaffolding protein contributes to the global stability of phage P22 procapsids J. Mol. Biol. 359 1097-106
96. Zlotnick A 2003 Are weak protein-protein interactions the general rule in capsid assembly? Virol. 315 269-74
97. Jack R L, Hagan M F and Chandler D 2007 Fluctuation-dissipation ratios in the dynamics of self-assembly Phys. Rev. E 76 021119
98. Hagan M F 2010 Understanding the concentration dependence of viral capsid assembly kinetics-the origin of the lag time and identifying the critical nucleus size Biophys. J. 98 1065-74
99. Kaper J M 1975 The chemical basis of virus structure, dissociation and reassembly Frontiers in Biology vol 39 (Amsterdam: North-Holland) pp 1-485
100. Johnson J E and Argos P 1985 The Plant Viruses Chapter Virus Particle Stability and Structure (New York: Plenum)
101. Zandi R, van der Schoot P, Reguera D, Kegel W and Reiss H 2006 Classical nucleation theory of virus capsids Biophys. J. 90 1939-48
102. Zlotnick A, Aldrich R, Johnson J M, Ceres P and Young M J 2000 Mechanism of capsid assembly for an icosahedral plant virus Virology 277 450-6
103. Sorger P K, Stockley P G and Harrison S C 1986 Structure and assembly of turnip crinkle virus. 2. Mechanism of reassembly in vitro J. Mol. Biol. 191 639-58
104. Dellago C, Bolhuis P G and Geissler P L 2002 Transition Path Sampling Advances in Chemical Physics vol 123 (New York: Wiley) pp 1-78
105. McGhee J D and Hippel P H V 1974 Theoretical aspects of DNA-protein interactions-cooperative and non-cooperative binding of large ligands to a one-dimensional homogeneous lattice J. Mol. Bioessays 86 469-89
106. Knobler C and Gelbart W 2010 Private communication
107. Zhang W, Olson N H, Baker T S, Faulkner L, Agbandje-McKenna M, Boulton M I, Davies J W and McKenna R 2001 Structure of the maize streak virus germinate particle Virology 279 471-7