Skip to main content
SpringerLink
Log in

Cell Crawling Driven by Spontaneous Actin Polymerization Waves

  • Chapter
  • First Online:
Physical Models of Cell Motility

Part of the book series: Biological and Medical Physics, Biomedical Engineering ((BIOMEDICAL))

Abstract

Cell motility is a signature of life. Crawling of eukaryotic cells on solid substrates is, for example, used to feed, to evade unfavorable environments, or to heal wounds and to fight pathogens in organisms. This process is driven by the actin cytoskeleton and can occur in the absence of external cues. The crawling of some cells appears to be random on large time scales, whereas others move directionally with a high persistence. The latter is even observed for cell fragments not containing the nucleus or microtubules. How the actin cytoskeleton is orchestrated during spontaneous cell motility is largely unknown. In this context, spontaneous polymerization waves that have been observed in many cell types offer a promising concept. Here, we discuss theoretical approaches for studying cell motility driven by spontaneous actin waves. We start by reviewing experimental results. Then, we give an introduction into physical descriptions of actin dynamics and discuss possible mechanisms for wave generation. In the next step, we describe methods to theoretically study the coupling of the actin network to the cell membrane. Our analysis shows that spontaneous polymerization waves offer a unifying framework for explaining directional and erratic cell motility. We conclude by indicating possible directions of future studies.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Notes

  1. 1.

    The Wiskott-Aldrich syndrome protein (WASP) family is identified as the major regulators of the Arp2/3 complex The WASP family consists of two principal classes of protein: WASP and SCAR/WAVE. WAVE was discovered by homology with WASP, but in mammalian cells WAVE is now more commonly used. SCAR is mostly used for the Dictyostelium protein and its mammalian homologues.

References

  1. B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, P. Walter, Molecular Biology of The Cell, 5th edn. (Garland Science, New York, 2008)

    Google Scholar 

  2. F. Backouche, L. Haviv, D. Groswasser, A. Bernheim-Groswasser, Active gels: dynamics of patterning and self-organization. Phys. Biol. 3, 264–273 (2006)

    Article  ADS  Google Scholar 

  3. A. Bernheim-Groswasser, S. Wiesner, R.M. Golsteyn, M.-F. Carlier, C. Sykes, The dynamics of actin-based motility depend on surface parameters. Nature 417, 308–311 (2002)

    Article  ADS  Google Scholar 

  4. E. Bernitt, C.G. Koh, N. Gov, H.-G. Döbereiner, Dynamics of actin waves on patterned substrates: a quantitative analysis of circular dorsal ruffles. PLoS One 10, e0115857 (2015)

    Article  Google Scholar 

  5. J.S. Bois, F. Julicher, S.W. Grill, Pattern formation in active fluids. Phys. Rev. Lett. 106, 028103 (2011)

    Article  ADS  Google Scholar 

  6. M. Bonny, E. Fischer-Friedrich, M. Loose, P. Schwille, K. Kruse, Membrane binding of MinE allows for a comprehensive description of min-protein pattern formation. PLoS Comput. Biol. 9, e1003347 (2013)

    Article  ADS  Google Scholar 

  7. T. Bretschneider, S. Diez, K. Anderson, J. Heuser, M. Clarke, A. Muller-Taubenberger, J. Kohler, G. Gerisch, Dynamic actin patterns and Arp2/3 assembly at the substrate-attached surface of motile cells. Curr. Biol. 14, 1–10 (2004)

    Article  Google Scholar 

  8. T. Bretschneider, K. Anderson, M. Ecke, A. Mueller-Taubenberger, B. Schroth-Diez, H.C. Ishikawa-Ankerhold, G. Gerisch, The three-dimensional dynamics of actin waves, a model of cytoskeletal self-organization. Biophys. J. 96, 2888–2900 (2009)

    Google Scholar 

  9. D.T. Burnette, S. Manley, P. Sengupta, R. Sougrat, M.W. Davidson, B. Kachar, J. Lippincott-Schwartz, A role for actin arcs in the leading-edge advance of migrating cells. Nat. Cell Biol. 13, 371–382 (2011)

