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Computational Virology: Molecular Simulations of Virus Dynamics and Interactions

  • Elizabeth E. Jefferys
  • Mark S. P. SansomEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1215)

Abstract

Molecular modelling and simulations play a key role in computational virology, allowing us to study viruses and their components. This allows experimental structures and related information to be integrated into a single coherent model, enabling predictions about the behaviour of a viral system to go beyond what could be obtained experimentally. In this way, computational approaches provide a powerful complement to more traditional experimental and structural methods. In this chapter, we describe three main areas of computational virology to showcase the power of methods within this field. We begin by describing relatively small simulation systems and focusing on the behaviour of fusion peptides. Then, extending to longer timescales and larger systems, we discuss computational studies of viral capsid assembly and genome encapsidation. Finally, we describe recent developments which allow entire viral particles to be simulated.

Keywords

Fusion peptide Capsid Envelope Molecular dynamics simulation 

Notes

Acknowledgements

Work in M.S.P.S.’s group is supported by grants from BBSRC, EPSRC, the Leverhulme Trust, and Wellcome; EEJ is supported by Wellcome.

References

  1. 1.
    Hulo C, de Castro E, Masson P, Bougueleret L, Bairoch A, Xenarios I, Le Mercier P (2011) ViralZone: a knowledge resource to understand virus diversity. Nucleic Acids Res 39:D576–D582.  https://doi.org/10.1093/nar/gkq901 CrossRefPubMedGoogle Scholar
  2. 2.
    Plummer EM, Manchester M (2011) Viral nanoparticles and virus-like particles: platforms for contemporary vaccine design. Wiley Interdiscip Rev Nanomed Nanobiotechnol 3(2):174–196.  https://doi.org/10.1002/wnan.119 CrossRefPubMedGoogle Scholar
  3. 3.
    Yildiz I, Shukla S, Steinmetz NF (2011) Applications of viral nanoparticles in medicine. Curr Opin Biotechnol 22(6):901–908.  https://doi.org/10.1016/j.copbio.2011.04.020 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Cattaneo R, Russell SJ (2017) How to develop viruses into anticancer weapons. PLoS Pathog 13(3):e1006190.  https://doi.org/10.1371/journal.ppat.1006190 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Schmid M, Ernst P, Honegger A, Suomalainen M, Zimmermann M, Braun L, Stauffer S, Thom C, Dreier B, Eibauer M, Kipar A, Vogel V, Greber UF, Medalia O, Plückthun A (2018) Adenoviral vector with shield and adapter increases tumor specificity and escapes liver and immune control. Nat Commun 9:450.  https://doi.org/10.1038/s41467-017-02707-6 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Fischlechner M, Donath E (2007) Viruses as building blocks for materials and devices. Angew Chem Int Ed 46(18):3184–3193.  https://doi.org/10.1002/anie.200603445 CrossRefGoogle Scholar
  7. 7.
    Butterfield GL, Lajoie MJ, Gustafson HH, Sellers DL, Nattermann U, Ellis D, Bale JB, Ke S, Lenz GH, Yehdego A, Ravichandran R, Pun SH, King NP, Baker D (2017) Evolution of a designed protein assembly encapsulating its own RNA genome. Nature 552:415–420.  https://doi.org/10.1038/nature25157 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Reddy T, Sansom MSP (2016a) Computational virology: from the inside out. BBA-Biomembranes 1858:1610–1618CrossRefGoogle Scholar
  9. 9.
    Mohammadi P, Desfarges S, Bartha I, Joos B, Zangger N, Munoz M, Gunthard HF, Beerenwinkel N, Telenti A, Ciuffi A (2013) 24 hours in the life of HIV-1 in a T cell line. PLoS Pathog 9(1):e1003161.  https://doi.org/10.1371/journal.ppat.1003161 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Beerenwinkel N, Montazeri H, Schuhmacher H, Knupfer P, von Wyl V, Furrer H, Battegay M, Hirschel B, Cavassini M, Vernazza P, Bernasconi E, Yerly S, Boni J, Klimkait T, Cellerai C, Gunthard HF, Swiss HIVCS (2013) The individualized genetic barrier predicts treatment response in a large cohort of HIV-1 infected patients. PLoS Comput Biol 9(8):e1003203.  https://doi.org/10.1371/journal.pcbi.1003203 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Sharma D, Priyadarshini P, Vrati S (2015) Unraveling the web of viroinformatics: computational tools and databases in virus research. J Virol 89(3):1489–1501.  https://doi.org/10.1128/jvi.02027-14 CrossRefPubMedGoogle Scholar
  12. 12.
