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Fluctuating Nonlinear Spring Model of Mechanical Deformation of Biological Particles

DOI: 10.1371/journal.pcbi.1004729

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Abstract:

The mechanical properties of virus capsids correlate with local conformational dynamics in the capsid structure. They also reflect the required stability needed to withstand high internal pressures generated upon genome loading and contribute to the success of important events in viral infectivity, such as capsid maturation, genome uncoating and receptor binding. The mechanical properties of biological nanoparticles are often determined from monitoring their dynamic deformations in Atomic Force Microscopy nanoindentation experiments; but a comprehensive theory describing the full range of observed deformation behaviors has not previously been described. We present a new theory for modeling dynamic deformations of biological nanoparticles, which considers the non-linear Hertzian deformation, resulting from an indenter-particle physical contact, and the bending of curved elements (beams) modeling the particle structure. The beams’ deformation beyond the critical point triggers a dynamic transition of the particle to the collapsed state. This extreme event is accompanied by a catastrophic force drop as observed in the experimental or simulated force (F)-deformation (X) spectra. The theory interprets fine features of the spectra, including the nonlinear components of the FX-curves, in terms of the Young’s moduli for Hertzian and bending deformations, and the structural damage dependent beams’ survival probability, in terms of the maximum strength and the cooperativity parameter. The theory is exemplified by successfully describing the deformation dynamics of natural nanoparticles through comparing theoretical curves with experimental force-deformation spectra for several virus particles. This approach provides a comprehensive description of the dynamic structural transitions in biological and artificial nanoparticles, which is essential for their optimal use in nanotechnology and nanomedicine applications.