    Article  Google Scholar 

  10. L.A. Cameron, M.J. Footer, A. van Oudenaarden, J.A. Theriot, Motility of ActA protein-coated microspheres driven by actin polymerization. Proc. Natl. Acad. Sci. U.S.A. 96, 4908–4913 (1999)

    Article  ADS  Google Scholar 

  11. A.E. Carlsson, Dendritic actin filament nucleation causes traveling waves and patches. Phys. Rev. Lett. 104, 228102 (2010)

    Article  ADS  Google Scholar 

  12. L.B. Case, C. Waterman, Adhesive F-actin waves: a novel integrin-mediated adhesion complex coupled to ventral actin polymerization. PLoS One 6, e26631 (2011)

    Article  ADS  Google Scholar 

  13. H.-G. Doebereiner, B.J. Dubin-Thaler, J.M. Hofman, H.S. Xenias, T.N. Sims, G. Giannone, M.L. Dustin, C.H. Wiggins, M.P. Sheetz, Lateral membrane waves constitute a universal dynamic pattern of motile cells. Phys. Rev. Lett. 97, 038102 (2006)

    Article  ADS  Google Scholar 

  14. K. Doubrovinski, K. Kruse, Self-organization of treadmilling filaments. Phys. Rev. Lett. 99, 228104 (2007)

    Article  ADS  Google Scholar 

  15. K. Doubrovinski, K. Kruse, Cytoskeletal waves in the absence of molecular motors. Europhys. Lett. 83, 18003 (2008)

    Article  ADS  Google Scholar 

  16. K. Doubrovinski, K. Kruse, Self-organization in systems of treadmilling filaments. Eur. Phys. J. E 31, 95–104 (2010)

    Article  Google Scholar 

  17. K. Doubrovinski, K. Kruse, Cell motility resulting from spontaneous polymerization waves. Phys. Rev. Lett. 107, 258103 (2011)

    Article  ADS  Google Scholar 

  18. A. Dreher, I.S. Aranson, K. Kruse, Spiral actin-polymerization waves can generate amoeboidal cell crawling. New J. Phys. 16, 055007 (2014)

    Article  ADS  Google Scholar 

  19. M.K. Driscoll, X. Sun, C. Guven, J.T. Fourkas, W. Losert, Cellular contact guidance through dynamic sensing of nanotopography. ACS Nano 8, 3546–3555 (2014)

    Article  Google Scholar 

  20. C. Erlenkämper, K. Kruse, Treadmilling and length distributions of active polar filaments. J. Chem. Phys. 139, 164907 (2013)

    Article  ADS  Google Scholar 

  21. U. Euteneuer, M. Schliwa, Persistent, directional motility of cells and cytoplasmic fragments in the absence of microtubules. Nature 310, 58–61 (1984)

    Article  ADS  Google Scholar 

  22. F. Gerbal, P. Chaikin, Y. Rabin, J. Prost, An elastic analysis of Listeria monocytogenes propulsion. Biophys. J. 79, 2259–2275 (2000)

    Article  Google Scholar 

  23. M. Gerhardt, M. Ecke, M. Walz, A. Stengl, C. Beta, G. Gerisch, Actin and PIP3 waves in giant cells reveal the inherent length scale of an excited state. J. Cell Sci. 127, 4507–4517 (2014)

    Article  Google Scholar 

  24. G. Gerisch, T. Bretschneider, A. Muller-Taubenberger, E. Simmeth, M. Ecke, S. Diez, K. Anderson, Mobile actin clusters and traveling waves in cells recovering from actin depolymerization. Biophys. J. 87, 3493–3503 (2004)

    Google Scholar 

  25. A. Gholami, M. Enculescu, M. Falcke, Membrane waves driven by forces from actin filaments. New J. Phys. 14, 115002 (2012)

    Article  ADS  Google Scholar 

  26. G. Giannone, B.J. Dubin-Thaler, H.-G. Dobereiner, N. Kieffer, A.R. Bresnick, M.P. Sheetz, Periodic lamellipodial contractions correlate with rearward actin waves. Cell 116, 431–443 (2004)

