Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1998 Sep;75(3):1541–1552. doi: 10.1016/S0006-3495(98)74073-1

Cell transit analysis of ligand-induced stiffening of polymorphonuclear leukocytes.

R Nossal 1
PMCID: PMC1299829  PMID: 9726956

Abstract

A mathematical treatment of the mechanical behavior of transiently bonded polymer networks is used to interpret measurements of the pressure-induced passage of plant cells through microporous membranes. Cell transit times are inferred to be proportional to the instantaneous shear modulus of the cell cortex, a parameters that we then relate to properties of the cortical F-actin matrix. These theoretical results are used to analyze published data on chemoattractant-induced changes of rigidity of polymorphonuclear leukocytes. We thereby rationalize previously noted, peculiar, power-law logarithmic dependences of transit time on ligand concentration. As a consequence, we are able to deduce a linear relationship between the extent of F-actin polymerization and the logarithm of the chemoattractant concentration. The latter is examined with regard to the G-protein activation that is known to occur when chemoattractants bind to receptors on the surfaces of polymorphonuclear cells.

Full Text

The Full Text of this article is available as a PDF (127.3 KB).

Selected References

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

  1. Bray D., Heath J., Moss D. The membrane-associated 'cortex' of animal cells: its structure and mechanical properties. J Cell Sci Suppl. 1986;4:71–88. doi: 10.1242/jcs.1986.supplement_4.5. [DOI] [PubMed] [Google Scholar]
  2. Carlier M. F., Laurent V., Santolini J., Melki R., Didry D., Xia G. X., Hong Y., Chua N. H., Pantaloni D. Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J Cell Biol. 1997 Mar 24;136(6):1307–1322. doi: 10.1083/jcb.136.6.1307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Coates T. D., Watts R. G., Hartman R., Howard T. H. Relationship of F-actin distribution to development of polar shape in human polymorphonuclear neutrophils. J Cell Biol. 1992 May;117(4):765–774. doi: 10.1083/jcb.117.4.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. Fechheimer M., Zigmond S. H. Focusing on unpolymerized actin. J Cell Biol. 1993 Oct;123(1):1–5. doi: 10.1083/jcb.123.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Frank R. S. Time-dependent alterations in the deformability of human neutrophils in response to chemotactic activation. Blood. 1990 Dec 15;76(12):2606–2612. [PubMed] [Google Scholar]
  8. Frank R. S., Tsai M. A. The behavior of human neutrophils during flow through capillary pores. J Biomech Eng. 1990 Aug;112(3):277–282. doi: 10.1115/1.2891185. [DOI] [PubMed] [Google Scholar]
  9. Howard T. H., Oresajo C. O. A method for quantifying F-actin in chemotactic peptide activated neutrophils: study of the effect of tBOC peptide. Cell Motil. 1985;5(6):545–557. doi: 10.1002/cm.970050609. [DOI] [PubMed] [Google Scholar]
  10. Howard T. H., Oresajo C. O. The kinetics of chemotactic peptide-induced change in F-actin content, F-actin distribution, and the shape of neutrophils. J Cell Biol. 1985 Sep;101(3):1078–1085. doi: 10.1083/jcb.101.3.1078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Janmey P. A., Hvidt S., Lamb J., Stossel T. P. Resemblance of actin-binding protein/actin gels to covalently crosslinked networks. Nature. 1990 May 3;345(6270):89–92. doi: 10.1038/345089a0. [DOI] [PubMed] [Google Scholar]
  12. Koutsouris D., Guillet R., Wenby R. B., Meiselman H. J. Determination of erythrocyte transit times through micropores. II. Influence of experimental and physicochemical factors. Biorheology. 1989;26(5):881–898. [PubMed] [Google Scholar]
  13. MacKintosh FC, Käs J, Janmey PA. Elasticity of semiflexible biopolymer networks. Phys Rev Lett. 1995 Dec 11;75(24):4425–4428. doi: 10.1103/PhysRevLett.75.4425. [DOI] [PubMed] [Google Scholar]
  14. Machesky L. M., Goldschmidt-Clermont P. J., Pollard T. D. The affinities of human platelet and Acanthamoeba profilin isoforms for polyphosphoinositides account for their relative abilities to inhibit phospholipase C. Cell Regul. 1990 Nov;1(12):937–950. doi: 10.1091/mbc.1.12.937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Machesky L. M., Poland T. D. Profilin as a potential mediator of membrane-cytoskeleton communication. Trends Cell Biol. 1993 Nov;3(11):381–385. doi: 10.1016/0962-8924(93)90087-h. [DOI] [PubMed] [Google Scholar]
