Skip to main content
Log in

Diffusive–stochastic–viscoelastic model for specific adhesion of viscoelastic solids via molecular bonds

  • Research Paper
  • Published:
Acta Mechanica Sinica Aims and scope Submit manuscript

Abstract

A diffusive–stochastic–viscoelastic model is proposed for the specific adhesion of viscoelastic solids via stochastically formed molecular bonds. In this model, it is assumed that molecular-level behaviors, including the diffusion of mobile adhesion molecules and stochastic reaction between adhesion molecules and binding sites, are Markovian stochastic processes, while the mesoscopic deformation of the viscoelastic media is governed by continuum mechanics. Systematic Monte Carlo simulations of this model are used to investigate how competition between the time scales of molecular diffusion, reaction, and deformation creep of the solids may influence the lifetime and dynamic strength of their adhesion. The results reveal that there exists an optimal characteristic time for molecular diffusion corresponding to the longest lifetime and greatest adhesion strength, which is in good agreement with experimentally observed characteristic time scales of molecular diffusion in cell membranes. In addition, the results show that the viscosity of the media can significantly increase the lifetime and dynamic strength, since deformation creep and stress relaxation can effectively reduce the concentration of interfacial stress and increase the rebinding probability of molecular bonds.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Lo, C.M., Wang, H.B., Dembo, M., et al.: Cell movement is guided by the rigidity of the substrate. Biophys. J. 79, 144–152 (2000). https://doi.org/10.1016/S0006-3495(00)76279-5

    Article  Google Scholar 

  2. Discher, D.E., Janmey, P., Wang, Y.: Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139–1143 (2005). https://doi.org/10.1126/science.1116995

    Article  Google Scholar 

  3. Peyton, S.R., Putnam, A.J.: Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J. Cell. Physiol. 204, 198–209 (2005). https://doi.org/10.1002/jcp.20274

    Article  Google Scholar 

  4. Gao, H.: Probing mechanical principles of cell–nanomaterial interactions. J. Mech. Phys. Solids 62, 312–339 (2014). https://doi.org/10.1016/j.jmps.2013.08.018

    Article  Google Scholar 

  5. Chaudhuri, O., Gu, L., Klumpers, D., et al.: Hydrogels with tunable stress relaxation. Nat. Mater. 15, 326–334 (2016). https://doi.org/10.1038/nmat4489

    Article  Google Scholar 

  6. Perinpanayagam, H., Zaharias, R., Stanford, C., et al.: Early cell adhesion events differ between osteoporotic and non-osteoporotic osteoblasts. J. Orthop. Res. 19, 993–1000 (2001). https://doi.org/10.1016/S0736-0266(01)00045-6

    Article  Google Scholar 

  7. Giancotti, F.G., Ruoslahti, E.: Integrin signaling. Science 285, 1028–1033 (1999). https://doi.org/10.1126/science.285.5430.1028

    Article  Google Scholar 

  8. Zhao, W., Hanson, L., Lou, H.Y., et al.: Nanoscale manipulation of membrane curvature for probing endocytosis in live cells. Nat. Nanotechnol. 12, 750–756 (2017). https://doi.org/10.1038/nnano.2017.98

    Article  Google Scholar 

  9. Long, M., Zhao, H., Huang, K.S., et al.: Kinetic measurements of cell surface E-selectin/carbohydrate ligand interactions. Ann. Biomed. Eng. 29, 935–946 (2001). https://doi.org/10.1114/1.1415529

    Article  Google Scholar 

  10. Long, M., Goldsmith, H.L., Tees, D.F.J., et al.: Probabilistic modeling of shear-induced formation and breakage of doublets cross-linked by receptor–ligand bonds. Biophys. J. 76, 1112–1128 (1999). https://doi.org/10.1016/S0006-3495(99)77276-0

    Article  Google Scholar 

  11. Mücksch, J., Blumhardt, P., Strauss, M.T., et al.: Quantifying reversible surface binding via surface-integrated fluorescence correlation spectroscopy. Nano Lett. 18, 3185–3192 (2018). https://doi.org/10.1021/acs.nanolett.8b00875

