The polyelectrolyte behavior of actin filaments: A Mg-25 NMR study

Under physiological conditions, filamentous actin (F-actin) is a polyanioni c protein filament. Key features of the behavior of F-actin are shared with other well-characterized polyelectrolytes, in particular, duplex DNA. For example, the bundle formation of F-actin by polyvalent cations, including d ivalent metal ions such as Mg2+, has been proposed to be a natural conseque nce of the polyelectrolyte nature of actin filaments [Tang and Janmey (1996 ) J. Biol. Chem. 271, 8556-8563]. This recently proposed model also suggest s that weak interactions between F-actin and Mg2+ ions reflect a nonspecifi c trapping of counterions in the electric field surrounding F-actin due to its polyelectrolyte nature. To test this hypothesis, we have performed Mg-2 5 NMR measurements in F-actin solutions. Based on the NMR data, we estimate that the rotational correlation times of Mg2+ are independent of the overa ll rotational dynamics of the actin filaments. Moreover, competitive bindin g experiments demonstrate a facile displacement of F-actin-bound Mg2+ by Co (NH3)(6)(3+). At higher Co(NH3)(6)(3+) concentrations, a fraction of the ma gnesium ions are trapped as actin filaments aggregate. ATP also competes ef fectively with actin filaments for binding to Mg2+. These results support t he hypothesis that magnesium ions bind loosely and nonspecifically to actin filaments, and thus show a behavior typical of counterions in polyelectrol yte solutions. The observed features mimic to some extent the well-document ed behavior of counterions in DNA solutions.