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A bio-mechanical model for coupling cell contractility with focal adhesion formation. (English) Zbl 1171.74381
Summary: Focal adhesions (FAs) are large, multi-protein complexes that provide a mechanical link between the cytoskeletal contractile machinery and the extracellular matrix. They exhibit mechanosensitive properties; they self-assemble upon application of pulling forces and dissociate when these forces are decreased. We rationalize this mechano-sensitivity from thermodynamic considerations and develop a continuum framework in which the cytoskeletal contractile forces generated by stress fibers drive the assembly of the FA multi-protein complexes. The FA model has three essential features: (i) the low and high affinity integrins co-exist in thermodynamic equilibrium, (ii) the low affinity integrins within the plasma membrane are mobile, and (iii) the contractile forces generated by the stress fibers are in mechanical equilibrium and change the free energies of the integrins. A general two-dimensional framework is presented and the essential features of the model illustrated using one-dimensional examples. Consistent with observations, the coupled stress fiber and FA model predict that (a) the FAs concentrate around the periphery of the cell; (b) the fraction of the cell covered by FAs increases with decreasing cell size while the total FA intensity increases with increasing cell size; and (c) the FA intensity decreases substantially when cell contractility is curtailed.

MSC:
74L15 Biomechanical solid mechanics
92C10 Biomechanics
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[1] Balaban, N.Q.; Schwarz, U.S.; Riveline, D.; Goichberg, P.; Tzur, G.; Sabanay, I.; Mahalu, D.; Safran, S.; Bershadskay, A.; Addadi, L.; Geiger, B., Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates, Nat. cell biol., 3, 466-472, (2001)
[2] Bell, G.I., Models for the specific adhesions of cells to cells, Science, 200, 618-627, (1978)
[3] Bell, G.I.; Dembo, M.; Bongrand, P., Cell adhesion, Biophys. J., 45, 1051-1064, (1984)
[4] Bershadsky, A.D.; Balaban, N.Q.; Geiger, B., Adhesion dependent cell mechanosensitivity, Annu. rev. cell dev. biol, 19, 677-695, (2003)
[5] Boulbitch, A.; Guttenberg, Z.; Sackmann, E., Kinetics of membrane adhesion mediated by ligand-receptor interaction studied with a biomimetic system, Biophys. J, 81, 2743-2751, (2001)
[6] Brock, A.; Chang, E.; Ho, C.-C.; Leduc, P.; Jiang, X.; Whitesides, G.M.; Ingber, D.E., Geometric determinants of directional cell motility revealed using microcontact printing, Langmuir, 19, 1611-1617, (2003)
[7] Burridge, K.; Chrzanowska-Wodnicka, M., Focal adhesions, contractility and signaling, Annu. rev. cell dev. biol., 12, 463-469, (1996)
[8] Carman, C.V.; Springer, T.A., Integrin avidity regulation: are changes in affinity and conformation underemphasized?, Curr. opinion cell biol., 15, 547-556, (2003)
[9] Chen, C.S.; Alonso, J.L.; Ostuni, E.; Whitesides, G.M.; Ingber, D.E., Cell shape provides global control of focal adhesion assembly, Biochem. biophys. res. commun., 307, 355-361, (2003)
[10] Cluzel, C.; Saltel, F.; Lussi, J.; Paulhe, F.; Imhof, B.A.; Wehrle-Haller, B., The mechanisms and dynamics of αvβ3 integrin clustering in living cells, J. cell biol., 171, 383-392, (2005)
[11] Dembo, M.; Torney, D.C.; Saxman, K.; Hammer, D., The reaction-limited kinetics of membrane-to-surface adhesion and detachment, Proc. R. soc., B, 234, 55-83, (1988)
[12] Deshpande, V.S.; McMeeking, R.M.; Evans, A.G., A bio-chemo-mechanical model for cell contractility, Proc. nat. acad. sci. USA, 103, 14015-14020, (2006)
[13] Deshpande, V.S.; McMeeking, R.M.; Evans, A.G., A model for the contractility of the cytoskeleton including the effects of stress fiber formation and dissociation, Proc. R. soc., London, A, 463, 787-815, (2007) · Zbl 1131.92025
[14] Evans, E.A., Detailed mechanics of membrane-membrane adhesion and separation. I. continuum of molecular cross-bridges, Biophys. J., 48, 175-183, (1985)
[15] 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
[16] Gaskell, D.R., Introduction to metallurgical thermodynamics, (1973), McGraw-Hill
[17] Hill, A.V., The heat of shortening and the dynamic constants of muscle, Proc. R. soc., London. B, 126, 136-195, (1938)
[18] Hirth, J.P.; Lothe, J., Theory of dislocations, (1968), McGraw-Hill New York
[19] Hotchin, N.A.; Hall, A., The assembly of integrin adhesion complexes requires both extracellular matrix and intracellular rho/rac gtpases, J. cell biol., 131, 1857-1865, (1995)
[20] Hynes, R.O., Integrins: versatility, modulation and signalling in cell adhesion, Cell, 69, 11-25, (1992)
[21] Irvine, D.J.; Hue, K.-A.; Mayes, A.M.; Griffith, L.G., Simulations of cell-surface integrin binding to nanoscale clustered adhesion ligands, Biophys. J., 82, 120-132, (2002)
[22] Lauffenburger, D.A.; Linderman, J., Receptors. models for binding, trafficking, and signaling, (1996), Oxford University Press UK
[23] Leckband, D.; Israelachvili, J., Intermolecular forces in biology, Q. rev. biophys., 34, 105-267, (2001)
[24] Lennard-Jones, J.E., Cohesion, Proc. phys. soc., 43, 461-482, (1931) · Zbl 0002.37202
[25] Liu, P.; Zhang, Y.W.; Cheng, Q.H.; Lu, C., Simulations of the spreading of a vesicle on a substrate surface mediated by receptor – ligand binding, J. mech. phys. solids., 55, 1166-1181, (2007) · Zbl 1178.74108
[26] Lodish, H.; Berk, A.; Matsudaira, P.; Kaiser, C.A.; Krieger, M.; Scott, M.P.; Zipursky, S.L.; Darnell, J., Molecular cell biology, (2004), W.H. Freeman & Co. USA
[27] Malvern, L.E., Introduction to the mechanics of a continuum medium, (1969), Prentice-Hall Englewood Cliffs, NJ, USA · Zbl 0181.53303
[28] McCleverty, C.J.; Liddington, R.C., Engineered allosteric mutants of the integrin αMβ2 I domain: structural and functional studies, Biochem. J., 372, 121-127, (2003)
[29] Merkel, R.; Nassoy, P.; Leung, A.; Ritchie, K.; Evans, E., Energy landscapes of receptor – ligand bonds explored with dynamic force spectroscopy, Nature, 397, 50-53, (1999)
[30] Mullins, W.W., Theory of thermal grooving, J. appl. phy., 28, 333-339, (1957)
[31] Nicolas, A.; Safran, S.A., Limitation of cell adhesion by the elasticity of the extracellular matrix, Biophys. J., 91, 61-73, (2006)
[32] Nicolas, A.; Geiger, B.; Safran, S.A., Cell mechanosensitivity controls the anisotropy of focal adhesions, Proc. nat. acad. sci. USA, 101, 12520-12525, (2004)
[33] Novak, I.L.; Slepchenko, B.M.; Mogilner, A.; Loew, L.M., Cooperativity between cell contractility and adhesion, Phys. rev. lett., 93, 268109-1-268109-4, (2004)
[34] Parker, K.K.; Brock, A.L.; Brangwynne, C.; Mannix, R.J.; Wang, N.; Ostuni, E.; Geisse, N.A.; Adams, J.C.; Whitesides, G.M.; Ingber, D.E., Directional control of lamellipodia extension by constraining cell shape and orienting cell tractional forces, Faseb j, 16, 1195-1204, (2002)
[35] Pathak, A., Deshpande, V.S., McMeeking, R.M., Evans, A.G., 2007. Analysis of stress fiber and focal adhesion distributions of cells on micro-patterned substrates. J. R. Soc Interface, to appear.
[36] Petroll, W.M.; Ma, L.; Jester, J.V., Direct correlation of collagen matrix deformation with focal adhesion dynamics in living corneal fibroblasts, J. cell sci., 116, 1481-1491, (2003)
[37] Rinko, L.J.; Lawrence, M.B.; Guilford, W.H., The molecular mechanics of P- and L-selectin lectin domains binding to PSGL-1, Biophy. J., 86, 544-554, (2004)
[38] Shemesh, T.; Geiger, B.; Bershadsky, A.D.; Kozlov, M.M., Focal adhesions as mechanosensors: a physical mechanism, Proc. nat. acad. sci. USA, 102, 12383-12388, (2005)
[39] Tan, J.L.; Tien, J.; Pirone, D.M.; Gray, D.S.; Bhadriraju, K.; Chen, C.S., Cells lying on a bed of microneedles: an approach to isolate mechanical force, Proc. nat. acad. sci. USA, 100, 1484-1489, (2003)
[40] Théry, M.; Pépin, A.; Dressaire, E.; Chen, Y.; Bornens, M., Cell distribution of stress fibres in response to the geometry of the adhesive environment, Cell motil. cytoskeleton, 63, 341-355, (2006)
[41] Wei, Z., Deshpande, V.S., McMeeking, R.M., Evans, A.G., 2007. Analysis and interpretation of stress fiber organization in cells subject to cyclic stretch. J. Biomech. Eng. ASME, to appear.
[42] Xiao, T.J.; Takagi, B.S.; Coller, J.-H.; Wang; Springer, T.A., Structural basis for allostery in integrins and binding to fibrinogen-mimetic therapeutics, Nature, 432, 59-67, (2004)
[43] Zhu, C.; Bao, G.; Wang, N., Cell mechanics: mechanical response, cell adhesion, and molecular deformation, Ann. rev. cell and dev. biol., 02, 189-226, (2000)
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