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Nonlinear mechanical modeling of cell adhesion. (English) Zbl 1397.92057

Summary: Cell adhesion, which is mediated by the receptor-ligand bonds, plays an essential role in various biological processes. Previous studies often described the force-extension relationship of receptor-ligand bond with linear assumption. However, the force-extension relationship of the bond is intrinsically nonlinear, which should have significant influence on the mechanical behavior of cell adhesion. In this work, a nonlinear mechanical model for cell adhesion is developed, and the adhesive strength was studied at various bond distributions. We find that the nonlinear mechanical behavior of the receptor-ligand bonds is crucial to the adhesive strength and stability. This nonlinear behavior allows more bonds to achieve large bond force simultaneously, and therefore the adhesive strength becomes less sensitive to the change of bond density at the outmost periphery of the adhesive area. In this way, the strength and stability of cell adhesion are soundly enhanced. The nonlinear model describes the cell detachment behavior better than the linear model.

MSC:

92C10 Biomechanics
92C37 Cell biology
74L15 Biomechanical solid mechanics
Full Text: DOI

References:

[1] Arnold, M.; Cavalcanti-Adam, E.A.; Glass, R.; Blummel, J.; Eck, W.; Kantlehner, M.; Kessler, H.; Spatz, J.P., Activation of integrin function by nanopatterned adhesive interfaces, Chemphyschem, 5, 383-388, (2004)
[2] Bayas, M.V.; Schulten, K.; Leckband, D., Forced detachment of the CD2-CD58 complex, Biophys. J., 84, 2223-2233, (2003)
[3] Bell, G.I.; Dembo, M.; Bongrand, P., Cell adhesion. competition between nonspecific repulsion and specific bonding, Biophys. J., 45, 1051-1064, (1984)
[4] Brown, E.J., Adhesive interactions in the immune system, Trends cell biol., 7, 289-295, (1997)
[5] Buehler, M.J.; Yao, H.; Gao, H.; Ji, B., Cracking and adhesion at small scales: atomistic and continuum studies of flaw tolerant nanostructures, Modell. simul. mater. sci. eng., 14, 799-816, (2006)
[6] Cavalcanti-Adam, E.A.; Tomakidi, P.; Bezler, M.; Spatz, J.P., Geometric organization of the extracellular matrix in the control of integrin-mediated adhesion and cell function in osteoblasts, Progr. orthodont., 6, 232-237, (2005)
[7] Dembo, M.; Torney, D.C.; Saxman, K.; Hammer, D., The reaction-limited kinetics of membrane-to-surface adhesion and detachment, Proc. R. soc. lond. ser. B, 234, 55-83, (1988)
[8] DiMilla, P.A.; Barbee, K.; Lauffenburger, D.A., Mathematical model for the effects of adhesion and mechanics on cell migration speed, Biophys. J., 60, 15-37, (1991)
[9] Evans, E.A., Bending elastic modulus of red blood cell membrane derived from buckling instability in micropipet aspiration tests, Biophys. J., 43, 27-30, (1983)
[10] Evans, E.A., Detailed mechanics of membrane-membrane adhesion and separation. I. continuum of molecular cross-bridges, Biophys. J., 48, 175-183, (1985)
[11] Evans, E.A., Detailed mechanics of membrane-membrane adhesion and separation. II. discrete kinetically trapped molecular cross-bridges, Biophys. J., 48, 185-192, (1985)
[12] Evans, E.; Ritchie, K., Dynamic strength of molecular adhesion bonds, Biophys. J., 72, 1541-1555, (1997)
[13] Freund, L.B.; Lin, Y., The role of binder mobility in spontaneous adhesive contact and implications for cell adhesion, J. mech. phys. solids, 52, 2455-2472, (2004) · Zbl 1084.74034
[14] Gallant, N.D.; Michael, K.E.; Garcia, A.J., Cell adhesion strengthening: contributions of adhesive area, integrin binding, and focal adhesion assembly, Mol. biol. cell, 16, 4329-4340, (2005)
[15] Gallant, N.D.; Garcıa, A.J., Model of integrin-mediated cell adhesion strengthening, J. biomech., 40, 1301-1309, (2007)
[16] Gao, H.; Ji, B., Modeling fracture in nanomaterials via a virtual internal bond method, Eng. fract. mech., 70, 1777-1791, (2003)
[17] Gao, H.; Yao, H., Shape insensitive optimal adhesion of nanoscale fibrillar structures, Proc. natl. acad. sci. USA, 101, 7851-7856, (2004)
