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Mechanisms of Cell Motion in ConfinedGeometries

Published online by Cambridge University Press:  03 February 2010

R. J. Hawkins  and
R. Voituriez
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Abstract

We present a simple mechanism of cell motility in a confined geometry, inspired by recentmotility assays in microfabricated channels. This mechanism relies mainly on the couplingof actin polymerisation at the cell membrane to geometric confinement. We first showanalytically using a minimal model of polymerising viscoelastic gel confined in a narrowchannel that spontaneous motion occurs due to polymerisation alone. Interestingly, thismechanism does not require specific adhesion with the channel walls, and yields velocitiespotentially larger than the polymerisation velocity of the gel. We then study the effectof the contractile activity of myosin motors, and show that whilst it is not necessary toinduce motion, it quantitatively increases the velocity of motion in the polymerisationmechanism we describe. Our model qualitatively accounts for recent experiments which showthat cells without specific adhesion proteins are motile only in confined environmentswhile they are unable to move on a flat surface. It also constitutes a first step in thestudy of cell migration in more complex confined geometries such as living tissues.

Keywords

cell motilityactive geltheoryhydrodynamics
Type
Research Article
Information
Mathematical Modelling of Natural Phenomena , Volume 5 , Issue 1: Cell migration , 2010 , pp. 84 - 105
Copyright
© EDP Sciences, 2010

