1932

Abstract

Viruses are nanoscale entities containing a nucleic acid genome encased in a protein shell called a capsid and in some cases are surrounded by a lipid bilayer membrane. This review summarizes the physics that govern the processes by which capsids assemble within their host cells and in vitro. We describe the thermodynamics and kinetics for the assembly of protein subunits into icosahedral capsid shells and how these are modified in cases in which the capsid assembles around a nucleic acid or on a lipid bilayer. We present experimental and theoretical techniques used to characterize capsid assembly, and we highlight aspects of virus assembly that are likely to receive significant attention in the near future.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-physchem-040214-121637
2015-04-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/physchem/66/1/annurev-physchem-040214-121637.html?itemId=/content/journals/10.1146/annurev-physchem-040214-121637&mimeType=html&fmt=ahah

Literature Cited

  1. Ban N, McPherson A. 1.  1995. The structure of satellite panicum mosaic virus at 1.9 Å resolution. Nat. Struct. Mol. Biol. 2:882–90 [Google Scholar]
  2. Philippe N, Legendre M, Doutre G, Couté Y, Poirot O. 2.  et al. 2013. Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341:281–86 [Google Scholar]
  3. Fraenkel-Conrat H, Williams RC. 3.  1955. Reconstitution of active tobacco mosaic virus from its inactive protein and nucleic acid components. Proc. Natl. Acad. Sci. USA 41:690–98 [Google Scholar]
  4. Mateu MG. 4.  2013. Assembly, stability and dynamics of virus capsids. Arch. Biochem. Biophys. 531:65–79 [Google Scholar]
  5. Hagan MF. 5.  2014. Modeling viral capsid assembly. Adv. Chem. Phys. 155:1–68 [Google Scholar]
  6. Caspar DLD, Klug A. 6.  1962. Physical principles in construction of regular viruses. Cold Spring Harb. Symp. Quant. Biol. 27:1–24 [Google Scholar]
  7. Johnson JE, Speir JA. 7.  1997. Quasi-equivalent viruses: a paradigm for protein assemblies. J. Mol. Biol. 269:665–75 [Google Scholar]
  8. Zlotnick A. 8.  2005. Theoretical aspects of virus capsid assembly. J. Mol. Recognit. 18:479–90 [Google Scholar]
  9. Reddy VS, Natarajan P, Okerberg B, Li K, Damodaran KV. 9.  et al. 2001. Virus Particle Explorer (VIPER), a website for virus capsid structures and their computational analyses. J. Virol. 75:11943–47 [Google Scholar]
  10. Prevelige PE Jr, Thomas D, King J. 10.  1993. Nucleation and growth phases in the polymerization of coat and scaffolding subunits into icosahedral procapsid shells. Biophys. J. 64:824–35 [Google Scholar]
  11. Zlotnick A, Johnson JM, Wingfield PW, Stahl SJ, Endres D. 11.  1999. A theoretical model successfully identifies features of hepatitis B virus capsid assembly. Biochemistry 38:14644–52 [Google Scholar]
  12. Zlotnick A, Aldrich R, Johnson JM, Ceres P, Young MJ. 12.  2000. Mechanism of capsid assembly for an icosahedral plant virus. Virology 277:450–56 [Google Scholar]
  13. Casini GL, Graham D, Heine D, Garcea RL, Wu DT. 13.  2004. In vitro papillomavirus capsid assembly analyzed by light scattering. Virology 325:320–27 [Google Scholar]
  14. Chen C, Kao CC, Dragnea B. 14.  2008. Self-assembly of brome mosaic virus capsids: insights from shorter time-scale experiments. J. Phys. Chem. A 112:9405–12 [Google Scholar]
  15. Berthet-Colominas C, Cuillel M, Koch MHJ, Vachette P, Jacrot B. 15.  1987. Kinetic study of the self-assembly of brome mosaic virus capsid. Eur. Biophys. J. 15:159–68 [Google Scholar]
  16. Kler S, Asor R, Li C, Ginsburg A, Harries D. 16.  et al. 2012. RNA encapsidation by SV40-derived nanoparticles follows a rapid two-state mechanism. J. Am. Chem. Soc. 134:8823–30 [Google Scholar]
