Intracellular pressure is a motive force for cell motion in Amoeba proteus
M. Yanai
Meakins-Christie Laboratories, McGill University Clinic and Royal Victoria Hospital, Montreal, Quebec, Canada
Search for more papers by this authorC.M. Kenyon
Meakins-Christie Laboratories, McGill University Clinic and Royal Victoria Hospital, Montreal, Quebec, Canada
Search for more papers by this authorJ.P. Butler
Physiology Program, Harvard School of Public Health, Boston, Massachusetts
Search for more papers by this authorP.T. Macklem
Meakins-Christie Laboratories, McGill University Clinic and Royal Victoria Hospital, Montreal, Quebec, Canada
Search for more papers by this authorCorresponding Author
S.M. Kelly
Physiology Program, Harvard School of Public Health, Boston, Massachusetts
Physiology Program, Harvard School of Public Health, 665 Huntington Ave., Boston, MA 02115Search for more papers by this authorM. Yanai
Meakins-Christie Laboratories, McGill University Clinic and Royal Victoria Hospital, Montreal, Quebec, Canada
Search for more papers by this authorC.M. Kenyon
Meakins-Christie Laboratories, McGill University Clinic and Royal Victoria Hospital, Montreal, Quebec, Canada
Search for more papers by this authorJ.P. Butler
Physiology Program, Harvard School of Public Health, Boston, Massachusetts
Search for more papers by this authorP.T. Macklem
Meakins-Christie Laboratories, McGill University Clinic and Royal Victoria Hospital, Montreal, Quebec, Canada
Search for more papers by this authorCorresponding Author
S.M. Kelly
Physiology Program, Harvard School of Public Health, Boston, Massachusetts
Physiology Program, Harvard School of Public Health, 665 Huntington Ave., Boston, MA 02115Search for more papers by this authorAbstract
The cortical filament layer of free-living amoebae contains concentrated actomyosin, suggesting that it can contract and produce an internal hydrostatic pressure. We report here on direct and dynamic intracellular pressure (Pic) measurements in Amoeba proteus made using the servo-null technique. In resting apolar A. proteus, Pic increased while the cells remained immobile and at apparently constant volume. Pic then decreased approximately coincident with pseudopod formation. There was a positive correlation between Pic at the onset of movement and the rate of pseudopod formation. These results are the first direct evidence that hydrostatic pressure may be a motive force for cell motion. We postulate that contractile elements in the amoeba's cortical layer contract and increase Pic and that this Pic is utilized to overcome the viscous flow resistance of the intracellular contents during pseudopod formation. © 1996 Wiley-Liss, Inc.
References
- Bhattacharya, J., and Staub, N. C. (1980): Direct measurement of microvascular pressures in the isolated perfused dog lung. Science 210: 327–328.
- Bizal, C. L., Butler, J. P., and Valberg, P. A. (1991): Viscoelastic and motile properties of hamaster lung and peritoneal macrophages. J. Leukoc. Biol. 50: 240–251.
- Bray, D., and White, J. G. (1988): Cortical flow in animal cells. Science 239: 883–888.
- Chalkley, H. W. (1929): Changes in water content in amoeba in relation to changes in its protoplasmic structure. Physiol. Zool. 2: 535–574.
- Condeelis, J., Bresnick, A., Demma, M., Dharmawardhane, S., Eddy, R., Hall, A. L., Sauterer, R., and Warren, V. (1990): Mechanisms of amoeboid chemotaxis: An evaluation of the cortical expansion model. Dev. Gen. 11: 333–340.
- Dembo, M. (1989): Mechanics and control of the cytoskeleton in Amoeba proteus. Biophys. J. 55: 1053–1080.
- Fein, H. (1972): Microdimensional pressure measurements in elecrolytes. J. Appl. Physiol. 32: 560–564.
- Fox, J. R., and Wiederhielm, C. A. (1973): Characteristics of the servo-controlled micropipette pressure system. Microvasc. Res. 5: 324–335.
- Gollinick, F., Meyer, R., and Stockem, W. (1991): Visualization and measurement of calcium transients in Amoeba proteus by fura-2 fluorescence. Eur. J. Cell Biol. 55: 262–271.
- Grebecka, L. (1980): Reversal of motory polarity of Amoeba proteus by suction. Protoplasma 102: 361–375.
- Grebecka, L., and Grebecki, A. (1981): Testing motor functions of the frontal zone in the locomotion of Amoeba proteus. Cell Biol. Int. Reports 5: 587–594.
- Hiramoto, Y. (1963): Mechanical properties of sea urchin eggs. I. Surface force and elastic modulus of the cell membrane. Exp. Cell Res. 32: 59–75.
- Hiramoto, Y. (1986): Determination of the mechanical properties of the egg surface by elastimetry. Methods Cell Biol. 27: 435–442.
- Hoffmann-Berling, H. (1956): Das kontraktile eiweiss undifferenzierter zellen. Biochim. Biophys. Acta 19: 453–463.
- Janson, L. W., and Taylor, D. L. (1993): In vitro models of tail contraction and cytoplasmic streaming in amoeboid cells. J. Cell Biol. 123: 345–356.
- Jeon, K. W., and Jeon, M. S. (1976): Scanning electron microscope observations of Amoeba proteus during phagocytosis. J. Protozool. 23: 83–86.
- Kelly, S. M., and Macklem, P. T. (1991): Direct measurement of intracellular pressure. Am. J. Physiol. 260: C652–657.
- Kenyon, C. M., Yanai, M., and Macklem, P. T. (1994): Edge detection, three-dimensional cell boundary reconstruction and volume and surface area estimation from differential interference contrast images. J. Microsc. 176: 152–157.
- Lee, J., Ishihara, A., Theriot, J. A., and Jacobson, K. (1993): Principles of locomotion for simple-shaped cells. Nature 362: 167–171.
- Lorch, I. J., and Danielli, J. F. (1953): Nuclear transplantation in amoebae. I. Some species characteristics of Amoeba proteus and Amoeba discoides. Quart. J. Microsc. Sci. 94: 445–460.
- Mast, S. O. (1926): Structure, movement, locomotion, and stimulation in amoeba. J. Morphol. Physiol. 41: 347–425.
-
Mast, S. O.
(1931):
Locomotion in Amoeba proteus (Leidy).
Protoplasma
14:
321–330.
10.1007/BF01604911 Google Scholar
- Murray, J., Vawter-Hugart, H., Voss, E., and Soll, D. R. (1992): Three-dimensional motility cycle in leukocytes. Cell Motil. Cytoskeleton 22: 211–223.
- Needham, D., and Hochmuth, R. M. (1990): Rapid flow of passive neutrophils into a 4 micron pipet and measurement of cytoplasmic viscosity. J. Biomech. Engin. 112: 269–276.
- Rand, R. P., and Burton, A. C. (1964): Mechanical properties of the red cell membrane. I. Membrane stiffness and intracellular pressure. Biophys. J. 4: 115–135.
- Rinaldi, R., Opas, M., and Hrebenda, B. (1975): Contractility of glycerinated Amoeba proteus and Chaos-chaos. J. Protozool. 22: 286–292.
- Stockem, W., Hoffmann, H.-U., and Gawlitta, W. (1982): Spatial organization and fine structure of the cortical filament layer in normal locomoting Amoeba proteus. Cell Tissue Res. 221: 505–519.
- Stockem, W., Naib-Majani, W., Wohlfarth-Bottermann, K.-E., Osborn, M., and Weber, K. (1983): Pinocytosis and locomotion of amoebae. XIX. Immunocytochemical demonstration of actin and myosin in Amoeba proteus. Eur. J. Cell Biol. 29: 171–178.
- Taylor, D. L., and Fechheimer, M. (1982): Cytoplasmic structure and contractility: The solation-contraction coupling hypothesis. Philos. Trans. R. Soc. Lond. Biol. 299: 185–197.
- Taylor, D. L., Hellewell, S. B., Virgin, H. W., and Heiple, J. (1979): The solation-contraction hypothesis of cell movements. In S. Hatano, I. Ishikawa, H. Sato (eds.): Cell Motility: Molecules and Organization Tokyo: University of Tokyo Press, pp. 363–377.
- Taylor, D. L., Wang, Y.-L., and Heiple, J. M. (1980a): Contractile basis of amoeboid movement VII. The distrubution of fluorescently labelled actin in living amoebas. J. Cell Biol. 86: 590–599.
- Taylor, D. L., Blinks, J. R., and Reynolds, G. (1980b): Contractile basis of amoeboid movement VIII. Aequorin luminescence during amoeboid movement, endocytosis and capping. J. Cell Biol. 86: 599–607.
- Theriot, J. A., and Mitchison, T. J. (1991): Actin microfilament dynamics in locomoting cells. Nature 352: 126–131.
- Valberg, P., and Butler, J. P. (1987): Magnetic particle motions within living cells: Physical theory and techniques. Biophys. J. 52: 537–550.
- Wang, N., and Ingber, D. L. (1994): Control of cytoskeletal mechanics by extracellular matrix, cell shape, and mechanical tension. Biophys. J. 66: 2181–2189.
- Watts, R. G., Crispens, M. A., and Howard, T. H. (1991): A quantitative study of the role of F-actin in producing neutrophil shape. Cell Motil. Cytoskeleton 19: 159–168.
- Yoneda, M. (1980): Tension at the highly stretched surface of seaurchin eggs. Development 22: 39–47.
- Zhu, C., and Skalak, R. (1988): A continuum model of protrusion of pseudopods in leukocytes. Biophys. J. 54: 1115–1137.