Choosing orientation

Influence of cargo geometry and ActA polarization on actin comet tails

Catherine I. Lacayo, Paula A G Soneral, Jie Zhu, Mark A. Tsuchida, Matthew J. Footer, Frederick S. Soo, Yu Lu, Younan Xia, Alexander Mogilner, Julie A. Theriot

Research output: Contribution to journalArticle

Abstract

Networks of polymerizing actin filaments can propel intracellular pathogens and drive movement of artificial particles in reconstituted systems. While biochemical mechanisms activating actin network assembly have been well characterized, it remains unclear how particle geometry and large-scale force balance affect emergent properties of movement. We reconstituted actin-based motility using ellipsoidal beads resembling the geometry of Listeria monocytogenes. Beads coated uniformly with the L. monocytogenes ActA protein migrated equally well in either of two distinct orientations, with their long axes parallel or perpendicular to the direction of motion, while intermediate orientations were unstable. When beads were coated with a fluid lipid bilayer rendering ActA laterally mobile, beads predominantly migrated with their long axes parallel to the direction of motion, mimicking the orientation of motile L. monocytogenes. Generating an accurate biophysical model to account for our observations required the combination of elastic-propulsion and tethered-ratchet actin-polymerization theories. Our results indicate that the characteristic orientation of L. monocytogenes must be due to polarized ActA rather than intrinsic actin network forces. Furthermore, viscoelastic stresses, forces, and torques produced by individual actin filaments and lateral movement of molecular complexes must all be incorporated to correctly predict large-scale behavior in the actin-based movement of nonspherical particles.

Original languageEnglish (US)
Pages (from-to)614-629
Number of pages16
JournalMolecular Biology of the Cell
Volume23
Issue number4
DOIs
StatePublished - Feb 15 2012

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Actins
Listeria monocytogenes
Actin Cytoskeleton
Torque
Lipid Bilayers
Polymerization
Direction compound

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

Cite this

Lacayo, C. I., Soneral, P. A. G., Zhu, J., Tsuchida, M. A., Footer, M. J., Soo, F. S., ... Theriot, J. A. (2012). Choosing orientation: Influence of cargo geometry and ActA polarization on actin comet tails. Molecular Biology of the Cell, 23(4), 614-629. https://doi.org/10.1091/mbc.E11-06-0584

Choosing orientation : Influence of cargo geometry and ActA polarization on actin comet tails. / Lacayo, Catherine I.; Soneral, Paula A G; Zhu, Jie; Tsuchida, Mark A.; Footer, Matthew J.; Soo, Frederick S.; Lu, Yu; Xia, Younan; Mogilner, Alexander; Theriot, Julie A.

In: Molecular Biology of the Cell, Vol. 23, No. 4, 15.02.2012, p. 614-629.

Research output: Contribution to journalArticle

Lacayo, CI, Soneral, PAG, Zhu, J, Tsuchida, MA, Footer, MJ, Soo, FS, Lu, Y, Xia, Y, Mogilner, A & Theriot, JA 2012, 'Choosing orientation: Influence of cargo geometry and ActA polarization on actin comet tails', Molecular Biology of the Cell, vol. 23, no. 4, pp. 614-629. https://doi.org/10.1091/mbc.E11-06-0584
Lacayo, Catherine I. ; Soneral, Paula A G ; Zhu, Jie ; Tsuchida, Mark A. ; Footer, Matthew J. ; Soo, Frederick S. ; Lu, Yu ; Xia, Younan ; Mogilner, Alexander ; Theriot, Julie A. / Choosing orientation : Influence of cargo geometry and ActA polarization on actin comet tails. In: Molecular Biology of the Cell. 2012 ; Vol. 23, No. 4. pp. 614-629.
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