    Article  Google Scholar 

  27. E. Gouin, M.D. Welch, P. Cossart, Actin-based motility of intracellular pathogens. Curr. Opin. Microbiol. 8, 35–45 (2005)

    Article  Google Scholar 

  28. N.S. Gov, A. Gopinathan, Dynamics of membranes driven by actin polymerization. Biophys. J. 90, 454–469 (2006)

    Article  ADS  Google Scholar 

  29. S. Guenther, K. Kruse, Spontaneous waves in muscle fibres. New J. Phys. 9, 417–417 (2007)

    Article  ADS  Google Scholar 

  30. C.-H. Huang, M. Tang, C. Shi, P.A. Iglesias, P.N. Devreotes, An excitable signal integrator couples to an idling cytoskeletal oscillator to drive cell migration. Nat. Cell Biol. 15, 1307–1318 (2013)

    Article  Google Scholar 

  31. K.L. Hui, S.I. Kwak, A. Upadhyaya, Adhesion-dependent modulation of actin dynamics in jurkat T cells. Cytoskeleton (Hoboken) 71, 119–135 (2014)

    Article  Google Scholar 

  32. H.U. Keller, M. Bessis, Migration and chemotaxis of anucleate cytoplasmic leukocyte fragments. Nature 258, 723–724 (1975)

    Article  ADS  Google Scholar 

  33. A.J. Koch, H. Meinhardt, Biological pattern-formation - from basic mechanisms to complex structures. Rev. Mod. Phys. 66, 1481–1507 (1994)

    Article  ADS  Google Scholar 

  34. K. Kruse, J.-F. Joanny, F. Julicher, J. Prost, K. Sekimoto, Asters, vortices, and rotating spirals in active gels of polar filaments. Phys. Rev. Lett. 92, 078101 (2004)

    Article  ADS  Google Scholar 

  35. T.P. Loisel, R. Boujemaa, D. Pantaloni, M.F. Carlier, Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401, 613–616 (1999)

    Article  ADS  Google Scholar 

  36. M.L. Lombardi, D.A. Knecht, M. Dembo, J. Lee, Traction force microscopy in Dictyostelium reveals distinct roles for myosin II motor and actin-crosslinking activity in polarized cell movement. J. Cell Sci. 120, 1624–1634 (2007)

    Article  Google Scholar 

  37. M. Loose, E. Fischer-Friedrich, J. Ries, K. Kruse, P. Schwille, Spatial regulators for bacterial cell division self-organize into surface waves in vitro. Science 320, 789–792 (2008)

    Article  ADS  Google Scholar 

  38. M. Loose, K. Kruse, P. Schwille, Protein self-organization: lessons from the min system. Annu. Rev. Biophys. 40, 315–336 (2011)

    Article  Google Scholar 

  39. M. Machacek, G. Danuser, Morphodynamic profiling of protrusion phenotypes. Biophys. J. 90, 1439–1452 (2006)

    Article  ADS  Google Scholar 

  40. S.E. Malawista, A. De Boisfleury Chevance, The cytokineplast - purified, stable, and functional motile machinery from human-blood polymorphonuclear leukocytes - possible formative role of heat-induced centrosomal dysfunction. J. Cell Biol. 95, 960–973 (1982)

    Article  Google Scholar 

  41. J.T. Mandeville, R.N. Ghosh, F.R. Maxfield, Intracellular calcium levels correlate with speed and persistent forward motion in migrating neutrophils. Biophys. J. 68, 1207–1217 (1995)

    Article  Google Scholar 

  42. A.C. Martin, M. Kaschube, E.F. Wieschaus, Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457, 495–499 (2009)

    Article  ADS  Google Scholar 

  43. K. Mellstrom, A.S. Hoglund, M. Nister, C.H. Heldin, B. Westermark, U. Lindberg, The effect of platelet-derived growth-factor on morphology and motility of human glial-cells. J. Muscle Res. Cell Motil. 4, 589–609 (1983)