  17. Kler S, Wang JCY, Dhason M, Oppenheim A, Zlotnick A. 17.  2013. Scaffold properties are a key determinant of the size and shape of self-assembled virus-derived particles. ACS Chem. Biol. 8:2753–61 [Google Scholar]
  18. Zhou K, Li L, Tan Z, Zlotnick A, Jacobson SC. 18.  2011. Characterization of hepatitis B virus capsids by resistive-pulse sensing. J. Am. Chem. Soc. 133:1618–21 [Google Scholar]
  19. Stockley PG, Rolfsson O, Thompson GS, Basnak G, Francese S. 19.  et al. 2007. A simple, RNA-mediated allosteric switch controls the pathway to formation of a T = 3 viral capsid. J. Mol. Biol. 369:541–52 [Google Scholar]
  20. Basnak G, Morton VL, Rolfsson O, Stonehouse NJ, Ashcroft AE, Stockley PG. 20.  2010. Viral genomic single-stranded RNA directs the pathway toward a T = 3 capsid. J. Mol. Biol. 395:924–36 [Google Scholar]
  21. Uetrecht C, Barbu IM, Shoemaker GK, van Duijn E, Heck AJR. 21.  2011. Interrogating viral capsid assembly with ion mobility-mass spectrometry. Nat. Chem. 3:126–32 [Google Scholar]
  22. Tresset G, Le Coeur C, Bryche JF, Tatou M, Zeghal M. 22.  et al. 2013. Norovirus capsid proteins self-assemble through biphasic kinetics via long-lived stave-like intermediates. J. Am. Chem. Soc. 135:15373–81 [Google Scholar]
  23. Pierson EE, Keifer DZ, Selzer L, Lee LS, Contino NC. 23.  et al. 2014. Detection of late intermediates in virus capsid assembly by charge detection mass spectrometry. J. Am. Chem. Soc. 136:3536–41 [Google Scholar]
  24. Baumgärtel V, Müller B, Lamb DC. 24.  2012. Quantitative live-cell imaging of human immunodeficiency virus (HIV-1) assembly. Viruses 4:777–99 [Google Scholar]
  25. Jouvenet N, Simon SM, Bieniasz PD. 25.  2011. Visualizing HIV-1 assembly. J. Mol. Biol. 410:501–11 [Google Scholar]
  26. Borodavka A, Tuma R, Stockley PG. 26.  2012. Evidence that viral RNAs have evolved for efficient, two-stage packaging. Proc. Natl. Acad. Sci. USA 109:15769–74 [Google Scholar]
  27. Zlotnick A. 27.  1994. To build a virus capsid: an equilibrium model of the self-assembly of polyhedral protein complexes. J. Mol. Biol. 241:59–67 [Google Scholar]
  28. Endres D, Zlotnick A. 28.  2002. Model-based analysis of assembly kinetics for virus capsids or other spherical polymers. Biophys. J. 83:1217–30 [Google Scholar]
  29. Becker R, Döring W. 29.  1935. Kinetische Behandlung der Keimbildung in übersättigten Dämpfen. Ann. Phys. 416:719–52 [Google Scholar]
  30. van der Schoot P, Zandi R. 30.  2007. Kinetic theory of virus capsid assembly. Phys. Biol. 4:296–304 [Google Scholar]
  31. Morozov AY, Bruinsma RF, Rudnick J. 31.  2009. Assembly of viruses and the pseudo-law of mass action. J. Chem. Phys. 131:155101 [Google Scholar]
  32. Moisant P, Neeman H, Zlotnick A. 32.  2010. Exploring the paths of (virus) assembly. Biophys. J. 99:1350–57 [Google Scholar]
  33. Zhang Q, Gupta S, Emrick T, Russell T. 33.  2006. Surface-functionalized CdSe nanorods for assembly in diblock copolymer templates. J. Am. Chem. Soc. 128:3898–99 [Google Scholar]
  34. Keef T, Micheletti C, Twarock R. 34.  2006. Master equation approach to the assembly of viral capsids. J. Theor. Biol. 242:713–21 [Google Scholar]
  35. Hemberg M, Yaliraki S, Barahona M. 35.  2006. Stochastic kinetics of viral capsid assembly based on detailed protein structures. Biophys. J. 90:3029–42 [Google Scholar]
  36. Dykeman EC, Stockley PG, Twarock R. 36.  2013. Building a viral capsid in the presence of genomic RNA. Phys. Rev. E 87:022717 [Google Scholar]
  37. Smith GR, Xie L, Lee B, Schwartz R. 37.  2014. Applying molecular crowding models to simulations of virus capsid assembly in vitro. Biophys. J. 106:310–20 [Google Scholar]
  38. Bortz AB, Kalos MH, Lebowitz JL. 38.  1975. New algorithm for Monte Carlo simulation of Ising spin systems. J. Comput. Phys. 17:10–18 [Google Scholar]
  39. Gillespie DT. 39.  1977. Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem. 81:2340–61 [Google Scholar]