References

[1]  Roos WH, Bruinsma R, Wuite GJL. Physical virology. Nat Phys. 2010;6:733–743. doi: 10.1038/nphys1797.
[2]  Ivanovska IL, de Pablo PJ, Ibarra B, Sgalari G, MacKintosh FC, Carrascosa JL, et al. Bacteriophage capsids: Tough nanoshells with complex elastic properties. Proc Natl Acad Sci USA. 2004;101(20):7600–7605. doi: 10.1073/pnas.0308198101. pmid:15133147
[3]  Hernando-Pèrez M, Pascual E, Aznar M, Ionel A, Castón JR, Luque A, et al. The interplay between mechanics and stability of viral cages. Nanoscale. 2014;6:2702–2709. doi: 10.1039/c3nr05763a.
[4]  Roos WH, Gertsman I, May ER, Brooks CL 3rd, Johnson JE, Wuite GJL. Mechanics of bacteriophage maturation. Proc Natl Acad Sci USA. 2012;109:2342–2347. doi: 10.1073/pnas.1109590109. pmid:22308333
[5]  Kol N, Shi Y, Tsvitov M, Barlam D, Shneck RZ, Kay MS, et al. A Stiffness Switch in Human Immunodeficiency Virus. Biophys J. 2007;92(5):1777–1783. doi: 10.1529/biophysj.106.093914. pmid:17158573
[6]  Perez-Berna AJ, Ortega-Esteban A, Menendez-Conejero R, Winkler DC, Menendez M, Steven AC, et al. The role of capsid maturation on adenovirus priming for sequential uncoating. J Biol Chem. 2012;287:31582–31595. doi: 10.1074/jbc.M112.389957. pmid:22791715
[7]  Roos WH, Radtke K, Kniesmeijer E, Geertsema H, Sodeik B, Wuite GJL. Scaffold expulsion and genome packaging trigger stabilization of herpes simplex virus capsid. Proc Natl Acad Sci USA. 2009;106:9673–9678. doi: 10.1073/pnas.0901514106. pmid:19487681
[8]  Snijder J, Reddy VS, May ER, Roos WH, Nemerow GR, Wuite GJL. Integrin and defensin modulate the mechanical properties of adenovirus. J Virol. 2013;87:2756. doi: 10.1128/JVI.02516-12. pmid:23269786
[9]  Baclayon M, Shoemaker GK, Uetrecht C, Crawford S, Estes M, Prasad B, Heck AJ, Wuite GJL, Roos WH. Pre-stress strenghtens the shell of Norwalk virus nanoparticles. Nano Lett. 2011;11:4865–4869. doi: 10.1021/nl202699r. pmid:21967663
[10]  Carrasco C, Carreira A, Schaap IAT, Serena PA, Gomez-Herrero J, Mateu MG, et al. DNA-mediated anisotropic mechanical reinforcement of a virus. Proc Natl Acad Sci USA. 2006;103:13706–13711. doi: 10.1073/pnas.0601881103. pmid:16945903
[11]  Michel JP, Ivanovska IL, Gibbons MM, Klug WS, Knobler CM, Wuite GJL, et al. Nanoindentation studies of full and empty viral capsids and the effects of capsid protein mutations on elasticity and strength. Proc Natl Acad Sci USA. 2006;103:6184–6189. doi: 10.1073/pnas.0601744103. pmid:16606825
[12]  Snijder J, Uetrecht C, Rose R, Sanchez R, Marti G, Agirre J, et al. Probing the biophysical interplay between a viral genome and its capsid. Nat Chem. 2013;5:502–509. doi: 10.1038/nchem.1627. pmid:23695632
[13]  Vaughan R, Tragesser B, Ni P, Ma X, Dragnea B, Kao CC. The tripartite virions of the brome mosaic virus have distinct physical properties that affect the timing of the infection process. J Virol. 2014;88:6483–6491. doi: 10.1128/JVI.00377-14. pmid:24672042
[14]  Ni P, Wang Z, Ma X, Das NC, Sokol P, Chiu W, et al. An examination of the electrostatic interactions between the N-terminal tail of the Brome Mosaic Virus coat protein and encapsidated RNAs. J Mol Biol. 2012;419:284–300. doi: 10.1016/j.jmb.2012.03.023. pmid:22472420
[15]  Kononova O, Snijder J, Brasch M, Cornelissen J, Dima RI, Marx KA, et al. Structural transitions and energy landscape for cowpea chlorotic mottle virus capsid mechanics from nanomanipulation in vitro and in silico. Biophys J. 2013;105(8):1893–1903. doi: 10.1016/j.bpj.2013.08.032. pmid:24138865
[16]  Gibbons MM, Klug WS. Influence of nonuniform geometry on nanoindentation of viral capsids. Biophys J. 2008;95:3640–3649. doi: 10.1529/biophysj.108.136176. pmid:18621831
[17]  Tama F, Brooks CL 3rd. Diversity and identity of mechanical properties of icosahedral viral capsids studied with elastic network normal mode analysis. J Mol Biol. 2005;345:299–314. doi: 10.1016/j.jmb.2004.10.054. pmid:15571723
[18]  Yang Z, Bahar I, Widom M. Vibrational dynamics of icosahedrally symmetric biomolecular assemblies compared with predictions based on continuum elasticity. Biophys J. 2009;96:4438–4448. doi: 10.1016/j.bpj.2009.03.016. pmid:19486668
