Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2008 May 15;94(10):3810-23.
doi: 10.1529/biophysj.107.120980. Epub 2008 Jan 28.

Depolymerization-driven flow in nematode spermatozoa relates crawling speed to size and shape

Mark Zajac  1 , Brian Dacanay, William A Mohler, Charles W Wolgemuth
Affiliations

Depolymerization-driven flow in nematode spermatozoa relates crawling speed to size and shape

Mark Zajac et al. Biophys J. .

Abstract

Cell crawling is an inherently physical process that includes protrusion of the leading edge, adhesion to the substrate, and advance of the trailing cell body. Research into advance of the cell body has focused on actomyosin contraction, with cytoskeletal disassembly regarded as incidental, rather than causative; however, extracts from nematode spermatozoa, which use Major Sperm Protein rather than actin, provide at least one example where cytoskeletal disassembly apparently generates force in the absence of molecular motors. To test whether depolymerization can explain force production during nematode sperm crawling, we constructed a mathematical model that simultaneously describes the dynamics of both the cytoskeleton and the cytosol. We also performed corresponding experiments using motile Caenorhabditis elegans spermatozoa. Our experiments reveal that crawling speed is an increasing function of both cell size and anterior-posterior elongation. The quantitative, depolymerization-driven model robustly predicts that cell speed should increase with cell size and yields a cytoskeletal disassembly rate that is consistent with previous measurements. Notably, the model requires anisotropic elasticity, with the cell being stiffer along the direction of motion, to accurately reproduce the dependence of speed on elongation. Our simulations also predict that speed should increase with cytoskeletal anisotropy and disassembly rate.

PubMed Disclaimer

Figures

FIGURE 1
FIGURE 1
Side-view schematic of a crawling nematode sperm. Polymerization at the leading edge pushes the front of the cell forward. Spatially varying adhesion anchors the cell to the substrate and provides traction. Depolymerization of the cytoskeleton produces contractile force which pulls the cell body forward. Pseudocolor roughly represents polymer volume fraction.
FIGURE 2
FIGURE 2
(A) Surface striations are visible in a DIC image of a crawling C. elegans spermatozoon, suggesting ridges and furrows of unequal cytoskeletal density, inside the cell. Pointers show the beginning, middle and end of one ridge. (B) In a time series of images, taken at 3-min intervals, a cultured MSP fiber complex grows shorter and fainter simultaneously. The column becomes increasingly faint as loss of MSP decreases the optical density. Axial shrinkage exceeds radial shrinkage, suggesting anisotropic cytoskeletal stress. Fiber complex images (B) from Miao et al. (21). (Reprinted with permission from the American Association for the Advancement of Science.)
FIGURE 3
FIGURE 3
(A) Surface ridges on C. elegans spermatozoa resemble corresponding features of A. suum in which a sparse network of MSP filaments connects dense fiber complexes. Anterior-posterior compression (B) then meets resistance from high density ridges, which act as stiff springs, while transverse compression (C) can simply move the ridges closer together by distorting low-density intervening material, in regions which act as pliable springs, with a greater effective spring constant for stiff and pliable springs in parallel, compared to stiff and pliable springs in series.
FIGURE 4
FIGURE 4
A typical C. elegans spermatozoon advances nearly 3 μm in 5 s (A and B), with little change in shape. The cell has a domed body at the rear (C) and a laminar foot, at the front. Given an empirically determined shape, simulations predict the peripheral cytoskeletal assembly rate (C) for a steadily crawling cell, with a maximum of 0.4 μm/s at the leading edge. Simulations represent transmembrane adhesion as external drag (D), with strong adhesion at the front and weak adhesion under the cell body. Relative to the assembly rate, arrows for fluid flux (E), cytosolic velocity (G) and cytoskeletal velocity (I) are scaled by factors of 500, 5, and 1, respectively. For ease of comparison with preexisting empirical data, transmembrane fluid flow and cytosolic velocity are plotted in a frame that moves with the cell while cytoskeletal velocity is plotted in a fixed laboratory reference frame. Simulations also yield cytosolic gauge pressure (F) and the magnitude of cytoskeletal stress (H), determined from anterior-posterior and transverse components.
FIGURE 5
FIGURE 5
Trackable features of a crawling spermatozoon manifest as surface mottling in a DIC image (above). Feature tracking gives an average speed near 0.4 μm/s for the cell body (below). Velocities for the anterior cytoskeleton are markedly lower and, from observation, slightly retrograde. Near the edge of the cell, tracking detects the stationary background, resulting in spuriously low values at some peripheral pixels.
FIGURE 6
FIGURE 6
Speed versus size (B) and shape (C). Simulations employ real cell shapes with a range of elongations (shapes A, corresponding points B). (B and C) Scattered data points show the experimental results. Working in dimensionless variables allows scaling of each shape to cover the full range of areas. Simultaneous regression shows that crawling speed depends on both cell elongation and the square root of cell area (R2 = 0.57). Compared to the best fit (black lines, B and C), results for simulations with anisotropy (white lines, R2 = 0.52) fall within one standard deviation (gray shading). The fit for simulations without anisotropy (dashed lines) is not as good (R2 = 0.25). All coefficients of determination are statistically significant (p < 0.001)
FIGURE 7
FIGURE 7
Fitting simulation results to experimental data yields an increased coefficient of determination (R2) as cytoskeletal anisotropy increases. Simulations with greater intracellular drag (ζ0) require less anisotropy to achieve the same degree of agreement with experiments.
FIGURE 8
FIGURE 8
Simulations allow independent manipulation of cytoskeletal anisotropy and disassembly, with cell size and all other parameters held fixed. With disassembly fixed, crawling speed increases rapidly with anisotropy (A). With fixed anisotropy, crawling speed increases with increasingly rapid cytoskeletal disassembly (B).
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Huttenlocher, A., R. R. Sandborg, and A. F. Horwitz. 1995. Adhesion in cell-migration. Curr. Opin. Cell Biol. 7:697–706. - PubMed
    1. Lauffenburger, D., and A. F. Horwitz. 1996. Cell migration: a physically integrated molecular process. Cell. 84:359–369. - PubMed
    1. Mitchison, T. J., and L. P. Cramer. 1996. Actin based cell motility and cell locomotion. Cell. 84:371–379. - PubMed
    1. Rafelski, S. M., and J. A. Theriot. 2004. Crawling toward a unified model of cell motility: spatial and temporal regulation of actin dynamics. Annu. Rev. Biochem. 73:209–239. - PubMed
    1. Rodriguez, O. C., A. W. Schaefer, C. A. Mandato, P. Forscher, W. M. Bement, and C. M. Waterman-Storer. 2003. Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 5:599–609. - PubMed

Publication types

LinkOut - more resources