Growth of Branched Actin Networks against Obstacles

Carlsson, Anders

doi:10.1016/s0006-3495(01)75842-0

Cited by 137 publications

(187 citation statements)

References 42 publications

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“…These include the thermal ratchet model for polymerization-dependent force Oster, 1996a,b, 2003), filament side-branching (Carlsson, 2001(Carlsson, , 2003, and filament-turnover (Mogilner and EdelsteinKeshet, 2002;Grimm et al, 2003). An overarching recent objective has been to start combining diverse aspects of cell motility into a framework of a spatial cell.…”

Section: Discussionmentioning

confidence: 99%

Polarization and Movement of Keratocytes: A Multiscale Modelling Approach

et al. 2006

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Section: Discussionmentioning

confidence: 99%

Polarization and Movement of Keratocytes: A Multiscale Modelling Approach

et al. 2006

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“…In the case of L. monocytogenes, it is an important feature because these bacteria have to cross cell membranes to disseminate: they must keep moving against the force exerted by these obstacles. Various force-velocity relations have been predicted by different theoretical models of actin-based propulsion (30,(34)(35)(36)) (see ref. 37 for review).…”

Section: Discussionmentioning

confidence: 99%

Forces generated during actin-based propulsion: A direct measurement by micromanipulation

Marcy

Prost

Carlier

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

235

208

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Dynamic actin networks generate forces for numerous types of movements such as lamellipodia protrusion or the motion of endocytic vesicles. The actin-based propulsive movement of Listeria monocytogenes or of functionalized microspheres have been extensively used as model systems to identify the biochemical components that are necessary for actin-based motility. However, quantitative force measurements are required to elucidate the mechanism of force generation, which is still under debate. To directly probe the forces generated in the process of actin-based propulsion, we developed a micromanipulation experiment. A comet growing from a coated polystyrene bead is held by a micropipette while the bead is attached to a force probe, by using a specially designed ''flexible handle.'' This system allows us to apply both pulling and pushing external forces up to a few nanonewtons. By pulling the actin tail away from the bead at high speed, we estimate the elastic modulus of the gel and measure the force necessary to detach the tail from the bead. By applying a constant force in the range of ؊1.7 to 4.3 nN, the force-velocity relation is established. We find that the relation is linear for pulling forces and decays more weakly for pushing forces. This behavior is explained by using a dimensional elastic analysis.T he growth of a polymer against a barrier is a general mechanism for production of force in cell biology (1). Spatially controlled polymerization of actin is responsible for a large variety of changes in cell shape leading to cell movement, like the protrusion of the lamellipodium (2), or the intracellular propulsion of vesicles (3, 4) and pathogens (5, 6). Actin assembly in these processes is controlled by various proteins present in the cytoplasm, which have been identified over the last 10 years (see refs. 7 and 8 for review). It is now well established that the Arp2͞3 complex associates with Wiskott-Aldrich Syndrome protein (WASp) family proteins to create new filaments locally by branching them (9), thus generating the dendritic organization of the actin array (10, 11). Because pure actin treadmilling is too slow to account for polymerization speed observed in these systems, this process has to be speeded up by regulatory proteins (8). One experimental model that has been used widely for the identification of these proteins is the bacteria Listeria monocytogenes, which are propelled inside cells by actin polymerization. The minimal subset of proteins necessary and sufficient to reconstitute the Listeria movement has been identified (12). In addition to Arp2͞3 and actin, the regulatory proteins ADF͞ cofilin, profilin, and a capping protein are necessary to enhance the efficiency of treadmilling (13) and control the life time and average length of filaments (14, 15). The essential role of these proteins has been confirmed recently (16) in vivo by using a RNA interference strategy.Biomimetic systems are useful for analyzing the physical aspects of actin-based motility. Listeria movement can be mimicked by fun...

