Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 2001 Dec;81(6):3166–3177. doi: 10.1016/S0006-3495(01)75953-X

Aspiration of human neutrophils: effects of shear thinning and cortical dissipation.

J L Drury 1, M Dembo 1
PMCID: PMC1301777  PMID: 11720983

Abstract

It is generally accepted that the human neutrophil can be mechanically represented as a droplet of polymeric fluid enclosed by some sort of thin slippery viscoelastic cortex. Many questions remain however about the detailed rheology and chemistry of the interior fluid and the cortex. To address these quantitative issues, we have used a finite element method to simulate the dynamics of neutrophils during micropipet aspiration using various plausible assumptions. The results were then systematically compared with aspiration experiments conducted at eight different combinations of pipet size and pressure. Models in which the cytoplasm was represented by a simple Newtonian fluid (i.e., models without shear thinning) were grossly incapable of accounting for the effects of pressure on the general time scale of neutrophil aspiration. Likewise, models in which the cortex was purely elastic (i.e., models without surface viscosity) were unable to explain the effects of pipet size on the general aspiration rate. Such models also failed to explain the rapid acceleration of the aspiration rate during the final phase of aspiration nor could they account for the geometry of the neutrophil during various phases of aspiration. Thus, our results indicate that a minimal mechanical model of the neutrophil needs to incorporate both shear thinning and surface viscosity to remain valid over a reasonable range of conditions. At low shear rates, the surface dilatation viscosity of the neutrophil was found to be on the order of 100 poise-cm, whereas the viscosity of the interior cytoplasm was on the order of 1000 poise. Both the surface viscosity and the interior viscosity seem to decrease in a similar fashion when the shear rate exceeds approximately 0.05 s(-1). Unfortunately, even models with both surface viscosity and shear thinning studied are still not sufficient to fully explain all the features of neutrophil aspiration. In particular, the very high rate of aspiration during the initial moments after ramping of pressure remains mysterious.

