Abstract
Using Dictyostelium discoideum as a model organism of specific and nonspecific adhesion, we studied the kinetics of shear flow-induced cell detachment. For a given cell, detachment occurs for values of the applied hydrodynamic stress above a threshold. Cells are removed from the substrate with an apparent first-order rate constant that strongly depends on the applied stress. The threshold stress depends on cell size and physicochemical properties of the substrate, but is not affected by depolymerization of the actin and tubulin cytoskeleton. In contrast, the kinetics of cell detachment is almost independent of cell size, but is strongly affected by a modification of the substrate and the presence of an intact actin cytoskeleton. These results are interpreted in the framework of a peeling model. The threshold stress and the cell-detachment rate measure the local equilibrium energy and the dissociation rate constant of the adhesion bridges, respectively.
Full Text
The Full Text of this article is available as a PDF (471.7 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Albelda S. M., Buck C. A. Integrins and other cell adhesion molecules. FASEB J. 1990 Aug;4(11):2868–2880. [PubMed] [Google Scholar]
- Ashworth J. M., Watts D. J. Metabolism of the cellular slime mould Dictyostelium discoideum grown in axenic culture. Biochem J. 1970 Sep;119(2):175–182. doi: 10.1042/bj1190175. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baumgartner W., Hinterdorfer P., Ness W., Raab A., Vestweber D., Schindler H., Drenckhahn D. Cadherin interaction probed by atomic force microscopy. Proc Natl Acad Sci U S A. 2000 Apr 11;97(8):4005–4010. doi: 10.1073/pnas.070052697. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bell G. I. Models for the specific adhesion of cells to cells. Science. 1978 May 12;200(4342):618–627. doi: 10.1126/science.347575. [DOI] [PubMed] [Google Scholar]
- Bozzaro S., Ponte E. Cell adhesion in the life cycle of Dictyostelium. Experientia. 1995 Dec 18;51(12):1175–1188. doi: 10.1007/BF01944735. [DOI] [PubMed] [Google Scholar]
- Carl P., Kwok C. H., Manderson G., Speicher D. W., Discher D. E. Forced unfolding modulated by disulfide bonds in the Ig domains of a cell adhesion molecule. Proc Natl Acad Sci U S A. 2001 Jan 30;98(4):1565–1570. doi: 10.1073/pnas.031409698. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chan P. Y., Lawrence M. B., Dustin M. L., Ferguson L. M., Golan D. E., Springer T. A. Influence of receptor lateral mobility on adhesion strengthening between membranes containing LFA-3 and CD2. J Cell Biol. 1991 Oct;115(1):245–255. doi: 10.1083/jcb.115.1.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chia C. P. A 130-kDa plasma membrane glycoprotein involved in Dictyostelium phagocytosis. Exp Cell Res. 1996 Sep 15;227(2):182–189. doi: 10.1006/excr.1996.0265. [DOI] [PubMed] [Google Scholar]
- Cornillon S., Pech E., Benghezal M., Ravanel K., Gaynor E., Letourneur F., Brückert F., Cosson P. Phg1p is a nine-transmembrane protein superfamily member involved in dictyostelium adhesion and phagocytosis. J Biol Chem. 2000 Nov 3;275(44):34287–34292. doi: 10.1074/jbc.M006725200. [DOI] [PubMed] [Google Scholar]
- Cozens-Roberts C., Quinn J. A., Lauffenberger D. A. Receptor-mediated adhesion phenomena. Model studies with the Radical-Flow Detachment Assay. Biophys J. 1990 Jul;58(1):107–125. doi: 10.1016/S0006-3495(90)82357-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cozens-Roberts C., Quinn J. A., Lauffenburger D. A. Receptor-mediated cell attachment and detachment kinetics. II. Experimental model studies with the radial-flow detachment assay. Biophys J. 1990 Oct;58(4):857–872. doi: 10.1016/S0006-3495(90)82431-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- De Lozanne A., Spudich J. A. Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science. 1987 May 29;236(4805):1086–1091. doi: 10.1126/science.3576222. [DOI] [PubMed] [Google Scholar]
- Dembo M., Torney D. C., Saxman K., Hammer D. The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proc R Soc Lond B Biol Sci. 1988 Jun 22;234(1274):55–83. doi: 10.1098/rspb.1988.0038. [DOI] [PubMed] [Google Scholar]
- DiMilla P. A., Barbee K., Lauffenburger D. A. Mathematical model for the effects of adhesion and mechanics on cell migration speed. Biophys J. 1991 Jul;60(1):15–37. doi: 10.1016/S0006-3495(91)82027-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DiMilla P. A., Stone J. A., Quinn J. A., Albelda S. M., Lauffenburger D. A. Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength. J Cell Biol. 1993 Aug;122(3):729–737. doi: 10.1083/jcb.122.3.729. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dunon D., Piali L., Imhof B. A. To stick or not to stick: the new leukocyte homing paradigm. Curr Opin Cell Biol. 1996 Oct;8(5):714–723. doi: 10.1016/s0955-0674(96)80114-1. [DOI] [PubMed] [Google Scholar]