  40. Schwartz R, Shor PW, Prevelige PE Jr, Berger B. 40.  1998. Local rules simulation of the kinetics of virus capsid self-assembly. Biophys. J. 75:2626–36 [Google Scholar]
  41. Hagan MF, Chandler D. 41.  2006. Dynamic pathways for viral capsid assembly. Biophys. J. 91:42–54 [Google Scholar]
  42. Hicks SD, Henley CL. 42.  2006. Irreversible growth model for virus capsid assembly. Phys. Rev. E 74:031912 [Google Scholar]
  43. Nguyen HD, Reddy VS, Brooks CL. 43.  2007. Deciphering the kinetic mechanism of spontaneous self-assembly of icosahedral capsids. Nano Lett. 7:338–44 [Google Scholar]
  44. Wilber AW, Doye JPK, Louis AA, Noya EG, Miller MA, Wong P. 44.  2007. Reversible self-assembly of patchy particles into monodisperse icosahedral clusters. J. Chem. Phys. 127:085106 [Google Scholar]
  45. Nguyen HD, Reddy VS, Brooks CL. 45.  2009. Invariant polymorphism in virus capsid assembly. J. Am. Chem. Soc. 131:2606–14 [Google Scholar]
  46. Johnston IG, Louis AA, Doye JPK. 46.  2010. Modelling the self-assembly of virus capsids. J. Phys. Condens. Matter 22:104101 [Google Scholar]
  47. Rapaport DC, Johnson JE, Skolnick J. 47.  1999. Supramolecular self-assembly: molecular dynamics modeling of polyhedral shell formation. Comput. Phys. Commun. 122:231–35 [Google Scholar]
  48. Rapaport D. 48.  2008. The role of reversibility in viral capsid growth: a paradigm for self-assembly. Phys. Rev. Lett. 101:186101 [Google Scholar]
  49. Elrad O, Hagan MF. 49.  2010. Encapsulation of a polymer by an icosahedral virus. Phys. Biol. 7:045003 [Google Scholar]
  50. Mahalik JP, Muthukumar M. 50.  2012. Langevin dynamics simulation of polymer-assisted virus-like assembly. J. Chem. Phys. 136:135101 [Google Scholar]
  51. Rapaport DC. 51.  2012. Molecular dynamics simulation of reversibly self-assembling shells in solution using trapezoidal particles. Phys. Rev. E 86:051917 [Google Scholar]
  52. Perkett MR, Hagan MF. 52.  2014. Using Markov state models to study self-assembly. J. Chem. Phys. 140:214101 [Google Scholar]
  53. Lavelle L, Gingery M, Phillips M, Gelbart WM, Knobler CM. 53.  et al. 2009. Phase diagram of self-assembled viral capsid protein polymorphs. J. Phys. Chem. B 113:3813–19 [Google Scholar]
  54. Safran S. 54.  1994. Statistical Thermodynamics of Surfaces, Interfaces, and Membranes New York: Addison-Wesley
  55. Bruinsma RF, Gelbart WM, Reguera D, Rudnick J, Zandi R. 55.  2003. Viral self-assembly as a thermodynamic process. Phys. Rev. Lett. 90:248101 [Google Scholar]
  56. Ceres P, Zlotnick A. 56.  2002. Weak protein-protein interactions are sufficient to drive assembly of hepatitis B virus capsids. Biochemistry 41:11525–31 [Google Scholar]
  57. Whitelam S, Jack RL. 57.  2015. The statistical mechanics of dynamic pathways to self-assembly. Annu. Rev. Phys. Chem. 66:143–63 [Google Scholar]
  58. del Alamo M, Mateu MG. 58.  2005. Electrostatic repulsion, compensatory mutations, and long-range non-additive effects at the dimerization interface of the HIV capsid protein. J. Mol. Biol. 345:893–906 [Google Scholar]
  59. Kegel WK, van der Schoot P. 59.  2006. Physical regulation of the self-assembly of tobacco mosaic virus coat protein. Biophys. J. 91:1501–12 [Google Scholar]
  60. Chandler D. 60.  2005. Interfaces and the driving force of hydrophobic assembly. Nature 437:640–47 [Google Scholar]
  61. Hagan MF. 61.  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 [Google Scholar]
  62. Zandi R, van der Schoot P, Reguera D, Kegel W, Reiss H. 62.  2006. Classical nucleation theory of virus capsids. Biophys. J. 90:1939–48 [Google Scholar]
  63. Singh S, Zlotnick A. 63.  2003. Observed hysteresis of virus capsid disassembly is implicit in kinetic models of assembly. J. Biol. Chem. 278:18249–55 [Google Scholar]