    Leelananda SP, Lindert S (2016) Computational methods in drug discovery. Beilstein J Org Chem 12:2694–2718.  https://doi.org/10.3762/bjoc.12.267 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Mortier J, Rakers C, Bermudez M, Murgueitio MS, Riniker S, Wolber G (2015) The impact of molecular dynamics on drug design: applications for the characterization of ligand-macromolecule complexes. Drug Discov Today 20(6):686–702.  https://doi.org/10.1016/j.drudis.2015.01.003 CrossRefPubMedGoogle Scholar
  14. 14.
    Allen MP, Tildesley DJ (2017) Computer simulation of liquids, 2nd edn. Oxford University Press, OxfordCrossRefGoogle Scholar
  15. 15.
    Marrink SJ, Tieleman DP (2013) Perspective on the Martini model. Chem Soc Rev 42(16):6801–6822.  https://doi.org/10.1039/c3cs60093a CrossRefPubMedGoogle Scholar
  16. 16.
    Marrink SJ, Risselada J, Yefimov S, Tieleman DP, de Vries AH (2007) The MARTINI force field: coarse grained model for biomolecular simulations. J Phys Chem B 111:7812–7824CrossRefGoogle Scholar
  17. 17.
    Rapaport DC (2004) Self-assembly of polyhedral shells: a molecular dynamics study. Phys Rev E 70(5):051905.  https://doi.org/10.1103/PhysRevE.70.051905 CrossRefGoogle Scholar
  18. 18.
    Rapaport DC, Johnson JE, Skolnick J (1999) Supramolecular self-assembly: molecular dynamics modeling of polyhedral shell formation. Comput Phys Commun 121:231–235.  https://doi.org/10.1016/s0010-4655(99)00319-7 CrossRefGoogle Scholar
  19. 19.
    Laio A, Parrinello M (2002) Escaping free-energy minima. Proc Natl Acad Sci U S A 99(20):12562–12566.  https://doi.org/10.1073/pnas.202427399 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Hamelberg D, Mongan J, McCammon JA (2004) Accelerated molecular dynamics: a promising and efficient simulation method for biomolecules. J Chem Phys 120(24):11919–11929.  https://doi.org/10.1063/1.1755656 CrossRefPubMedGoogle Scholar
  21. 21.
    Darve E, Pohorille A (2001) Calculating free energies using average force. J Chem Phys 115(20):9169–9183.  https://doi.org/10.1063/1.1410978 CrossRefGoogle Scholar
  22. 22.
    Huang Q, Chen C-L, Herrmann A (2004) Bilayer conformation of fusion peptide of influenza virus hemagglutinin: a molecular dynamics simulation study. Biophys J 87(1):14–22.  https://doi.org/10.1529/biophysj.103.024562 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Grime JMA, Dama JF, Ganser-Pornillos BK, Woodward CL, Jensen GJ, Yeager M, Voth GA (2016) Coarse-grained simulation reveals key features of HIV-1 capsid self-assembly. Nat Commun 7:11568.  https://doi.org/10.1038/ncomms11568 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Reddy T, Shorthouse D, Parton DL, Jefferys E, Fowler PW, Chavent M, Baaden M, Sansom MS (2015) Nothing to sneeze at: a dynamic and integrative computational model of an influenza A virion. Structure 23(3):584–597.  https://doi.org/10.1016/j.str.2014.12.019 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Zlotnick A (1994) To build a virus capsid – an equilibrium-model of the self-assembly of polyhedral protein complexes. J Mol Biol 241(1):59–67.  https://doi.org/10.1006/jmbi.1994.1473 CrossRefPubMedGoogle Scholar
  26. 26.
    Nguyen TT, Bruinsma RF, Gelbart WM (2006) Continuum theory of retroviral capsids. Phys Rev Lett 96(7):078102.  https://doi.org/10.1103/PhysRevLett.96.078102 CrossRefPubMedGoogle Scholar
  27. 27.
    Harrison SC (2015) Viral membrane fusion. Virology 479:498–507.  https://doi.org/10.1016/j.virol.2015.03.043 CrossRefPubMedGoogle Scholar
  28. 28.
    Issa ZK, Manke CW, Jena BP, Potoff JJ (2010) Ca2+ bridging of apposed phospholipid bilayers. J Phys Chem B 114(41):13249–13254.  https://doi.org/10.1021/jp105781z CrossRefPubMedGoogle Scholar
  29. 29.
    Knecht V, Marrink SJ (2007) Molecular dynamics simulations of lipid vesicle fusion in atomic detail. Biophys J 92(12):4254–4261.  https://doi.org/10.1529/biophysj.106.103572 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Risselada HJ, Grubmuller H (2012) How SNARE molecules mediate membrane fusion: recent insights from molecular simulations. Curr Opin Struct Biol 22(2):187–196.  https://doi.org/10.1016/j.sbi.2012.01.007 CrossRefPubMedGoogle Scholar
  31. 31.