  16. Mahama P. A., Linderman J. J. A Monte Carlo study of the dynamics of G-protein activation. Biophys J. 1994 Sep;67(3):1345–1357. doi: 10.1016/S0006-3495(94)80606-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mahama P. A., Linderman J. J. Monte Carlo simulations of membrane signal transduction events: effect of receptor blockers on G-protein activation. Ann Biomed Eng. 1995 May-Jun;23(3):299–307. doi: 10.1007/BF02584430. [DOI] [PubMed] [Google Scholar]
  18. Nachmias V. T. Small actin-binding proteins: the beta-thymosin family. Curr Opin Cell Biol. 1993 Feb;5(1):56–62. doi: 10.1016/s0955-0674(05)80008-0. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Nossal R. On the elasticity of cytoskeletal networks. Biophys J. 1988 Mar;53(3):349–359. doi: 10.1016/S0006-3495(88)83112-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Omann G. M., Allen R. A., Bokoch G. M., Painter R. G., Traynor A. E., Sklar L. A. Signal transduction and cytoskeletal activation in the neutrophil. Physiol Rev. 1987 Jan;67(1):285–322. doi: 10.1152/physrev.1987.67.1.285. [DOI] [PubMed] [Google Scholar]
  22. Pantaloni D., Carlier M. F. How profilin promotes actin filament assembly in the presence of thymosin beta 4. Cell. 1993 Dec 3;75(5):1007–1014. doi: 10.1016/0092-8674(93)90544-z. [DOI] [PubMed] [Google Scholar]
  23. Pécsvárady Z., Fisher T. C., Fabók A., Coates T. D., Meiselman H. J. Kinetics of granulocyte deformability following exposure to chemotactic stimuli. Blood Cells. 1992;18(2):333–358. [PubMed] [Google Scholar]
  24. Richardson R. M., Haribabu B., Ali H., Snyderman R. Cross-desensitization among receptors for platelet activating factor and peptide chemoattractants. Evidence for independent regulatory pathways. J Biol Chem. 1996 Nov 8;271(45):28717–28724. doi: 10.1074/jbc.271.45.28717. [DOI] [PubMed] [Google Scholar]
  25. Sato M., Schwarz W. H., Pollard T. D. Dependence of the mechanical properties of actin/alpha-actinin gels on deformation rate. 1987 Feb 26-Mar 4Nature. 325(6107):828–830. doi: 10.1038/325828a0. [DOI] [PubMed] [Google Scholar]
  26. Shea L., Linderman J. J. Mechanistic model of G-protein signal transduction. Determinants of efficacy and effect of precoupled receptors. Biochem Pharmacol. 1997 Feb 21;53(4):519–530. doi: 10.1016/s0006-2952(96)00768-x. [DOI] [PubMed] [Google Scholar]
  27. Sklar L. A., Omann G. M., Painter R. G. Relationship of actin polymerization and depolymerization to light scattering in human neutrophils: dependence on receptor occupancy and intracellular Ca++. J Cell Biol. 1985 Sep;101(3):1161–1166. doi: 10.1083/jcb.101.3.1161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Theriot J. A. Regulation of the actin cytoskeleton in living cells. Semin Cell Biol. 1994 Jun;5(3):193–199. doi: 10.1006/scel.1994.1024. [DOI] [PubMed] [Google Scholar]
  29. Tsai M. A., Frank R. S., Waugh R. E. Passive mechanical behavior of human neutrophils: effect of cytochalasin B. Biophys J. 1994 Jun;66(6):2166–2172. doi: 10.1016/S0006-3495(94)81012-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Wallace P. J., Wersto R. P., Packman C. H., Lichtman M. A. Chemotactic peptide-induced changes in neutrophil actin conformation. J Cell Biol. 1984 Sep;99(3):1060–1065. doi: 10.1083/jcb.99.3.1060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Watts R. G., Crispens M. A., Howard T. H. A quantitative study of the role of F-actin in producing neutrophil shape. Cell Motil Cytoskeleton. 1991;19(3):159–168. doi: 10.1002/cm.970190304. [DOI] [PubMed] [Google Scholar]
  33. Worthen G. S., Schwab B., 3rd, Elson E. L., Downey G. P. Mechanics of stimulated neutrophils: cell stiffening induces retention in capillaries. Science. 1989 Jul 14;245(4914):183–186. doi: 10.1126/science.2749255. [DOI] [PubMed] [Google Scholar]
  34. Wymann M. P., Kernen P., Bengtsson T., Andersson T., Baggiolini M., Deranleau D. A. Corresponding oscillations in neutrophil shape and filamentous actin content. J Biol Chem. 1990 Jan 15;265(2):619–622. [PubMed] [Google Scholar]
  35. Wymann M. P., Kernen P., Deranleau D. A., Baggiolini M. Respiratory burst oscillations in human neutrophils and their correlation with fluctuations in apparent cell shape. J Biol Chem. 1989 Sep 25;264(27):15829–15834. [PubMed] [Google Scholar]
  36. 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]
  37. Zhelev D. V., Needham D., Hochmuth R. M. Role of the membrane cortex in neutrophil deformation in small pipets. Biophys J. 1994 Aug;67(2):696–705. doi: 10.1016/S0006-3495(94)80529-6. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES