Turnover and flow of the cell membrane for cell migration

Abstract

The role of cell membrane dynamics in cell migration is unclear. To examine whether total cell surface area changes are required for cell migration, Dictyostelium cells were flattened by agar-overlay. Scanning electron microscopy demonstrated that flattened migrating cells have no membrane reservoirs such as projections and membrane folds. Similarly, optical sectioning fluorescence microscopy showed that the cell surface area does not change during migration. Interestingly, staining of the cell membrane with a fluorescent lipid analogue demonstrated that the turnover rate of cell membrane is closely related to the cell migration velocity. Next, to clarify the mechanism of cell membrane circulation, local photobleaching was separately performed on the dorsal and ventral cell membranes of rapidly moving cells. The bleached zones on both sides moved rearward relative to the cell. Thus, the cell membrane moves in a fountain-like fashion, accompanied by a high membrane turnover rate and actively contributing to cell migration.

Apicomplexan motility depends on the operation of an endocytic-secretory cycle

“…Interestingly, in this study a direct relationship between cell migration and membrane turnover rate was observed, suggesting that the cells establish a fluid drive that contributes to the generation of force required for motility, as suggested previously (4). Importantly, it appears that myosin and actin have only a supporting function in the establishment of the fluid drive, since treatment with actin-or myosin-disrupting drugs, such as latrunculin B or blebbistatin, did not significantly affect membrane movement (10). In good agreement, retrograde membrane flow in apicomplexan parasites is not strictly dependent on parasite actin, as shown for Plasmodium sporozoites and Toxoplasma tachyzoites (7,11).…”

“…During motility, most eukaryotic cells show a capping activity of surface ligands, which is dependent on actin, microtubules, and a secretory-endocytic cycle, leading to the establishment of a retrograde membrane flow (4,9). A recent study on Dictyostelium provided direct evidences for the fluid flow model during cell migration (10). This study demonstrated that, during migration of Dictyostelium, the membrane volume of the cell remains constant due to the occurrence of a secretory-endocytic cycle.…”

“…It is well accepted that gliding motility of apicomplexans depends on the regulated secretion of the apically localised micronemes (12). While this dependency was previously contributed to the secretion of surface ligands, such as MIC2, that are required as force transmitters, it is also possible that polarised secretion is required for the generation of retrograde membrane flow, akin to the fountain flow model (10) and as previously suggested for T. gondii (7,13). However, to date it is not fully understood how apicomplexan parasites ensure a constant cell surface during motility by removing excess membrane deposited on the surface due to microneme secretion.…”

Apicomplexan F‐actin is required for efficient nuclear entry during host cell invasion

“…According to the Glideosome model, the force generated for motility and invasion relies exclusively on F‐actin polymerised at the apical tip of the parasite by the action of Formin‐1 and translocated within the narrow space (~30 nm) between the IMC and PM of the parasite . However, recent studies suggest that the parasite can also use other motility systems, such as a secretory‐endocytic cycle that produces retrograde membrane flow , similar to the fountain flow model suggested for other eukaryotes .…”

The dynamic interplay between ATP/ADP levels and autophagy sustain neuronal migrationin vivo

“…In the postnatal RMS, neuroblasts travel in chains ensheathed by astrocytic processes along blood vessels (Kaneko et al, 2010;Snapyan et al, 2009;Whitman et al, 2009). Cell migration is a very dynamic process composed of migratory phases intercalated with stationary periods and is accompanied by structural remodeling, organelles dynamic and protein trafficking and turnover (Tanaka et al, 2017;Webb et al, 2002). Cell migration also entails a considerable bioenergetic demand, and it is still unclear how migrating cells regulate cellular homeostasis by clearing damaged organelles and aggregated/misfolded proteins, and how the metabolic requirements of neuroblasts are dynamically regulated during the different phases of cell migration.…”