A microscopic formulation for the actin-driven motion of Listeria in curved paths

Biophysical Journal

Volumn 99, Issue 4, 2010, Pages 1043-1052

  Lin, Yuan ^a   Shenoy, V B ^b   Hu, Bin ^a   Bai, Limiao ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b Brown University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); LISTERIA;

EID: 77958195525     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.06.001     Document Type: Article

References (41)

1. Preston, T. M., C. A. King, and J. S. Hyams. 1990. The Cytoskeleton and Cell Motility. Blackie, Glasgow.
2. Theriot, J. A., and T. J. Mitchison. 1991. Actin microfilament dynamics in locomoting cells. Nature. 352:126-131.
3. Sanger, J. M., J. W. Sanger, and F. S. Southwick. 1992. Host cell actin assembly is necessary and likely to provide the propulsive force for intracellular movement of Listeria monocytogenes. Infect. Immun. 60:3609-3619.
4. Theriot, J. A., T. J. Mitchison, ..., D. A. Portnoy. 1992. The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization. Nature. 357:257-260.
5. Tilney, L. G., and D. A. Portnoy. 1989. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 109:1597-1608.
6. Cameron, L. A., M. J. Footer, ..., J. A. Theriot. 1999. Motility of ActA protein-coated microspheres driven by actin polymerization. Proc. Natl. Acad. Sci. USA. 96:4908-4913.
7. Cameron, L. A., T. M. Svitkina, ..., G. G. Borisy. 2001. Dendritic organization of actin comet tails. Curr. Biol. 11:130-135.
8. Smith, G. A., J. A. Theriot, and D. A. Portnoy. 1996. The tandem repeat domain in the Listeria monocytogenes ActA protein controls the rate of actin-based motility, the percentage of moving bacteria, and the localization of vasodilator-stimulated phosphoprotein and profilin. J. Cell Biol. 135:647-660.
9. Kocks, C., R. Hellio, ..., P. Cossart. 1993. Polarized distribution of Listeria monocytogenes surface protein ActA at the site of directional actin assembly. J. Cell Sci. 105:699-710.
10. Rafelski, S. M., and J. A. Theriot. 2005. Bacterial shape and ActA distribution affect initiation of Listeria monocytogenes actin-based motility. Biophys. J. 89:2146-2158.
11. Rafelski, S. M., and J. A. Theriot. 2006. Mechanism of polarization of Listeria monocytogenes surface protein ActA. Mol. Microbiol. 59:1262-1279.
12. Rafelski, S. M., J. B. Alberts, and G. M. Odell. 2009. An experimental and computational study of the effect of ActA polarity on the speed of Listeria monocytogenes actin-based motility. PLoS Comput. Biol. 7:e1000434.
13. Peskin, C. S., G. M. Odell, and G. F. Oster. 1993. Cellular motions and thermal fluctuations: the Brownian ratchet. Biophys. J. 65:316-324.
14. Mogilner, A., and G. Oster. 1996. Cell motility driven by actin polymerization. Biophys. J. 71:3030-3045.
15. Kuo, S. C., and J. L. McGrath. 2000. Steps and fluctuations of Listeria monocytogenes during actin-based motility. Nature. 407:1026-1029.
16. Gerbal, F., V. Laurent, ..., J. Prost. 2000. Measurement of the elasticity of the actin tail of Listeria monocytogenes. Eur. Biophys. J. 29:134-140.
17. Mogilner, A., and G. Oster. 2003. Force generation by actin polymerization II: the elastic ratchet and tethered filaments. Biophys. J. 84:1591-1605.
18. Dickinson, R. B., and D. L. Purich. 2002. Clamped-filament elongation model for actin-based motors. Biophys. J. 82:605-617.
19. Dickinson, R. B., L. Caro, and D. L. Purich. 2004. Force generation by cytoskeletal filament end-tracking proteins. Biophys. J. 87:2838-2854.
20. Gerbal, F., P. Chaikin, ..., J. Prost. 2000. An elastic analysis of Listeria monocytogenes propulsion. Biophys. J. 79:2259-2275.
21. Schwartz, I. M., M. Ehrenberg, ..., J. L. McGrath. 2004. The role of substrate curvature in actin-based pushing forces. Curr. Biol. 14:1094-1098.
22. Upadhyaya, A., and A. van Oudenaarden. 2004. Actin polymerization: forcing flat faces forward. Curr. Biol. 14:R467-R469.
23. Carlsson, A. E. 2001. Growth of branched actin networks against obstacles. Biophys. J. 81:1907-1923.
24. Dayel, M. J., O. Akin, ..., R. D. Mullins. 2009. In silico reconstitution of actin-based symmetry breaking and motility. PLoS Biol. 7:e1000201.
25. Alberts, J. B., and G. M. Odell. 2004. In silico reconstitution of Listeria propulsion exhibits nano-saltation. PLoS Biol. 2:e412.
26. Lee, K.-C., and A. J. Liu. 2008. New proposed mechanism of actin-polymerization-driven motility. Biophys. J. 95:4529-4539.
27. Lin, Y. 2009. Mechanics model for actin-based motility. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 79:021916.
28. Upadhyaya, A., J. R. Chabot, ..., A. van Oudenaarden. 2003. Probing polymerization forces by using actin-propelled lipid vesicles. Proc. Natl. Acad. Sci. USA. 100:4521-4526.
29. Dickinson, R. B., and D. L. Purich. 2006. Diffusion rate limitations in actin-based propulsion of hard and deformable particles. Biophys. J. 91:1548-1563.
30. Soo, F. S., and J. A. Theriot. 2005. Large-scale quantitative analysis of sources of variation in the actin polymerization-based movement of Listeria monocytogenes. Biophys. J. 89:703-723.
31. Shenoy, V. B., D. T. Tambe, ..., J. A. Theriot. 2007. A kinematic description of the trajectories of Listeria monocytogenes propelled by actin comet tails. Proc. Natl. Acad. Sci. USA. 104:8229-8234.
32. Rutenberg, A. D., and M. Grant. 2001. Curved tails in polymerization-based bacterial motility. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 64:021904.
33. Robbins, J. R., and J. A. Theriot. 2003. Listeria monocytogenes rotates around its long axis during actin-based motility. Curr. Biol. 13:R754-R756.
34. Mogilner, A. 2009. Mathematics of cell motility: have we got its number? J. Math. Biol. 58:105-134.
35. Evans, E., and K. Ritchie. 1999. Strength of a weak bond connecting flexible polymer chains. Biophys. J. 76:2439-2447.
36. Press, W. H., S. A. Teukolsky, ..., B. P. Flannery. 1992. Numerical Recipes in FORTRAN: The Art of Scientific Computing, 2nd ed. Cambridge University, Cambridge, United Kingdom.
37. Plastino, J., S. Olivier, and C. Sykes. 2004. Actin filaments align into hollow comets for rapid VASP-mediated propulsion. Curr. Biol. 14:1766-1771.
38. Mogilner, A., and L. Edelstein-Keshet. 2002. Regulation of actin dynamics in rapidly moving cells: a quantitative analysis. Biophys. J. 83:1237-1258.
39. Akin, O., and R. D. Mullins. 2008. Capping protein increases the rate of actin-based motility by promoting filament nucleation by the Arp2/3 complex. Cell. 133:841-851.
40. Boujemaa-Paterski, R., E. Gouin, ..., D. Pantaloni. 2001. Listeria protein ActA mimics WASp family proteins: it activates filament barbed end branching by Arp2/3 complex. Biochemistry. 40: 11390-11404.
41. Svitkina, T. M., A. B. Verkhovsky, ..., G. G. Borisy. 1997. Analysis of the actin-myosin II system in fish epidermal keratocytes: mechanism of cell body translocation. J. Cell Biol. 139:397-415.