×

Approaches to myosin modelling in a two-phase flow model for cell motility. (English) Zbl 1373.92022

Summary: A wide range of biological processes rely on the ability of cells to move through their environment. Mathematical models have been developed to improve our understanding of how cells achieve motion. Here we develop models that explicitly track the cell’s distribution of myosin within a two-phase flow framework. Myosin is a small motor protein which is important for contracting the cell’s actin cytoskeleton and enabling cell motion. The two phases represent the actin network and the cytosol in the cell. We start from a fairly general description of myosin kinetics, advection and diffusion in the two-phase flow framework, then identify a number of sub-limits of the model that may be relevant in practice, two of which we investigate further via linear stability analyses and numerical simulations. We demonstrate that myosin-driven contraction of the actin network destabilizes a stationary steady state leading to cell motion, but that rapid diffusion of myosin and rapid unbinding of myosin from the actin network are stabilizing. We use numerical simulation to investigate travelling-wave solutions relevant to a steadily gliding cell and we consider a reduction of the model in which the cell adheres strongly to the substrate on which it is crawling. This work demonstrates that a number of existing models for the effect of myosin on cell motility can be understood as different sub-limits of our two-phase flow model.

MSC:

92C17 Cell movement (chemotaxis, etc.)
35Q92 PDEs in connection with biology, chemistry and other natural sciences

Software:

PETSc
Full Text: DOI

References:

