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Diffusion-Limited Speed of an Actin-Propelled Particle Near a Surface

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Abstract

Some invasive pathogens and other particles are propelled intracellularly by the polymerization of actin at the particle surface into a dense “comet tail” of filamentous actin. As new monomers are added to the filament (+)-ends located the junction between the particle and its comet tail, the particle is propelled forward. The molecular origin of force generation and how the elongating comet tail remains attached to the particle surface via nucleation promoting factors such as N-WASP remain unresolved questions. Recently, based on measurements of biomimetic particles coated with RickA, a bacterial homolog to N-WASP, Shaevitz and Fletcher [Proc. Natl. Acad. Sci. U.S.A. 104:15688–15692, 2007] reported that particle speed depends on the separation distance from a nearby wall (slide surface), a result which they interpreted as the effect of hydrodynamic coupling to the wall damping fluctuations and inhibiting monomer addition, consistent with the well-known “Brownian ratchet” model for force generation. Based on a reaction-diffusion model for monomer transport and consumption at the particle surface, we show here that the experimentally observed speed-separation distance profile is completely consistent with hindered monomer diffusion due to the presence of the nearby wall. That is, the observed reduction in speed can be entirely explained by hindered diffusion, without invoking any hydrodynamic effect.

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References

  1. Bernheim-Groswasser, A., J. Prost, C. Sykes. Mechanism of actin-based motility: a dynamic state diagram. Biophys J. 89:1411-1419. 2005.

    Article  Google Scholar 

  2. Bernheim-Groswasser, A., 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  Google Scholar 

  3. Brebbia, C.A. 1984 Boundary Element Techniques. New York: Springer-Verlag. 1984.

    MATH  Google Scholar 

  4. Bugyi, B., C. Le Clainche, G. Romet-Lemonne, M. F. Carlier. How do in vitro reconstituted actin-based motility assays provide insight into in vivo behavior? FEBS Lett. 582(14):2086–2092, 2008.

    Article  Google Scholar 

  5. Cameron, L.A., T.M. Svitkina, D. Vignjevic, J.A. Theriot, G.G. Borisy. Dendritic organization of actin comet tails. Curr Biol. 11:130-135. 2001.

    Article  Google Scholar 

  6. Co, C., D.T. Wong, S. Gierke, V. Chang, J. Taunton. Mechanism of actin network attachment to moving membranes: barbed end capture by N-WASP WH2 domains. Cell. 128:901-913. 2007.

    Article  Google Scholar 

  7. Dickinson, R.B. A multiscale model for actin-propelled bacteria. Cellular and Molecular Bioengineering. 1:110-121. 2008.

    Article  Google Scholar 

  8. Dickinson, R.B. Models for actin polymerization motors. J Math Biol. 58:81-103. 2009.

    Article  MATH  MathSciNet  Google Scholar 

  9. Dickinson, R.B., L. Caro, D.L. Purich. Force generation by cytoskeletal filament end-tracking proteins. Biophys J. 87:2838-2854. 2004.

    Article  Google Scholar 

  10. Dickinson, R.B., D.L. Purich. Clamped-filament elongation model for actin-based motors. Biophys J. 82:605-617. 2002.

    Article  Google Scholar 

  11. Dickinson, R.B., D.L. Purich. Diffusion rate limitations in actin-based propulsion of hard and deformable particles. Biophys J. 91:1548-1563. 2006.

    Article  Google Scholar 

  12. Gouin, E., C. Egile, P. Dehoux, V. Villiers, J. Adams, F. Gertler, R. Li, P. Cossart. The RickA protein of Rickettsia conorii activates the Arp2/3 complex. Nature. 427:457-461. 2004.

    Article  Google Scholar 

  13. Hill, T.L. Microfilament or microtubule assembly or disassembly against a force. Proc Natl Acad Sci U S A. 78:5613-5617. 1981.

    Article  Google Scholar 

  14. Lacayo, C.I., Z. Pincus, M.M. VanDuijn, C.A. Wilson, D.A. Fletcher, F.B. Gertler, A. Mogilner, J.A. Theriot. Emergence of large-scale cell morphology and movement from local actin filament growth dynamics. PLoS Biol. 5:e233. 2007.

    Article  Google Scholar 

  15. McGrath, J.L., N.J. Eungdamrong, C.I. Fisher, F. Peng, L. Mahadevan, T.J. Mitchison, S.C. Kuo. The force-velocity relationship for the actin-based motility of Listeria monocytogenes. Curr Biol. 13:329-332. 2003.

