Filament rigidity causes F-actin depletion from nonbinding surfaces

Charles I. Fisher, Scot C. Kuo

Research output: Contribution to journalArticle

Abstract

Proximity to membranes is required of actin networks for many key cell functions, including mechanics and motility. However, F-actin rigidity should hinder a filament's approach to surfaces. Using confocal microscopy, we monitor the distribution of fluorescent actin near nonadherent glass surfaces. Initially uniform, monomers polymerize to create a depletion zone where F-actin is absent at the surface but increases monotonically with distance from the surface. At its largest, depletion effects can extend >35 μm, comparable with the average, mass-weighted filament length. Increasing the rigidity of actin filaments with phalloidin increases the extent of depletion, whereas shortening filaments by using capping protein reduces it proportionally. In addition, depletion kinetics are faster with higher actin concentrations, consistent with faster polymerization and faster Brownian-ratchet-driven motion. Conversely, the extent of depletion decreases with actin concentration, suggesting that entropy is the thermodynamic driving force. Quantitatively, depletion kinetics and extent match existing actin kinetics, rigidity, and lengths. However, explaining depletion profiles and concentration dependence (power-law of -1) requires modifying the rigid rod model. Within cells, surface depletion should slow membrane-associated F-actin reactions another ≈10-fold beyond hydrodynamically slowed diffusion of filaments (≈10-fold). In addition, surface depletion should cause membranes to bend spontaneously toward filaments. Such depletion principles underlie the thermodynamics of all surface-associated reactions with mechanical structures, ranging from DNA to filaments to networks. For various functions, cells must actively resist the thermodynamics of depletion.

Original languageEnglish (US)
Pages (from-to)133-138
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume106
Issue number1
DOIs
StatePublished - Jan 6 2009

Keywords

  • Confocal microscopy
  • Cytoskeleton
  • Fluorescence
  • Polymer depletion
  • Polymer physics

ASJC Scopus subject areas

  • General

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