Mechanical properties of the icosahedral shell of southern bean mosaic virus: A molecular dynamics study

Biophysical Journal

Volumn 96, Issue 4, 2009, Pages 1350-1363

  Zink, Mareike ^a   Grubmüller, Helmut ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; MOLECULAR DYNAMICS; MOLECULAR MODEL; MOSAIC VIRUS; NONHUMAN; SIMULATION; SOUTHERN BEAN MOSAIC VIRUS; SURFACE PROPERTY; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS ENVELOPE; VIRUS INFECTION; ALGORITHM; BEAN; BIOMECHANICS; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER PROGRAM; COMPUTER SIMULATION; ELASTICITY; FRICTION; INSTRUMENTATION; PROTEIN DATABASE; STATISTICAL MODEL; ULTRASTRUCTURE; VIROLOGY;

MIRIDAE; SOUTHERN BEAN MOSAIC VIRUS;

ALGORITHMS; BIOMECHANICS; CAPSID; COMPUTER SIMULATION; DATABASES, PROTEIN; ELASTICITY; FRICTION; LINEAR MODELS; MICROSCOPY, ATOMIC FORCE; MODELS, CHEMICAL; MODELS, MOLECULAR; MOSAIC VIRUSES; PHASEOLUS; SOFTWARE;

EID: 62649155309     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.11.028     Document Type: Article

References (72)