    Article  Google Scholar 

  44. A. Millius, S.N. Dandekar, A.R. Houk, O.D. Weiner, Neutrophils establish rapid and robust WAVE complex polarity in an actin-dependent fashion. Curr. Biol. 19, 253–259 (2009)

    Article  Google Scholar 

  45. K. Murthy, P. Wadsworth, Dual role for microtubules in regulating cortical contractility during cytokinesis. J. Cell Sci. 121, 2350–2359 (2008)

    Article  Google Scholar 

  46. S. Najem, M. Grant, Phase-field approach to chemotactic driving of neutrophil morphodynamics. Phys. Rev. E 88, 034702 (2013)

    Article  ADS  Google Scholar 

  47. F.J. Nedelec, T. Surrey, A.C. Maggs, S. Leibler, Self-organization of microtubules and motors. Nature 389, 305–308 (1997)

    Article  ADS  Google Scholar 

  48. N. Okamura, S. Ishiwata, Spontaneous oscillatory contraction of sarcomeres in skeletal myofibrils. J. Muscle Res. Cell Motil. 9, 111–119 (1988)

    Article  Google Scholar 

  49. B. Peleg, A. Disanza, G. Scita, N. Gov, Propagating cell-membrane waves driven by curved activators of actin polymerization. PLoS One 6, e18635 (2011)

    Article  ADS  Google Scholar 

  50. P.Y. Placais, M. Balland, T. Guerin, J.-F. Joanny, P. Martin, Spontaneous oscillations of a minimal actomyosin system under elastic loading. Phys. Rev. Lett. 103, 158102 (2009)

    Article  ADS  Google Scholar 

  51. T.D. Pollard, Regulation of actin filament assembly by Arp2/3 complex and formins. Annu. Rev. Biophys. Biomol. Struct. 36, 451–477 (2007)

    Article  Google Scholar 

  52. T.D. Pollard, G.G. Borisy, Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453–465 (2003)

    Article  Google Scholar 

  53. J. Prost, C. Barbetta, J.-F. Joanny, Dynamical control of the shape and size of stereocilia and microvilli. Biophys. J. 93, 1124–1133 (2007)

    Article  ADS  Google Scholar 

  54. J. Prost, F. Jülicher, J.-F. Joanny, Active gel physics. Nat. Phys. 11, 111–117 (2015)

    Article  Google Scholar 

  55. M. Radszuweit, S. Alonso, H. Engel, M. Bär, Intracellular mechanochemical waves in an active poroelastic model. Phys. Rev. Lett. 110, 138102 (2013)

    Article  ADS  Google Scholar 

  56. M. Radszuweit, H. Engel, M. Bär, An active poroelastic model for mechanochemical patterns in protoplasmic droplets of Physarum polycephalum. PLoS One 9, e99220 (2014)

    Google Scholar 

  57. G.L. Ryan, N. Watanabe, D. Vavylonis, A review of models of fluctuating protrusion and retraction patterns at the leading edge of motile cells. Cytoskeleton (Hoboken) 69, 195–206 (2012)

    Article  Google Scholar 

  58. D. Sasaki, H. Fujita, N. Fukuda, S. Kurihara, S. Ishiwata, Auto-oscillations of skinned myocardium correlating with heartbeat. J. Muscle Res. Cell Motil. 26, 93–101 (2005)

    Article  Google Scholar 

  59. V. Schaller, C. Weber, C. Semmrich, E. Frey, A.R. Bausch, Polar patterns of driven filaments. Nature 467, 73–77 (2010)

    Article  ADS  Google Scholar 

  60. D. Shao, W.-J. Rappel, H. Levine, Computational model for cell morphodynamics. Phys. Rev. Lett. 105, 108104 (2010)

    Article  ADS  Google Scholar 

  61. A.D. Shenderov, M.P. Sheetz, Inversely correlated cycles in speed and turning in an ameba: an oscillatory model of cell locomotion. Biophys. J. 72, 2382–2389 (1997)

    Article  ADS  Google Scholar 

  62. R. Shlomovitz, N.S. Gov, Membrane waves driven by actin and myosin. Phys. Rev. Lett. 98, 168103 (2007)

    Article  ADS  Google Scholar 

  63. J. Solon, A. Kaya-Copur, J. Colombelli, D. Brunner, Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell 137, 1331–1342 (2009)

