Biomimetic Systems for Studying Actin-Based Motility

Actin polymerization provides a major driving force for eukaryotic cell motility. Successive intercalation of monomeric actin subunits between the plasma membrane and the filamentous actin network results in protrusions of the membrane enabling the cell to move or to change shape. One of the challenges in understanding eukaryotic cell motility is to dissect the elementary biochemical and biophysical steps that link actin polymerization to mechanical force generation. Recently, significant progress was made using biomimetic, in vitro systems that are inspired by the actin-based motility of bacterial pathogens such as Listeria monocytogenes. Polystyrene microspheres and synthetic phospholipid vesicles coated with proteins that initiate actin polymerization display motile behavior similar to Listeria, mimicking the leading edge of lamellipodia and filopodia. A major advantage of these biomimetic systems is that both biochemical and physical parameters can be controlled precisely. These systems provide a test bed for validating theoretical models on force generation and polarity establishment resulting from actin polymerization. In this review, we discuss recent experimental progress using biomimetic systems propelled by actin polymerization and discuss these results in the light of recent theoretical models on actin-based motility.

[1]  Paul A. Janmey,et al.  Corequirement of Specific Phosphoinositides and Small GTP-binding Protein Cdc42 in Inducing Actin Assembly in Xenopus Egg Extracts , 1998, The Journal of cell biology.

[2]  M. Magnasco,et al.  Measurement of the persistence length of polymerized actin using fluorescence microscopy. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

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

[4]  K. Kinosita,et al.  Protrusive growth from giant liposomes driven by actin polymerization. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[5]  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.

[6]  T. Svitkina,et al.  Actin machinery: pushing the envelope. , 2000, Current opinion in cell biology.

[7]  P. Cossart,et al.  Intracellular pathogens and the actin cytoskeleton. , 1998, Annual review of cell and developmental biology.

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

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

[10]  J. Howard,et al.  Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape , 1993, The Journal of cell biology.

[11]  T. Roberts,et al.  Reconstitution In Vitro of the Motile Apparatus from the Amoeboid Sperm of Ascaris Shows That Filament Assembly and Bundling Move Membranes , 1996, Cell.

[12]  M. Carlier,et al.  Actin-based motility: from molecules to movement. , 2003, BioEssays : news and reviews in molecular, cellular and developmental biology.

[13]  T. Mitchison,et al.  Actin-Based Cell Motility and Cell Locomotion , 1996, Cell.

[14]  I. Nabi The polarization of the motile cell. , 1999, Journal of cell science.

[15]  Julie A. Theriot,et al.  Secrets of actin-based motility revealed by a bacterial pathogen , 2000, Nature Reviews Molecular Cell Biology.

[16]  Lakshminarayanan Mahadevan,et al.  The Force-Velocity Relationship for the Actin-Based Motility of Listeria monocytogenes , 2003, Current Biology.

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

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

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

[20]  Michael P. Sheetz,et al.  Cell Spreading and Lamellipodial Extension Rate Is Regulated by Membrane Tension , 2000, The Journal of cell biology.

[21]  J. Wehland,et al.  The bacterial actin nucleator protein ActA of Listeria monocytogenes contains multiple binding sites for host microfilament proteins , 1995, Current Biology.

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

[23]  C S Peskin,et al.  Cellular motions and thermal fluctuations: the Brownian ratchet. , 1993, Biophysical journal.

[24]  Evans,et al.  Entropy-driven tension and bending elasticity in condensed-fluid membranes. , 1990, Physical review letters.

[25]  C. Kocks,et al.  The unrelated surface proteins ActA of Listeria monocytogenes and lcsA of Shigella flexneri are sufficient to confer actin‐based motility on Listeria innocua and Escherichia coli respectively , 1995, Molecular microbiology.

[26]  Alexander van Oudenaarden,et al.  Probing polymerization forces by using actin-propelled lipid vesicles , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[27]  A. Carlsson Growth velocities of branched actin networks. , 2003, Biophysical journal.

[28]  P. Chaikin,et al.  Measurement of the elasticity of the actin tail of Listeria monocytogenes , 2000, European Biophysics Journal.

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

[30]  Reinhard Lipowsky,et al.  Structure and dynamics of membranes , 1995 .

[31]  H. Hotani,et al.  Morphological changes in liposomes caused by polymerization of encapsulated actin and spontaneous formation of actin bundles. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

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

[33]  T. Pollard,et al.  The Arp2/3 complex nucleates actin filament branches from the sides of pre-existing filaments , 2001, Nature Cell Biology.

[34]  E. Elson,et al.  Actin polymerization induces a shape change in actin-containing vesicles. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[35]  T. L. Hill,et al.  Bioenergetics and kinetics of microtubule and actin filament assembly-disassembly. , 1982, International review of cytology.

[36]  U. Walter,et al.  A focal adhesion factor directly linking intracellularly motile Listeria monocytogenes and Listeria ivanovii to the actin‐based cytoskeleton of mammalian cells. , 1995, The EMBO journal.

[37]  T D Pollard,et al.  Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. , 2001, Annual review of biochemistry.

[38]  B. Yurke,et al.  Measurement of the force-velocity relation for growing microtubules. , 1997, Science.

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

[40]  H. Isambert,et al.  Flexibility of actin filaments derived from thermal fluctuations. Effect of bound nucleotide, phalloidin, and muscle regulatory proteins , 1995, The Journal of Biological Chemistry.

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

[42]  Matthew D. Welch,et al.  The Wiskott–Aldrich syndrome protein directs actin-based motility by stimulating actin nucleation with the Arp2/3 complex , 1999, Current Biology.

[43]  M. Kirschner,et al.  The Interaction between N-WASP and the Arp2/3 Complex Links Cdc42-Dependent Signals to Actin Assembly , 1999, Cell.

[44]  D. Fletcher,et al.  Compression forces generated by actin comet tails on lipid vesicles , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[45]  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.

[46]  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.

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

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

[49]  E. J. Ambrose,et al.  CELL MOVEMENTS. , 1965, Endeavour.

[50]  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.

[51]  T. Pollard,et al.  Cellular Motility Driven by Assembly and Disassembly of Actin Filaments , 2003, Cell.

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

[53]  D. DeRosier,et al.  How Listeria exploits host cell actin to form its own cytoskeleton. I. Formation of a tail and how that tail might be involved in movement , 1992, The Journal of cell biology.

[54]  D. Lauffenburger,et al.  Cell Migration: A Physically Integrated Molecular Process , 1996, Cell.

[55]  Thomas D Pollard,et al.  Cellular Motility Driven by Assembly and Disassembly of Actin Filaments , 2003, Cell.

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

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

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

[59]  D. Purich,et al.  Clamped-filament elongation model for actin-based motors. , 2002, Biophysical journal.

[60]  U. Walter,et al.  The 46/50 kDa phosphoprotein VASP purified from human platelets is a novel protein associated with actin filaments and focal contacts. , 1992, The EMBO journal.