Advances in Cytokinesis Research. On the Mechanism of Cleavage Furrow Ingression in Dictyostelium.

Abstract

ABSTRACT. The ability of Dictyostelium cells to divide without myosin II in a cell cycle-coupled manner has opened two questions about the mechanism of cleavage furrow ingression. First, are there other possible functions for myosin II in this process except for generating contraction of the furrow by a sliding filament mechanism? Second, what could be an alternative mechanical basis for the furrowing? Using aberrant changes of the cell shape and anomalous localization of the actin-binding protein cortexillin I during asymmetric cytokinesis in myosin IIdeficient cells as clues, it is proposed that myosin II filaments act as a mechanical lens in cytokinesis. The mechanical lens serves to focus the forces that induce the furrowing to the center of the midzone, a cortical region where cortexillins are enriched in dividing cells. Additionally, continual disassembly of a filamentous actin meshwork at the midzone is a prerequisite for normal ingression of the cleavage furrow and a successful cytokinesis. If this process is interrupted, as it occurs in cells that lack cortexillins, an overassembly of filamentous actin at the midzone obstructs the normal cleavage. Disassembly of the crosslinked actin network can generate entropic contractile forces in the cortex, and may be considered as an alternative mechanism for driving ingression of the cleavage furrow. Instead of invoking different types of cytokinesis that operate under attached and unattached conditions in Dictyostelium, it is anticipated that these cells use a universal multifaceted mechanism to divide, which is only moderately sensitive to elimination of its constituent mechanical processes.Key words: cytokinesis/cell division/mechanical lens/actin disassembly/bending stiffness/cortexillin Since the discovery of myosin II-independent mitotic cell division in Dictyostelium discoideum (Neujahr et al., 1997a), several attempts have been undertaken to clarify its mechanism and relate it to the classical model of cytokinesis, which is based on the concept of contractile ring Uyeda et al., 2000). Basic assumption in these propositions is that cytokinesis in wild-type Dictyostelium cells is driven by contraction of a contractile ring, an annular structure that assembles at the central zone of a dividing cell and consists of actin and myosin II filaments. Thus, cells that express myosin II are assumed to divide primarily by the standard sliding-filament mechanism, and this mode of cell division was termed cytokinesis A. It was argued that myosin II-null cells use a different mechanism to divide by a process termed cytokinesis B, apparently not used by wild-type cells. In this view, cytokinesis B depends on expansion of the polar regions of a dividing cell, which induces a passive ingression at the cleavage furrow by drawing the cytoplasmic material out of the midzone (Uyeda et al., 2000). Traction forces between the ventral cell surface and a substratum are viewed as necessary in order to support the polar expansion. A sufficient magnitude of the traction forces and t...

Physics of Bacterial Morphogenesis

“…In Dictyostelium discoidium, cell division does not require myosin to actively generate forces. Instead, actin cross-linking proteins are recruited to generate contraction (145,168). Thus, similar mechanisms of force generation are at play during division in eukaryotic cells.…”

Cytoskeletal Cross-linking and Bundling in Motor-Independent Contraction

“…In two organisms, however, there is evidence that this is not the sole mechanism driving constriction of the division site. Dictyostelium discoideum cells that are adhered to a substrate can divide even when myosin is absent; cells in suspension, however, still require myosin in order to divide [22,23]. Interestingly, the actin-bundling protein cortexillin concentrates near the division furrow and facilitates contraction [24].…”