  64. Uetrecht C, Watts NR, Stahl SJ, Wingfield PT, Steven AC, Heck AJR. 64.  2010. Subunit exchange rates in hepatitis B virus capsids are geometry- and temperature-dependent. Phys. Chem. Chem. Phys. 12:13368–71 [Google Scholar]
  65. Whitelam S, Rogers C, Pasqua A, Paavola C, Trent J, Geissler PL. 65.  2009. The impact of conformational fluctuations on self-assembly: cooperative aggregation of archaeal chaperonin proteins. Nano Lett. 9:292–97 [Google Scholar]
  66. Sorger PK, Stockley PG, Harrison SC. 66.  1986. Structure and assembly of turnip crinkle virus. II. Mechanism of reassembly in vitro. J. Mol. Biol. 191:639–58 [Google Scholar]
  67. Stray SJ, Bourne CR, Punna S, Lewis WG, Finn MG, Zlotnick A. 67.  2005. A heteroaryldihydropyrimidine activates and can misdirect hepatitis B virus capsid assembly. Proc. Natl. Acad. Sci. USA 102:8138–43 [Google Scholar]
  68. Parent KN, Suhanovsky MM, Teschke CM. 68.  2007. Polyhead formation in phage P22 pinpoints a region in coat protein required for conformational switching. Mol. Microbiol. 65:1300–10 [Google Scholar]
  69. Zlotnick A. 69.  2003. Are weak protein-protein interactions the general rule in capsid assembly?. Virology 315:269–74 [Google Scholar]
  70. Ruigrok RWH, Crepin T, Kolakofsky D. 70.  2011. Nucleoproteins and nucleocapsids of negative-strand RNA viruses. Curr. Opin. Microbiol. 14:504–10 [Google Scholar]
  71. Speir JA, Munshi S, Wang GJ, Baker TS, Johnson JE. 71.  1995. Structures of the native and swollen forms of cowpea chlorotic mottle virus determined by X-ray crystallography and cryoelectron microscopy. Structure 3:63–78 [Google Scholar]
  72. Hohn T. 72.  1969. Role of RNA in the assembly process of bacteriophage fr. J. Mol. Biol. 43:191–200 [Google Scholar]
  73. Bancroft J, Hiebert E, Bracker CE. 73.  1969. The effects of various polyanions on shell formation of some spherical viruses. Virology 39:924–30 [Google Scholar]
  74. Chen C, Kwak ES, Stein B, Kao CC, Dragnea B. 74.  2005. Packaging of gold particles in viral capsids. J. Nanosci. Nanotechnol. 5:2029–33 [Google Scholar]
  75. Sun J, DuFort C, Daniel MC, Murali A, Chen C. 75.  et al. 2007. Core-controlled polymorphism in virus-like particles. Proc. Natl. Acad. Sci. USA 104:1354–59 [Google Scholar]
  76. Hu Y, Zandi R, Anavitarte A, Knobler CM, Gelbart WM. 76.  2008. Packaging of a polymer by a viral capsid: the interplay between polymer length and capsid size. Biophys. J. 94:1428–36 [Google Scholar]
  77. Sikkema FD, Comellas-Aragones M, Fokkink RG, Verduin BJM, Cornelissen JJLM, Nolte RJM. 77.  2007. Monodisperse polymer-virus hybrid nanoparticles. Org. Biomol. Chem. 5:54–57 [Google Scholar]
  78. Brasch M, Cornelissen JJLM. 78.  2012. Relative size selection of a conjugated polyelectrolyte in virus-like protein structures. Chem. Commun. 48:1446–48 [Google Scholar]
  79. Kostiainen MA, Pietsch C, Hoogenboom R, Nolte RJM, Cornelissen JJLM. 79.  2011. Temperature-switchable assembly of supramolecular virus-polymer complexes. Adv. Funct. Mater. 21:2012–19 [Google Scholar]
  80. Goicochea NL, De M, Rotello VM, Mukhopadhyay S, Dragnea B. 80.  2007. Core-like particles of an enveloped animal virus can self-assemble efficiently on artificial templates. Nano Lett. 7:2281–90 [Google Scholar]
  81. Loo L, Guenther RH, Lommel SA, Franzen S. 81.  2007. Encapsidation of nanoparticles by red clover necrotic mosaic virus. J. Am. Chem. Soc. 129:11111–17 [Google Scholar]
  82. Kwak M, Minten IJ, Anaya DM, Musser AJ, Brasch M. 82.  et al. 2010. Virus-like particles templated by DNA micelles: a general method for loading virus nanocarriers. J. Am. Chem. Soc. 132:7834–35 [Google Scholar]
  83. Chang CB, Knobler CM, Gelbart WM, Mason TG. 83.  2008. Curvature dependence of viral protein structures on encapsidated nanoemulsion droplets. ACS Nano 2:281–86 [Google Scholar]
  84. Malyutin AG, Dragnea B. 84.  2013. Budding pathway in the templated assembly of viruslike particles. J. Phys. Chem. B 117:10730–36 [Google Scholar]
  85. Cheng F, Tsvetkova IB, Khuong YL, Moore AW, Arnold RJ. 85.  et al. 2013. The packaging of different cargo into enveloped viral nanoparticles. Mol. Pharm. 10:51–58 [Google Scholar]
  86. Siber A, Bozic AL, Podgornik R. 86.  2012. Energies and pressures in viruses: contribution of nonspecific electrostatic interactions. Phys. Chem. Chem. Phys. 14:3746–65 [Google Scholar]
  87. Zandi R, van der Schoot P. 87.  2009. Size regulation of ss-RNA viruses. Biophys. J. 96:9–20 [Google Scholar]
  88. Hagan MF. 88.  2009. A theory for viral capsid assembly around electrostatic cores. J. Chem. Phys. 130:114902 [Google Scholar]
  89. Zlotnick A, Porterfield JZ, Wang JCY. 89.  2013. To build a virus on a nucleic acid substrate. Biophys. J. 104:1595–604 [Google Scholar]
  90. Belyi VA, Muthukumar M. 90.  2006. Electrostatic origin of the genome packing in viruses. Proc. Natl. Acad. Sci. USA 103:17174–78 [Google Scholar]
  91. Hu T, Zhang R, Shklovskii BI. 91.  2008. Electrostatic theory of viral self-assembly. Physica A 387:3059–64 [Google Scholar]
  92. Newman M, Chua PK, Tang FM, Su PY, Shih C. 92.  2009. Testing an electrostatic interaction hypothesis of hepatitis B virus capsid stability by using an in vitro capsid disassembly/reassembly system. J. Virol. 83:10616–26 [Google Scholar]
  93. Venter PA, Marshall D, Schneemann A. 93.  2009. Dual roles for an arginine-rich motif in specific genome recognition and localization of viral coat protein to RNA replication sites in flock house virus-infected cells. J. Virol. 83:2872–82 [Google Scholar]
  94. Le Pogam S, Chua PK, Newman M, Shih C. 94.  2005. Exposure of RNA templates and encapsidation of spliced viral RNA are influenced by the arginine-rich domain of human hepatitis B virus core antigen (HBcAg 165–173). J. Virol. 79:1871–87 [Google Scholar]
  95. Ni P, Wang Z, Ma X, Das NC, Sokol P. 95.  et al. 2012. An examination of the electrostatic interactions between the N-terminal tail of the coat protein and RNA in brome mosaic virus. J. Mol. Biol. 419:284–300 [Google Scholar]
  96. Porterfield JZ, Dhason MS, Loeb DD, Nassal M, Stray SJ, Zlotnick A. 96.  2010. Full-length hepatitis B virus core protein packages viral and heterologous RNA with similarly high levels of cooperativity. J. Virol. 84:7174–84 [Google Scholar]
  97. Kao CC, Ni P, Hema M, Huang XL, Dragnea B. 97.  2011. The coat protein leads the way: an update on basic and applied studies with the brome mosaic virus coat protein. Mol. Plant Pathol. 12:403–12 [Google Scholar]
  98. Comas-Garcia M, Cadena-Nava RD, Rao ALN, Knobler CM, Gelbart WM. 98.  2012. In vitro quantification of the relative packaging efficiencies of single-stranded RNA molecules by viral capsid protein. J. Virol. 86:12271–82 [Google Scholar]
  99. Perlmutter JD, Qiao C, Hagan MF. 99.  2013. Viral genome structures are optimal for capsid assembly. eLife 2:e00632 [Google Scholar]
  100. van der Schoot P, Bruinsma R. 100.  2005. Electrostatics and the assembly of an RNA virus. Phys. Rev. E 71:061928 [Google Scholar]
  101. Siber A, Podgornik R. 101.  2008. Nonspecific interactions in spontaneous assembly of empty versus functional single-stranded RNA viruses. Phys. Rev. E 78:051915 [Google Scholar]
  102. Ting CL, Wu J, Wang ZG. 102.  2011. Thermodynamic basis for the genome to capsid charge relationship in viral encapsidation. Proc. Natl. Acad. Sci. USA 108:16986–91 [Google Scholar]
  103. Manning GS. 103.  1969. Limiting laws and counterion condensation in polyelectrolyte solutions I. Colligative properties. J. Chem. Phys. 51:924–33 [Google Scholar]
