Minimalistic coarse-grained modeling of viral capsid assembly

Johnson, 1997, Quasi-equivalent viruses: a paradigm for protein assemblies, J Mol Biol, 269, 665, 10.1006/jmbi.1997.1068 Hesketh, 2018, The 3.3Å structure of a plant geminivirus using cryo-EM, Nat Commun, 9, 10.1038/s41467-018-04793-6 Todd, 1991, Comparison of three animal viruses with circular single-stranded DNA genomes, Arch Virol, 117, 129, 10.1007/BF01310498 Legendre, 2014, Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology, Proc Natl Acad Sci USA, 111, 4274, 10.1073/pnas.1320670111 Caspar, 1962, Physical principles in the construction of regular viruses, Cold Spring Harb Symp Quant Biol, 27, 1, 10.1101/SQB.1962.027.001.005 Twarock, 2019, Structural puzzles in virology solved with an overarching icosahedral design principle, Nat Commun, 10, 10.1038/s41467-019-12367-3 Luque, 2010, The structure of elongated viral capsids, Biophys J, 98, 2993, 10.1016/j.bpj.2010.02.051 Fox, 1998, Comparison of the native CCMV virion with in vitro assembled CCMV virions by cryoelectron microscopy and image reconstruction, Virology, 244, 212, 10.1006/viro.1998.9107 Garcea, 1987, Site-directed mutation affecting polyomavirus capsid self-assembly in vitro, Nature, 329, 86, 10.1038/329086a0 Salunke, 1989, Polymorphism in the assembly of polyomavirus capsid protein VP1, Biophys J, 56, 887, 10.1016/S0006-3495(89)82735-3 Flint, 2000 Yu, 2013, Unclosed HIV-1 capsids suggest a curled sheet model of assembly, J Mol Biol, 425, 112, 10.1016/j.jmb.2012.10.006 Zlotnick, 1994, To build a virus capsid: an equilibrium model of the self assembly of polyhedral protein complexes, J Mol Biol, 241, 59, 10.1006/jmbi.1994.1473 Li, 2018, Why large icosahedral viruses need scaffolding proteins, Proc Natl Acad Sci USA, 115, 10.1073/pnas.1807706115 Bancroft, 1968, Properties of cowpea chlorotic mottle virus, its protein and nucleic acid, Virology, 34, 224, 10.1016/0042-6822(68)90232-8 Bancroft, 1967, A study of the self-assembly process in a small spherical virus formation of organized structures from protein subunits in vitro, Virology, 31, 354, 10.1016/0042-6822(67)90180-8 Burns, 2010, Altering the energy landscape of virus self-assembly to generate kinetically trapped nanoparticles, Biomacromolecules, 11, 439, 10.1021/bm901160b Zlotnick, 2000, Mechanism of capsid assembly for an icosahedral plant virus, Virology, 277, 450, 10.1006/viro.2000.0619 Tang, 2006, The role of subunit hinges and molecular “switches” in the control of viral capsid polymorphism, J Struct Biol, 154, 59, 10.1016/j.jsb.2005.10.013 Antal, 2017, Predicting the initial steps of salt-stable cowpea chlorotic mottle virus capsid assembly with atomistic force fields, J Chem Inf Model, 57, 910, 10.1021/acs.jcim.7b00078 Bancroft, 1973, A salt-stable mutant of cowpea chlorotic mottle virus, J Gen Virol, 21, 507, 10.1099/0022-1317-21-3-507 Berger, 1994, Local rule-based theory of virus shell assembly, Proc Natl Acad Sci USA, 91, 7732, 10.1073/pnas.91.16.7732 Schwartz, 1998, Local rules simulation of the kinetics of virus capsid self-assembly, Biophys J, 75, 2626, 10.1016/S0006-3495(98)77708-2 Arkhipov, 2006, Stability and dynamics of virus capsids described by coarse-grained modeling, Structure, 14, 1767, 10.1016/j.str.2006.10.003 Roos, 