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. 2000 Nov;79(5):2259–2275. doi: 10.1016/S0006-3495(00)76473-3

An elastic analysis of Listeria monocytogenes propulsion.

F Gerbal 1, P Chaikin 1, Y Rabin 1, J Prost 1
PMCID: PMC1301115  PMID: 11053107

Abstract

The bacterium Listeria monocytogenes uses the energy of the actin polymerization to propel itself through infected tissues. In steady state, it continuously adds new polymerized filaments to its surface, pushing on its tail, which is made from previously cross-linked actin filaments. In this paper we introduce an elastic model to describe how the addition of actin filaments to the tail results in the propulsive force on the bacterium. Filament growth on the bacterial surface produces stresses that are relieved at the back of the bacterium as it moves forward. The model leads to a natural competition between growth from the sides and growth from the back of the bacterium, with different velocities and strengths for each. This competition can lead to the periodic motion observed in a Listeria mutant.

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Selected References

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  1. Alt W., Dembo M. Cytoplasm dynamics and cell motion: two-phase flow models. Math Biosci. 1999 Mar 1;156(1-2):207–228. doi: 10.1016/s0025-5564(98)10067-6. [DOI] [PubMed] [Google Scholar]
  2. Bray D., Money N. P., Harold F. M., Bamburg J. R. Responses of growth cones to changes in osmolality of the surrounding medium. J Cell Sci. 1991 Apr;98(Pt 4):507–515. doi: 10.1242/jcs.98.4.507. [DOI] [PubMed] [Google Scholar]
  3. Cameron L. A., Footer M. J., van Oudenaarden A., Theriot J. A. Motility of ActA protein-coated microspheres driven by actin polymerization. Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):4908–4913. doi: 10.1073/pnas.96.9.4908. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Clerc P., Sansonetti P. J. Entry of Shigella flexneri into HeLa cells: evidence for directed phagocytosis involving actin polymerization and myosin accumulation. Infect Immun. 1987 Nov;55(11):2681–2688. doi: 10.1128/iai.55.11.2681-2688.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cossart P., Kocks C. The actin-based motility of the facultative intracellular pathogen Listeria monocytogenes. Mol Microbiol. 1994 Aug;13(3):395–402. doi: 10.1111/j.1365-2958.1994.tb00434.x. [DOI] [PubMed] [Google Scholar]
  6. Cudmore S., Cossart P., Griffiths G., Way M. Actin-based motility of vaccinia virus. Nature. 1995 Dec 7;378(6557):636–638. doi: 10.1038/378636a0. [DOI] [PubMed] [Google Scholar]
  7. Dabiri G. A., Sanger J. M., Portnoy D. A., Southwick F. S. Listeria monocytogenes moves rapidly through the host-cell cytoplasm by inducing directional actin assembly. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6068–6072. doi: 10.1073/pnas.87.16.6068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dogterom M., Yurke B. Measurement of the force-velocity relation for growing microtubules. Science. 1997 Oct 31;278(5339):856–860. doi: 10.1126/science.278.5339.856. [DOI] [PubMed] [Google Scholar]
  9. Evans E. New physical concepts for cell amoeboid motion. Biophys J. 1993 Apr;64(4):1306–1322. doi: 10.1016/S0006-3495(93)81497-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Evans E., Yeung A. Apparent viscosity and cortical tension of blood granulocytes determined by micropipet aspiration. Biophys J. 1989 Jul;56(1):151–160. doi: 10.1016/S0006-3495(89)82660-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gerbal F., Laurent V., Ott A., Carlier M. F., Chaikin P., Prost J. Measurement of the elasticity of the actin tail of Listeria monocytogenes. Eur Biophys J. 2000;29(2):134–140. doi: 10.1007/s002490050258. [DOI] [PubMed] [Google Scholar]
  12. Goldberg M. B., Theriot J. A., Sansonetti P. J. Regulation of surface presentation of IcsA, a Shigella protein essential to intracellular movement and spread, is growth phase dependent. Infect Immun. 1994 Dec;62(12):5664–5668. doi: 10.1128/iai.62.12.5664-5668.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Goldberg M. B., Theriot J. A. Shigella flexneri surface protein IcsA is sufficient to direct actin-based motility. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6572–6576. doi: 10.1073/pnas.92.14.6572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Heidemann S. R., Buxbaum R. E. Cell crawling: first the motor, now the transmission. J Cell Biol. 1998 Apr 6;141(1):1–4. doi: 10.1083/jcb.141.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kocks C., Gouin E., Tabouret M., Berche P., Ohayon H., Cossart P. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell. 1992 Feb 7;68(3):521–531. doi: 10.1016/0092-8674(92)90188-i. [DOI] [PubMed] [Google Scholar]
  16. Kocks C., Hellio R., Gounon P., Ohayon H., Cossart P. Polarized distribution of Listeria monocytogenes surface protein ActA at the site of directional actin assembly. J Cell Sci. 1993 Jul;105(Pt 3):699–710. doi: 10.1242/jcs.105.3.699. [DOI] [PubMed] [Google Scholar]
  17. Lasa I., David V., Gouin E., Marchand J. B., Cossart P. The amino-terminal part of ActA is critical for the actin-based motility of Listeria monocytogenes; the central proline-rich region acts as a stimulator. Mol Microbiol. 1995 Nov;18(3):425–436. doi: 10.1111/j.1365-2958.1995.mmi_18030425.x. [DOI] [PubMed] [Google Scholar]
  18. Lasa I., Gouin E., Goethals M., Vancompernolle K., David V., Vandekerckhove J., Cossart P. Identification of two regions in the N-terminal domain of ActA involved in the actin comet tail formation by Listeria monocytogenes. EMBO J. 1997 Apr 1;16(7):1531–1540. doi: 10.1093/emboj/16.7.1531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Loisel T. P., Boujemaa R., Pantaloni D., Carlier M. F. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature. 1999 Oct 7;401(6753):613–616. doi: 10.1038/44183. [DOI] [PubMed] [Google Scholar]
  20. Marchand J. B., Moreau P., Paoletti A., Cossart P., Carlier M. F., Pantaloni D. Actin-based movement of Listeria monocytogenes: actin assembly results from the local maintenance of uncapped filament barbed ends at the bacterium surface. J Cell Biol. 1995 Jul;130(2):331–343. doi: 10.1083/jcb.130.2.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Merrifield C. J., Moss S. E., Ballestrem C., Imhof B. A., Giese G., Wunderlich I., Almers W. Endocytic vesicles move at the tips of actin tails in cultured mast cells. Nat Cell Biol. 1999 May;1(1):72–74. doi: 10.1038/9048. [DOI] [PubMed] [Google Scholar]
  22. Mitchison T. J., Cramer L. P. Actin-based cell motility and cell locomotion. Cell. 1996 Feb 9;84(3):371–379. doi: 10.1016/s0092-8674(00)81281-7. [DOI] [PubMed] [Google Scholar]
  23. Mogilner A., Oster G. Cell motility driven by actin polymerization. Biophys J. 1996 Dec;71(6):3030–3045. doi: 10.1016/S0006-3495(96)79496-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mounier J., Ryter A., Coquis-Rondon M., Sansonetti P. J. Intracellular and cell-to-cell spread of Listeria monocytogenes involves interaction with F-actin in the enterocytelike cell line Caco-2. Infect Immun. 1990 Apr;58(4):1048–1058. doi: 10.1128/iai.58.4.1048-1058.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Noireaux V., Golsteyn R. M., Friederich E., Prost J., Antony C., Louvard D., Sykes C. Growing an actin gel on spherical surfaces. Biophys J. 2000 Mar;78(3):1643–1654. doi: 10.1016/S0006-3495(00)76716-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sechi A. S., Wehland J., Small J. V. 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. 1997 Apr 7;137(1):155–167. doi: 10.1083/jcb.137.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Smith G. A., Portnoy D. A., Theriot J. A. Asymmetric distribution of the Listeria monocytogenes ActA protein is required and sufficient to direct actin-based motility. Mol Microbiol. 1995 Sep;17(5):945–951. doi: 10.1111/j.1365-2958.1995.mmi_17050945.x. [DOI] [PubMed] [Google Scholar]
  28. Southwick F. S., Purich D. L. Listeria and Shigella actin-based motility in host cells. Trans Am Clin Climatol Assoc. 1998;109:160–173. [PMC free article] [PubMed] [Google Scholar]
  29. Theriot J. A., Mitchison T. J., Tilney L. G., Portnoy D. A. The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization. Nature. 1992 May 21;357(6375):257–260. doi: 10.1038/357257a0. [DOI] [PubMed] [Google Scholar]
  30. Tilney L. G., Portnoy D. A. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol. 1989 Oct;109(4 Pt 1):1597–1608. doi: 10.1083/jcb.109.4.1597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wang Y. L. Exchange of actin subunits at the leading edge of living fibroblasts: possible role of treadmilling. J Cell Biol. 1985 Aug;101(2):597–602. doi: 10.1083/jcb.101.2.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Welch M. D., Iwamatsu A., Mitchison T. J. Actin polymerization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes. Nature. 1997 Jan 16;385(6613):265–269. doi: 10.1038/385265a0. [DOI] [PubMed] [Google Scholar]
  33. Welch M. D., Rosenblatt J., Skoble J., Portnoy D. A., Mitchison T. J. Interaction of human Arp2/3 complex and the Listeria monocytogenes ActA protein in actin filament nucleation. Science. 1998 Jul 3;281(5373):105–108. doi: 10.1126/science.281.5373.105. [DOI] [PubMed] [Google Scholar]
  34. Zhukarev V., Ashton F., Sanger J. M., Sanger J. W., Shuman H. Organization and structure of actin filament bundles in Listeria-infected cells. Cell Motil Cytoskeleton. 1995;30(3):229–246. doi: 10.1002/cm.970300307. [DOI] [PubMed] [Google Scholar]

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