[19]  Zink M, Grubmuller H. Mechanical Properties of the Icosahedral Shell of Southern Bean Mosaic Virus: A Molecular Dynamics Study. Biophys J. 2009;96:1350–1363. doi: 10.1016/j.bpj.2008.11.028. pmid:19217853
[20]  Zink M, Grubmuller H. Primary changes of the mechanical properties of Southern Bean Mosaic Virus upon calcium removal. Biophys J. 2010;98:687–695. doi: 10.1016/j.bpj.2009.10.047. pmid:20159165
[21]  Arkhipov A, Roos WH, Wuite GJL, Schulten K. Elucidating the mechanism behind irreversible deformation of viral capsids. Biophys J. 2009;97:2061–2069. doi: 10.1016/j.bpj.2009.07.039. pmid:19804738
[22]  Cieplak M, Robbins MO. Nanoindentation of virus capsids in a molecular model. J Chem Phys. 2010;132:015101. doi: 10.1063/1.3276287. pmid:20078182
[23]  May ER, Aggarwal A, Klug WS, Brooks CL 3rd. Viral capsid equilibrium dynamics reveals nonuniform elastic properties. Biophys J. 2011;100:L59–L61. doi: 10.1016/j.bpj.2011.04.026. pmid:21641297
[24]  Zhmurov A, Dima RI, Kholodov Y, Barsegov V. SOP-GPU: Accelerating biomolecular simulations in the centisecond timescale using graphics processors. Proteins. 2010;78(14):2984–2999. doi: 10.1002/prot.22824. pmid:20715052
[25]  Zhmurov A, Rybnikov K, Kholodov Y, Barsegov V. Generation of random numbers on graphics processors: Forced indentation in silico of the Bacteriophage HK97. J Phys Chem B. 2011;115(18):5278–5288. doi: 10.1021/jp109079t. pmid:21194190
[26]  Kononova O, Kholodov Y, Theisen KE, Marx KA, Dima RI, Ataullakhanov FI, et al. Tubulin bond energies and microtubule biomechanics determined from nanoindentation in silico. J Am Chem Soc. 2014;136(49):17036–17045. doi: 10.1021/ja506385p. pmid:25389565
[27]  Ishikura T, Hatano T, Yamato T. Atomic stress tensor analysis of proteins. Chem Phys Lett. 2012;539–540:144–150.
[28]  Rafii-Tabar H. Computational modelling of thermo-mechanical and transport properties of carbon nanotubes. Phys Rep. 2004;390:235. doi: 10.1016/j.physrep.2003.10.012.
[29]  Landau LD, Lifshitz EM. Theory of Elasticity. Pergamon Press; 1986.
[30]  Johnson KL. Contact Mechanics. Cambridge University Press; 1985.
[31]  Timoshenko SP. Theory of Elastic Stability. McGraw-Hill Book Company, Inc; 1961.
[32]  Gumbel EJ. Statistics of Extremes. Dover Publications; 2004.
[33]  Gibbons MM, Klug WS. Nonlinear finite-element analysis of nanoindentation of viral capsids. Phys Rev E. 2007;75:031901. doi: 10.1103/PhysRevE.75.031901.
[34]  Zlotnick A. Viruses and the physics of soft condensed matter. Proc. Natl. Acad. Sci. USA. 2004;101:15549–15550. doi: 10.1073/pnas.0406935101. pmid:15505200
[35]  Zhmurov A, Kononova O, Litvinov RI, Dima RI, Barsegov V, Weisel JW. Mechanical transition from α-helical coiled coils to β-sheets in fibrin(ogen). J Am Chem Soc. 2012;134(50):20396–20402. doi: 10.1021/ja3076428. pmid:22953986
[36]  Hyeon C, Dima RI, Thirumalai D. Pathways and kinetic barriers in mechanical unfolding and refolding of RNA and proteins. Structure. 2006;14(11):1633–1645. doi: 10.1016/j.str.2006.09.002. pmid:17098189
[37]  Mickler M, Dima RI, Dietz H, Hyeon C, Thirumalai D, Rief M. Revealing the bifurcation in the unfolding pathways of GFP using single molecule experiments and simulations. Proc Natl Acad Sci USA. 2007;104(51):20268–20273. doi: 10.1073/pnas.0705458104. pmid:18079292
[38]  Snijder J, Ivanovska IL, Baclayon M, Roos WH, Wuite GJL. Probing the impact of loading rate on the mechanical properties of viral nanoparticles. Micron. 2012;43:1343–1350. doi: 10.1016/j.micron.2012.04.011. pmid:22609100
[39]  Baclayon M, Wuite GJL, Roos WH. Imaging and manipulation of single viruses by atomic force microscopy. Soft Matter. 2010;6:5273–5285. doi: 10.1039/b923992h.
[40]  de Pablo PJ, Schaap IAT, MacKintosh FC, Schmidt CF. Deformation and collapse of microtubules on the nanometer scale. Phys Rev Lett. 2003;91:098101–098104. doi: 10.1103/PhysRevLett.91.098101. pmid:14525215

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