2010, Physical virology, Nat Phys, 6, 733, 10.1038/nphys1797 Choi, 2000, Packaging of tobacco mosaic virus subgenomic RNAs by brome mosaic virus coat protein exhibits RNA controlled polymorphism, Virology, 275, 249, 10.1006/viro.2000.0532 Elrad, 2010, Encapsulation of a polymer by an icosahedral virus, Phys Biol, 7, 045003, 10.1088/1478-3975/7/4/045003 ElSawy, 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, 10.1016/j.jmb.2010.05.037 Morton, 2010, The impact of viral RNA on assembly pathway selection, J Mol Biol, 401, 298, 10.1016/j.jmb.2010.05.059 Cadena-Nava, 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, 10.1128/JVI.06566-11 Perlmutter, 2013, Viral genome structures are optimal for capsid assembly, Elife, 2, e00632, 10.7554/eLife.00632 Hagan, 2014, Modeling viral capsid assembly, Adv Chem Phys, 155, 1 Li, 2017, Impact of a nonuniform charge distribution on virus assembly, Phys Rev E, 96, 10.1103/PhysRevE.96.022401 van Galen, 2019, Allosteric pathway selection in templated assembly, Sci Adv, 5, 10.1126/sciadv.aaw3353 de Rosier, 1968, Reconstruction of three dimensional structures from electron micrographs, Nature, 217, 130, 10.1038/217130a0 Jiang, 2017, Atomic cryo-EM structures of viruses, Curr Opin Struct Biol, 46, 122, 10.1016/j.sbi.2017.07.002 Li, 2013, Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM, Nat Methods, 10, 584, 10.1038/nmeth.2472 Goetschius, 2019, Asymmetry in icosahedral viruses, Curr Opin Virol, 36, 67, 10.1016/j.coviro.2019.05.006 Heymann, 2003, Dynamics of herpes simplex virus capsid maturation visualized by time-lapse cryo-electron microscopy, Nat Struct Mol Biol, 10, 334, 10.1038/nsb922 Buchta, 2019, Enterovirus particles expel capsid pentamers to enable genome release, Nat Commun, 10, 1138, 10.1038/s41467-019-09132-x Subramaniam, 2016, Resolution advances in cryo-EM enable application to drug discovery, Curr Opin Struct Biol, 41, 194, 10.1016/j.sbi.2016.07.009 Baker, 2018, Cryo-electron microscopy shapes up, Nature, 561, 565, 10.1038/d41586-018-06791-6 Herzik, 2019, A multi-model approach to assessing local and global cryo-EM map quality, Structure, 27, 344, 10.1016/j.str.2018.10.003 Ho, 2018, VIPERdb: a tool for virus research, Annu Rev Virol, 5, 477, 10.1146/annurev-virology-092917-043405 Chevreuil, 2018, Nonequilibrium self-assembly dynamics of icosahedral viral capsids packaging genome or polyelectrolyte, Nat Commun, 9, 10.1038/s41467-018-05426-8 Uetrecht, 2010, Interrogating viral capsid assembly with ion mobility–mass spectrometry, Nat Chem, 3, 126, 10.1038/nchem.947 Snijder, 2013, Studying 18 MDa virus assemblies with native mass spectrometry, Angew Chem Int Ed, 52, 4020, 10.1002/anie.201210197 Ceres, 2002, Weak protein-protein interactions are sufficient to drive assembly of hepatitis B virus capsids, Biochemistry, 41, 11525, 10.1021/bi0261645 Ayton, 2007, Multiscale modeling of biomolecular systems: in serial and in parallel, Curr Opin Struct Biol, 17, 192, 10.1016/j.sbi.2007.03.004 May, 2012, Multiscale modeling of virus structure, assembly, and dynamics, 167 Wang, 2019, A multiscale model for the self-assembly of coat proteins in bacteriophage MS2, J Chem Inf Model, 59, 3899, 10.1021/acs.jcim.9b00514 Wales, 1999, Global optimization of clusters, crystals and biomolecules, Science, 285, 1368, 10.1126/science.285.5432.1368 Wales, 2002, Discrete path sampling, Mol Phys, 100, 3285, 10.1080/00268970210162691 Zlotnick, 2007, Distinguishing reversible from irreversible virus capsid assembly, J Mol Biol, 366, 14, 10.1016/j.jmb.2006.11.034 Steven, 2005, Virus maturation: dynamics and mechanism of a stabilizing structural transition that leads to infectivity, Curr Opin Struct Biol, 15, 227, 10.1016/j.sbi.2005.03.008 Buck, 2005, Maturation of papillomavirus capsids, J Virol, 79, 2839, 10.1128/JVI.79.5.2839-2846.2005 Mukherjee, 2008, A quantitative description of in vitro assembly of human papillomavirus 16 virus-like particles, J Mol Biol, 381, 229, 10.1016/j.jmb.2008.05.079 Duda, 1998, Protein chainmail: catenated protein in viral capsids, Cell, 94, 55, 10.1016/S0092-8674(00)81221-0 Wikoff, 2000, Topologically linked protein rings in the bacteriophage HK97 capsid, Science, 289, 2129, 10.1126/science.289.5487.2129 Stone, 2019, Principles for enhancing virus capsid capacity and stability from a thermophilic virus capsid structure, Nat Commun, 10, 10.1038/s41467-019-12341-z Prevelige, 1993, Nucleation and growth phases in the polymerization of coat and scaffolding subunits into icosahedral procapsid shells, Biophys J, 64, 824, 10.1016/S0006-3495(93)81443-7 Rapaport, 1999, Supramolecular self-assembly: molecular dynamics modeling of polyhedral shell formation, Comput Phys Commun, 121–122, 231, 10.1016/S0010-4655(99)00319-7 Rapaport, 2004, Self-assembly of polyhedral shells: a molecular dynamics study, Phys Rev E, 70, 10.1103/PhysRevE.70.051905 Rapaport, 2008, Role of reversibility in viral capsid growth: a paradigm for self-assembly, Phys Rev Lett, 101, 10.1103/PhysRevLett.101.186101 Hagan, 2006, Dynamic pathways for viral capsid assembly, Biophys J, 91, 42, 10.1529/biophysj.105.076851 Nguyen, 2007, Deciphering the kinetic mechanism of spontaneous self-assembly of icosahedral capsids, Nano Lett, 7, 338, 10.1021/nl062449h Nguyen, 2009, Invariant polymorphism in virus capsid assembly, J Am Chem Soc, 131, 2606, 10.1021/ja807730x Van Workum, 2006, Symmetry, equivalence, and molecular self-assembly, Phys Rev E, 73, 1, 10.1103/PhysRevE.73.031502 Zandi, 2004, Origin of icosahedral symmetry in viruses, Proc Natl Acad Sci USA, 101, 10.1073/pnas.0405844101 Thomson, 1904, On the structure of the atom: an investigation of the stability and periods of oscillation of a number of corpuscles arranged at equal intervals around the circumference of a circle; with applications of the results to the theory of atomic structure, Philos Mag, 7, 237, 10.1080/14786440409463107 Tammes, 1930, On the origin of number and arrangement of the places of exit on the surface of pollen-grains, Recl Trav Bot Néerl, 27, 1 Bruinsma, 2003, Viral self-assembly as a thermodynamic process, Phys Rev Lett, 90, 10.1103/PhysRevLett.90.248101 Moody, 1965, The shape of the T-even bacteriophage head, Virology, 26, 567, 10.1016/0042-6822(65)90319-3 Moody, 1999, Geometry of phage head construction, J Mol Biol, 293, 401, 10.1006/jmbi.1999.3011 Luque, 2010, Optimal architectures of elongated viruses, Proc Natl Acad Sci USA, 107, 5323, 10.1073/pnas.0915122107 Karlin, 1988, Charge configurations in viral proteins, Proc Natl Acad Sci USA, 85, 9396, 10.1073/pnas.85.24.9396 