Literature DB >> 17485664

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

V B Shenoy1, D T Tambe, A Prasad, J A Theriot.   

Abstract

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 large-amplitude 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.

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Year:  2007        PMID: 17485664      PMCID: PMC1895934          DOI: 10.1073/pnas.0702454104

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  23 in total

Review 1.  Secrets of actin-based motility revealed by a bacterial pathogen.

Authors:  L A Cameron; P A Giardini; F S Soo; J A Theriot
Journal:  Nat Rev Mol Cell Biol       Date:  2000-11       Impact factor: 94.444

Review 2.  Actin-based motility of intracellular microbial pathogens.

Authors:  M B Goldberg
Journal:  Microbiol Mol Biol Rev       Date:  2001-12       Impact factor: 11.056

3.  Growth of branched actin networks against obstacles.

Authors:  A E Carlsson
Journal:  Biophys J       Date:  2001-10       Impact factor: 4.033

4.  Curved tails in polymerization-based bacterial motility.

Authors:  A D Rutenberg; M Grant
Journal:  Phys Rev E Stat Nonlin Soft Matter Phys       Date:  2001-07-19

Review 5.  Mechanism of actin-based motility.

Authors:  D Pantaloni; C Le Clainche; M F Carlier
Journal:  Science       Date:  2001-05-25       Impact factor: 47.728

6.  Force generation by actin polymerization II: the elastic ratchet and tethered filaments.

Authors:  Alex Mogilner; George Oster
Journal:  Biophys J       Date:  2003-03       Impact factor: 4.033

7.  Ultrastructure of Rickettsia rickettsii actin tails and localization of cytoskeletal proteins.

Authors:  L S Van Kirk; S F Hayes; R A Heinzen
Journal:  Infect Immun       Date:  2000-08       Impact factor: 3.441

8.  The force-velocity relationship for the actin-based motility of Listeria monocytogenes.

Authors:  James L McGrath; Narat J Eungdamrong; Charles I Fisher; Fay Peng; Lakshminarayanan Mahadevan; Timothy J Mitchison; Scot C Kuo
Journal:  Curr Biol       Date:  2003-02-18       Impact factor: 10.834

9.  VASP governs actin dynamics by modulating filament anchoring.

Authors:  Léa Trichet; Otger Campàs; Cécile Sykes; Julie Plastino
Journal:  Biophys J       Date:  2006-11-10       Impact factor: 4.033

10.  A biomimetic motility assay provides insight into the mechanism of actin-based motility.

Authors:  Sebastian Wiesner; Emmanuele Helfer; Dominique Didry; Guylaine Ducouret; Françoise Lafuma; Marie-France Carlier; Dominique Pantaloni
Journal:  J Cell Biol       Date:  2003-01-27       Impact factor: 10.539

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  17 in total

1.  A microscopic formulation for the actin-driven motion of listeria in curved paths.

Authors:  Yuan Lin; V B Shenoy; Bin Hu; Limiao Bai
Journal:  Biophys J       Date:  2010-08-09       Impact factor: 4.033

2.  Observation and kinematic description of long actin tracks induced by spherical beads.

Authors:  Hyeran Kang; David S Perlmutter; Vivek B Shenoy; Jay X Tang
Journal:  Biophys J       Date:  2010-11-03       Impact factor: 4.033

3.  Stathmin recruits tubulin to Listeria monocytogenes-induced actin comets and promotes bacterial dissemination.

Authors:  Ana Catarina Costa; Filipe Carvalho; Didier Cabanes; Sandra Sousa
Journal:  Cell Mol Life Sci       Date:  2018-12-01       Impact factor: 9.261

4.  Curvature and torsion in growing actin networks.

Authors:  Joshua W Shaevitz; Daniel A Fletcher
Journal:  Phys Biol       Date:  2008-06-16       Impact factor: 2.583

5.  Non-Gaussian curvature distribution of actin-propelled biomimetic colloid trajectories.

Authors:  Stephan Schmidt; Jasper van der Gucht; P Maarten Biesheuvel; Richard Weinkamer; Emmanuèle Helfer; Andreas Fery
Journal:  Eur Biophys J       Date:  2008-05-20       Impact factor: 1.733

Review 6.  Mathematics of cell motility: have we got its number?

Authors:  Alex Mogilner
Journal:  J Math Biol       Date:  2008-05-07       Impact factor: 2.259

7.  A circle swimmer at low Reynolds number.

Authors:  R Ledesma-Aguilar; H Löwen; J M Yeomans
Journal:  Eur Phys J E Soft Matter       Date:  2012-08-08       Impact factor: 1.890

8.  A novel pseudopodial component of the dendritic cell anti-fungal response: the fungipod.

Authors:  Aaron K Neumann; Ken Jacobson
Journal:  PLoS Pathog       Date:  2010-02-12       Impact factor: 6.823

9.  Mechanistic insights from a quantitative analysis of pollen tube guidance.

Authors:  Shannon F Stewman; Matthew Jones-Rhoades; Prabhakar Bhimalapuram; Martin Tchernookov; Daphne Preuss; Aaron R Dinner
Journal:  BMC Plant Biol       Date:  2010-02-22       Impact factor: 4.215

10.  Helical twist controls the thickness of F-actin bundles.

Authors:  M M A E Claessens; C Semmrich; L Ramos; A R Bausch
Journal:  Proc Natl Acad Sci U S A       Date:  2008-06-25       Impact factor: 11.205

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