- Evans E., Leung A. Adhesivity and rigidity of erythrocyte membrane in relation to wheat germ agglutinin binding. J Cell Biol. 1984 Apr;98(4):1201–1208. doi: 10.1083/jcb.98.4.1201. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hynes R. O. Integrins: a family of cell surface receptors. Cell. 1987 Feb 27;48(4):549–554. doi: 10.1016/0092-8674(87)90233-9. [DOI] [PubMed] [Google Scholar]
- Kamath K. R., Danilich M. J., Marchant R. E., Park K. Platelet interactions with plasma-polymerized ethylene oxide and N-vinyl-2-pyrrolidone films and linear poly(ethylene oxide) layer. J Biomater Sci Polym Ed. 1996;7(11):977–988. doi: 10.1163/156856296x00381. [DOI] [PubMed] [Google Scholar]
- Kay R. R., Williams J. G. The Dictyostelium genome project: an invitation to species hopping. Trends Genet. 1999 Aug;15(8):294–297. doi: 10.1016/s0168-9525(99)01770-9. [DOI] [PubMed] [Google Scholar]
- Manstein D. J., Schuster H. P., Morandini P., Hunt D. M. Cloning vectors for the production of proteins in Dictyostelium discoideum. Gene. 1995 Aug 30;162(1):129–134. doi: 10.1016/0378-1119(95)00351-6. [DOI] [PubMed] [Google Scholar]
- Morio T., Urushihara H., Saito T., Ugawa Y., Mizuno H., Yoshida M., Yoshino R., Mitra B. N., Pi M., Sato T. The Dictyostelium developmental cDNA project: generation and analysis of expressed sequence tags from the first-finger stage of development. DNA Res. 1998 Dec 31;5(6):335–340. doi: 10.1093/dnares/5.6.335. [DOI] [PubMed] [Google Scholar]
- Oliver J. M., Krawiec J. A., Berlin R. D. A carbamate herbicide causes microtubule and microfilament disruption and nuclear fragmentation in fibroblasts. Exp Cell Res. 1978 Oct 1;116(1):229–237. doi: 10.1016/0014-4827(78)90079-4. [DOI] [PubMed] [Google Scholar]
- Palecek S. P., Loftus J. C., Ginsberg M. H., Lauffenburger D. A., Horwitz A. F. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature. 1997 Feb 6;385(6616):537–540. doi: 10.1038/385537a0. [DOI] [PubMed] [Google Scholar]
- Pierres A., Benoliel A. M., Bongrand P. Measuring the lifetime of bonds made between surface-linked molecules. J Biol Chem. 1995 Nov 3;270(44):26586–26592. doi: 10.1074/jbc.270.44.26586. [DOI] [PubMed] [Google Scholar]
- Pierres A., Benoliel A. M., Bongrand P., van der Merwe P. A. Determination of the lifetime and force dependence of interactions of single bonds between surface-attached CD2 and CD48 adhesion molecules. Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15114–15118. doi: 10.1073/pnas.93.26.15114. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pierres A., Tissot O., Malissen B., Bongrand P. Dynamic adhesion of CD8-positive cells to antibody-coated surfaces: the initial step is independent of microfilaments and intracellular domains of cell-binding molecules. J Cell Biol. 1994 May;125(4):945–953. doi: 10.1083/jcb.125.4.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rees D. A., Lloyd C. W., Thom D. Control of grip and stick in cell adhesion through lateral relationships of membrane glycoproteins. Nature. 1977 May 12;267(5607):124–128. doi: 10.1038/267124a0. [DOI] [PubMed] [Google Scholar]
- Simson R., Wallraff E., Faix J., Niewöhner J., Gerisch G., Sackmann E. Membrane bending modulus and adhesion energy of wild-type and mutant cells of Dictyostelium lacking talin or cortexillins. Biophys J. 1998 Jan;74(1):514–522. doi: 10.1016/S0006-3495(98)77808-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takeichi M. Cadherins: a molecular family important in selective cell-cell adhesion. Annu Rev Biochem. 1990;59:237–252. doi: 10.1146/annurev.bi.59.070190.001321. [DOI] [PubMed] [Google Scholar]
- Thoumine O., Ott A., Louvard D. Critical centrifugal forces induce adhesion rupture or structural reorganization in cultured cells. Cell Motil Cytoskeleton. 1996;33(4):276–287. doi: 10.1002/(SICI)1097-0169(1996)33:4<276::AID-CM4>3.0.CO;2-7. [DOI] [PubMed] [Google Scholar]
- Truskey G. A., Proulx T. L. Relationship between 3T3 cell spreading and the strength of adhesion on glass and silane surfaces. Biomaterials. 1993;14(4):243–254. doi: 10.1016/0142-9612(93)90114-h. [DOI] [PubMed] [Google Scholar]
- Turner D. C., Chang C., Fang K., Brandow S. L., Murphy D. B. Selective adhesion of functional microtubules to patterned silane surfaces. Biophys J. 1995 Dec;69(6):2782–2789. doi: 10.1016/S0006-3495(95)80151-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vogel G., Thilo L., Schwarz H., Steinhart R. Mechanism of phagocytosis in Dictyostelium discoideum: phagocytosis is mediated by different recognition sites as disclosed by mutants with altered phagocytotic properties. J Cell Biol. 1980 Aug;86(2):456–465. doi: 10.1083/jcb.86.2.456. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Williams K. L., Kessin R. H., Newell P. C. Genetics of growth in axenic medium of the cellular slime mould Dictyostelium discoideum. Nature. 1974 Jan 18;247(5437):142–143. doi: 10.1038/247142a0. [DOI] [PubMed] [Google Scholar]
- Zhu C. Kinetics and mechanics of cell adhesion. J Biomech. 2000 Jan;33(1):23–33. doi: 10.1016/s0021-9290(99)00163-3. [DOI] [PubMed] [Google Scholar]