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.

Fig. 1.

Chemotaxis chamber.

Fig. 2.

Chemotaxis of amoebae toward a cAMP source. (A) Developing Ax2 cells were suspended in KK2 buffer containing 10% Ficoll and placed in a Ficoll gradient in the chamber. A needle loaded with 0.1 mM cAMP was placed in the chamber so that its tip was about 1.5 mm from the base of the chamber. Cell movement was followed in an inverted microscope using a 5× objective taking images in the plane of the needle tip every 20 s (Movie S1). The cells can be seen to move toward and to congregate around the tip. Times are indicated in minutes. (Scale bar, 0.1 mm.) (B) z-Stack taken at the end of the experiment shown in Fig. 2A. A series of images was taken from −300 μm to +300 μm in 15-μm steps (Movie S2); every fifth image is shown. The position below or above the needle tip is indicated. The cells crowd around the needle tip, showing that their motion is in three dimensions. (Scale bar, 0.2 mm.)

Fig. 3.

The shape of amoebae as they swim. An amoeba whose surface was labeled with cAR1-GFP chemotaxes toward the cAMP source (just above the top of the images). z-Stacks of images (from −9 μm to +9 μm in 3-μm steps) were collected every10 s, and the images were collapsed into a single plane. Shown is a series of consecutive images with the times indicated in seconds (taken from Movie S3). Because each image was collected over a period of about 3 s, images shown are not true instantaneous volume images. The cell changes shape surprisingly quickly; arrowheads indicate features that apparently can be traced from one image to the next. (Scale bar, 10 μm.)

Fig. 4.

Chemotaxis of neutrophils toward an FMLP source. Fresh neutrophils were suspended in RPMI medium containing 5% FCS, 10% Ficoll, and about 9% Histodenz (a small molecule that increases the medium density). This mixture was incorporated in a density gradient in the chamber, and the motion of the cells was observed as in Fig. 2A, using a 10× objective. Polymorphonuclear leukocytes migrate to the needle tip where they attach, forming a large blob. In a control experiment without FMLP in the needle, chemotaxis did not occur. A z-stack (taken as in Fig. 2B) indicated that the needle tip is far from the base of the chamber. Images were collected every 30 s for a total of 200 min (see Movie S4). Times are indicated in minutes. (Scale bar, 20 μm.)

Fig. 5.

Schemes for how cells might swim. (A) Rotating screw. (B) Flexible oar. This scheme covers a variety of complex movements involving any series of nonreciprocal shape changes. (C) Cross-section through a toroidal cell. (D) Circulating membrane through the cell’s interior. (A–C are taken from ref. ; D is adapted from ref. .)