  104. Gopal A, Zhou Z, Knobler C, Gelbart W. 104.  2012. Visualizing large RNA molecules in solution. RNA 18:284–99 [Google Scholar]
  105. Erdemci-Tandogan G, Wagner J, van der Schoot P, Podgornik R, Zandi R. 105.  2014. RNA topology remolds electrostatic stabilization of viruses. Phys. Rev. E 89:032707 [Google Scholar]
  106. Yoffe AM, Prinsen P, Gopal A, Knobler CM, Gelbart WM, Ben-Shaul A. 106.  2008. Predicting the sizes of large RNA molecules. Proc. Natl. Acad. Sci. USA 105:16153–58 [Google Scholar]
  107. Stehle T, Gamblin SJ, Yan YW, Harrison SC. 107.  1996. The structure of simian virus 40 refined at 3.1 Å resolution. Structure 4:165–82 [Google Scholar]
  108. Cadena-Nava RD, Comas-Garcia M, Garmann RF, Rao ALN, Knobler CM, Gelbart WM. 108.  2012. Self-assembly of viral capsid protein and RNA molecules of different sizes: requirement for a specific high protein/RNA mass ratio. J. Virol. 86:3318–26 [Google Scholar]
  109. Garmann RF, Comas-Garcia M, Gopal A, Knobler CM, Gelbart WM. 109.  2014. The assembly pathway of an icosahedral single-stranded RNA virus depends on the strength of inter-subunit attractions. J. Mol. Biol. 426:1050–60 [Google Scholar]
  110. Perlmutter JD, Perkett MR, Hagan MF. 110.  2014. Pathways for virus assembly around nucleic acids. J. Mol. Biol. 426:3148–65 [Google Scholar]
  111. Zhang R, Linse P. 111.  2013. Icosahedral capsid formation by capsomers and short polyions. J. Chem. Phys. 138:154901 [Google Scholar]
  112. Zhang R, Wernersson E, Linse P. 112.  2013. Icosahedral capsid formation by capsomer subunits and a semiflexible polyion. RSC Adv. 3:25258–67 [Google Scholar]
  113. Comas-Garcia M, Garmann RF, Singaram SW, Ben-Shaul A, Knobler CM, Gelbart WM. 113.  2014. Characterization of viral capsid protein self-assembly around short single-stranded RNA. J. Phys. Chem. B 118:7510–19 [Google Scholar]
  114. Kivenson A, Hagan M. 114.  2010. Mechanisms of viral capsid assembly around a polymer. Biophys. J. 99:619–28 [Google Scholar]
  115. Hu T, Shklovskii BI. 115.  2007. Kinetics of viral self-assembly: role of the single-stranded RNA antenna. Phys. Rev. E 75:051901 [Google Scholar]
  116. McPherson A. 116.  2005. Micelle formation and crystallization as paradigms for virus assembly. Bioessays 27:447–58 [Google Scholar]
  117. Hagan MF. 117.  2008. Controlling viral capsid assembly with templating. Phys. Rev. E 77:051904 [Google Scholar]
  118. Devkota B, Petrov AS, Lemieux S, Boz MB, Tang L. 118.  et al. 2009. Structural and electrostatic characterization of pariacoto virus: implications for viral assembly. Biopolymers 91:530–38 [Google Scholar]
  119. Garmann RF, Comas-Garcia M, Koay MS, Cornelissen JJLM, Knobler CM, Gelbart WM. 119.  2014. The role of electrostatics in the assembly pathway of a single-stranded RNA virus. J. Virol. 88:10472–79 [Google Scholar]
  120. Routh A, Domitrovic T, Johnson JE. 120.  2012. Host RNAs, including transposons, are encapsidated by a eukaryotic single-stranded RNA virus. Proc. Natl. Acad. Sci. USA 109:1907–12 [Google Scholar]
  121. Larson SB, Koszelak S, Day J, Greenwood A, Dodds JA, McPherson A. 121.  1993. Double-helical RNA in satellite tobacco mosaic virus. Nature 361:179–82 [Google Scholar]
  122. Larson SB, Day J, Greenwood A, McPherson A. 122.  1998. Refined structure of satellite tobacco mosaic virus at 1.8 Å resolution. J. Mol. Biol. 277:37–59 [Google Scholar]
  123. Larson SB, McPherson A. 123.  2001. Satellite tobacco mosaic virus RNA: structure and implications for assembly. Curr. Opin. Struct. Biol. 11:59–65 [Google Scholar]
  124. Schroeder SJ, Stone JW, Bleckley S, Gibbons T, Mathews DM. 124.  2011. Ensemble of secondary structures for encapsidated satellite tobacco mosaic virus RNA consistent with chemical probing and crystallography constraints. Biophys. J. 101:167–75 [Google Scholar]