del Álamo, 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, 10.1016/j.jmb.2004.10.086 Lošdorfer Božič, 2013, Statistical analysis of sizes and shapes of virus capsids and their resulting elastic properties, J Biol Phys, 39, 215, 10.1007/s10867-013-9302-3 Lošdorfer Božič, 2012, How simple can a model of an empty viral capsid be? Charge distributions in viral capsids, J Biol Phys, 38, 657, 10.1007/s10867-012-9278-4 Siber, 2007, Role of electrostatic interactions in the assembly of empty spherical viral capsids, Phys Rev E, 76, 10.1103/PhysRevE.76.061906 Bourne, 2006, Global structural changes in hepatitis B virus capsids induced by the assembly effector HAP1, J Virol, 80, 11055, 10.1128/JVI.00933-06 Zlotnick, 2007, In vitro screening for molecules that affect virus capsid assembly (and other protein association reactions), Nat Protoc, 2, 490, 10.1038/nprot.2007.60 Zhou, 2018, Electrostatic interactions in protein structure, folding, binding, and condensation, Chem Rev, 118, 1691, 10.1021/acs.chemrev.7b00305 Minton, 1983, The effect of volume occupancy upon the thermodynamic activity of proteins: some biochemical consequences, Mol Cell Biochem, 55, 119, 10.1007/BF00673707 del Alamo, 2005, Effect of macromolecular crowding agents on human immunodeficiency virus type 1 capsid protein assembly in vitro, J Virol, 79, 14271, 10.1128/JVI.79.22.14271-14281.2005 Smith, 2014, Applying molecular crowding models to simulations of virus capsid assembly in vitro, Biophys J, 106, 310, 10.1016/j.bpj.2013.11.022 Doye, 1995, The effect of the range of the potential on the structures of clusters, J Chem Phys, 103, 4234, 10.1063/1.470729 Doye, 1996, The effect of the range of the potential on the structure and stability of simple liquids: from clusters to bulk, from sodium to C60, J Phys B Atomic Mol Phys, 29, 4859, 10.1088/0953-4075/29/21/002 Wales, 2003 Wales, 2005, The energy landscape as a unifying theme in molecular science, Phil Trans R Soc A, 363, 357, 10.1098/rsta.2004.1497 Becker, 1997, The topology of multidimensional potential energy surfaces: theory and application to peptide structure and kinetics, J Chem Phys, 106, 1495, 10.1063/1.473299 Wales, 1998, Archetypal energy landscapes, Nature, 394, 758, 10.1038/29487 Calvo, 2016, Grand and semigrand canonical basin-hopping, J Chem Theory Comput, 12, 902, 10.1021/acs.jctc.5b00962 Johnston, 2010, Modelling the self-assembly of virus capsids, J Phys Condens Matter, 22, 10.1088/0953-8984/22/10/104101 Fejer, 2009, Energy landscapes for shells assembled from pentagonal and hexagonal pyramids, Phys Chem Chem Phys, 11, 2098, 10.1039/b818062h Fejer, 2010, Emergent complexity from simple anisotropic building blocks: shells, tubes and spirals, ACS Nano, 4, 219, 10.1021/nn9013565 Paramonov, 2005, The directional contact distance of two ellipsoids: coarse-grained potentials for anisotropic interactions, J Chem Phys, 123, 10.1063/1.2102897 Fejer, 2007, Helix self-assembly from anisotropic molecules, Phys Rev Lett, 99, 10.1103/PhysRevLett.99.086106 Fejer, 2011, Self-assembly of anisotropic particles, Soft Matter, 7, 3553, 10.1039/c0sm01289k Olesen, 2011, A left-handed building block self-assembles into right- and left-handed helices, RSC Adv, 3, 3553 Forman, 2013, Local frustration determines