    Article  Google Scholar 

  12. Kramers, H.A.: Brownian motion in a field of force and the diffusion model of chemical reactions. Physica 7, 284–304 (1940). https://doi.org/10.1016/S0031-8914(40)90098-2

    Article  MathSciNet  MATH  Google Scholar 

  13. Bell, G.I.: Models for the specific adhesion of cells to cells. Science 200, 618–627 (1978). https://doi.org/10.1126/science.347575

    Article  Google Scholar 

  14. Bell, G.I., Dembo, M., Bongrand, P.: Cell adhesion. Competition between nonspecific repulsion and specific bonding. Biophys. J. 45, 1051–1064 (1984). https://doi.org/10.1016/s0006-3495(84)84252-6

    Article  Google Scholar 

  15. Raible, M., Evstigneev, M., Reimann, P., et al.: Theoretical analysis of dynamic force spectroscopy experiments on ligand–receptor complexes. J. Biotechnol. 112, 13–23 (2004). https://doi.org/10.1016/j.jbiotec.2004.04.017

    Article  Google Scholar 

  16. Bartels, F.W., Baumgarth, B., Anselmetti, D., et al.: Specific binding of the regulatory protein ExpG to promoter regions of the galactoglucan biosynthesis gene cluster of Sinorhizobium meliloti-a combined molecular biology and force spectroscopy investigation. J. Struct. Biol. 143, 145–152 (2003). https://doi.org/10.1016/S1047-8477(03)00127-8

    Article  Google Scholar 

  17. Li, D., Ji, B.: Predicted rupture force of a single molecular bond becomes rate independent at ultralow loading rates. Phys. Rev. Lett. 112, 078302 (2014). https://doi.org/10.1103/PhysRevLett.112.078302

    Article  Google Scholar 

  18. Chen, X., Li, D., Ji, B., et al.: Reconciling bond strength of a slip bond at low loading rates with rebinding. Europhys. Lett. 109, 68002 (2015). https://doi.org/10.1209/0295-5075/109/68002

    Article  Google Scholar 

  19. Evans, E.: Probing the relation between force-lifetime- and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. Struct. 30, 105–128 (2001). https://doi.org/10.1002/chin.200151281

    Article  Google Scholar 

  20. Li, F., Redick, S.D., Erickson, et al.: Force measurements of the α5 β1 integrin–fibronectin interaction. Biophys. J. 84, 1252–1262 (2003). https://doi.org/10.1016/s0006-3495(03)74940-6

    Article  Google Scholar 

  21. Merkel, R., Nassoy, P., Leung, A., et al.: Energy landscapes of receptor–ligand bonds explored with dynamic force spectroscopy. Nature 397, 50–53 (1999). https://doi.org/10.1038/16219

    Article  Google Scholar 

  22. Erdmann, T., Schwarz, U.S.: Stability of adhesion clusters under constant force. Phys. Rev. Lett. 92, 108102 (2004). https://doi.org/10.1103/PhysRevLett.92.108102

    Article  Google Scholar 

  23. Erdmann, T., Schwarz, U.S.: Stochastic dynamics of adhesion clusters under shared constant force and with rebinding. J. Chem. Phys. 121, 8997–9017 (2004). https://doi.org/10.1063/1.1805496

    Article  Google Scholar 

  24. Chen, A., Moy, V.T.: Cross-linking of cell surface receptors enhances cooperativity of molecular adhesion. Biophys. J. 78, 2814–2820 (2000). https://doi.org/10.1016/S0006-3495(00)76824-X

    Article  Google Scholar 

  25. Sulchek, T., Friddle, R.W., Noy, A.: Strength of multiple parallel biological bonds. Biophys. J. 90, 4686–4691 (2006). https://doi.org/10.1529/biophysj.105.080291

    Article  Google Scholar 

  26. Sun, L., Cheng, Q.H., Gao, H.J., et al.: Effect of loading conditions on the dissociation behaviour of catch bond clusters. J. R. Soc. Interface 9, 928–937 (2011). https://doi.org/10.1098/rsif.2011.0553