1. Roos, W. H., I. L. Ivanovska, A. Evilevitch, and G. J. L. Wuite. 2007. Viral capsids: mechanical characteristics, genome packaging and delivery mechanisms. Cell. Mol. Life Sci. 64:1484-1497.
2. Caspar, D. L. D., and A. Klug. 1962. Physical principles in the construction of regular viruses. Cold Spring Harb. Symp. Quant. Biol. 27:1-50.
3. Douglas, T., and M. Young. 1999. Virus particles as templates for materials synthesis. Adv. Mater. 8:1-3. (Pubitemid 129675496)
4. Klug, W. S., R. F. Bruinsma, J. -P. Michel, C. M. Knobler, I. L. Ivanovska, et al. 2006. Failure of viral shells. Phys. Rev. Lett. 97:228101.
5. Hagan, M. F., and D. Chandler. 2006. Dynamic pathways for viral capsid assembly. Biophys. J. 91:42-54. (Pubitemid 44018054)
6. Smith, D. E., S. J. Tans, S. B. Smith, S. Grimes, D. L. Anderson, et al. 2001. The bacteriophage f29 portal motor can package DNA against a large internal force. Nature. 413:748-752.
7. Shields, S. A., M. J. Brisco, T. M. A. Wilson, and R. Hull. 1989. Southern bean mosaic virus RNA remains associated with swollen virions during translation in wheat germ cell-free extracts. Virology. 171:602-606.
8. Santos, N. C., and M. A. R. B. Castanho. 2004. An overview of the biophysical applications of atomic force microscopy. Biophys. Chem. 107:133-149. (Pubitemid 38220955)
9. Falvo, M. R., S. Washburn, R. Superfine, M. Finch, J. F. P. Brooks, et al. 1997. Manipulation of individual viruses: friction and mechanical properties. Biophys. J. 72:1396-1403.
10. Ohnesorge, F. M., J. K. H. Härber, W. Häberle, C. Czerny, D. P. E. Smith, et al. 1997. AFM review study on pox viruses and living cells. Biophys. J. 73:2183-2194.
11. Kuznetsov, Y. G., A. J. Malkin, R. W. Lucas, M. Plomp, and A. McPherson. 2001. Imaging of viruses by atomic force microscopy. J. Gen. Virol. 82:2025-2034. (Pubitemid 32827582)
12. Kuznetsov, Y. G., J. R. Gurnon, J. L. V. Etten, and A. McPherson. 2005. Atomic force microscopy investigation of a chlorella virus, PBCV-1. J. Struct. Biol. 149:256-263. (Pubitemid 40250059)
13. Michel, J. P., I. L. Ivanovska, M. M. Gibbons, W. S. Klug, C. M. Knobler, et al. 2006. Nanoindentation studies of full and empty viral capsids and the effects of capsid protein mutations on elasticity and strength. Proc. Natl. Acad. Sci. USA. 103:6184-6189.
14. Schmatulla, A., N. Maghelli, and O. Marti. 2007. Micromechanical properties of tobacco mosaic viruses. J. Microsc. 225:264-268. (Pubitemid 46434878)
15. Uetrecht, C., C. Versluis, N. R. Watts, W. H. Roos, G. J. L. Wuite, et al. 2008. High-resolution mass spectrometry of viral assemblies: molecular composition and stability of dimorphic hepatitis B virus capsids. Proc. Natl. Acad. Sci. USA. 105:9216-9220.
16. Lyobschenko, Y. L., P. I. Oden, D. Lampner, S. M. Lindsay, and K. A. Dunker. 1993. Atomic force microscopy of DNA and bacteriophage in air, water and propanol: the role of adhesion forces. Nucleic Acids Res. 21:1117-1123.
17. Plomp, M., M. K. Rice, E. K. Wagner, A. McPherson, and A. J. Malkin. 2002. Rapid visualization at high resolution of pathogens by atomc force microscopy: structural studies of herpes simplex virus-1. Am. J. Pathol. 160:1959-1966.
18. Kuznetsov, Y. G., S. Daijogo, J. Zhou, B. L. Semler, and A. McPherson. 2007. Atomic force microscopy analysis of icosahedral virus RNA. J. Mol. Biol. 347:41-52.
19. Kol, N., Y. Shi, D. Barlam, R. Z. Shneck, M. S. Kay, et al. 2007. A stiffness switch in human immunodeficiency virus. Biophys. J. 92:1777-1783.
20. Kol, N., M. Gladnikoff, D. Barlam, R. Z. Shneck, A. Rein, et al. 2006. Mechanical properties of murine leukemia virus particles: effect of maturation. Biophys. J. 91:767-774.
21. vanovska, I. L., P. J. de Pablo, B. Ibarra, G. Sgalari, F. C. MacKintosh, et al. 2004. Bacteriophage capsids: tough nanoshells with complex elastic properties. Proc. Natl. Acad. Sci. USA. 101:7600-7605.
22. Ivanovska, I., G. Wuite, B. Joensson, and A. Evilevitch. 2007. Internal DNA pressure modifies stability of WT phage. Proc. Natl. Acad. Sci. USA. 104:9603-9608. (Pubitemid 47175313)