  125. Zeng Y, Larson S, Heitsch C, McPherson A, Harvey S. 125.  2012. A model for the structure of satellite tobacco mosaic virus. J. Struct. Biol. 180:110–16 [Google Scholar]
  126. Archer EJ, Simpson MA, Watts NJ, O'Kane R, Wang B. 126.  et al. 2013. Long-range architecture in a viral RNA genome. Biochemistry 52:3182–90 [Google Scholar]
  127. Athavale SS, Gossett JJ, Bowman JC, Hud NV, Williams LD, Harvey SC. 127.  2013. In vitro secondary structure of the genomic RNA of satellite tobacco mosaic virus. PLoS ONE 8:e54384 [Google Scholar]
  128. Rao A. 128.  2006. Genome packaging by spherical plant RNA viruses. Annu. Rev. Phytopathol. 44:61–87 [Google Scholar]
  129. Stockley PG, Twarock R, Bakker SE, Barker AM, Borodavka A. 129.  et al. 2013. Packaging signals in single-stranded RNA viruses: nature's alternative to a purely electrostatic assembly mechanism. J. Biol. Phys. 39:277–87 [Google Scholar]
  130. Pappalardo L, Kerwood DJ, Pelczer I, Borer PN. 130.  1998. Three-dimensional folding of an RNA hairpin required for packaging HIV-1. J. Mol. Biol. 282:801–18 [Google Scholar]
  131. Lu K, Heng X, Summers MF. 131.  2011. Structural determinants and mechanism of HIV-1 genome packaging. J. Mol. Biol. 410:609–33 [Google Scholar]
  132. D'Souza V, Summers MF. 132.  2005. How retroviruses select their genomes. Nat. Rev. Microbiol. 3:643–55 [Google Scholar]
  133. Bunka DHJ, Lane SW, Lane CL, Dykeman EC, Ford RJ. 133.  et al. 2011. Degenerate RNA packaging signals in the genome of satellite tobacco necrosis virus: implications for the assembly of a T = 1 capsid. J. Mol. Biol. 413:51–65 [Google Scholar]
  134. Dykeman EC, Grayson NE, Toropova K, Ranson NA, Stockley PG, Twarock R. 134.  2011. Simple rules for efficient assembly predict the layout of a packaged viral RNA. J. Mol. Biol. 408:399–407 [Google Scholar]
  135. Dykeman EC, Stockley PG, Twarock R. 135.  2013. Packaging signals in two single-stranded RNA viruses imply a conserved assembly mechanism and geometry of the packaged genome. J. Mol. Biol. 425:3235–49 [Google Scholar]
  136. ElSawy KM, Caves LSD, Twarock R. 136.  2010. The impact of viral RNA on the association rates of capsid protein assembly: bacteriophage MS2 as a case study. J. Mol. Biol. 400:935–47 [Google Scholar]
  137. Morton VL, Dykeman EC, Stonehouse NJ, Ashcroft AE, Twarock R, Stockley PG. 137.  2010. The impact of viral RNA on assembly pathway selection. J. Mol. Biol. 401:298–308 [Google Scholar]
  138. Dykeman EC, Stockley PG, Twarock R. 138.  2014. Solving a Levinthal's paradox for virus assembly identifies a unique antiviral strategy. Proc. Natl. Acad. Sci. USA 111:5361–66 [Google Scholar]
  139. Johnson JM, Willits DA, Young MJ, Zlotnick A. 139.  2004. Interaction with capsid protein alters RNA structure and the pathway for in vitro assembly of cowpea chlorotic mottle virus. J. Mol. Biol. 335:455–64 [Google Scholar]
  140. Annamalai P, Rofail F, DeMason DA, Rao ALN. 140.  2008. Replication-coupled packaging mechanism in positive-strand RNA viruses: synchronized coexpression of functional multigenome RNA components of an animal and a plant virus in Nicotiana benthamiana cells by agroinfiltration. J. Virol. 82:1484–95 [Google Scholar]
  141. Hurley JH, Boura E, Carlson LA, Róycki B. 141.  2010. Membrane budding. Cell 143:875–87 [Google Scholar]
  142. Sundquist WI, Krausslich HG. 142.  2012. HIV-1 assembly, budding, and maturation. Cold Spring Harb. Perspect. Med. 2:a006924 [Google Scholar]
  143. Welsch S, Müller B, Kräusslich HG. 143.  2007. More than one door: budding of enveloped viruses through cellular membranes. FEBS Lett. 581:2089–97 [Google Scholar]
  144. Garoff H, Sjöberg M, Cheng RH. 144.  2004. Budding of alphaviruses. Virus Res. 106:103–16 [Google Scholar]