    Risselada HJ, Bubnis G, Grubmuller H (2014) Expansion of the fusion stalk and its implication for biological membrane fusion. Proc Natl Acad Sci U S A 111(30):11043–11048.  https://doi.org/10.1073/pnas.1323221111 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Calder LJ, Rosenthal PB (2016) Cryomicroscopy provides structural snapshots of influenza virus membrane fusion. Nat Struct Mol Biol 23(9):853–858.  https://doi.org/10.1038/nsmb.3271 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Armstrong RT, Kushnir AS, White JM (2000) The transmembrane domain of influenza hemagglutinin exhibits a stringent length requirement to support the hemifusion to fusion transition. J Cell Biol 151(2):425–437.  https://doi.org/10.1083/jcb.151.2.425 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Carr CM, Chaudhry C, Kim PS (1997) Influenza hemagglutinin is spring-loaded by a metastable native conformation. Proc Natl Acad Sci U S A 94(26):14306–14313.  https://doi.org/10.1073/pnas.94.26.14306 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Lai AL, Park H, White JM, Tamm LK (2006) Fusion peptide of influenza hemagglutinin requires a fixed angle boomerang structure for activity. J Biol Chem 281(9):5760–5770.  https://doi.org/10.1074/jbc.M512280200 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Steinhauer DA, Wharton SA, Skehel JJ, Wiley DC (1995) Studies of the membrane-fusion activities of fusion peptide mutants of influenza-virus hemagglutinin. J Virol 69(11):6643–6651PubMedPubMedCentralGoogle Scholar
  37. 37.
    Han X, Tamm LK (2000) A host-guest system to study structure-function relationships of membrane fusion peptides. Proc Natl Acad Sci U S A 97(24):13097–13102.  https://doi.org/10.1073/pnas.230212097 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Harter C, James P, Bachi T, Semenza G, Brunner J (1989) Hydrophobic binding of the ectodomain of influenza hemagglutinin to membranes occurs through the fusion peptide. J Biol Chem 264(11):6459–6464PubMedGoogle Scholar
  39. 39.
    Lear JD, Degrado WF (1987) Membrane-binding and conformational properties of peptides representing the NH2 terminus of influenza HA-2. J Biol Chem 262(14):6500–6505PubMedGoogle Scholar
  40. 40.
    Wharton SA, Martin SR, Ruigrok RWH, Skehel JJ, Wiley DC (1988) Membrane-fusion by peptide analogs of influenza-virus hemagglutinin. J Gen Virol 69:1847–1857.  https://doi.org/10.1099/0022-1317-69-8-1847 CrossRefPubMedGoogle Scholar
  41. 41.
    Epand RM (2003) Fusion peptides and the mechanism of viral fusion. Biochim Biophys Acta 1614(1):116–121.  https://doi.org/10.1016/s0005-2736(03)00169-x CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Schrodinger, LLC (2010) The PyMOL molecular graphics system, Version 1.3r1Google Scholar
  43. 43.
    Larsson P, Kasson PM (2013) Lipid tail protrusion in simulations predicts fusogenic activity of influenza fusion peptide mutants and conformational models. PLoS Comput Biol 9(3):e1002950.  https://doi.org/10.1371/journal.pcbi.1002950 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Mirjanian D, Dickey AN, Hoh JH, Woolf TB, Stevens MJ (2010) Splaying of aliphatic tails plays a central role in barrier crossing during liposome fusion. J Phys Chem B 114(34):11061–11068.  https://doi.org/10.1021/jp1055182 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Nishizawa M, Nishizawa K (2013) Molecular dynamics simulation analysis of membrane defects and pore propensity of hemifusion diaphragms. Biophys J 104(5):1038–1048.  https://doi.org/10.1016/j.bpj.2013.01.022 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Smeijers AF, Markvoort AJ, Pieterse K, Hilbers PAJ (2006) A detailed look at vesicle fusion. J Phys Chem B 110(26):13212–13219.  https://doi.org/10.1021/jp060824o CrossRefPubMedGoogle Scholar
  47. 47.
    Bonnafous P, Stegmann T (2000) Membrane perturbation and fusion pore formation in influenza hemagglutinin-mediated membrane fusion – a new model for fusion. J Biol Chem 275(9):6160–6166.  https://doi.org/10.1074/jbc.275.9.6160 CrossRefPubMedGoogle Scholar
  48. 48.
    Donald JE, Zhang Y, Fiorin G, Carnevale V, Slochower DR, Gai F, Klein ML, DeGrado WF (2011) Transmembrane orientation and possible role of the fusogenic peptide from parainfluenza virus 5 (PIV5) in promoting fusion. Proc Natl Acad Sci U S A 108(10):3958–3963.  https://doi.org/10.1073/pnas.1019668108 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Engel A, Walter P (2008) Membrane lysis during biological membrane fusion: collateral damage by misregulated fusion machines. J Cell Biol 183(2):181–186.  https://doi.org/10.1083/jcb.200805182 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Lee KK (2010) Architecture of a nascent viral fusion pore. EMBO J 29(7):1299–1311.  https://doi.org/10.1038/emboj.2010.13 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Legare S, Laggue P (2014) The influenza fusion peptide promotes lipid polar head intrusion through hydrogen bonding with phosphates and N-terminal membrane insertion depth. Proteins: Struct Funct Bioinf 82(9):2118–2127.  https://doi.org/10.1002/prot.24568 CrossRefGoogle Scholar
  52. 52.
    Victor BL, Lousa D, Antunes JM, Soares CM (2015) Self-assembly molecular dynamics simulations shed light into the interaction of the influenza fusion peptide with a membrane bilayer. J Chem Inf Model 55(4):795–805.  https://doi.org/10.1021/ci500756v CrossRefPubMedGoogle Scholar
  53. 53.
    Ayton GA, Noid WG, Voth GA (2007) Multiscale modeling of biomolecular systems: in serial and in parallel. Curr Opin Struct Biol 17:192–198CrossRefGoogle Scholar
  54. 54.
    Gurtovenko AA, Anwar J, Vattulainen I (2010) Defect-mediated trafficking across cell membranes: insights from in silico modeling. Chem Rev 110(10):6077–6103.  https://doi.org/10.1021/cr1000783 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Lindahl E, Sansom MSP (2008) Membrane proteins: molecular dynamics simulations. Curr Opin Struct Biol 18:425–431CrossRefGoogle Scholar
  56. 56.
    Marrink SJ, de Vries AH, Tieleman DP (2009) Lipids on the move: simulations of membrane pores, domains, stalks and curves. Biochim Biophys Acta 1788:149–168CrossRefGoogle Scholar
  57. 57.
    Bullough P, Hughson F, Skehel J, Wiley D (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37–42CrossRefGoogle Scholar
  58. 58.
    Lague P, Roux B, Pastor RW (2005) Molecular dynamics simulations of the influenza hemagglutinin fusion peptide in micelles and bilayers: conformational analysis of peptide and lipids. J Mol Biol 354(5):1129–1141.  https://doi.org/10.1016/j.jmb.2005.10.038 CrossRefPubMedGoogle Scholar
  59. 59.
    Li JY, Das P, Zhou RH (2010) Single mutation effects on conformational change and membrane deformation of influenza hemagglutinin fusion peptides. J Phys Chem B 114(26):8799–8806.  https://doi.org/10.1021/jp1029163 CrossRefPubMedGoogle Scholar
  60. 60.
    Vaccaro L, Cross KJ, Kleinjung J, Straus SK, Thomas DJ, Wharton SA, Skehel JJ, Fraternali F (2005) Plasticity of influenza haemagglutinin fusion peptides and their interaction with lipid bilayers. Biophys J 88(1):25–36.  https://doi.org/10.1529/biophysj.104.044537 CrossRefPubMedGoogle Scholar
  61. 61.
    Kasson PM, Pande VS (2007) Control of membrane fusion mechanism by lipid composition: predictions from ensemble molecular dynamics. PLoS Comput Biol 3(11):2228–2238.  https://doi.org/10.1371/journal.pcbi.0030220 CrossRefGoogle Scholar
  62. 62.
    Kasson PM, Lindahl E, Pande VS (2010) Atomic-resolution simulations predict a transition state for vesicle fusion defined by contact of a few lipid tails. PLoS Comput Biol 6(6):e1000829.  https://doi.org/10.1371/journal.pcbi.1000829 CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Kawamoto S, Shinoda W (2014) Free energy analysis along the stalk mechanism of membrane fusion. Soft Matter 10(17):3048–3054.  https://doi.org/10.1039/c3sm52344f CrossRefPubMedGoogle Scholar
  64. 64.
    Pannuzzo M, De Jong DH, Raudino A, Marrink SJ (2014) Simulation of polyethylene glycol and calcium-mediated membrane fusion. J Chem Phys 140(12):124905.  https://doi.org/10.1063/1.4869176 CrossRefPubMedGoogle Scholar
  65. 65.
    Shirts M, Pande VS (2000) Computing – screen savers of the world unite! Science 290(5498):1903–1904.  https://doi.org/10.1126/science.290.5498.1903 CrossRefGoogle Scholar
  66. 66.
