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On the Influence of Discrete Adhesive Patterns for Cell Shape and Motility: A Computational Approach

Published online by Cambridge University Press:  03 February 2010

C. Franco
Affiliation:
Laboratoire TIMC-IMAG, Equipe DynaCell, UMR CNRS 5525, Institut d’Ingénierie et de l’Information de Santé (In3S), Pavillon Taillefer, Faculté de Médecine de Grenoble, 38706 La Tronche Cedex, France
T. Tzvetkova-Chevolleau
Affiliation:
LTM, UMR CNRS 5129, c/o CEA Grenoble, 17 rue des martyrs, 38054 Grenoble Cedex 9, France
A. Stéphanou
Affiliation:
Laboratoire TIMC-IMAG, Equipe DynaCell, UMR CNRS 5525, Institut d’Ingénierie et de l’Information de Santé (In3S), Pavillon Taillefer, Faculté de Médecine de Grenoble, 38706 La Tronche Cedex, France LTM, UMR CNRS 5129, c/o CEA Grenoble, 17 rue des martyrs, 38054 Grenoble Cedex 9, France
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Abstract

In this paper, we propose a computational model to investigate the coupling between cell’s adhesions and actin fibres and how this coupling affects cell shape and stability. To accomplish that, we take into account the successive stages of adhesion maturation from adhesion precursors to focal complexes and ultimately to focal adhesions, as well as the actin fibres evolution from growing filaments, to bundles and finally contractile stress fibres.

We use substrates with discrete patterns of adhesive patches, whose inter-patches distance can be modulated in order to control the location of the adhesions and the resulting fibres architecture. We then investigate the emergence of stable cell morphologies as a function of the inter-patches distance, for two different cell phenotypes generated from the model. Force generated by the stress fibres on the focal adhesions and specifically the influence of the cell contractility are also investigated.

Our results suggest that adhesion lifetime and fibre growing rate are the key parameters in the emergence of stable cell morphologies and the limiting factors for the magnitude of the mean tension force from the fibres on the focal adhesions.