[1] Bray, D., Cell Movements: From Molecules to Motility (2001), Garland Science: Garland Science New York
[2] Vallotton, P.; Gupton, S.; Waterman-Storer, C.; Danuser, G., Simultaneous mapping of filamentous actin flow and turnover in migrating cells by quantitative fluorescent speckle microscopy, Proc. Natl. Acad. Sci. USA, 101, 26, 9660-9665 (2004)
[3] Verkhovsky, A.; Svitkina, T.; Borisy, G., Self-polarization and directional motility of cytoplasm, Curr. Biol., 9, 1, 11-20 (1999)
[4] Svitkina, T.; Verkhovsky, A.; McQuade, K.; Borisy, G., Analysis of the actin-myosin II system in fish epidermal keratocytes: mechanism of cell body translocation, J. Cell Biol., 139, 2, 397-415 (1997)
[5] Pollard, T.; Borisy, G., Cellular motility driven by assembly and disassembly of actin filaments, Cell, 112, 4, 453-465 (2003)
[6] Schaub, S.; Bohnet, S.; Laurent, V.; Meister, J.; Verkhovsky, A., Comparative maps of motion and assembly of filamentous actin and myosin II in migrating cells, Mol. Biol. Cell, 18, 10, 3723-3732 (2007)
[7] Vallotton, P.; Danuser, G.; Bohnet, S.; Meister, J.; Verkhovsky, A., Tracking retrograde flow in keratocytes: news from the front, Mol. Biol. Cell, 16, 3, 1223-1231 (2005)
[8] Fuhs, T.; Goegler, M.; Brunner, C. A.; Wolgemuth, C. W.; Kaes, J. A., Causes of retrograde flow in fish keratocytes, Cytoskeleton, 71, 1, 24-35 (2014)
[9] Palecek, S.; Loftus, J.; Ginsberg, M.; Lauffenburger, D.; Horwitz, A., Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness, Nature, 385, 537-540 (1997)
[10] Mogilner, A.; Oster, G., Cell motility driven by actin polymerization, Biophys. J., 71, 6, 3030-3045 (1996)
[11] Marée, A.; Grieneisen, V.; Edelstein-Keshet, L., How cells integrate complex stimuli: The effect of feedback from phosphoinositides and cell shape on cell polarization and motility, PLoS Comput. Biol., 8, 3, e1002402 (2012)
[12] Herant, M.; Dembo, M., Form and function in cell motility: from fibroblasts to keratocytes, Biophys. J., 98, 8, 1408-1417 (2010)
[13] Danuser, G.; Allard, J.; Mogilner, A., Mathematical modeling of eukaryotic cell migration: insights beyond experiments, Annu. Rev. Cell Dev. Biol., 29, 501 (2013)
[14] Edelstein-Keshet, L.; Holmes, W.; Zajac, M.; Dutot, M., From simple to detailed models for cell polarization, Philos. Trans. R. Soc. London, Ser. B, 368, 1629, 20130003 (2013)
[15] Holmes, W.; Edelstein-Keshet, L., A comparison of computational models for eukaryotic cell shape and motility, PLoS Comput. Biol, 8, 12, e1002793 (2012)
[16] Mogilner, A., Mathematics of cell motility: have we got its number?, J. Math. Biol., 58, 1, 105-134 (2009) · Zbl 1161.92022
[17] Dembo, M.; Harlow, F.; Alt, W., The biophysics of cell surface motility, (Cell Surface Dynamics: Concepts and Models (1984), Marcel Deckker)
[18] Alt, W.; Bock, M.; Möhl, C., Coupling of cytoplasm and adhesion dynamics determines cell polarization and locomotion, (Cell Mechanics: From Single-Scale Based Models to Multiscale Modeling (2010), Chapman and Hall/CRC) · Zbl 1404.92031
[19] Alt, W.; Dembo, M., Cytoplasm dynamics and cell motion: two-phase flow models, Math. Biosci., 156, 1-2, 207-228 (1999) · Zbl 0934.92009
[20] Dembo, M., Mechanics and control of the cytoskeleton in amoeba proteus, Biophys. J., 55, 1053-1080 (1989)
[21] Dembo, M.; Harlow, F., Cell motion, contractile networks, and the physics of interpenetrating reactive flow, Biophys. J., 50, 1, 109-121 (1986)
[22] Herant, M.; Marganski, W.; Dembo, M., The mechanics of neutrophils: synthetic modeling of three experiments, Biophys. J., 84, 5, 3389-3413 (2003)
[23] King, J.; Oliver, J., Thin-film modelling of poroviscous free surface flows, European J. Appl. Math., 16, 04, 519-553 (2005) · Zbl 1112.76021
[24] Kuusela, E.; Alt, W., Continuum model of cell adhesion and migration, J. Math. Biol., 58, 1, 135-161 (2009) · Zbl 1161.92004
[25] Oliver, J.; King, J.; McKinlay, K.; Brown, P.; Grant, D.; Scotchford, C.; Wood, J., Thin-film theories for two-phase reactive flow models of active cell motion, Math. Med. Biol., 22, 1, 53 (2005) · Zbl 1069.92002
[26] Zajac, M.; Dacanay, B.; Mohler, W.; Wolgemuth, C., Depolymerization-driven flow in nematode spermatozoa relates crawling speed to size and shape, Biophys. J., 94, 10, 3810-3823 (2008)