Full Text

The Full Text of this article is available as a PDF (290.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Buxbaum R. E., Dennerll T., Weiss S., Heidemann S. R. F-actin and microtubule suspensions as indeterminate fluids. Science. 1987 Mar 20;235(4795):1511–1514. doi: 10.1126/science.2881354. [DOI] [PubMed] [Google Scholar]
  2. Cano M. L., Lauffenburger D. A., Zigmond S. H. Kinetic analysis of F-actin depolymerization in polymorphonuclear leukocyte lysates indicates that chemoattractant stimulation increases actin filament number without altering the filament length distribution. J Cell Biol. 1991 Nov;115(3):677–687. doi: 10.1083/jcb.115.3.677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dong C., Skalak R. Leukocyte deformability: finite element modeling of large viscoelastic deformation. J Theor Biol. 1992 Sep 21;158(2):173–193. doi: 10.1016/s0022-5193(05)80716-7. [DOI] [PubMed] [Google Scholar]
  4. Dong C., Skalak R., Sung K. L. Cytoplasmic rheology of passive neutrophils. Biorheology. 1991;28(6):557–567. doi: 10.3233/bir-1991-28607. [DOI] [PubMed] [Google Scholar]
  5. Dong C., Skalak R., Sung K. L., Schmid-Schönbein G. W., Chien S. Passive deformation analysis of human leukocytes. J Biomech Eng. 1988 Feb;110(1):27–36. doi: 10.1115/1.3108402. [DOI] [PubMed] [Google Scholar]
  6. Drury J. L., Dembo M. Hydrodynamics of micropipette aspiration. Biophys J. 1999 Jan;76(1 Pt 1):110–128. doi: 10.1016/S0006-3495(99)77183-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Evans E., Kukan B. Passive material behavior of granulocytes based on large deformation and recovery after deformation tests. Blood. 1984 Nov;64(5):1028–1035. [PubMed] [Google Scholar]
  8. Evans E., Yeung A. Apparent viscosity and cortical tension of blood granulocytes determined by micropipet aspiration. Biophys J. 1989 Jul;56(1):151–160. doi: 10.1016/S0006-3495(89)82660-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. He X., Dembo M. On the mechanics of the first cleavage division of the sea urchin egg. Exp Cell Res. 1997 Jun 15;233(2):252–273. doi: 10.1006/excr.1997.3585. [DOI] [PubMed] [Google Scholar]
  10. Hochmuth R. M., Needham D. The viscosity of neutrophils and their transit times through small pores. Biorheology. 1990;27(6):817–828. doi: 10.3233/bir-1990-27603. [DOI] [PubMed] [Google Scholar]
  11. Hochmuth R. M., Ting-Beall H. P., Beaty B. B., Needham D., Tran-Son-Tay R. Viscosity of passive human neutrophils undergoing small deformations. Biophys J. 1993 May;64(5):1596–1601. doi: 10.1016/S0006-3495(93)81530-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hoffman R., Gross L. The modulation contrast microscope. Nature. 1975 Apr 17;254(5501):586–588. doi: 10.1038/254586a0. [DOI] [PubMed] [Google Scholar]
  13. Janmey P. A. Mechanical properties of cytoskeletal polymers. Curr Opin Cell Biol. 1991 Feb;3(1):4–11. doi: 10.1016/0955-0674(91)90159-v. [DOI] [PubMed] [Google Scholar]
  14. Lipowsky H. H., Riedel D., Shi G. S. In vivo mechanical properties of leukocytes during adhesion to venular endothelium. Biorheology. 1991;28(1-2):53–64. doi: 10.3233/bir-1991-281-206. [DOI] [PubMed] [Google Scholar]
  15. Needham D., Hochmuth R. M. A sensitive measure of surface stress in the resting neutrophil. Biophys J. 1992 Jun;61(6):1664–1670. doi: 10.1016/S0006-3495(92)81970-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Needham D., Hochmuth R. M. Rapid flow of passive neutrophils into a 4 microns pipet and measurement of cytoplasmic viscosity. J Biomech Eng. 1990 Aug;112(3):269–276. doi: 10.1115/1.2891184. [DOI] [PubMed] [Google Scholar]
  17. Sato M., Schwartz W. H., Selden S. C., Pollard T. D. Mechanical properties of brain tubulin and microtubules. J Cell Biol. 1988 Apr;106(4):1205–1211. doi: 10.1083/jcb.106.4.1205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Schmid-Schönbein G. W., Shih Y. Y., Chien S. Morphometry of human leukocytes. Blood. 1980 Nov;56(5):866–875. [PubMed] [Google Scholar]
  19. Schmid-Schönbein G. W., Sung K. L., Tözeren H., Skalak R., Chien S. Passive mechanical properties of human leukocytes. Biophys J. 1981 Oct;36(1):243–256. doi: 10.1016/S0006-3495(81)84726-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Shao J. Y., Hochmuth R. M. The resistance to flow of individual human neutrophils in glass capillary tubes with diameters between 4.65 and 7.75 microns. Microcirculation. 1997 Mar;4(1):61–74. doi: 10.3109/10739689709148318. [DOI] [PubMed] [Google Scholar]
  21. Sung K. L., Dong C., Schmid-Schönbein G. W., Chien S., Skalak R. Leukocyte relaxation properties. Biophys J. 1988 Aug;54(2):331–336. doi: 10.1016/S0006-3495(88)82963-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ting-Beall H. P., Needham D., Hochmuth R. M. Volume and osmotic properties of human neutrophils. Blood. 1993 May 15;81(10):2774–2780. [PubMed] [Google Scholar]
  23. Tran-Son-Tay R., Needham D., Yeung A., Hochmuth R. M. Time-dependent recovery of passive neutrophils after large deformation. Biophys J. 1991 Oct;60(4):856–866. doi: 10.1016/S0006-3495(91)82119-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Tsai M. A., Frank R. S., Waugh R. E. Passive mechanical behavior of human neutrophils: power-law fluid. Biophys J. 1993 Nov;65(5):2078–2088. doi: 10.1016/S0006-3495(93)81238-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Xu J., Schwarz W. H., Käs J. A., Stossel T. P., Janmey P. A., Pollard T. D. Mechanical properties of actin filament networks depend on preparation, polymerization conditions, and storage of actin monomers. Biophys J. 1998 May;74(5):2731–2740. doi: 10.1016/S0006-3495(98)77979-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Yeung A., Evans E. Cortical shell-liquid core model for passive flow of liquid-like spherical cells into micropipets. Biophys J. 1989 Jul;56(1):139–149. doi: 10.1016/S0006-3495(89)82659-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Zaner K. S., Stossel T. P. Some perspectives on the viscosity of actin filaments. J Cell Biol. 1982 Jun;93(3):987–991. doi: 10.1083/jcb.93.3.987. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES