Nanoindentation of 35 Virus Capsids in a Molecular Model: Relating Mechanical Properties to Structure

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Cieplak, Marek ^a   Robbins, Mark O ^b  

^a INSTITUTE OF PHYSICS   (Poland)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; COVALENT BOND; COWPEA MOSAIC VIRUS; ELASTICITY; MOLECULAR MODEL; MOSAIC VIRUS; NONHUMAN; PROTEIN STRUCTURE; SIMULATION; STRUCTURE ANALYSIS; TEMPERATURE DEPENDENCE; VIRUS CAPSID; VIRUS DETECTION;

ALGORITHMS; BIOMECHANICAL PHENOMENA; CAPSID; COMPUTER SIMULATION; MODELS, MOLECULAR; MODELS, THEORETICAL; TEMPERATURE;

MIRIDAE; PANICUM MOSAIC SATELLITE VIRUS; SPARTINA MOTTLE VIRUS;

EID: 84879059545     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063640     Document Type: Article

References (41)

1. Buenemann M, Lenz P, (2007) Mechanical limits of viral capsids. Proc Natl Acad Sci USA 104: 9925-9930.
2. Buenemann M, Lenz P, (2008) Elastic properties and mechanical stability of chiral and filled capsids. Phys Rev E 78: 051924.
3. Roos WH, Bruisma R, Wuite GJL, (2010) Physical virology. Nature Physics 6: 733-743.
4. Caspar D, Klug A, (1962) Cold Spring Harbor Symposium on Quantitative Biology. 27: 1-24.
5. Carrillo-Tripp M, Shepherd CM, Borelli IA, Venkataraman S, Lander G, et al. (2009) VIPERdb2: and enhanced and web API enabled relational database for structural virology. Nucl Acids Res 37: D436-D442 Available: http://viperdb.scripps.edu/.
6. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The Protein Data Bank. Nucl Acids Res 28: 235-242.
7. Carrasco C, Carreira A, Schaap IAT, Serena PA, Gomez-Herrero J, et al. (2006) DNA-mediated anisotropic mechanical reinforcement of a virus. Proc Natl Acad Sci USA 103: 13706-13711.
8. Carrasco C, Castellanos M, de Pablo PJ, Mateu MG, (2008) Manipulation of the mechanical properties of a virus by protein engineering. Proc Natl Acad Sci USA 105: 4150-4155.
9. Castellanos M, Perez R, Carillo PJP, de Pablo PJ, Mateu MG, (2012) Mechanical disassembly of single virus particles reveals kinetic intermediates predicted by theory. Bioph J 102: 2615-2624.
10. Michel JP, Ivanovska IL, Gibbons MM, Klug WS, Knobler CM, 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.
11. Klug WS, Bruinsma RF, Michel JP, Knobler CM, Ivanovska IL, et al. (2006) Failure of viral shells. Phys Rev Lett 97: 228101.
12. Baclayon M, Shoemaker GK, Uetrecht C, Crawford SE, Estes MK, et al. (2011) Prestress strengthens the shell of Norwalk virus nanoparticles. Nano Lett 11: 4865-4869.
13. Arkhipov A, RoosWH, Wuite GJL, Schulten K, (2009) Elucidating the mechanism behind irreversible deformation of viral capsids. Biophys J 97: 2061-2069.
14. Roos WH, Gibbons MM, Arkhipov A, Uetrecht C, Watts NR, et al. (2010) Sqeezing protein shells: How continuum elastic models, molecular dynamics simulations and experiments coalesce at the 15 nanoscale. Biophys J 99: 1175-1181.
15. Roos WH, Gertsman I, May ER, Brooks III CL, Johnson JE, et al. (2012) Mechanics of bacteriophage maturation. Proc Natl Acad Sci USA 109: 2342-2347.
16. Cieplak M, Robbins MO, (2010) Nanoindentation of virus capsids in a molecular model. J Chem Phys 132: 015101.
17. Ding J, Smith AD, Geisler SC, Ma X, Arnold GF, et al. (2002) Crystal structure of a human rhinovirus that displays part of the HIV-1 V3 loop and induces neutralizing antibodies against HIV-1. Structure 10: 999-1011.
18. Cieplak M, Hoang TX, (2003) Universality classes in folding times of proteins Biophys J. 84: 475-488.