[18] Gao, H.; Ji, B.; Jager, I.L.; Arzt, E.; Fratzl, P., From the cover: materials become insensitive to flaws at nanoscale: lessons from nature, Proc. natl. acad. sci. USA, 100, 5597-5600, (2003)
[19] Gao, H.; Shi, W.; Freund, L.B., Mechanics of receptor-mediated endocytosis, Proc. natl. acad. sci. USA, 102, 9469-9474, (2005)
[20] Geiger, B.; Bershadsky, A., Assembly and mechanosensory function of focal contacts, Curr. opin. cell biol., 13, 584-592, (2001)
[21] Gimbrone, M.A.; Nagel, T.; Topper, J.N., Biomechanical activation: an emerging paradigm in endothelial adhesion biology, J. clin. invest., 99, 1809-1813, (1997)
[22] Gracheva, M.E.; Othmer, H.G., A continuum model of motility in ameboid cells, Bull. math. biol., 66, 167-193, (2004) · Zbl 1334.92055
[23] Gumbiner, B.M., Cell adhesion: the molecular basis of tissue architecture and morphogenesis, Cell, 84, 345-357, (1996)
[24] Hanley, W.; McCarty, O.; Jadhav, S.; Tseng, Y.; Wirtz, D.; Konstantopoulos, K., Single molecule characterization of P-selectin/ligand binding, J. biol. chem., 278, 10556-10561, (2003)
[25] Ji, B.; Gao, H., Mechanical properties of nanostructure of biological materials, J. mech. phys. solids, 52, 1963-1990, (2004) · Zbl 1115.74348
[26] Ji, B.; Gao, H., A study of fracture mechanisms in biological nano-composites via the virtual internal bond model, Mater. sci. eng. A, 366, 96-103, (2004)
[27] Lu, S.; Long, M., Forced dissociation of selectin – ligand complexes using steered molecular dynamics simulation, Mol. cell biomech., 2, 161-177, (2004)
[28] Marshall, B.T.; Long, M.; Piper, J.W.; Yago, T.; McEver, R.P.; Zhu, C., Direct observation of catch bonds involving cell-adhesion molecules, Nature, 423, 190-193, (2003)
[29] Marshall, B.T.; Sarangapani, K.K.; Lou, J.H.; McEver, R.P.; Zhu, C., Force history dependence of receptor – ligand dissociation, Biophys. J., 88, 1458-1466, (2005)
[30] Martinez, E.J.P.; Lanir, Y.; Einav, S., Effects of contact-induced membrane stiffening on platelet adhesion, Biomech. model. mechanobiol., 2, 157-167, (2004)
[31] Palsson, E.; Othmer, H.G., A model for individual and collective cell movement in dictyostelium discoideum, Proc. natl. acad. sci. USA, 97, 10448-10453, (2000)
[32] Sengers, B.G.; Taylor, M.; Please, C.P.; Oreffo, R.O.C., Computational modelling of cell spreading and tissue regeneration in porous scaffolds, Biomaterials, 28, 1926-1940, (2007)
[33] Tawil, N.; Wilson, P.; Carbonetto, S., Integrins in point contacts mediate cell spreading: factors that regulate integrin accumulation in point contacts vs. focal contacts, J. cell biol., 120, 261-271, (1993)
[34] Walter, N.; Selhuber, C.; Kessler, H.; Spatz, J.P., Cellular unbinding forces of initial adhesion processes on nanopatterned surfaces probed with magnetic tweezers, Nano lett., 6, 398-402, (2006)
[35] Ward, M.D.; Dembo, M.; Hammer, D.A., Kinetics of cell detachment: peeling of discrete receptor clusters, Biophys. J., 67, 2522-2534, (1994)
[36] Ward, M.D.; Hammer, D.A., A theoretical analysis for the effect of focal contact formation on cell-substrate attachment strength, Biophys. J., 64, 936-959, (1993)
[37] Wayner, E.A.; Orlando, R.A.; Cheresh, D.A., Integrins alpha v beta 3 and alpha v beta 5 contribute to cell attachment to vitronectin but differentially distribute on the cell surface, J. cell biol., 113, 919-929, (1991)
[38] Wehrle-Haller, B.; Imhof, B.A., The inner lives of focal adhesions, Trends cell biol., 12, 382-389, (2002)
[39] Yao, H.; Gao, H., Mechanics of robust and releasable adhesion in biology: bottom-up designed hierarchical structures of gecko, J. mech. phys. solids, 54, 1120-1146, (2006) · Zbl 1120.74636
[40] Zhu, C., Kinetics and mechanics of cell adhesion, J. biomech., 33, 23-33, (2000)
[41] Zhu, C.; Bao, G.; Wang, N., Cell mechanics: mechanical response, cell adhesion, and molecular deformation, Annu. rev. biomed. eng., 2, 189-226, (2000)
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