Actin filaments are major dynamic components of the cytoskeleton of eukaryotic cells. Assembly of filaments from monomeric actin occurs with expenditure of energy, the tightly bound ATP being irreversibly hydrolyzed during polymerization. This dissipation of energy perturbs the laws of reversible helical polymerization defined by Oosawa and Asakura (1975), and affects the dynamics of actin filaments. We have shown that ATP hydrolysis destabilizes actin-actin interactions in the filament. The destabilization is linked to the liberation of Pi that follows cleavage of gamma-phosphate. Pi release therefore plays the role of a conformational switch. Because ATP hydrolysis is uncoupled from polymerization, the nucleotide content of the filaments changes during the polymerization process, and filaments grow with a stabilizing "cap" of terminal ADP-Pi subunits. The fact that the dynamic properties of F-actin are affected by ATP hydrolysis results in a non-linear dependence of the rate of filament elongation on monomer concentration. Possible modes of regulation of filament assembly may be anticipated from the basic properties of actin. We have shown that the tightly bound divalent metal ion (Ca2+ or Mg2+) interacts with the beta- and gamma-phosphates of ATP bound to actin, and that the Me-ATP bidentate chelate is bound to G-actin in the A configuration. The nature of the bound metal ion affects the conformation of actin and the rate of ATP hydrolysis. In motile living cells, a large pool of actin is maintained unpolymerized by interaction with G-actin binding proteins such as thymosin beta 4 and its variants or profilin. Part of this pool is released to increase the F-actin pool upon cell stimulation. The role of G-actin polymerizing proteins may be crucial in defining the patterns of filament assembly in these situations. The myosin head (myosin subfragment-1) may be considered as a model actin polymerizing protein, may be the closest model to the short tailed myosin I family. The mechanism of assembly of decorated filaments from G-actin and myosin subfragment-1 has therefore been examined.