  145. McMahon HT, Gallop JL. 145.  2005. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438:590–96 [Google Scholar]
  146. Doherty GJ, McMahon HT. 146.  2009. Mechanisms of endocytosis. Annu. Rev. Biochem. 78:857–902 [Google Scholar]
  147. Taylor MP, Koyuncu OO, Enquist LW. 147.  2011. Subversion of the actin cytoskeleton during viral infection. Nat. Rev. Microbiol. 9:427–39 [Google Scholar]
  148. Gladnikoff M, Shimoni E, Gov NS, Rousso I. 148.  2009. Retroviral assembly and budding occur through an actin-driven mechanism. Biophys. J. 97:2419–28 [Google Scholar]
  149. Balasubramaniam M, Freed EO. 149.  2011. New insights into HIV assembly and trafficking. Physiology 26:236–51 [Google Scholar]
  150. Rossman JS, Lamb RA. 150.  2013. Viral membrane scission. Annu. Rev. Cell Dev. Biol. 29:551–69 [Google Scholar]
  151. Matthews R, Likos C. 151.  2012. Influence of fluctuating membranes on self-assembly of patchy colloids. Phys. Rev. Lett. 109:178302 [Google Scholar]
  152. Matthews R, Likos CN. 152.  2013. Dynamics of self-assembly of model viral capsids in the presence of a fluctuating membrane. J. Phys. Chem. B 117:8283–92 [Google Scholar]
  153. Ruiz-Herrero T, Hagan MF. 153.  2014. Virus assembly on a membrane is facilitated by membrane microdomains. Biophys. J. In press. doi: 10.1016/j.bpj.2014.12.017
  154. Helfrich W. 154.  1973. Elastic properties of lipid bilayers: theory and possible experiments. Z. Nat. C 28:693–703 [Google Scholar]
  155. Tzlil S, Deserno M, Gelbart WM, Ben-Shaul A. 155.  2004. A statistical-thermodynamic model of viral budding. Biophys. J. 86:2037–48 [Google Scholar]
  156. Lerner DM, Deutsch JM, Oster GF. 156.  1993. How does a virus bud?. Biophys. J. 65:73–79 [Google Scholar]
  157. Barrow E, Nicola AV, Liu J. 157.  2013. Multiscale perspectives of virus entry via endocytosis. Virol. J. 10:177 [Google Scholar]
  158. Zhang R, Nguyen T. 158.  2008. Model of human immunodeficiency virus budding and self-assembly: role of the cell membrane. Phys. Rev. E 78:051903 [Google Scholar]
  159. Waheed AA, Freed EO. 159.  2010. The role of lipids in retrovirus replication. Viruses 2:1146–80 [Google Scholar]
  160. Rossman JS, Lamb RA. 160.  2011. Influenza virus assembly and budding. Virology 411:229–36 [Google Scholar]
  161. Prevelige PE Jr. 161.  2011. New approaches for antiviral targeting of HIV assembly. J. Mol. Biol. 410:634–40 [Google Scholar]
  162. Zlotnick A, Mukhopadhyay S. 162.  2011. Virus assembly, allostery and antivirals. Trends Microbiol. 19:14–23 [Google Scholar]
  163. Plevka P, Perera R, Yap ML, Cardosa J, Kuhn RJ, Rossmann MG. 163.  2013. Structure of human enterovirus 71 in complex with a capsid-binding inhibitor. Proc. Natl. Acad. Sci. USA 110:5463–67 [Google Scholar]
  164. Colibus LD, Wang X, Spyrou JAB, Kelly J, Ren J. 164.  et al. 2014. More-powerful virus inhibitors from structure-based analysis of HEV71 capsid-binding molecules. Nat. Struct. Mol. Biol. 21:282–88 [Google Scholar]
  165. Katen SP, Chirapu SR, Finn MG, Zlotnick A. 165.  2010. Trapping of hepatitis B virus capsid assembly intermediates by phenylpropenamide assembly accelerators. ACS Chem. Biol. 5:1125–36 [Google Scholar]
  166. Katen SP, Tan Z, Chirapu SR, Finn MG, Zlotnick A. 166.  2013. Assembly-directed antivirals differentially bind quasiequivalent pockets to modify hepatitis B virus capsid tertiary and quaternary structure. Structure 21:1406–16 [Google Scholar]
  167. Bamunusinghe D, Seo JK, Rao ALN. 167.  2011. Subcellular localization and rearrangement of endoplasmic reticulum by brome mosaic virus capsid protein. J. Virol. 85:2953–63 [Google Scholar]
/content/journals/10.1146/annurev-physchem-040214-121637
Loading
/content/journals/10.1146/annurev-physchem-040214-121637
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error