    Lousa D, Pinto ART, Victor BL, Laio A, Veiga AS, Castanho M, Soares CM (2016) Fusing simulation and experiment: the effect of mutations on the structure and activity of the influenza fusion peptide. Sci Rep 6:28099.  https://doi.org/10.1038/srep28099 CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Risselada HJ, Marelli G, Fuhrmans M, Smirnova YG, Grubmuller H, Marrink SJ, Muller M (2012) Line-tension controlled mechanism for influenza fusion. PLoS One 7(6):e38302.  https://doi.org/10.1371/journal.pone.0038302 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Fuhrmans M, Marrink SJ (2012) Molecular view of the role of fusion peptides in promoting positive membrane curvature. J Am Chem Soc 134(3):1543–1552.  https://doi.org/10.1021/ja207290b CrossRefPubMedGoogle Scholar
  69. 69.
    Li YL, Han X, Lai AL, Bushweller JH, Cafiso DS, Tamm LK (2005) Membrane structures of the hemifusion-inducing fusion peptide mutant G1S and the fusion-blocking mutant G1V of influenza virus hemagglutinin suggest a mechanism for pore opening in membrane fusion. J Virol 79(18):12065–12076.  https://doi.org/10.1128/jvi.79.18.12065-12076.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Siegel DP, Epand RM (2000) Effect of influenza hemagglutinin fusion peptide on lamellar/inverted phase transitions in dipalmitoleoylphosphatidylethanolamine: implications for membrane fusion mechanisms. Biochim Biophys Acta 1468(1–2):87–98.  https://doi.org/10.1016/s0005-2736(00)00246-7 CrossRefPubMedGoogle Scholar
  71. 71.
    Wilber AW, Doye JPK, Louis AA, Noya EG, Miller MA, Wong P (2007) Reversible self-assembly of patchy particles into monodisperse icosahedral clusters. J Chem Phys 127(8):085106.  https://doi.org/10.1063/1.2759922 CrossRefPubMedGoogle Scholar
  72. 72.
    Fraenkelconrat H, Williams RC (1955) Reconstitution of active tobacco mosaic virus from its inactive protein and nucleic acid components. Proc Natl Acad Sci U S A 41(10):690–698.  https://doi.org/10.1073/pnas.41.10.690 CrossRefGoogle Scholar
  73. 73.
    Richards KE, Williams RC (1972) Assembly of tobacco mosaic virus in-vitro – effect of state of polymerization of protein component. Proc Natl Acad Sci U S A 69(5):1121–1124.  https://doi.org/10.1073/pnas.69.5.1121 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Harvey SC, Petrov AS, Devkota B, Boz MB (2009) Viral assembly: a molecular modeling perspective. Phys Chem Chem Phys 11(45):10553–10564.  https://doi.org/10.1039/b912884k CrossRefPubMedGoogle Scholar
  75. 75.
    Hagan MF (2014) Modeling viral capsid assembly. In: Rice SA, Dinner AR (eds) Advances in chemical physics, vol 155, pp 1–67Google Scholar
  76. 76.
    Nguyen HD, Reddy VS, Brooks CL (2007) Deciphering the kinetic mechanism of spontaneous self-assembly of icosahedral capsids. Nano Lett 7(2):338–344.  https://doi.org/10.1021/nl062449h CrossRefPubMedGoogle Scholar
  77. 77.
    Baschek JE, Klein HCR, Schwarz US (2012) Stochastic dynamics of virus capsid formation: direct versus hierarchical self-assembly. BMC Biophys 5(1):22.  https://doi.org/10.1186/2046-1682-5-22 CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Boettcher MA, Klein HCR, Schwarz US (2015) Role of dynamic capsomere supply for viral capsid self-assembly. Phys Biol 12(1):016014.  https://doi.org/10.1088/1478-3975/12/1/016014 CrossRefPubMedGoogle Scholar
  79. 79.
    Berger B, Shor PW, Tuckerkellogg L, King J (1994) Local rule-based theory of virus shell assembly. Proc Natl Acad Sci U S A 91(16):7732–7736.  https://doi.org/10.1073/pnas.91.16.7732 CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Schwartz R, Shor PW, Prevelige PE, Berger B (1998) Local rules simulation of the kinetics of virus capsid self-assembly. Biophys J 75(6):2626–2636.  https://doi.org/10.1016/s0006-3495(98)77708-2 CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Hagan MF, Chandler D (2006) Dynamic pathways for viral capsid assembly. Biophys J 91(1):42–54.  https://doi.org/10.1529/biophysj.105.076851 CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Xie L, Smith GR, Feng X, Schwartz R (2012) Surveying capsid assembly pathways through simulation-based data fitting. Biophys J 103(7):1545–1554.  https://doi.org/10.1016/j.bpj.2012.08.057 CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Krishna V, Ayton GS, Voth GA (2010) Role of protein interactions in defining HIV-1 viral capsid shape and stability: a coarse-grained analysis. Biophys J 98(1):18–26.  https://doi.org/10.1016/j.bpj.2009.09.049 CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Chen B, Tycko R (2011) Simulated self-assembly of the HIV-1 capsid: protein shape and native contacts are sufficient for two-dimensional lattice formation. Biophys J 100(12):3035–3044.  https://doi.org/10.1016/j.bpj.2011.05.025 CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Grime JMA, Voth GA (2012) Early stages of the HIV-1 capsid protein lattice formation. Biophys J 103(8):1774–1783.  https://doi.org/10.1016/j.bpj.2012.09.007 CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Qiao X, Jean J, Weber J, Zhu FQ, Chen B (2015) Mechanism of polymorphism and curvature of HIV capsid assemblies probed by 3D simulations with a novel coarse grain model. Biochim Biophys Acta 1850(11):2353–2367.  https://doi.org/10.1016/j.bbagen.2015.08.017 CrossRefPubMedGoogle Scholar
  87. 87.