molecular and macroscopic helix structures, J Phys Chem B, 117, 7918, 10.1021/jp4040503 Fejer, 2014, Design principles for Bernal spirals and helices with tunable pitch, Nanoscale, 6, 9448, 10.1039/C4NR00324A Fejer, 2015, Design of a Kagome lattice from soft anisotropic particles, Soft Matter, 11, 6663, 10.1039/C5SM01191D Llorente, 2014, A minimal representation of the self-assembly of virus capsids, Soft Matter, 10, 3560, 10.1039/c4sm00087k Mannige, 2010, Periodic table of virus capsids: implications for natural selection and design, PLoS One, 5, 10.1371/journal.pone.0009423 Cusack, 1983, Structure of the top a-t component of alfalfa mosaic-virus—a non-icosahedral virion, J Mol Biol, 171, 139, 10.1016/S0022-2836(83)80350-7 Reguera, 2019, Kinetics of empty viral capsid assembly in a minimal model, Soft Matter, 15, 7166, 10.1039/C9SM01593K Li, 2000, Image reconstructions of helical assemblies of the HIV-1 CA protein, Nature, 407, 409, 10.1038/35030177 Kingston, 2000, Structure and self-association of the Rous sarcoma virus capsid protein, Structure, 8, 617, 10.1016/S0969-2126(00)00148-9 Cardone, 2009, Visualization of a missing link in retrovirus capsid assembly, Nature, 457, 694, 10.1038/nature07724 Grime, 2016, Coarse-grained simulation reveals key features of HIV-1 capsid self-assembly, Nat Commun, 7, 10.1038/ncomms11568 Asensio, 2016, A selection for assembly reveals that a single amino acid mutant of the bacteriophage MS2 coat protein forms a smaller virus-like particle, Nano Lett, 16, 5944, 10.1021/acs.nanolett.6b02948 Grimes, 1998, The atomic structure of the bluetongue virus core, Nature, 395, 470, 10.1038/26694 Rossmann, 1999, Courageous science: structural studies of bluetongue virus core, Structure, 7, R43, 10.1016/S0969-2126(99)80031-8 Nakagawa, 2003, The atomic structure of rice dwarf virus reveals the self-assembly mechanism of component proteins, Structure, 11, 1227, 10.1016/j.str.2003.08.012 Iwasaki, 2008, Pleomorphic configuration of the trimeric capsid proteins of rice dwarf virus that allows formation of both the outer capsid and tubular crystals, J Mol Biol, 383, 252, 10.1016/j.jmb.2008.08.021 Rochal, 2016, Hidden symmetry of small spherical viruses and organization principles in “anomalous” and double-shelled capsid nanoassemblies, Nanoscale, 8, 16976, 10.1039/C6NR04930C Stubbs, 2012, 631 Durham, 1971, States of aggregation of tobacco mosaic virus protein, Nat New Biol, 229, 37, 10.1038/newbio229037a0 Klug, 1999, The tobacco mosaic virus particle: structure and assembly, Philos Trans R Soc B, 354, 531, 10.1098/rstb.1999.0404 Butler, 1999, Self-assembly of tobacco mosaic virus: the role of an intermediate aggregate in generating both specificity and speed, Philos Trans R Soc B, 354, 537, 10.1098/rstb.1999.0405 Correia, 1985, Sedimentation equilibrium measurements of the intermediate-size tobacco mosaic virus protein polymers, Biochemistry, 24, 3292, 10.1021/bi00334a033 Aksyuk, 2011, Bacteriophage assembly, Viruses, 3, 172, 10.3390/v3030172 Botstein, 1980, A theory of modular evolution for bacteriophages, Ann N Y Acad Sci, 354, 484, 10.1111/j.1749-6632.1980.tb27987.x Fejer, 2018, Designing hierarchical molecular complexity: icosahedra of addressable icosahedra, Mol Phys, 116, 2954, 10.1080/00268976.2018.1439190