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“…A very recent experiment (16) that considers the temperature dependence of the speed of motile bacteria finds an activated Arrhenius behavior consistent with the breaking of tethered bonds. In addition, branching of the filaments at the surface can also influence the force-velocity curve (9). To accommodate all these possible scenarios, we will assume a general force-velocity relation ṡ ϭ v 0 (F), where the right-hand side can assume any functional form depending on the dominant physical mechanism limiting the bacterial speed.…”

Section: Dynamical Model For 2d Motionmentioning

confidence: 99%

“…With the knowledge of polymerization kinetics at the single filament level, is it possible to predict propulsive forces/torques at the macroscale? Several models (8)(9)(10) have partly addressed this question by considering the relation between the force exerted by the actin network and the velocity of the cargo it propels. Measurements (11-13) of the force-velocity relationships have been reported for both Listeria and beads, but consensus has not been reached on a satisfactory theoretical model due to significant qualitative (and quantitative) differences between the measurements themselves.…”

mentioning

confidence: 99%

A kinematic description of the trajectories of Listeria monocytogenes propelled by actin comet tails

Shenoy

Tambe

Prasad

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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The bacterial pathogen Listeria monocytogenes propels itself in the cytoplasm of the infected cells by forming a filamentous comet tail assembled by the polymerization of the cytoskeletal protein actin. Although a great deal is known about the molecular processes that lead to actin-based movement, most macroscale aspects of motion, including the nature of the trajectories traced out by the motile bacteria, are not well understood. Here, we present 2D trajectories of Listeria moving between a glass-slide and coverslip in a Xenopus frog egg extract motility assay. We observe that the bacteria move in a number of fascinating geometrical trajectories, including winding S curves, translating figure eights, small-and largeamplitude sine curves, serpentine shapes, circles, and a variety of spirals. We then develop a dynamic model that provides a unified description of these seemingly unrelated trajectories. A key ingredient of the model is a torque (not included in any microscopic models of which we are aware) that arises from the rotation of the propulsive force about the body axis of the bacterium. We show that a large variety of trajectories with a rich mathematical structure are obtained by varying the rate at which the propulsive force moves about the long axis. The trajectories of bacteria executing both steady and saltatory motion are found to be in excellent agreement with the predictions of our dynamic model. When the constraints that lead to planar motion are removed, our model predicts motion along regular helical trajectories, observed in recent experiments. motility ͉ bacteria P olymerization of the cytoskeletal protein actin into a network of filaments is necessary for the motility of several infectious bacteria. These bacterial pathogens hijack the actin machinery of the host cell to form ''comet tails'' due to unidirectional actin assembly at one of their poles. The force generated by the actin network allows the bacteria to move within the infected cell and to other cells in it's neighborhood. The biochemistry of the tail formation process has been well studied in the case of the Grampositive bacterium Listeria monocytogenes (1-3). In particular, it has been shown that only one bacterial surface factor, ActA, is required for the movement of Listeria in a medium containing a few other actin-related proteins from the cytoplasm of the host cell. This observation has led to in vitro motility assays in which polystyrene beads (4) or disks (5) and phospholipid vesicles (6, 7) coated with ActA are propelled by the comet tails formed by actin polymerization. Many of the proteins responsible for the movement of Listeria have also been found in the front end of a crawling cell, also referred to as the lamellopodium (1). Listeria is therefore a model system that has provided important molecular level insights on actin-based motility.Although progress has been made at the molecular level, the connection between biochemical processes and force generation has not been fully elucidated. With the knowledge of polymeri...

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Growth of Branched Actin Networks against Obstacles

Cited by 137 publications

References 42 publications

Polarization and Movement of Keratocytes: A Multiscale Modelling Approach

Polarization and Movement of Keratocytes: A Multiscale Modelling Approach

Forces generated during actin-based propulsion: A direct measurement by micromanipulation

A kinematic description of the trajectories of Listeria monocytogenes propelled by actin comet tails

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