    Smith GR, Xie L, Lee B, Schwartz R (2014) Applying molecular crowding models to simulations of virus capsid assembly in vitro. Biophys J 106(1):310–320.  https://doi.org/10.1016/j.bpj.2013.11.022 CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Hicks SD, Henley CL (2006) Irreversible growth model for virus capsid assembly. Phys Rev E 74(3):031912.  https://doi.org/10.1103/PhysRevE.74.031912 CrossRefGoogle Scholar
  89. 89.
    Levandovsky A, Zandi R (2009) Nonequilibirum assembly, retroviruses, and conical structures. Phys Rev Lett 102(19):198102.  https://doi.org/10.1103/PhysRevLett.102.198102 CrossRefPubMedGoogle Scholar
  90. 90.
    Yu ZH, Dobro MJ, Woodward CL, Levandovsky A, Danielson CM, Sandrin V, Shi J, Aiken C, Zandi R, Hope TJ, Jensen GJ (2013) Unclosed HIV-1 capsids suggest a curled sheet model of assembly. J Mol Biol 425(1):112–123.  https://doi.org/10.1016/j.jmb.2012.10.006 CrossRefPubMedGoogle Scholar
  91. 91.
    Zhao G, Perilla JR, Yufenyuy EL, Meng X, Chen B, Ning J, Ahn J, Gronenborn AM, Schulten K, Aiken C, Zhang P (2013) Mature HIV-1 capsid structure by cryo-electron microscopy and all-atom molecular dynamics. Nature 497(7451):643–646.  https://doi.org/10.1038/nature12162 CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Bruinsma RF (2006) Physics of RNA and viral assembly. Eur Phys J E 19(3):303–310.  https://doi.org/10.1140/epje/i2005-10071-1 CrossRefPubMedGoogle Scholar
  93. 93.
    Roos WH, Bruinsma R, Wuite GJL (2010) Physical virology. Nat Phys 6(10):733–743.  https://doi.org/10.1038/nphys1797 CrossRefGoogle Scholar
  94. 94.
    Chang CB, Knobler CM, Gelbart WM, Mason TG (2008) Curvature dependence of viral protein structures on encapsidated nanoemulsion droplets. ACS Nano 2(2):281–286.  https://doi.org/10.1021/nn700385z CrossRefPubMedGoogle Scholar
  95. 95.
    Hu YF, Zandi R, Anavitarte A, Knobler CM, Gelbart WM (2008) Packaging of a polymer by a viral capsid: the interplay between polymer length and capsid size. Biophys J 94(4):1428–1436.  https://doi.org/10.1529/biophysj.107.117473 CrossRefPubMedGoogle Scholar
  96. 96.
    Johnson KN, Tang L, Johnson JE, Ball LA (2004) Heterologous RNA encapsidated in pariacoto virus-like particles forms a dodecahedral cage similar to genomic RNA in wild-type virions. J Virol 78(20):11371–11378.  https://doi.org/10.1128/jvi.78.20.11371-11378.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Sun J, DuFort C, Daniel MC, Murali A, Chen C, Gopinath K, Stein B, De M, Rotello VM, Holzenburg A, Kao CC, Dragnea B (2007) Core-controlled polymorphism in virus-like particles. Proc Natl Acad Sci U S A 104(4):1354–1359.  https://doi.org/10.1073/pnas.0610542104 CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    ElSawy KM, Caves LSD, Twarock R (2011) On the origin of order in the genome organization of ssRNA viruses. Biophys J 101(4):774–780.  https://doi.org/10.1016/j.bpj.2011.07.005 CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Perlmutter JD, Qiao C, Hagan MF (2013) Viral genome structures are optimal for capsid assembly. eLife 2:e00632.  https://doi.org/10.7554/eLife.00632 CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Chen C, Kwak ES, Stein B, Kao CC, Dragnea B (2005) Packaging of gold particles in viral capsids. J Nanosci Nanotechnol 5(12):2029–2033.  https://doi.org/10.1166/jnn.2005.506 CrossRefPubMedGoogle Scholar
  101. 101.