    Article  Google Scholar 

  27. Wang, J., Yao, J., Gao, H.: Specific adhesion of a soft elastic body on a wavy surface. Theor. Appl. Mech. Lett. 2, 014002 (2012). https://doi.org/10.1063/2.1201402

    Article  Google Scholar 

  28. He, S., Su, Y., Ji, B., et al.: Some basic questions on mechanosensing in cell–substrate interaction. J. Mech. Phys. Solids 70, 116–135 (2014). https://doi.org/10.1016/j.jmps.2014.05.016

    Article  MathSciNet  MATH  Google Scholar 

  29. Li, L., Tang, H., Wang, J., et al.: Rolling adhesion of cell in shear flow: a theoretical model. J. Mech. Phys. Solids 119, 369–381 (2018). https://doi.org/10.1016/j.jmps.2018.07.013

    Article  MathSciNet  Google Scholar 

  30. Ward, M.D., Dembo, M., Hammer, D.A.: Kinetics of cell detachment: peeling of discrete receptor clusters. Biophys. J. 67, 2522–2534 (1994). https://doi.org/10.1016/S0006-3495(94)80742-8

    Article  Google Scholar 

  31. Li, L., Yao, H., Wang, J.: Dynamic strength of molecular bond clusters under displacement- and force-controlled loading conditions. J. Appl. Mech. 83, 021004 (2016). https://doi.org/10.1115/1.4031802

    Article  Google Scholar 

  32. Liu, J., Wang, Y.L., Goh, W.I., et al.: Talin determines the nanoscale architecture of focal adhesions. Proc. Natl. Acad. Sci. 17, E4673–E4864 (2015). https://doi.org/10.1073/pnas.1512025112

    Google Scholar 

  33. Li, N., Lu, S.Q., Zhang, Y., et al.: Mechanokinetics of receptor–ligand interaction in cell adhesion. Acta. Mech. Sin. 31, 248–258 (2015). https://doi.org/10.1007/s10409-015-0407-8

    Article  Google Scholar 

  34. Cone, R.A.: Rotational diffusion of rhodopsin in the visual receptor membrane. Nature 236, 39–43 (1972). https://doi.org/10.1002/jss.400010411

    Google Scholar 

  35. Paszek, M.J., Boettiger, D., Weaver, V.M., et al.: Integrin clustering is driven by mechanical resistance from the glycocalyx and the substrate. PLoS Comput. Biol. 5, e1000604 (2009). https://doi.org/10.1371/journal.pcbi.1000604

    Article  MathSciNet  Google Scholar 

  36. Smith, A.S., Sengupta, K., Goennenwein, S., et al.: Force-induced growth of adhesion domains is controlled by receptor mobility. Proc. Natl. Acad. Sci. 105, 6906–6911 (2008). https://doi.org/10.1073/pnas.0801706105

    Article  Google Scholar 

  37. Xu, G.K., Qian, J., Hu, J.: The glycocalyx promotes cooperative binding and clustering of adhesion receptors. Soft Matter 12, 4572–4583 (2016). https://doi.org/10.1039/c5sm03139g

    Article  Google Scholar 

  38. Engler, A.J., Sen, S., Sweeney, H.L., et al.: Matrix elasticity directs stem cell lineage specification. Cell 126, 677–689 (2006). https://doi.org/10.1016/j.cell.2006.06.044

    Article  Google Scholar 

  39. Wang, J., Gao, H.: Clustering instability in adhesive contact between elastic solids via diffusive molecular bonds. J. Mech. Phys. Solids 56, 251–266 (2008). https://doi.org/10.1016/j.jmps.2007.05.011

    Article  MathSciNet  MATH  Google Scholar 

  40. Qian, J., Wang, J., Lin, Y., et al.: Lifetime and strength of periodic bond clusters between elastic media under inclined loading. Biophys. J. 97, 2438–2445 (2009). https://doi.org/10.1016/j.bpj.2009.08.027

    Article  Google Scholar 

  41. Gao, H., Qian, J., Chen, B.: Probing mechanical principles of focal contacts in cell–matrix adhesion with a coupled stochastic–elastic modelling framework. J. R. Soc. Interface 8, 1217–1232 (2011). https://doi.org/10.1098/rsif.2011.0157

    Article  Google Scholar 

  42. Chen, B., Ji, B., Gao, H.: Modeling active mechanosensing in cell–matrix interactions. Annu. Rev. Biophys. 44, 1–32 (2015). https://doi.org/10.1146/annurev-biophys-051013-023102

    Article  Google Scholar 

  43. Qian, J., Wang, J., Gao, H.: Lifetime and strength of adhesive molecular bond clusters between elastic media. Langmuir 24, 1262–1270 (2008). https://doi.org/10.1021/la702401b

    Article  Google Scholar 

  44. Wang, J., Gao, H.: Size and shape dependent steady-state pull-off force in molecular adhesion between soft elastic materials. Int. J. Fract. 166, 13–19 (2010). https://doi.org/10.1007/s10704-010-9463-z

    Article  Google Scholar 

  45. Zhang, W., Lin, Y., Qian, J., et al.: Tuning molecular adhesion via material anisotropy. Adv. Funct. Mater. 23, 4729–4738 (2013). https://doi.org/10.1002/adfm.201300069

    Google Scholar 

  46. Qian, J., Gao, H.: Soft matrices suppress cooperative behaviors among receptor–ligand bonds in cell adhesion. PLoS ONE 5, e12342 (2010). https://doi.org/10.1371/journal.pone.0012342

    Article  Google Scholar 

  47. Zhang, W., Qian, J., Yao, H., et al.: Effects of functionally graded materials on dynamics of molecular bond clusters. Sci. China-Phys. Mech. Astron. 55, 980–988 (2012). https://doi.org/10.1007/s11433-012-4726-5

    Article  Google Scholar 

  48. Chen, B., Gao, H.: Mechanical principle of enhancing cell–substrate adhesion via pre-tension in the cytoskeleton. Biophys. J. 98, 2154–2162 (2010). https://doi.org/10.1016/j.bpj.2010.02.007

    Article  Google Scholar 

  49. Chen, B., Gao, H.: Motor force homeostasis in skeletal muscle contraction. Biophys. J. 101, 396–403 (2011). https://doi.org/10.1016/j.bpj.2011.05.061

    Article  Google Scholar 

  50. Qian, J., Liu, H., Lin, Y., et al.: A mechanochemical model of cell reorientation on substrates under cyclic stretch. PLoS ONE 8, e65864 (2013). https://doi.org/10.1371/journal.pone.0065864

    Article  Google Scholar 

  51. Xu, G.K., Li, B., Feng, X.Q., et al.: A tensegrity model of cell reorientation on cyclically stretched substrates. Biophys. J. 111, 1478–1486 (2016). https://doi.org/10.1016/j.bpj.2016.08.036

    Article  Google Scholar 

  52. Qian, J., Lin, J., Xu, G.K., et al.: Thermally assisted peeling of an elastic strip in adhesion with a substrate via molecular bonds. J. Mech. Phys. Solids 101, 197–208 (2017). https://doi.org/10.1016/j.jmps.2017.01.007

    Article  MathSciNet  Google Scholar 

  53. Wei, Y.A.: Stochastic description on the traction–separation law of an interface with non-covalent bonding. J. Mech. Phys. Solids 70, 227–241 (2014). https://doi.org/10.1016/j.jmps.2014.05.014

    Article  MathSciNet  MATH  Google Scholar 

  54. Chaudhuri, O., Gu, L., Darnell, M., et al.: Substrate stress relaxation regulates cell spreading. Nat. Commun. 6, 6365 (2015). https://doi.org/10.1038/ncomms7365