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References

B. Alberts. Molecular biology of the cell, 4th ed., Garland Science, New York, 2002.
Bernheim-Groswasser, A., Wiesner, S., Golsteyn, R. M., Carlier, M. F. Sykes, C.. The dynamics of actin-based motility depend on surface parameters , Nature, 417 (2002), No. 6886, 308–311 CrossRefGoogle ScholarPubMed
Callan-Jones, A. C., Joanny, J.-F. Prost, J.. Viscous-fingering-like instability of cell fragments , Phys. Rev. Lett., 100 (2008), 258106 CrossRefGoogle ScholarPubMed
Calle, Y., Burns, S., Thrasher, A. J. Jones, G. E.. The leukocyte podosome. , Eur. J. Cell. Biol., 85 (2006), No. 3-4, 151–157 CrossRefGoogle ScholarPubMed
Le Clainche, C., Carlier, M.-F.. Regulation of actin assembly associated with protrusion and adhesion in cell migration. , Physiol. Rev., 88, (2008), No. 2, 489–513. CrossRefGoogle ScholarPubMed
Dogterom, M., Janson, M.E., Faivre-Moskalenko, C., Horst, A. van der, Kerssemakers, J.W.J., Tanase, C. Mulder, B.M.. Force generation by polymerizing microtubules , Applied Physics A: Materials Science & Processing, 75 (2002), No. 2, 331–336 CrossRefGoogle Scholar
Dombrowski, C., Cisneros, L., Chatkaew, S., Goldstein, R. E. Kessler, John O.. Self-concentration and large-scale coherence in bacterial dynamics , Phys. Rev. Lett., 93 (2004), No. 9, 098103 CrossRefGoogle ScholarPubMed
Faure-André, G., Vargas, P., Yuseff, M.-I., Heuzé, M., Diaz, J., Lankar, D., Steri, V., Manry, J., Hugues, S., Vascotto, F., Boulanger, J., Raposo, G., Bono, M.-R., Rosemblatt, M., Piel, M. Lennon-Duménil, A.-M.. Regulation of dendritic cell migration by CD74, the MHC class II-associated invariant chain. , Science, 322 (2008), No. 5908, 1705–1710 CrossRefGoogle ScholarPubMed
Gerbal, F., Chaikin, P., Rabin, Y. Prost, J.. An elastic analysis of listeria monocytogenes propulsion. , Biophys. J., 79 (2000), No. 5, 2259–2275 CrossRefGoogle ScholarPubMed
P. G. de Gennes, J. Prost. The Physics of Liquid Crystals. Oxford. Univ. Press, Oxford, 1993.
Hatwalne, Y., Ramaswamy, S., Rao, M. Simha, R. A.. Rheology of active-particle suspensions. , Phys. Rev. Lett., 92 (2004), No. 11, 118101 CrossRefGoogle ScholarPubMed
Hawkins, R. J., Piel, M., Faure-Andre, G., Lennon-Dumenil, A. M., Joanny, J. F., Prost, J. Voituriez, R.. Pushing off the walls: a mechanism of cell motility in confinement. , Phys. Rev. Lett., 102 (2009), No. 5, 058103 CrossRefGoogle ScholarPubMed
van Helden, S. F. G., Krooshoop, D. J. E. B., Broers, K. C. M., Raymakers, R. A. P., Figdor, C. G. van Leeuwen, F. N.. A critical role for prostaglandin e2 in podosome dissolution and induction of high-speed migration during dendritic cell maturation. , J. Immunol., 177 (2006), No. 3, 1567–1574 CrossRefGoogle ScholarPubMed
Julicher, F., Kruse, K., Prost, J. Joanny, J. F.. Active behavior of the cytoskeleton , Physics Reports, 449 (2007), No. 1-3, 3–28 CrossRefGoogle Scholar
Kruse, K., Joanny, J. F., Jülicher, F., Prost, J. Sekimoto, K.. Asters, vortices, and rotating spirals in active gels of polar filaments. , Phys. Rev. Lett., 92 (2004), No. 7, 078101 CrossRefGoogle ScholarPubMed
Kruse, K., Joanny, J. F., Jülicher, F., Prost, J. Sekimoto, K.. Generic theory of active polar gels: a paradigm for cytoskeletal dynamics. , Eur. Phys. J. E Soft Matter, 16 (2005), No. 1 , 5–16 CrossRefGoogle ScholarPubMed
Kruse, K., Joanny, J. F., Jülicher, F. Prost, J.. Contractility and retrograde flow in lamellipodium motion. , Phys Biol, 3 (2006), No. 2, 130–137 CrossRefGoogle ScholarPubMed
Lämmermann, T., Bader, B. L., Monkley, S. J., Worbs, T., Wedlich-Söldner, R., Hirsch, K., Keller, M., Förster, R., Critchley, D. R., Fässler, R. Sixt, M.. Rapid leukocyte migration by integrin-independent flowing and squeezing. , Nature, 453 (2008), No. 7191, 51–55 CrossRefGoogle ScholarPubMed
R. Larson. Constitutive equations for polymer melts and solutions. Butterworth-Heinemann, 1998.
Liverpool, T. B. Marchetti, M. C.. Instabilities of isotropic solutions of active polar filaments. , Phys Rev Lett, 90 (2003), No. 13, 138102 CrossRefGoogle ScholarPubMed
Malawista, S. E. Chevance, A. de Boisfleury. Random locomotion and chemotaxis of human blood polymorphonuclear leukocytes (pmn) in the presence of edta: Pmn in close quarters require neither leukocyte integrins nor external divalent cations. , Proc. Natl. Acad. Sci. USA, 94 (1997), No. 21, 11577–11582 CrossRefGoogle ScholarPubMed
Marenduzzo, D., Orlandini, E., Cates, M. E. Yeomans, J. M.. Steady-state hydrodynamic instabilities of active liquid crystals: Hybrid lattice boltzmann simulations , Phys. Rev. E, 76 (2007), No. 3, 031921 CrossRefGoogle ScholarPubMed
Marenduzzo, D., Orlandini, E., Cates, M. E. Yeomans, J. M.. Lattice boltzmann simulations of spontaneous flow in active liquid crystals: The role of boundary conditions , J. Non-Newton. Fluid Mech., 149 (2008), no. 1-3, 56–62 CrossRefGoogle Scholar
Mogilner, A. Oster, G.. Cell motility driven by actin polymerization , Biophys J., 71 (1996), no. 6, 3030–3045 CrossRefGoogle ScholarPubMed
Narayan, V., Ramaswamy, S. Menon, N.. Long-lived giant number fluctuations in a swarming granular nematic , Science, 317 (2007), No. 5834, 105–108 CrossRefGoogle Scholar
Nedelec, F. J., Surrey, T., Maggs, A. C. Leibler, S.. Self-organization of microtubules and motors , Nature, 389 (1997), No. 6648, 305–308 Google ScholarPubMed
Pollard, T. D. Borisy, G. G.. Cellular motility driven by assembly and disassembly of actin filaments. , Cell, 112 (2003), No. 4, 453–465 CrossRefGoogle ScholarPubMed
Serrador, J. M., Nieto, M. Sánchez-Madrid, F.. Cytoskeletal rearrangement during migration and activation of t lymphocytes. , Trends. Cell. Biol., 9 (1999), No. 6, 228–233 CrossRefGoogle ScholarPubMed
Simha, R. A. Ramaswamy, S.. Hydrodynamic fluctuations and instabilities in ordered suspensions of self-propelled particles. , Phys Rev Lett, 89 (2002), No. 5, 058101 Google Scholar
Theriot, J. A. Mitchison, T. J.. Actin microfilament dynamics in locomoting cells. , Nature, 352 (1991), No. 6331, 126–131 CrossRefGoogle ScholarPubMed
Toner, J., Tu, Y. Ramaswamy, S.. Hydrodynamics and phases of flocks. , Annals of Physics, 318 (2005), No. 1 , 170–244 CrossRefGoogle Scholar
Voituriez, R., Joanny, J. F. Prost, J.. Spontaneous flow transition in active polar gels , Europhys. Lett., 70 (2005), No. 3, 404–410 CrossRefGoogle Scholar
Voituriez, R., Joanny, J. F. Prost, J.. Generic phase diagram of active polar films. , Phys. Rev. Lett., 96 (2006), No. 2, 028102 CrossRefGoogle ScholarPubMed
Yam, P. T., Wilson, C. A., Ji, L., Hebert, B., Barnhart, E. L., Dye, N. A., Wiseman, P. W., Danuser, G. Theriot, J. A.. Actin myosin network reorganization breaks symmetry at the cell rear to spontaneously initiate polarized cell motility , The Journal of Cell Biology, 178 (2007), No. 7, 1207–1221 CrossRefGoogle ScholarPubMed
Zumdieck, A., Voituriez, R., Prost, J. Joanny, J. F.. Spontaneous flow of active polar gels in undulated channels , Faraday Discuss., 139 (2008), 369 CrossRefGoogle ScholarPubMed