    Dixit SK, Goicochea NL, Daniel MC, Murali A, Bronstein L, De M, Stein B, Rotello VM, Kao CC, Dragnea B (2006) Quantum dot encapsulation in viral capsids. Nano Lett 6(9):1993–1999.  https://doi.org/10.1021/nl061165u CrossRefPubMedGoogle Scholar
  102. 102.
    Dragnea B, Chen C, Kwak ES, Stein B, Kao CC (2003) Gold nanoparticles as spectroscopic enhancers for in vitro studies on single viruses. J Am Chem Soc 125(21):6374–6375.  https://doi.org/10.1021/ja0343609 CrossRefPubMedGoogle Scholar
  103. 103.
    Johnson JM, Tang JH, Nyame Y, Willits D, Young MJ, Zlotnick A (2005) Regulating self-assembly of spherical oligomers. Nano Lett 5(4):765–770.  https://doi.org/10.1021/nl050274q CrossRefPubMedGoogle Scholar
  104. 104.
    Elrad OM, Hagan MF (2008) Mechanisms of size control and polymorphism in viral capsid assembly. Nano Lett 8(11):3850–3857.  https://doi.org/10.1021/nl802269a CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Stockley PG, Twarock R, Bakker SE, Barker AM, Borodavka A, Dykeman E, Ford RJ, Pearson AR, Phillips SEV, Ranson NA, Tuma R (2013) Packaging signals in single-stranded RNA viruses: nature’s alternative to a purely electrostatic assembly mechanism. J Biol Phys 39(2):277–287.  https://doi.org/10.1007/s10867-013-9313-0 CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Tsiang M, Niedziela-Majka A, Hung M, Jin DB, Hu E, Yant S, Samuel D, Liu XH, Sakowicz R (2012) A trimer of dimers is the basic building block for human immunodeficiency Virus-1 capsid assembly. Biochemistry 51(22):4416–4428.  https://doi.org/10.1021/bi300052h CrossRefPubMedGoogle Scholar
  107. 107.
    Grayson P, Evilevitch A, Inamdar MM, Purohit PK, Gelbart WM, Knobler CM, Phillips R (2006) The effect of genome length on ejection forces in bacteriophage lambda. Virology 348(2):430–436.  https://doi.org/10.1016/j.virol.2006.01.003 CrossRefPubMedPubMedCentralGoogle Scholar
  108. 108.
    LaMarque JC, Le TVL, Harvey SC (2004) Packaging double-helical DNA into viral capsids. Biopolymers 73(3):348–355.  https://doi.org/10.1002/bip.10529 CrossRefPubMedGoogle Scholar
  109. 109.
    Locker CR, Harvey SC (2006) A model for viral genome packing. Multiscale Model Simul 5(4):1264–1279.  https://doi.org/10.1137/060650684 CrossRefGoogle Scholar
  110. 110.
    Petrov AS, Lim-Hing K, Harvey SC (2007) Packaging of DNA by bacteriophage Epsilon15: structure, forces, and thermodynamics. Structure 15(7):807–812.  https://doi.org/10.1016/j.str.2007.05.005 CrossRefPubMedGoogle Scholar
  111. 111.
    Petrov AS, Harvey SC (2008) Packaging double-helical DNA into viral capsids: structures, forces, and energetics. Biophys J 95(2):497–502.  https://doi.org/10.1529/biophysj.108.131797 CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Smith DE, Tans SJ, Smith SB, Grimes S, Anderson DL, Bustamante C (2001) The bacteriophage phi 29 portal motor can package DNA against a large internal force. Nature 413(6857):748–752.  https://doi.org/10.1038/35099581 CrossRefGoogle Scholar
  113. 113.
    Petrov AS, Harvey SC (2007) Structural and thermodynamic principles of viral packaging. Structure 15(1):21–27.  https://doi.org/10.1016/j.str2006.11.013 CrossRefPubMedGoogle Scholar
  114. 114.
    Forrey C, Muthukumar M (2006) Langevin dynamics simulations of genome packing in bacteriophage. Biophys J 91(1):25–41.  https://doi.org/10.1529/biophysj.105.073429 CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Locker CR, Fuller SD, Harvey SC (2007) DNA organization and thermodynamics during viral packing. Biophys J 93(8):2861–2869.  https://doi.org/10.1529/biophysj.106.094771 CrossRefPubMedPubMedCentralGoogle Scholar
  116. 116.
    Harrison SC, Olson AJ, Schutt CE, Winkler FK, Bricogne G (1978) Tomato bushy stunt virus at 2.9 Å resolution. Nature 276(5686):368–373.  https://doi.org/10.1038/276368a0 CrossRefPubMedPubMedCentralGoogle Scholar
  117. 117.