    Article  Google Scholar 

  64. S. Takagi, T. Ueda, Emergence and transitions of dynamic patterns of thickness oscillation of the plasmodium of the true slime mold Physarum polycephalum. Physica D 237, 420–427 (2008)

    Google Scholar 

  65. S. Takagi, T. Ueda, Annihilation and creation of rotating waves by a local light pulse in a protoplasmic droplet of the Physarum plasmodium. Physica D 239, 873–878 (2010)

    Google Scholar 

  66. T. Takenawa, S. Suetsugu, The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat. Rev. Mol. Cell Bio. 8, 37–48 (2007)

    Article  Google Scholar 

  67. A.M. Turing, The chemical basis of morphogenesis. Philos. Trans. R. Soc. B 237, 37–72 (1952)

    Article  ADS  MathSciNet  Google Scholar 

  68. D.M. Veltman, J.S. King, L.M. Machesky, R.H. Insall, SCAR knockouts in Dictyostelium: WASP assumes SCAR’s position and upstream regulators in pseudopods. J. Cell Biol. 198, 501–508 (2012)

    Article  Google Scholar 

  69. M.G. Vicker, Reaction-diffusion waves of actin filament polymerization/depolymerization in Dictyostelium pseudopodium extension and cell locomotion. Biophys. Chem. 84, 87–98 (2000)

    Article  Google Scholar 

  70. M.G. Vicker, Eukaryotic cell locomotion depends on the propagation of self-organized reaction-diffusion waves and oscillations of actin filament assembly. Exp. Cell Res. 275, 54–66 (2002)

    Article  Google Scholar 

  71. A. Wegner, Head to tail polymerization of actin. J. Mol. Biol. 108, 139–150 (1976)

    Article  Google Scholar 

  72. O.D. Weiner, W.A. Marganski, L.F. Wu, S.J. Altschuler, M.W. Kirschner, An actin-based wave generator organizes cell motility. PLoS Biol. 5, e221 (2007)

    Article  Google Scholar 

  73. S. Whitelam, T. Bretschneider, N.J. Burroughs, Transformation from spots to waves in a model of actin pattern formation. Phys. Rev. Lett. 102, 98103 (2009)

    Article  ADS  Google Scholar 

  74. F. Ziebert, S. Swaminathan, I.S. Aranson, Model for self-polarization and motility of keratocyte fragments. J. R. Soc. Interface 9, 1084–1092 (2012)

    Article  Google Scholar 

Download references

Acknowledgements

I thank my past and current collaborators, notably, I.S. Aranson, K. Doubrovinski, A. Dreher, and C. Erlenkamper, for countless interesting discussions on actin waves and cell motility. The work was funded in part by SFB 1027 of Deutsche Forschungsgemeinschaft.

Author information

Authors and Affiliations

  1. Theoretical Physics, Saarland University, Postfach 151150, 66041, Saarbrücken, Germany

    Karsten Kruse

Authors
  1. Karsten Kruse
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Karsten Kruse .

Editor information

Editors and Affiliations

  1. Argonne National Laboratory, Argonne, Illinois, USA

    Igor S. Aranson

2.1 Electronic Supplementary material

327960_1_En_2_MOESM1_ESM.mpg

ch2_video1.mpg (1,444 KB)

327960_1_En_2_MOESM2_ESM.mpg

ch2_video2.mpg (1,671 KB)

ch2_video3.mpg (1,666 KB)

ch2_video4.mpg (1,666 KB)

ch2_video5.mpg (1,666 KB)

ch2_video1.mpg (1,444 KB)

ch2_video2.mpg (1,671 KB)

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Kruse, K. (2016). Cell Crawling Driven by Spontaneous Actin Polymerization Waves. In: Aranson, I. (eds) Physical Models of Cell Motility. Biological and Medical Physics, Biomedical Engineering. Springer, Cham. https://doi.org/10.1007/978-3-319-24448-8_2

Download citation

Publish with us

Policies and ethics

Search

Navigation