The dynamics of actin-based motility depend on surface parameters

In cells, actin polymerization at the plasma membrane is induced by the recruitment of proteins such as the Arp2/3 complex, and the zyxin/VASP complex. The physical mechanism of force generation by actin polymerization has been described theoretically using various approaches, but lacks support from experimental data. By the use of reconstituted motility medium, we find that the Wiskott–Aldrich syndrome protein (WASP) subdomain, known as VCA, is sufficient to induce actin polymerization and movement when grafted on microspheres. Changes in the surface density of VCA protein or in the microsphere diameter markedly affect the velocity regime, shifting from a continuous to a jerky movement resembling that of the mutated ‘hopping’ Listeria. These results highlight how simple physical parameters such as surface geometry and protein density directly affect spatially controlled actin polymerization, and play a fundamental role in actin-dependent movement.

[1]  Marie-France Carlier,et al.  Mechanism of Actin-Based Motility , 2001, Science.

[2]  T. Pollard,et al.  Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins , 2000, Nature.

[3]  V. Noireaux,et al.  ActA and human zyxin harbour Arp2/3-independent actin-polymerization activity , 2001, Nature Cell Biology.

[4]  T. Mitchison,et al.  Actin dynamics in vivo. , 1997, Current opinion in cell biology.

[5]  A. Rutenberg,et al.  Curved tails in polymerization-based bacterial motility. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[6]  Gary G. Borisy,et al.  Arp2/3 Complex and Actin Depolymerizing Factor/Cofilin in Dendritic Organization and Treadmilling of Actin Filament Array in Lamellipodia , 1999, The Journal of cell biology.

[7]  T D Pollard,et al.  The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[8]  A. Carlsson,et al.  Growth of branched actin networks against obstacles. , 2001, Biophysical journal.

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

[10]  W. Almers,et al.  Endocytic vesicles move at the tips of actin tails in cultured mast cells , 1999, Nature Cell Biology.

[11]  K. Beningo,et al.  Nascent Focal Adhesions Are Responsible for the Generation of Strong Propulsive Forces in Migrating Fibroblasts , 2001, The Journal of cell biology.

[12]  T. Takenawa,et al.  WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. , 2001, Journal of cell science.

[13]  Timothy J. Mitchison,et al.  Actin polymerization is induced by Arp 2/3 protein complex at the surface of Listeria monocytogenes , 1997, Nature.

[14]  D. Portnoy,et al.  Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes , 1989, The Journal of cell biology.

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

[16]  V. Noireaux,et al.  Growing an actin gel on spherical surfaces. , 2000, Biophysical journal.

[17]  J A Theriot,et al.  Motility of ActA protein-coated microspheres driven by actin polymerization. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[18]  P. Cossart,et al.  Identification of two regions in the N‐terminal domain of ActA involved in the actin comet tail formation by Listeria monocytogenes , 1997, The EMBO journal.

[19]  Julie A. Theriot,et al.  Cooperative symmetry-breaking by actin polymerization in a model for cell motility , 1999, Nature Cell Biology.

[20]  M. Beckerle,et al.  PPPPS : EVH 1 domains and their proline-rich partners in cell polarity and migration , 2022 .

[21]  F. Jülicher,et al.  On the ‘listeria’ propulsion mechanism , 1999 .

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

[23]  Laura M. Machesky,et al.  Scar1 and the related Wiskott–Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex , 1998, Current Biology.

[24]  C. Larabell,et al.  Actin-Dependent Propulsion of Endosomes and Lysosomes by Recruitment of N-Wasp✪ , 2000, The Journal of cell biology.

[25]  J. Theriot,et al.  Effects of intermediate filaments on actin-based motility of Listeria monocytogenes. , 2001, Biophysical journal.

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

[27]  P. Gounon,et al.  The Arp2/3 complex branches filament barbed ends: functional antagonism with capping proteins , 2000, Nature Cell Biology.

[28]  P. Sansonetti,et al.  Activation of the Cdc42 Effector N-Wasp by the Shigella flexneri Icsa Protein Promotes Actin Nucleation by Arp2/3 Complex and Bacterial Actin-Based Motility , 1999, The Journal of cell biology.

[29]  James L. McGrath,et al.  Steps and fluctuations of Listeria monocytogenes during actin-based motility , 2000, Nature.