Actin-based propulsion of spatially extended objects

We propose a mathematical model of the actin-based propulsion of spatially extended obstacles. It starts from the properties of individual actin filaments and includes transient attachment to the obstacle, polymerization as well as cross-linking. Two particular geometries are discussed, which apply to the motion of protein-coated beads in a cell-like medium and the leading edge of a cell protrusion, respectively. The model gives rise to both steady and saltatory movement of beads and can explain the experimentally observed transitions of the dynamic regime with changing bead radius and protein surface density. Several spatiotemporal patterns are obtained with a soft obstacle under tension, including the experimentally observed spontaneous emergence of lateral traveling waves in crawling cells. Thus, we suggest a unifying mechanism for systems that are currently described by differential concepts.

[1]  Marie-France Carlier,et al.  The dynamics of actin-based motility depend on surface parameters , 2002, Nature.

[2]  Gaudenz Danuser,et al.  Supporting Material : Modeling of protrusion phenotypes driven by the actin-membrane interaction , 2009 .

[3]  Marie-France Carlier,et al.  Forces generated during actin-based propulsion: a direct measurement by micromanipulation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Alex Mogilner,et al.  Mathematics of Cell Motility: Have We Got Its Number? , 2022 .

[5]  Erwin Frey,et al.  Tracer studies on f-actin fluctuations. , 2002, Physical review letters.

[6]  K. Rottner,et al.  Differentially oriented populations of actin filaments generated in lamellipodia collaborate in pushing and pausing at the cell front , 2008, Nature Cell Biology.

[7]  P. Chaikin,et al.  An elastic analysis of Listeria monocytogenes propulsion. , 2000, Biophysical journal.

[8]  D. L. Taylor,et al.  The actin-based nanomachine at the leading edge of migrating cells. , 1999, Biophysical journal.

[9]  Erwin Frey,et al.  Velocity oscillations in actin-based motility , 2007, 0704.1390.

[10]  George Oster,et al.  Force generation by actin polymerization II: the elastic ratchet and tethered filaments. , 2003, Biophysical journal.

[11]  L. Blanchoin,et al.  Actin-Filament Stochastic Dynamics Mediated by ADF/Cofilin , 2007, Current Biology.

[12]  J. Joanny,et al.  Generic theory of active polar gels: a paradigm for cytoskeletal dynamics , 2004, The European physical journal. E, Soft matter.

[13]  Mark J. Dayel,et al.  In Silico Reconstitution of Actin-Based Symmetry Breaking and Motility , 2009, PLoS biology.

[14]  J. Small,et al.  The Isolated Comet Tail Pseudopodium of Listeria monocytogenes: A Tail of Two Actin Filament Populations, Long and Axial and Short and Random , 1997, The Journal of cell biology.

[15]  J. Prost,et al.  Mechanism of actin-based motility: a dynamic state diagram. , 2005, Biophysical journal.

[16]  T. Svitkina,et al.  Orientational order of the lamellipodial actin network as demonstrated in living motile cells. , 2003, Molecular biology of the cell.

[17]  Chris H Wiggins,et al.  Lateral membrane waves constitute a universal dynamic pattern of motile cells. , 2006, Physical review letters.

[18]  Martin Falcke,et al.  Leading-edge-gel coupling in lamellipodium motion. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[19]  F. Lafuma,et al.  A biomimetic motility assay provides insight into the mechanism of actin-based motility , 2003, The Journal of cell biology.

[20]  K. Kassner,et al.  Nonlinear study of symmetry breaking in actin gels: implications for cellular motility. , 2007, Physical review letters.

[21]  Entropic forces generated by grafted semiflexible polymers. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[22]  Marie-France Carlier,et al.  Reconstitution of actin-based motility of Listeria and Shigella using pure proteins , 1999, Nature.

[23]  T. Mitchison,et al.  Fascin-mediated propulsion of Listeria monocytogenes independent of frequent nucleation by the Arp2/3 complex , 2004, The Journal of cell biology.

[24]  Gary G. Borisy,et al.  Dendritic organization of actin comet tails , 2001, Current Biology.

[25]  G. Danuser,et al.  Morphodynamic profiling of protrusion phenotypes. , 2006, Biophysical journal.

[26]  E. Evans.  Probing the relation between force--lifetime--and chemistry in single molecular bonds. , 2001, Annual review of biophysics and biomolecular structure.

[27]  Werner Ebeling,et al.  Physik der Selbstorganisation und Evolution , 1984 .

[28]  Frey,et al.  Force-Extension Relation and Plateau Modulus for Wormlike Chains. , 1996, Physical review letters.

[29]  G. Oster,et al.  Cell motility driven by actin polymerization. , 1996, Biophysical journal.

[30]  Gary G. Borisy,et al.  Analysis of the Actin–Myosin II System in Fish Epidermal Keratocytes: Mechanism of Cell Body Translocation , 1997, The Journal of cell biology.

[31]  Alex Mogilner,et al.  Quantitative analysis of G-actin transport in motile cells. , 2008, Biophysical journal.

[32]  J. Joanny,et al.  Contractility and retrograde flow in lamellipodium motion , 2006, Physical biology.

[33]  M. Falcke,et al.  Dynamic regimes and bifurcations in a model of actin-based motility. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[34]  M. Cross,et al.  Pattern formation outside of equilibrium , 1993 .