Myosin I is located at the leading edges of locomoting Dictyostelium amoebae

Abstract

Movement of a eukaryotic cell along a substrate occurs by extension of lamellipodia and pseudopodia at the anterior and retraction at the posterior of the cell. The molecular and structural mechanisms of these movements are uncertain. Dictyostelium discoideum contains two forms of myosin. Here we show by immunofluorescence microscopy that non-filamentous myosin I occurs at the leading edges of the lamellipodial projections of migrating Dictyostelium amoebae, which are devoid of myosin II, whereas filamentous myosin II is concentrated in the posterior of the cells. On the basis of these locations of the two forms of myosin and their known biochemical and biophysical properties, we suggest that actomyosin I may contribute to the forces that cause extension at the leading edge of a motile cell, while the contraction of actomyosin II at the rear squeezes the cell mass forward. Myosin I isozymes might have similar roles in metazoan cells, for example at the leading edges of neuronal growth cones, and in the extension of lamellipodia and pseudopodia of leukocytes, macrophages and fibroblasts.

Molecular Mechanisms of Membrane Trafficking. What do we Learn from Dictyostelium discoideum?

“…It was proposed that class I myosins are important for localised actin polymerisation that cause deformation of the plasma membrane and generation of projections preceding the formation of macropinosomes/ phagosomes (Ostap and Pollard 1996). Myosins of the class I have been localised to membrane ruffles and phagocytic cups in D. discoideum (Fukui et al 1989;Morita et al 1996), Entamoeba histolytica (Voigt et al 1999), Acanthamoeba castellanii (Baines et al 1992;Baines et al 1995;Jontes et al 1998) and macrophages (Allen and Aderem 1995;Swanson et al 1999). D. discoideum cells lacking either myosin IB, IC or IK exhibit significant reduction of the initial rate of particle uptake [Jung et al 1996; Schwarz EC, Neuhaus EM, Kistler C, and Soldati T: Dictyostelium MyoK, a novel type of myosin with crucial functions in motility and maintenance of cortical integrity (submitted)], and double deletion mutants (myoA-/myoB-, myoC-/myoB-) show conditional defects in fluid-phase pinocytosis (Jung et al 1996;Novak et al 1995).…”

The distribution of myosin II in Dictyostelium discoideum slug cells.

“…In an amoeba undergoing directed locomotion, myosin II is localized to the posterior cortex, and myosin I is localized to the leading edge (Yumura et al ., 1984;Rubino et al ., 1984;Fukui et al, 1989) . On the other hand, actin is localized to both the posterior and anterior of cells .…”

Mammalian myosin I alpha, I beta, and I gamma: new widely expressed genes of the myosin I family.

“…For example, in Dictyostelium, myosin I was localized to the leading edge of motile cells and to the phagocytic cup upon ingestion of bacteria (Fukui et al, 1989). Similarly, in Acanthamoeba, myosin IC was found both at the plasma membrane and the contractile vacuole (Baines and , and in chick intestinal microvilli, BBMI forms the crossbridge between the actin bundle core and the plasma membrane (Mooseker and Tilney, 1975).…”