    Article  Google Scholar 

  55. Gong, Z., Szczesny, S.E., Caliari, S.R., et al.: Matching material and cellular timescales maximizes cell spreading on viscoelastic substrates. Proc. Natl. Acad. Sci. 115, E2686–E2695 (2018). https://doi.org/10.1073/pnas.1716620115

    Article  Google Scholar 

  56. Li, L., Zhang, W., Wang, J.: A viscoelastic–stochastic model of the effects of cytoskeleton remodelling on cell adhesion. R. Soc. Open Sci. 3, 160539 (2016). https://doi.org/10.1098/rsos.160539

    Article  MathSciNet  Google Scholar 

  57. Bihr, T., Seifert, U., Smith, A.S.: Multiscale approaches to protein-mediated interactions between membranes-relating microscopic and macroscopic dynamics in radially growing adhesions. New J. Phys. 17, 083016 (2015). https://doi.org/10.1088/1367-2630/17/8/083016

    Article  Google Scholar 

  58. Erdmann, T., Schwarz, U.S.: Bistability of cell–matrix adhesions resulting from nonlinear receptor–ligand dynamics. Biophys. J. 91, L60–L62 (2006). https://doi.org/10.1529/biophysj.106.090209

    Article  Google Scholar 

  59. Erdmann, T., Schwarz, U.S.: Impact of receptor–ligand distance on adhesion cluster stability. Eur. Phys. J. E 22, 123–137 (2007). https://doi.org/10.1140/epje/e2007-00019-8

    Article  Google Scholar 

  60. Van Kampen, N.G.: Stochastic Processes in Physics and Chemistry. North-Holland Personal Library, Amsterdam (1981)

    MATH  Google Scholar 

  61. Wang, J., Huang, Q.: A stochastic description on adhesion of molecular bond clusters between rigid media with curved interfaces. Int. J. Appl. Mech. 7, 1550071 (2015). https://doi.org/10.1142/S1758825115500714

    Article  Google Scholar 

  62. Gillespie, D.T.: A general method for numerically simulating the stochastic time evolution of coupled chemical reactions. J. Comput. Phys. 22, 403–434 (1976). https://doi.org/10.1016/0021-9991(76)90041-3

    Article  MathSciNet  Google Scholar 

  63. Gillespie, D.T.: Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem. 81, 2340–2361 (1977). https://doi.org/10.1063/1.2710253

    Article  Google Scholar 

  64. Zuckerman, D.M., Bruinsma, R.F.: Vesicle–vesicle adhesion by mobile lock-and-key molecules: Debye–Hückel theory and Monte Carlo simulation. Phys. Rev. E 57, 964 (1998). https://doi.org/10.1103/PhysRevE.57.964

    Article  Google Scholar 

  65. Arnold, M., Cavalcanti-Adam, E.A., Glass, R., et al.: Activation of integrin function by nanopatterned adhesive interfaces. ChemPhysChem 5, 383–388 (2004). https://doi.org/10.1002/cphc.200301014

    Article  Google Scholar 

  66. Kusumi, A., Sako, Y., Yamamoto, M.: Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys. J. 65, 2021–2040 (1993). https://doi.org/10.1016/s0006-3495(93)81253-0

    Article  Google Scholar 

  67. Schwarz, U.S., Safran, S.A.: Physics of adherent cells. Rev. Mod. Phys. 85, 1327 (2013). https://doi.org/10.1103/RevModPhys.85.1327

    Article  Google Scholar 

  68. Wu, T., Feng, J.J.: A biomechanical model for fluidization of cells under dynamic strain. Biophys. J. 108, 43–52 (2015). https://doi.org/10.1016/j.bpj.2014.11.015

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grants 11472119 and 11602099), the Fundamental Research Funds for the Central Universities (Grant lzujbky-2017-ot11), and the 111 Project (Grant B14044).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jizeng Wang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

He, K., Li, L. & Wang, J. Diffusive–stochastic–viscoelastic model for specific adhesion of viscoelastic solids via molecular bonds. Acta Mech. Sin. 35, 343–354 (2019). https://doi.org/10.1007/s10409-019-00848-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10409-019-00848-z

Keywords

Navigation