23. Carrasco, C., A. Carreira, I. A. T. Schaap, P. A. Serena, J.Gomez-Herrero, et al. 2006. DNA-mediated anisotropic mechanical reinforcement of a virus. Proc. Natl. Acad. Sci. USA. 103:13706-13711.
24. Tama, F., and C. L. Brooks III. 2005. Diversity and identity of mechanical properties of icosahedral viral capsids studied with elastic network normal mode analysis. J. Mol. Biol. 345:299-314. (Pubitemid 39574852)
25. Hespenheide, B. M., D. J. Jacobs, and M. F. Thorpe. 2004. Structural rigidity in the capsid assembly of cowpea chlorotic mottle virus. J. Phys. Condens. Matter. 16:S5055-S5064.
26. Zandi, R., and D. Reguera. 2005. Mechanical properties of viral capsids. Phys. Rev. E. 72:021917.
27. Vliegenthart, G. A., and G. Gompper. 2006. Mechanical deformation of spherical viruses with icosahedral symmetry. Biophys. J. 91:834-841. (Pubitemid 44161915)
28. Widom, M., J. Lidmar, and D. R. Nelson. 2007. Soft modes near the buckling transition of icosahedral shells. Phys. Rev. E. 76:031911. (Pubitemid 47443109)
29. Arkhipov, A., P. L. Freddolino, and K. Schulten. 2006. Stability and dynamics of virus capsids described by coarse-grained modeling. Structure. 14:1767-1777.
30. Gräter, F., J. Shen, H. Jiang, M. Gautel, and H. Grubmüller. 2005. Mechanically induced titin kinase activation studied by force-probe molecular dynamics simulations. Biophys. J. 88:790-804. (Pubitemid 40975919)
31. Marszalek, P. E., H. Lu, H. Li, M. Carrion-Vazquez, A. F. Oberhauser, et al. 1999. Mechanical unfolding intermediates in titin modules. Nature. 402:100-103.
32. Freddolino, P. L., A. S. Arkhipov, S. B. Larson, A. McPherson, and K. Schulten. 2006. Molecular dynamics simulations of the complete satellite tobacco mosaic virus. Structure. 14:437-449. (Pubitemid 43363477)
33. Rossmann, M. G., C. Abad-Zapatero, and M. R. N. Murthy. 1983. Structural comparisons of some small spherical plant viruses. J. Mol. Biol. 165:711-736.
34. Rossmann, M. G., and J. E. Johnson. 1989. Icosahedral RNA virus structures. Annu. Rev. Biochem. 58:533-573.
35. Hsu, C. H., O. P. Sehgal, and E. E. Pickett. 1976. Stabilizing effect of divalent metal ions on virions of southern bean mosaic virus. Virology. 69:587-595.
36. Hull, R. 1977. The stabilization of the particles of turnip rosette virus and other members of the southern bean mosaic virus group. Virology. 79:58-66. (Pubitemid 8129895)
37. Hull, R. 1978. The stabilization of the particles of turnip rosette virus: III. Divalent cations. Virology. 89:418-422.
38. Rayment, I., J. E. Johnson, and M. G. Rossmann. 1979. Metal-free southern bean mosaic virus crystals. J. Biol. Chem. 254:5243-5245. (Pubitemid 9227477)
39. Brisco, M., C. Haniff, R. Hull, T. M. A. Wilson, and D. B. Sattelle. 1986. The kinetics of swelling of southern bean mosaic virus: a study using photon correlation spectroscopy. Virology. 148:218-220.
40. Grubmüller, H., B. Heymann, and P. Tavan. 1996. Ligand binding: molecular mechanics calculation of the streptavidin-biotin rupture force. Science. 271:997-999.
41. Heymann, B., and H. Grubmüller. 2001. Molecular dynamics force probe simulations of antibody/antigen unbinding: entropic control and nonadditivity of unbinding forces. Biophys. J. 81:1295-1313.
42. Silva, A. M., and M. G. Rossmann. 1985. The refinement of southern bean mosaic virus in reciprocal space. Acta Crystallogr. B. 41:147-157.
43. Silva, A. M., and M. G. Rossmann. 1987. Refined structure of southern bean mosaic virus at 2.9 Å resolution. J. Mol. Biol. 197:69-87.
44. Reddy, V. S., P. Natarajan, B. Okerberg, K. Li, K. V. Damodaran, R. T. Morton, C. L. Brooks III, and J.E. Johnson. 2001. Virus Particle Explorer (VIPER), a website of viral capsid structures and their computational analyses. J. Virol. 75:11943-11947.
45. Natarajan, P., G. C. Lander, C. M. Shepherd, V. S. Reddy, C. L. Brooks, et al. 2005. Exploring icosahedral virus structures with VIPER. Nature. 3:809-817.
46. van der Spoel, D., E. Lindahl, B. Hess, G. Groenhof, A. E. Mark, et al. 2005. GROMACS: fast, flexible, and free. J. Comput. Chem. 26:1701-1718.
47. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