[27] Kimpton, L.; Whiteley, J.; Waters, S.; King, J.; Oliver, J., Multiple travelling-wave solutions in a minimal model for cell motility, Math. Med. Biol., 30, 3, 241-272 (2013) · Zbl 1272.92005
[28] Kimpton, L.; Whiteley, J.; Waters, S.; Oliver, J., The effect of membrane-regulated actin polymerization on a two-phase flow model for cell motility, IMA J. Appl. Math., 79, 4, 603-635 (2014) · Zbl 1328.92025
[29] Kimpton, L.; Whiteley, J.; Waters, S.; Oliver, J., On a poroviscoelastic model for cell crawling, J. Math. Biol., 70, 1-2, 133-171 (2015) · Zbl 1309.92028
[30] Cogan, N.; Guy, R., Multiphase flow models of biogels from crawling cells to bacterial biofilms, HFSP J., 4, 1, 11-25 (2010)
[31] Mitchison, T.; Charras, G.; Mahadevan, L., Implications of a poroelastic cytoplasm for the dynamics of animal cell shape, (Seminars in Cell & Developmental Biology, vol. 19 (2008), Elsevier), 215-223
[32] Moeendarbary, E.; Valon, L.; Fritzsche, M.; Harris, A.; Moulding, D.; Thrasher, A.; Stride, E.; Mahadevan, L.; Charras, G., The cytoplasm of living cells behaves as a poroelastic material, Nature Mater., 12, 3, 253-261 (2013)
[33] Larripa, K.; Mogilner, A., Transport of a 1D viscoelastic actin-myosin strip of gel as a model of a crawling cell, Physica A, 372, 1, 113-123 (2006)
[34] Mogilner, A.; Marland, E.; Bottino, D., A minimal model of locomotion applied to the steady gliding movement of fish keratocyte cells, (Maini, P.; Othmer, H., Mathematical Models for Biological Pattern Formation. Mathematical Models for Biological Pattern Formation, The IMA Volumes in Mathematics and its Applications, vol. 121 (2001), Springer: Springer New York), 269-293 · Zbl 1022.92006
[35] Wolgemuth, C.; Stajic, J.; Mogilner, A., Redundant mechanisms for stable cell locomotion revealed by minimal models, Biophys. J., 101, 3, 545-553 (2011)
[36] Craig, E. M.; Stricker, J.; Gardel, M.; Mogilner, A., Model for adhesion clutch explains biphasic relationship between actin flow and traction at the cell leading edge, Phys. Biol., 12, 3, Article 035002 pp. (2015)
[37] Sakamoto, Y.; Prudhomme, S.; Zaman, M., Viscoelastic gel-strip model for the simulation of migrating cells, Ann. Biomed. Eng., 39, 11, 2735-2749 (2011)
[38] Gracheva, M.; Othmer, H., A continuum model of motility in ameboid cells, Bull. Math. Biol., 66, 1, 167-193 (2004) · Zbl 1334.92055
[39] Barnhart, E.; Lee, K.; Keren, K.; Mogilner, A.; Theriot, J., An adhesion-dependent switch between mechanisms that determine motile cell shape, PLoS Biol., 9, 5, e1001059 (2011)
[41] Rubinstein, B.; Fournier, M.; Jacobson, K.; Verkhovsky, A.; Mogilner, A., Actin-myosin viscoelastic flow in the keratocyte lamellipod, Biophys. J., 97, 7, 1853-1863 (2009)
[42] De La Cruz, E.; Ostap, E., Kinetic and equilibrium analysis of the myosin atpase, Methods Enzymol., 455, 157-192 (2009)
[43] Borejdo, J.; Burlacu, S., Diffusion of heavy meromyosin in the presence of F-actin and ATP, J. Muscle Res. Cell Motil., 13, 1, 106-116 (1992)
[44] Ali, M.; Lu, H.; Bookwalter, C.; Warshaw, D.; Trybus, K., Myosin V and Kinesin act as tethers to enhance each others’ processivity, Proc. Natl. Acad. Sci. USA, 105, 12, 4691-4696 (2008)
[45] Liu, J., Mathematical modelling of keratocyte motility (2008), University of Oxford, (M.Sc. thesis)
[46] Kimpton, L., On two-phase flow models for cell motility (2013), Oxford University, (Ph.D. thesis)
[47] Cogan, N.; Keener, J., The role of the biofilm matrix in structural development, Math. Med. Biol., 21, 2, 147-166 (2004) · Zbl 1055.92034
[48] Borm, B.; Requardt, R.; Herzog, V.; Kirfel, G., Membrane ruffles in cell migration: indicators of inefficient lamellipodia adhesion and compartments of actin filament reorganization, Exp. Cell Res., 302, 1, 83-95 (2005)
[49] Giannone, G.; Dubin-Thaler, B.; Döbereiner, H.; Kieffer, N.; Bresnick, A.; Sheetz, M., Periodic lamellipodial contractions correlate with rearward actin waves, Cell, 116, 3, 431-443 (2004)
[50] Balay, S.; Gropp, W.; Curfman McInnes, L.; Smith, B., Efficient management of parallelism in object oriented numerical software libraries, (Modern Software Tools for Scientific Computing (1997), Birkhäuser Press) · Zbl 0882.65154
[53] Hinch, E., Perturbation Methods (1991), Cambridge University Press · Zbl 0746.34001
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.