Type
Research Article
Copyright
© EDP Sciences, 2010

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References

Bischofs, I., Klein, F., Lehnert, D., Bastmeyer, M. Schwarz, U.. Filamentous network mechanics and active contractility determine cell and tissue shape . Biophys. J, 95 (2008), 34883496 CrossRefGoogle ScholarPubMed
Block, M., Badowski, C., Millon-Fremillon, A., Bouvard, D., Bouin, A., Faurobert, E., Gerber-Scokaert, D., Planus, E. Albigès-Rizo, C.. Podosome type adhesions and focal adhesions, so alike and yet so different . Eur. J. Cell Biol., 87 (2008), 491506 CrossRefGoogle ScholarPubMed
Broussard, J., Webb, D. Kaverina, I.. Asymmetric focal adhesion disassembly in motile cells . Curr. Opin. Cell Biol., 20 (2008), 8590 CrossRefGoogle ScholarPubMed
Coskun, H., Li, Y. Mackey, M.. Ameboid cell motility: A model and inverse problem, with an application to live cell imaging data . J. Theor. Biol., 244 (2007), 169179 CrossRefGoogle ScholarPubMed
Deshpande>, V., McMeeking, R. Evans, A.. A bio-chemo-mechanical model for cell contractility . PNAS, 103 (2006), 14015-14020 CrossRefGoogle ScholarPubMed
Deshpande>, V., McMeeking, R. Evans, A.. A model for the contractility of the cytoskeleton including the effects of stress-fibre formation and dissociation . Proc. R. Soc. A, 463 (2007), 787-815 CrossRefGoogle Scholar
Efimov, A., Schiefermeier, N., Grigoriev, I., Brown, M., Turner, C., Small, J. Kaverina, I.. Paxillin-dependent stimulation of microtubule catastrophes at focal adhesion sites . J. Cell Sci., 121 (2008), 196204 CrossRefGoogle ScholarPubMed
Engler, A., Sen, S., Sweeney, H. Discher, D.. Matrix Elasticity Directs Stem Cell Lineage Specification . Cell, 126 (2006), 677689 CrossRefGoogle ScholarPubMed
Friedl, P. Wolf, K.. Tumour-cell invasion and migration: diversity and escape mechanisms . Nat. Rev. Cancer, 3 (2003), 362-374 CrossRefGoogle ScholarPubMed
Galbraith, C., Yamada, K. Sheetz, M.. The relationship between force and focal complex development . J. Cell Biol., 159 (2002), No. 4, 695705 CrossRefGoogle ScholarPubMed
Geiger, B., Spatz, J. Bershadsky, A.. Environmental sensing through focal adhesions . Nat. Rev. Mol. Cell Biol., 10 (2009), 2133 CrossRefGoogle ScholarPubMed
Giannone, G., Dubin-Thaler, B., Rossier, O., Cai, Y., Chaga, O., Jiang, G., Beaver, W., Dobereiner, H., Freund, Y., Borisy, G. Sheetz, M.. Lamellipodial actin mechanically links myosin activity with adhesion-site formation . Cell, 128 (2007), 561575 CrossRefGoogle ScholarPubMed
Guillou, H., Depraz-Depl, A., Planus, E., Vianay, B., Chaussy, J., Grichine, A., Albigès-Rizo, C. Block, M.. Lamellipodia nucleation by filopodia depends on integrin occupancy and downstream Rac1 signaling . Exp. Cell Res., 314 (2008), 478-488 CrossRefGoogle ScholarPubMed
Hotulainen, P. Lappalainen, P.. Stress fibers are generated by two distinct actin assembly mechanisms in motile cells . J. Cell Biol., 173 (2006), 383394 CrossRefGoogle ScholarPubMed
James, J., Goluch, E., Hu, H., Liu, C. Mrksich, M.. Subcellular Curvature at the Perimeter of Micropatterned Cells Influences Lamellipodial Distribution and Cell Polarity . Cell Motil. Cytoskeleton, 65 (2008), 841852 CrossRefGoogle ScholarPubMed
Jiang, G., Huang, A., Cai, Y., Tanase, M. Sheetz, M.. Rigidity sensing at the leading edge through α v β 3 integrins and RPTP α . Biophys. J., 90 (2006), 18041809 CrossRefGoogle Scholar
Kaunas, R., Hsu, H.. A kinematic model of stretch-induced stress fiber turnover and reorientation , J. Theor. Biol., 257 (2009), 320330. CrossRefGoogle ScholarPubMed
Kuusela, E. Alt, W.. Continuum model of cell adhesion and migration . J. Math. Biol., 58 (2009), 135161 CrossRefGoogle ScholarPubMed
Lazopoulos, K., Stamenovic, D.. A mathematical model of cell reorientation in response to substrate stretching . Mol. Cell. Biomech., 3 (2006), 43. Google ScholarPubMed
Lock, J., Wehrle-Haller, B. Strömblad, S.. Cell–matrix adhesion complexes: master control machinery of cell migration . International Journal of Solids and Structures, 18 (2008), 6576 Google ScholarPubMed
