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Proc Natl Acad Sci U S A. 2005 Jun 14;102(24):8543-8. Epub 2005 Jun 6.

Actin polymerization kinetics, cap structure, and fluctuations.

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Department of Chemical Engineering, Columbia University, New York, NY 10027, USA.


Polymerization of actin proteins into dynamic structures is essential to eukaryotic cell life, motivating many in vitro experiments measuring polymerization kinetics of individual filaments. Here, we model these kinetics, accounting for all relevant steps revealed by experiment: polymerization, depolymerization, random ATP hydrolysis, and release of phosphate (P(i)). We relate filament growth rates to the dynamics of ATP-actin and ADP-P(i)-actin caps that develop at filament ends. At the critical concentration of the barbed end, c(crit), we find a short ATP cap and a long fluctuation-stabilized ADP-P(i) cap. We show that growth rates and the critical concentration at the barbed end are intimately related to cap structure and dynamics. Fluctuations in filament lengths are described by the length diffusion coefficient, D. Recently Fujiwara et al. [Fujiwara, I., Takahashi, S., Takaduma, H., Funatsu, T. & Ishiwata, S. (2002) Nat. Cell Biol. 4, 666-673] and Kuhn and Pollard [Kuhn, J. & Pollard, T. D. (2005) Biophys. J. 88, 1387-1402] observed large length fluctuations slightly above c(crit), provoking speculation that growth may proceed by oligomeric rather than monomeric on-off events. For the single-monomer growth process, we find that D exhibits a pronounced peak below c(crit), due to filaments alternating between capped and uncapped states, a mild version of the dynamic instability of microtubules. Fluctuations just above c(crit) are enhanced but much smaller than those reported experimentally. Future measurements of D as a function of concentration can help identify the origin of the observed fluctuations.

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