19. Cieplak M, Hoang TX, Robbins MO, (2004) Thermal effects in stretching of Go-like models of titin and secondary structures. Proteins: Struct Funct Bio 56: 285-297.
20. Sułkowska JI, Cieplak M, (2007) Mechanical stretching of proteins - a theoretical survey of the Protein Data Bank. J Phys: Cond Mat 19: 283201.
21. Sułkowska JI, Cieplak M, (2008) Selection of optimal variants of Go-like models of proteins through studies of stretching. Biophys J 95: 3174-3191.
22. Sikora M, Sułkowska JI, Cieplak M, (2008) Mechanical strength of 17 132 model proteins and cysteine slipknots. PloS Comp Biol 5: e1000547.
23. Gibbons MM, Klug WS, (2007) Nonlinear finite-element analysis of nanoindentation of viral capsids. Phys Rev E 75: 031901.
24. GibbonsMM KlugWS, (2008) Influence of nonuniform geometry on nanoindentation of viral capsids. Biophys J 95: 3640-3649.
25. Allen MP, Tildesley DJ (1987) "Computer simulations of liquids". Oxford University Press, New York.
26. Tsai J, Taylor R, Chothia C, Gerstein M, (1999) The packing density in proteins: Standard radii and volumes. J Mol Biol 290: 253-266.
27. Reddy VS, Natarajan P, Okerberg B, Li K, Damodaran KV, et al. (2001) Virus Particle Explorer (VIPER), a website for virus capsid structures and their computational analyses. J Vir 75: 11943-11947.
28. Vriend G, Verduin BJM, Hemminga MA, (1986) Role of the N-terminal part of the coat protein in the assembly of cowpea chlorotic mottle virus. J Mol Biol 191: 453-460.
29. Speir JA, Munshi S, Wang G, Baker TS, Johnson JE, (1995) Structures of the native and swollen forms 16 of cowpea chlorotic mottle virus determined by X-ray crystallography and cro-electron microscopy. Structure 3: 63-78.
30. Grest GS, Kremer K, (1986) Molecular dynamics simulation for polymers in the presence of a heat bath. Phys Rev A 33: 3628-31.
31. Veitshans T, Klimov D, Thirumalai D, (1997) Protein folding kinetics: time scales, pathways, and energy landscapes in terms of sequence-dependent properties. Folding Des 2: 1-22.
32. Szymczak P, Cieplak M, (2006) Stretching of proteins in a uniform flow. J Chem Phys 125: 164903.
33. Steele WA, (1973) Physical interaction of gases with crystalline solids. 1. Gas-solid energies and properties of isolated adsorbed atoms. Surf Sci 36: 317-352.
34. Zink M, Grubmueller H, (2009) Mechanical properties of the icosahedral shell of southern bean mosaic virus: a molecular dynamics study. Biophys J 96: 1350-1363.
35. Feng S, Sen PN, (1984) Percolation on elastic networks: new exponent and threshold. Phys Rev Lett 52: 217-219.
36. Jacobs DJ, Thorpe MF, (1995) Generic rigidity percolation: The pebble game. Phys Rev Lett 75: 4051-4.
37. Mao X, Xu N, Lubensky TC, (2010) Soft modes and elasticity of nearly isostatic lattices: Randomness and dissipation. Phys Rev Lett 104: 085504.
38. Liu AJ, Nagel SR, (2010) The jamming transition and the marginally jammed solids. Annu Rev Condens Matter Phys 1: 347-369.
39. Arkhipov A, Freddolino PL, Schulten K, (2006) Stability and dynamics of virus capsids described by coarse-grained modeling. Structure 14: 1767-1777.
40. Arkhipov A, Wouter HR, Wuite GJL, Schulten K, (2009) Elucidating the mechanism behind irreversible deformation of viral capsids. Bioph J 97: 2061-2069.
41. Tama F, Brooks III CL, (2005) Diversity and identity of mechanical properties of icosahedral viral capsids studied with elastic network normal mode analysis. J Mol Biol 345: 299-314.