    Article  Google Scholar 

  16. McGrath, J.L., Y. Tardy, C.F. Dewey, Jr., J.J. Meister, J.H. Hartwig. Simultaneous measurements of actin filament turnover, filament fraction, and monomer diffusion in endothelial cells. Biophys J. 75:2070-2078. 1998.

    Article  Google Scholar 

  17. Mogilner, A., G. Oster. Cell motility driven by actin polymerization. Biophys J. 71:3030-3045. 1996.

    Article  Google Scholar 

  18. Mogilner, A., G. Oster. Force Generation by Actin Polymerization II: The Elastic Ratchet and Tethered Filaments. Biophys J. 84:1591-1605. 2003.

    Article  Google Scholar 

  19. Noireaux, V., R.M. Golsteyn, E. Friederich, J. Prost, C. Antony, D. Louvard, C. Sykes. Growing an actin gel on spherical surfaces. Biophys J. 78:1643-1654. 2000.

    Article  Google Scholar 

  20. Parekh, S.H., O. Chaudhuri, J.A. Theriot, D.A. Fletcher. Loading history determines the velocity of actin-network growth. Nat Cell Biol. 7:1119-1123. 2005.

    Article  Google Scholar 

  21. Peskin, C.S., G.M. Odell, G.F. Oster. Cellular motions and thermal fluctuations: the Brownian ratchet. Biophys J. 65:316-324. 1993.

    Article  Google Scholar 

  22. Plastino, J., I. Lelidis, J. Prost, C. Sykes. The effect of diffusion, depolymerization and nucleation promoting factors on actin gel growth. Eur Biophys J. 33:310-320. 2004.

    Article  Google Scholar 

  23. Pollard, T.D., L. Blanchoin, R.D. Mullins. Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct. 29:545-576. 2000.

    Article  Google Scholar 

  24. Samarin, S., S. Romero, C. Kocks, D. Didry, D. Pantaloni, M.F. Carlier. How VASP enhances actin-based motility. J Cell Biol. 163:131-142. 2003.

    Article  Google Scholar 

  25. Sechi, A.S., J. Wehland, J.V. Small. The isolated comet tail pseudopodium of Listeria monocytogenes: a tail of two actin filament populations, long and axial and short and random. J Cell Biol. 137:155-167. 1997.

    Article  Google Scholar 

  26. Shaevitz, J.W., D.A. Fletcher. Load fluctuations drive actin network growth. Proc Natl Acad Sci U S A. 104:15688-15692. 2007.

    Article  Google Scholar 

  27. Soo, F.S., J.A. Theriot. Adhesion controls bacterial actin polymerization-based movement. Proc Natl Acad Sci U S A. 102:16233-16238. 2005.

    Article  Google Scholar 

  28. Soo, F.S., J.A. Theriot. Large-scale quantitative analysis of sources of variation in the actin polymerzation-based movement of Listeria monocytogenes. Biophys J. 89:703-723. 2005.

    Article  Google Scholar 

  29. Stevens, J.M., E.E. Galyov, M.P. Stevens. Actin-dependent movement of bacterial pathogens. Nat Rev Microbiol. 4:91-101. 2006.

    Article  Google Scholar 

  30. Trichet, L., O. Campas, C. Sykes, J. Plastino. VASP governs actin dynamics by modulating filament anchoring. Biophys J. 92:1081-1089. 2007.

    Article  Google Scholar 

  31. Upadhyaya, A., J.R. Chabot, A. Andreeva, A. Samadani, A. van Oudenaarden. Probing polymerization forces by using actin-propelled lipid vesicles. Proc Natl Acad Sci U S A. 100:4521-4526. 2003.

    Article  Google Scholar 

  32. Wiesner, S., E. Helfer, D. Didry, G. Ducouret, F. Lafuma, M.F. Carlier, D. Pantaloni. A biomimetic motility assay provides insight into the mechanism of actin-based motility. J Cell Biol. 160:387-398. 2003.

    Article  Google Scholar 

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Acknowledgment

This work was supported by a grant from the National Science Foundation (CTS-0505929).

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Correspondence to Richard B. Dickinson.

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Dickinson, R.B. Diffusion-Limited Speed of an Actin-Propelled Particle Near a Surface. Cel. Mol. Bioeng. 2, 200–206 (2009). https://doi.org/10.1007/s12195-009-0056-8

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