Luo, Y., Xu, X., Lele, T., Kumar, S. Ingber, D.. A multi-modular tensegrity model of an actin stress fiber . J. Biomech., 41 (2008), 23792387 CrossRefGoogle ScholarPubMed
Naumanen, P., Lappalainen, P. Hotulainen, P.. Mechanisms of actin stress fibre assembly . J. Microsc., 231 (2008), 446-454 CrossRefGoogle ScholarPubMed
Pathak, A., Deshpande, V., McMeeking, R. Evans, A.. The simulation of stress fibre and focal adhesion development in cells on patterned substrates . J. R. Soc. Interface, 5 (2008), 507524 CrossRefGoogle ScholarPubMed
Pellegrin, S. Mellor, H.. Actin stress fibres . J. Cell Sci., 120 (2007), 34913499 CrossRefGoogle ScholarPubMed
Rid, R., Schiefermeier, N., Grigoriev, I., Small, J. Kaverina, I.. The Last but not the Least: The Origin and Significance of Trailing Adhesions in Fibroblastic Cells . Cell Motil. Cytoskeleton, 61 (2005), 161171 CrossRefGoogle Scholar
Saez, A., Ghibaudo, M., Buguin, A., Silberzan, P. Ladoux, B.. Rigidity-driven growth and migration of epithelial cells on microstructured anisotropic substrates . PNAS, 104 (2007), 82818286 CrossRefGoogle ScholarPubMed
Senju, Y. Miyata, H.. The role of actomyosin contractility in the formation and dynamics of actin bundles during fibroblasts spreading . J. Biochem., 145 (2008), 137-150 CrossRefGoogle ScholarPubMed
Small, J., Auinger, S., Nemethova, M., Koestler, S., Goldie, K., Hoenger, A. Resch, G.. Unravelling the structure of the lamellipodium . J. Microsc., 231 (2008), 479-485 CrossRefGoogle ScholarPubMed
Stamenovic, D.. Contractile torque as a steering mechanism for orientation of adherent cells . Mol. Cell. Biomech., 2 (2005), 69. Google ScholarPubMed
A. Stéphanou. A computational framework integrating cytoskeletal and adhesion dynamics for modelling cell motility. Cell Mechanics, From Single Scale-Based Models to Multiscale Modeling. Chapman & Hall / CRC Press, Ed. A. Chauvire, L.Preziosi & C. Verdier, 2009.
Stéphanou, A., Chaplain, M. Tracqui, P.. A mathematical model for the dynamics of large membrane deformations of isolated fibroblasts . Bull. Math. Biol., 66 (2004), 11191154 CrossRefGoogle ScholarPubMed
Stéphanou, A., Mylona, E., Chaplain, M. Tracqui, P.. A computational model of cell migration coupling the growth of focal adhesions with oscillatory cell protrusions . J. Theor. Biol., 253 (2008), 701716 CrossRefGoogle ScholarPubMed
Tan, J., Tien, J., Pirone, D., Gray, D., Bhadriraju, K. Chen, C.. Cells lying on a bed of microneedles: an approach to isolate mechanical force . PNAS, 100 (2003), 14841489 CrossRefGoogle ScholarPubMed
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 (2006), 341355 CrossRefGoogle ScholarPubMed
Tzvetkova-Chevolleau, T., Stéphanou, A., Fuard, D., Ohayon, J., Schiavone, P. Tracqui, P.. The motility of normal and cancer cells in response to the combined influence of the substrate rigidity and anisotropic microstructure . Biomaterials, 29 (2008), 15411551 CrossRefGoogle Scholar
Vicente-Manzanares, M., Choi, C. Horwitz, A.. Integrins in cell migration-the actin connection . J. Cell Sci., 122 (2009), 199206 CrossRefGoogle Scholar
Wolfenson, H., Henis, Y., Geiger, B. Bershadsky, A.. The heel and toe of the cell’s foot: a multifaceted approach for understanding the structure and dynamics of focal adhesions . Cell Motil. Cytoskeleton, 66 (2009), 10171029 CrossRefGoogle ScholarPubMed
Worth, D. Parsons, M.. Adhesion dynamics: Mechanisms and measurements . Int. J. Biochem. Cell Biol., 40 (2008), 2397-2409 CrossRefGoogle ScholarPubMed
Zaidel-Bar, R., Ballestrem, C., Kam, Z. Geiger, B.. Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells . J. Cell Sci., 116 (2003), 46054613 CrossRefGoogle ScholarPubMed
Zaidel-Bar, R., Cohen, M., Addadi, L. Geiger, B.. Hierarchical assembly of cell-matrix adhesion complexes . Biochem. Soc. Trans., 32 (2004), 416420 CrossRefGoogle ScholarPubMed
Zaidel-Bar, R., Itzkovitz, S., Ma’ayan, A., Iyengar, R. Geiger, B.. Functional atlas of the integrin adhesome . Nat. Cell Biol., 9 (2007), 858867 CrossRefGoogle ScholarPubMed