title: Fluctuating Nonlinear Spring Model of Mechanical Deformation of Biological Particles.
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.
authors.affiliation: Department of Chemistry, University of Massachusetts, Lowell, Massachusetts, United States of America.|Moscow Institute of Physics and Technology, Moscow Region, Russia.
authors.forename: Olga
authors.initials: O
authors.lastname: Kononova
authors.affiliation: Natuur- en Sterrenkunde and LaserLab, Vrije Universiteit, Amsterdam, The Netherlands.
authors.forename: Joost
authors.initials: J
authors.lastname: Snijder
authors.affiliation: Moscow Institute of Physics and Technology, Moscow Region, Russia.|Institute of Computer Aided Design Russian Academy of Science, Moscow, Russia.
authors.forename: Yaroslav
authors.initials: Y
authors.lastname: Kholodov
authors.affiliation: Department of Chemistry, University of Massachusetts, Lowell, Massachusetts, United States of America.
authors.forename: Kenneth A
authors.initials: KA
authors.lastname: Marx
authors.affiliation: Natuur- en Sterrenkunde and LaserLab, Vrije Universiteit, Amsterdam, The Netherlands.
authors.forename: Gijs J L
authors.initials: GJ
authors.lastname: Wuite
authors.affiliation: Moleculaire Biofysica, Zernike instituut, Rijksuniversiteit Groningen, Groningen, The Netherlands.
authors.forename: Wouter H
authors.initials: WH
authors.lastname: Roos
authors.affiliation: Department of Chemistry, University of Massachusetts, Lowell, Massachusetts, United States of America.|Moscow Institute of Physics and Technology, Moscow Region, Russia.
authors.forename: Valeri
authors.initials: V
authors.lastname: Barsegov
mesh_terms: D001696:Biomechanical Phenomena / Q000502:physiology*; D036022:Capsid Proteins / Q000737:chemistry / Q000502:physiology / Q000648:ultrastructure*; D019295:Computational Biology; D056004:Molecular Dynamics Simulation; D017711:Nonlinear Dynamics; D011487:Protein Conformation; D014771:Virion / Q000737:chemistry / Q000502:physiology / Q000648:ultrastructure*
chemical_list: D036022:Capsid Proteins
references.citation: Biophys J. 2009 Jun 3;96(11):4438-48
references.pmid: 19486668
references.citation: Proc Natl Acad Sci U S A. 2009 Jun 16;106(24):9673-8
references.pmid: 19487681
references.citation: Biophys J. 2009 Oct 7;97(7):2061-9
references.pmid: 19804738
references.citation: J Chem Phys. 2010 Jan 7;132(1):015101
references.pmid: 20078182
references.citation: Biophys J. 2010 Feb 17;98(4):687-95
references.pmid: 20159165
references.citation: Proteins. 2010 Nov 1;78(14):2984-99
references.pmid: 20715052
references.citation: J Phys Chem B. 2011 May 12;115(18):5278-88
references.pmid: 21194190
references.citation: Biophys J. 2011 Jun 8;100(11):L59-61
references.pmid: 21641297
references.citation: Nano Lett. 2011 Nov 9;11(11):4865-9
references.pmid: 21967663
references.citation: Proc Natl Acad Sci U S A. 2012 Feb 14;109(7):2342-7
references.pmid: 22308333
references.citation: J Mol Biol. 2012 Jun 22;419(5):284-300
references.pmid: 22472420
references.citation: Micron. 2012 Dec;43(12):1343-50
references.pmid: 22609100
references.citation: J Biol Chem. 2012 Sep 7;287(37):31582-95
references.pmid: 22791715
references.citation: J Am Chem Soc. 2012 Dec 19;134(50):20396-402
references.pmid: 22953986
references.citation: J Virol. 2013 Mar;87(5):2756-66
references.pmid: 23269786
references.citation: Nat Chem. 2013 Jun;5(6):502-9
references.pmid: 23695632
references.citation: Biophys J. 2013 Oct 15;105(8):1893-903
references.pmid: 24138865
references.citation: Nanoscale. 2014 Mar 7;6(5):2702-9
references.pmid: 24452242
references.citation: Phys Rev Lett. 2003 Aug 29;91(9):098101
references.pmid: 14525215
references.citation: Proc Natl Acad Sci U S A. 2004 May 18;101(20):7600-5
references.pmid: 15133147
references.citation: Proc Natl Acad Sci U S A. 2004 Nov 2;101(44):15549-50
references.pmid: 15505200
references.citation: J Mol Biol. 2005 Jan 14;345(2):299-314
references.pmid: 15571723
references.citation: Proc Natl Acad Sci U S A. 2006 Apr 18;103(16):6184-9
references.pmid: 16606825
references.citation: Proc Natl Acad Sci U S A. 2006 Sep 12;103(37):13706-11
references.pmid: 16945903
references.citation: Structure. 2006 Nov;14(11):1633-45
references.pmid: 17098189
references.citation: Biophys J. 2007 Mar 1;92(5):1777-83
references.pmid: 17158573
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2007 Mar;75(3 Pt 1):031901
references.pmid: 17500720
references.citation: Proc Natl Acad Sci U S A. 2007 Dec 18;104(51):20268-73
references.pmid: 18079292
references.citation: Biophys J. 2008 Oct;95(8):3640-9
references.pmid: 18621831
references.citation: Biophys J. 2009 Feb 18;96(4):1350-63
references.pmid: 19217853
references.citation: J Virol. 2014 Jun;88(11):6483-91
references.pmid: 24672042
references.citation: J Am Chem Soc. 2014 Dec 10;136(49):17036-45
references.pmid: 25389565