Dictyostelium amoebae and neutrophils can swim

Abstract

Animal cells migrating over a substratum crawl in amoeboid fashion; how the force against the substratum is achieved remains uncertain. We find that amoebae and neutrophils, cells traditionally used to study cell migration on a solid surface, move toward a chemotactic source while suspended in solution. They can swim and do so with speeds similar to those on a solid substrate. Based on the surprisingly rapidly changing shape of amoebae as they swim and earlier theoretical schemes for how suspended microorganisms can migrate (Purcell EM (1977) Life at low Reynolds number. Am J Phys 45:3-11), we suggest the general features these cells use to gain traction with the medium. This motion requires either the movement of the cell's surface from the cell's front toward its rear or protrusions that move down the length of the elongated cell. Our results indicate that a solid substratum is not a prerequisite for these cells to produce a forward thrust during movement and suggest that crawling and swimming are similar processes, a comparison we think is helpful in understanding how cells migrate.cell migration | cell swimming | chemotaxis T he leading front of an animal cell migrating over a substratum is differentiated from the rest of the cell by several properties believed to be linked to how the cells migrate (1, 2). It is the main site of actin filament formation (3) whose polymerizing force may impinge on the membrane at the front of the cell to force it forward and so advance the cell's front (4-7). It is also the site of exocytosis of recycling membrane from the cell's internal pools (8) whose area could provide the surface membrane required for the cell to extend itself forward (9). Whatever the actual process, as a cell moves up a chemotactic gradient the information which the cell's surface receptors collect to steer the cell toward the source must determine which part of the cell's surface constitutes the front and must activate a motor there to extend the cell toward the source.Cell migration and chemotaxis generally are studied as the cells crawl over various solid substrates. The possibility that amoebae might swim arises from the observation that a mutant of Dictyostelium discoideum, sadA, which attaches poorly to a substrate, appears nevertheless to migrate normally and does so with an enhanced speed. The product of this gene is a plasma membrane protein which, when expressed in sadA, restores normal attachment and behavior (10). However, the extent to which the sadA strain is able to form transient attachments to a substratum is unclear. We therefore sought to discover whether Dictyostelium amoebae require a substrate upon which to move or whether they can swim. ResultsTo find whether cells might move in the absence of a substrate, we tried to find whether amoebae could migrate at a liquid-liquid interface or an air-water interface. With Christien Merrifield (of this laboratory), we found that these cells indeed can move at both interfaces, as had many others (e.g., ref. 11). However, the difficulty in in...

Motile invaded neutrophils in the small intestine ofToxoplasma gondii-infected mice reveal a potential mechanism for parasite spread

“…5 E and F and Movie S4). These data are in line with previous reports that neutrophils can migrate through mucus and also can "swim" in solution (35)(36)(37). Together these findings confirm that parasite-containing neutrophils can traverse the intestinal epithelium and migrate through the lumen of the intestine, supporting a role for neutrophils in the spread of infection to neighboring or distant villi via the intestinal lumen.…”

Progress and perspectives in signal transduction, actin dynamics, and movement at the cell and tissue level: lessons fromDictyostelium

“…This has led to the suggestion that Dd has three modes of movement-walking, gliding and swimming [64]. In the swimming mode, the cell body is elongated and small protrusions that provide the momentum transfer needed for motion are propagated from front to rear [63,64]. Experimental observations on the movement of Dd cells reported in [63] and [64] have included cell-shape changes, speeds and periods of the cyclic motion.…”

“…Experimental observations on the movement of Dd cells reported in [63] and [64] have included cell-shape changes, speeds and periods of the cyclic motion. Van Haastert [64] reported an average of three protrusions, as illustrated by the cartoon model in figure 8a, while from the experimental images (figure 8b) of a swimming Dictyostelium reported in Barry et al [63], one sees that one protrusion travels along Figure 7. (a) A schematic of a suggested model for actin wave formation.…”

The filamins

“…Although certain cells can migrate without integrins or swim without attaching to a substrate, 84,85 most cells migrate in an integrin-dependent manner. Our current understanding of integrin function at focal adhesions in moving cells is summarized in Figure 4.…”