48. Jorgensen, W. L., and J. Tirado-Rives. 1988. The OPLS potential function for proteins. Energy minimization of cyclic peptides and crambin. J. Am. Chem. Soc. 110:1657-1666.
49. Berendsen, H. J. L., J. P. M. Postma, W. F. van Gunsteren, A. D. Nola, and J. R. Haak. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
50. Darden, T., D. York, and L. Pedersen. 1993. Particle mesh Ewald - an N log(N) method for Ewald sums in large systems. J. Chem. Phys. 98:10089-10092.
51. Hess, B., H. Bekker, H. J. C. Berendsen, and J. G. E. M. Fraaije. 1997. Lincs: a linear constraint solver for molecular simulations. J. Comput. Chem. 18:1463-1472.
52. Kutzner, C., D. van der Spoel, M. Fechner, E. Lindahl, U. W. Schmitt, et al. 2007. Speeding up parallel GROMACS on high-latency networks. J. Comput. Chem. 28:2075-2084.
53. Hess, B., C. Kutzner, D. van der Spoel, and E. Lindahl. 2008. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4:435-447.
54. Silva, A. M., R. E. Cachau, and D. J. Goldstein. 1987. Ion channels in southern bean mosaic virus capsid. Biophys. J. 52:595-602.
55. Jorgensen, W. L., and J. D. Madura. 1985. Temperature and size dependence for Monte Carlo simulations of TIP4P water. Mol. Phys. 56:1381-1392.
56. Bertolini, D., and A. Tani. 1995. Stress tensor and viscosity of water: molecular dynamics and generalized hydrodynamics results. Phys. Rev. E. 52:1699.
57. Bocquet, L., and J. -L. Barrat. 1993. Hydrodynamic boundary conditions, correlation functions, and Kubo relations for confined fluids. Phys. Rev. E. 49:3079-3092.
58. Schmidt, J. R., and J. L. Skinner. 2003. Hydrodynamic boundary conditions, the Stokes-Einstein law, the long-time tails in the Brownian limit. J. Chem. Phys. 119:8062-8068.
59. Raschke, T. M., J. Tsai, and M. Levitt. 2001. Quantification of the hydrophobic interaction by simulations of the aggregation of small hydrophobic solutes in water. Proc. Natl. Acad. Sci. USA. 98:5965-5969. (Pubitemid 32488176)
60. Reynolds, J. A., D. B. Gilbert, and C. Tanford. 1974. Empirical correlation between hydrophobic free energy and aqueous cavity surface area. Proc. Natl. Acad. Sci. USA. 71:2925-2927.
61. Merkel, R., P. Nassoy, A. Leung, K. Ritchie, and E. Evans. 1999. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature. 397:50-53. (Pubitemid 29038244)
62. Puchner, E., A. Alexandrovitch, B. Brandmeier, U. Hensen, L. Schäfer, et al. 2008. Mechanically activated ATP binding of the titin kinase domain revealed by single-molecule force spectroscopy. Proc. Natl. Acad. Sci. USA. 105:13385-13390.
63. Bell, G. I. 1978. Models for the specific adhesion of cells to cells. Science. 200:618-627.
64. Florin, E. L., V. T. Moy, and H. E. Gaub. 1994. Ligand binding: molecular mechanics calculation of the streptavidin-biotin rupture force. Science. 264:415-417.
65. Heymann, B., and H. Grubmüller. 2000. Dynamic force spectroscopy of molecular adhesion bonds. Phys. Rev. Lett. 84:6126-6128.
66. Hummer, G., and A. Szabo. 2003. Kinetics from nonequilibrium singlemolecule pulling experiments. Biophys. J. 85:5-15. (Pubitemid 36753612)
67. Evstigneev, M., and P. Reimann. 2004. Rate description in friction force microscopy. Europhys. Lett. 67:907-913. (Pubitemid 39315682)
68. Evans, E. A., and D. A. Calderwood. 2007. Forces and bond dynamics in cell adhesion. Science. 316:1148-1153. (Pubitemid 46877469)
69. Nguyen, T. T., R. F. Bruinsma, and W. M. Gelbart. 2005. Elasticity theory and shape transitions of viral shells. Phys. Rev. E. 72:051923.
70. Reddy, V. S., H. A. Giesing, R. T. Morton, A. Kumar, C. B. Post, et al. 2002. Energetics of quasiequivalence: computational analysis of protein-protein interactions in icosahedral viruses. Biophys. J. 74:546-558.
71. Zink, M., K. Samwer, W. L. Johnson, and S. G. Mayr. 2006. Validity of temperature and time equivalence in metallic glasses during shear deformation. Phys. Rev. B. 74:012201.
72. Ackbarow, T., X. Chen, S. Keten, and M. J. Buehler. 2007. Hierarchies, multiple energy barriers, and robustness govern the fracture mechanics of alpha-helical and beta-sheet protein domains. Proc. Natl. Acad. Sci. USA. 16:16410-16415.