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J Cell Biol. Sep 2, 1993; 122(6): 1295–1300.
PMCID: PMC2119861

Synchrony of cell spreading and contraction force as phagocytes engulf large pathogens

Abstract

A simple micromechanical method has been used to directly measure the force of contraction in single mammalian phagocytes (blood granulocytes) during engulfment of large yeast pathogens. Both the time course of cell spreading over the yeast particle and increase in cell body contractile force were quantitated at three temperatures in the range of 23-35 degrees C. The surprising feature of the phagocyte response was that engulfment and cell body contraction occurred in a serial sequence: i.e., the phagocyte spread rapidly over the particle at a steady rate with no detectable cell body contraction; when spreading stopped, contraction force in the cell body then rose steadily to a plateau level that remained stationary until the next sequence of spreading and contraction. Both spreading and contraction exhibited abrupt start/stop kinetics. Also impressive, the cell contraction force stimulated by phagocytosis was quite large (approximately 10(-8) N)-two orders of magnitude larger than the force necessary to deform passive phagocytes to the same extent. If distributed uniformly over the cell cross section, the contraction force is equivalent to an average contractile stress of approximately 10(3) N/m2 (0.01 Atm). These physical measurements in situ set critical requirements for the mechanism of force generation in granulocytes, imply that a major increase in network cross-linking accompanies build- up in contractile force and that subsequent network dissolution is necessary for locomotion.

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Selected References

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  • Abercrombie M, Heaysman JE, Pegrum SM. The locomotion of fibroblasts in culture. I. Movements of the leading edge. Exp Cell Res. 1970 Mar;59(3):393–398. [PubMed]
  • Abercrombie M, Heaysman JE, Pegrum SM. The locomotion of fibroblasts in culture. II. "RRuffling". Exp Cell Res. 1970 Jun;60(3):437–444. [PubMed]
  • Abercrombie M, Heaysman JE, Pegrum SM. The locomotion of fibroblasts in culture. 3. Movements of particles on the dorsal surface of the leading lamella. Exp Cell Res. 1970 Oct;62(2):389–398. [PubMed]
  • Chen WT. Induction of spreading during fibroblast movement. J Cell Biol. 1979 Jun;81(3):684–691. [PMC free article] [PubMed]
  • Evans E. Kinetics of granulocyte phagocytosis: rate limited by cytoplasmic viscosity and constrained by cell size. Cell Motil Cytoskeleton. 1989;14(4):544–551. [PubMed]
  • Evans E. New physical concepts for cell amoeboid motion. Biophys J. 1993 Apr;64(4):1306–1322. [PMC free article] [PubMed]
  • Evans E, Yeung A. Apparent viscosity and cortical tension of blood granulocytes determined by micropipet aspiration. Biophys J. 1989 Jul;56(1):151–160. [PMC free article] [PubMed]
  • Harris AK, Wild P, Stopak D. Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science. 1980 Apr 11;208(4440):177–179. [PubMed]
  • HUXLEY AF. Muscle structure and theories of contraction. Prog Biophys Biophys Chem. 1957;7:255–318. [PubMed]
  • Ishijima A, Doi T, Sakurada K, Yanagida T. Sub-piconewton force fluctuations of actomyosin in vitro. Nature. 1991 Jul 25;352(6333):301–306. [PubMed]
  • Janson LW, Kolega J, Taylor DL. Modulation of contraction by gelation/solation in a reconstituted motile model. J Cell Biol. 1991 Sep;114(5):1005–1015. [PMC free article] [PubMed]
  • Kishino A, Yanagida T. Force measurements by micromanipulation of a single actin filament by glass needles. Nature. 1988 Jul 7;334(6177):74–76. [PubMed]
  • Kron SJ, Spudich JA. Fluorescent actin filaments move on myosin fixed to a glass surface. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6272–6276. [PMC free article] [PubMed]
  • Lee J, Gustafsson M, Magnusson KE, Jacobson K. The direction of membrane lipid flow in locomoting polymorphonuclear leukocytes. Science. 1990 Mar 9;247(4947):1229–1233. [PubMed]
  • MacFarlane GD, Herzberg MC. Concurrent estimation of the kinetics of adhesion and ingestion of Staphylococcus aureus by human polymorphonuclear leukocytes (PMNs). J Immunol Methods. 1984 Jan 20;66(1):35–49. [PubMed]
  • Pollard TD, Cooper JA. Actin and actin-binding proteins. A critical evaluation of mechanisms and functions. Annu Rev Biochem. 1986;55:987–1035. [PubMed]
  • Rabinovitch M. The dissociation of the attachment and ingestion phases of phagocytosis by macrophages. Exp Cell Res. 1967 Apr;46(1):19–28. [PubMed]
  • Southwick FS, Stossel TP. Contractile proteins in leukocyte function. Semin Hematol. 1983 Oct;20(4):305–321. [PubMed]
  • Stendahl OI, Stossel TP. Actin-binding protein amplifies actomyosin contraction, and gelsolin confers calcium control on the direction of contraction. Biochem Biophys Res Commun. 1980 Jan 29;92(2):675–681. [PubMed]
  • Stossel TP. The structure of cortical cytoplasm. Philos Trans R Soc Lond B Biol Sci. 1982 Nov 4;299(1095):275–289. [PubMed]
  • Stossel TP, Hartwig JH, Yin HL, Stendahl O. The motor of amoeboid leucocytes. Biochem Soc Symp. 1980;45:51–63. [PubMed]
  • Taylor DL, Fechheimer M. Cytoplasmic structure and contractility: the solation--contraction coupling hypothesis. Philos Trans R Soc Lond B Biol Sci. 1982 Nov 4;299(1095):185–197. [PubMed]
  • Theriot JA, Mitchison TJ. Actin microfilament dynamics in locomoting cells. Nature. 1991 Jul 11;352(6331):126–131. [PubMed]

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