Ionic Wave Propagation along Actin Filaments
J. A. Tuszyn´ski,* S. Portet,* J. M. Dixon,* C. Luxford,* and H. F. Cantiello
*Department of Physics, University of Alberta, Edmonton, Alberta T6G 2J1, Canada; and
Massachusetts General Hospitaland Harvard Medical School, Charlestown, Massachusetts 02129 USA
ABSTRACT We investigate the conditions enabling actin ﬁlaments to act as electrical transmission lines for ion ﬂows alongtheir lengths. We propose a model in which each actin monomer is an electric element with a capacitive, inductive, and resistiveproperty due to the molecular structure of the actin ﬁlament and viscosity of the solution. Based on Kirchhoff’s laws taken in thecontinuum limit, a nonlinear partial differential equation is derived for the propagation of ionic waves. We solve this equation intwo different regimes. In the ﬁrst, the maximum propagation velocity wave is found in terms of Jacobi elliptic functions. In thegeneral case, we analyze the equation in terms of Fisher-Kolmogoroff modes with both localized and extended wavecharacteristics. We propose a new signaling mechanism in the cell, especially in neurons.
The cytoskeleton is a major component of all living cells. It is made up of three different types of ﬁlamental structures,including actin-based microﬁlaments (MFs), intermediateﬁlaments (e.g., neuroﬁlaments, keratin), and tubulin-basedmicrotubules (MTs). All of them are organized into net-works, which are interconnected through numerous partic-ular proteins, and which have speciﬁc roles to play in thefunctioning of the cell. The cytoskeletal networks are mainlyinvolved in the organization of different directed movementsin cell migration, cell division, or in the internal transport of materials. Polymerization of MFs is responsible for cellmigration and for the remodeling of the leading edge of cells.MTs attach to the chromosomes and mediate cell division.Molecular motors are protein complexes that are associatedwith the cytoskeleton and drive organelles along MTs andMFs in a ‘‘vectorial’’ transport.Actin is the most abundant protein in the cytoplasm of mammalian cells, accounting for 10–20% of the totalcytoplasmic protein content. Actin exists either as a globular monomer (Fig. 1), i.e., as the so-called G-actin, or asa ﬁlament, i.e., an MF: the globular monomers polymerizeinto polar two-stranded helical polymers, MFs, also calledF-actin. Under physiological conditions, actin ﬁlaments areone-dimensional polymers that behave as highly chargedpolyelectrolytes (Cantiello et al., 1991; Kobayasi, 1964;Kobayasi et al., 1964). The linear charge density of F-actin isestimated theoretically to be 4
m in vacuum, andalthough lower than that of DNA at physiological pH, it maysupport ionic condensation in buffer solutions as originallypredicted by Manning’s condensation theory (Manning,1978). This has recently been conﬁrmed experimentally bylight scattering (Tang and Janmey, 1996) although other experimental work arrives at linear charge densities that are much higher (Cantiello et al., 1991) of order 1.65
m. The latter value of charge density is consistent withother experiments and is associated with a highly uncom-pensated charge density of actin in solution. These experi-ments include the coexistence of different electric (Kobayasi,1964; Kobayasi et al., 1964) and magnetic (Torbet andDickens, 1984) dipole moments in F-actin, the anomalousDonnan potential, nonlinear electro-osmotic behavior of actin ﬁlaments in solution (Cantiello et al., 1991), and theability of F-actin to support ionic condensation-based waves(Lin and Cantiello, 1993).Many years ago, Manning (1978) postulated an elegant theory, which stated that polyelectrolytes may havecondensed ions in their surroundings. According to Mann-ing’s hypothesis, counterions ‘‘condense’’ along the stretchof polymer, if a sufﬁciently high linear charge density ispresent on the polymer’s surface. Thus, a linear polymer maybe surrounded by counterions from the saline solution suchthat counterions are more closely surrounding the polymer’ssurface, and co-ions of the salt solution are repelled such that a depletion area is also created. Some important details of theion distribution in polyelectrolytes regarding Manning’scondensation theory can be found in Le Bret and Zimm(1984). The sum of surface charges and associated counter-ions drops to values given by a formula that depends on thevalence of the counterions and the Bjerrum length. Thisparameter, in turn, is a phenomenological property of theion’s ability to compensate for the surface charges, depend-ing on the solvent and temperature of the solution. Bjerrumdeveloped a modiﬁcation of the Debye-Hu¨ckel theory in1926 for ion-pair formation provided that the ions are small,they are of high valence, and the dielectric constant of thesolvent is small (see MacInnes, 1961, for a comprehensiveexplanation of derivations of relevant equations). TheBjerrum length is the distance at which the Coulomb energyof the screened charges equals
, the thermal energy,creating an equilibrium under which the charges would not preferentially move from that equilibrium. See Eq. 1 below.
Submitted July 16, 2003, and accepted for publication November 14, 2003.
Address reprint requests to J. A. Tuszyn´ski, E-mail: email@example.com.J. M. Dixon’s permanent address is Dept. of Physics, University of Warwick, Coventry CV4 7AL, UK.
2004 by the Biophysical Society0006-3495/04/04/1890/14 $2.00
1890 Biophysical Journal Volume 86 April 2004 1890–1903