    Huber RG, Marzinek JK, Holdbrook DA, Bond PJ (2017) Multiscale molecular dynamics simulation approaches to the structure and dynamics of viruses. Prog Biophys Mol Biol 128:121–132.  https://doi.org/10.1016/j.pbiomolbio.2016.09.010 CrossRefPubMedGoogle Scholar
  118. 118.
    Stone JE, Phillips JC, Freddolino PL, Hardy DJ, Trabuco LG, Schulten K (2007) Accelerating molecular modeling applications with graphics processors. J Comput Chem 28(16):2618–2640.  https://doi.org/10.1002/jcc.20829 CrossRefPubMedGoogle Scholar
  119. 119.
    Freddolino PL, Arkhipov AS, Larson SB, McPherson A, Schulten K (2006) Molecular dynamics simulations of the complete satellite tobacco mosaic virus. Structure 14(3):437–449.  https://doi.org/10.1016/j.str.2005.11.014 CrossRefPubMedGoogle Scholar
  120. 120.
    Zeng YY, Larson SB, Heitsch CE, McPherson A, Harvey SC (2012) A model for the structure of satellite tobacco mosaic virus. J Struct Biol 180(1):110–116.  https://doi.org/10.1016/j.jsb.2012.06.008 CrossRefPubMedPubMedCentralGoogle Scholar
  121. 121.
    Arkhipov A, Freddolino PL, Schulten K (2006) Stability and dynamics of virus capsids described by coarse-grained modeling. Structure 14(12):1767–1777.  https://doi.org/10.1016/j.str.2006.10.003 CrossRefPubMedGoogle Scholar
  122. 122.
    Zink M, Grubmuller H (2010) Primary changes of the mechanical properties of southern bean mosaic virus upon calcium removal. Biophys J 98(4):687–695.  https://doi.org/10.1016/j.bpj.2009.10.047 CrossRefPubMedPubMedCentralGoogle Scholar
  123. 123.
    Larsson DSD, Liljas L, van der Spoel D (2012) Virus capsid dissolution studied by microsecond molecular dynamics simulations. PLoS Comput Biol 8(5):e1002502.  https://doi.org/10.1371/journal.pcbi.1002502 CrossRefPubMedPubMedCentralGoogle Scholar
  124. 124.
    Marzinek JK, Holdbrook DA, Huber RG, Verma C, Bond PJ (2016) Pushing the envelope: dengue viral membrane coaxed into shape by molecular simulations. Structure 24(8):1410–1420.  https://doi.org/10.1016/j.str.2016.05.014 CrossRefPubMedGoogle Scholar
  125. 125.
    Machado MR, Gonzalez HC, Pantano S (2017) MD simulations of virus like particles with supra CG solvation affordable to desktop computers. J Chem Theory Comput 13(10):5106–5116.  https://doi.org/10.1021/acs.jctc.7b00659 CrossRefPubMedGoogle Scholar
  126. 126.
    Mihai ME, Tecu C, Ivanciuc AE, Necula G, Lupulescu E, Onu A (2011) Survival of H5N1 influenza virus in water and its inactivation by chemical methods. Roum Arch Microbiol Immunol 70:78–84PubMedGoogle Scholar
  127. 127.
    Stallknecht DE, Shane SM, Kearney MT, Zwank PJ (1990) Persistence of avian influenza-viruses in water. Avian Dis 34(2):406–411.  https://doi.org/10.2307/1591428 CrossRefPubMedGoogle Scholar
  128. 128.
    Reddy T, Sansom MSP (2016b) The role of the membrane in the structure and biophysical robustness of the dengue virion envelope. Structure 24:375–382CrossRefGoogle Scholar
  129. 129.
    Rzepiela AJ, Schäfer LV, Goga N, Risselada HJ, de Vries AH, Marrink SJ (2010) Reconstruction of atomistic details from coarse grained structures. J Comput Chem 31:1333–1343PubMedGoogle Scholar
  130. 130.
    Stansfeld PJ, Sansom MSP (2011) From coarse-grained to atomistic: a serial multi-scale approach to membrane protein simulations. J Chem Theory Comput 7:1157–1166CrossRefGoogle Scholar
  131. 131.
    Barrera EE, Frigini EN, Porasso RD, Pantano S (2017) Modeling DMPC lipid membranes with SIRAH force-field. J Mol Model 23(9):259.  https://doi.org/10.1007/s00894-017-3426-5 CrossRefPubMedGoogle Scholar
  132. 132.
    Darre L, Machado MR, Brandner AF, Gonzalez HC, Ferreira S, Pantano S (2015) SIRAH: a structurally unbiased coarse-grained force field for proteins with aqueous solvation and long-range electrostatics. J Chem Theory Comput 11(2):723–739.  https://doi.org/10.1021/ct5007746 CrossRefPubMedGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of BiochemistryUniversity of OxfordOxfordUK

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