Abstract
We model theoretically the effect of localized forces on a fluid membrane anchored to a uniform elastic medium. We use this as a simple model for the plasma membrane of a cell. The atomic force microscope (AFM) has been used to apply such forces, but large membrane perturbations occurring in vivo are also treated within the same framework. Inclusions of this nature may include cell junctions, filipodia, caveolae, and similar membrane invaginations. The breakdown of linear elastic response, as observed by AFM, is predicted to occur for forces as small as 10 pN. We estimate the position of this crossover and the subsequent nonlinear behavior and make encouraging quantitative comparison with experiments. Intrinsic membrane inclusions interact through their overlapping strain fields. For similar, point force-like inclusions at large separations, this yields an attractive potential that scales like the inverse of their separation. For membranes that are intrinsically stiff or under tension, the binding force between inclusions can depend on the properties of the membrane and may be large enough to induce aggregation of inclusions, as observed experimentally. For inclusions that fix the magnitude of the membrane deformation, rather than the applied force, we demonstrate the possibility of metastable states, corresponding to finite separations. Finally, we discuss briefly the case in which inclusions couple to the membrane in more complex ways, such as via a torque (twist). In such cases, the interaction scales like a higher power of the separation, depends on the orientation of the inclusions, and can have either sign.
Full Text
The Full Text of this article is available as a PDF (124.1 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- A-Hassan E., Heinz W. F., Antonik M. D., D'Costa N. P., Nageswaran S., Schoenenberger C. A., Hoh J. H. Relative microelastic mapping of living cells by atomic force microscopy. Biophys J. 1998 Mar;74(3):1564–1578. doi: 10.1016/S0006-3495(98)77868-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Aranda-Espinoza H., Berman A., Dan N., Pincus P., Safran S. Interaction between inclusions embedded in membranes. Biophys J. 1996 Aug;71(2):648–656. doi: 10.1016/S0006-3495(96)79265-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bar-Ziv R, Menes R, Moses E, Safran SA. Local unbinding of pinched membranes. Phys Rev Lett. 1995 Oct 30;75(18):3356–3359. doi: 10.1103/PhysRevLett.75.3356. [DOI] [PubMed] [Google Scholar]
- Bruinsma R., Goulian M., Pincus P. Self-assembly of membrane junctions. Biophys J. 1994 Aug;67(2):746–750. doi: 10.1016/S0006-3495(94)80535-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Evans E., Ritchie K., Merkel R. Sensitive force technique to probe molecular adhesion and structural linkages at biological interfaces. Biophys J. 1995 Jun;68(6):2580–2587. doi: 10.1016/S0006-3495(95)80441-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haydon P. G., Lartius R., Parpura V., Marchese-Ragona S. P. Membrane deformation of living glial cells using atomic force microscopy. J Microsc. 1996 May;182(Pt 2):114–120. doi: 10.1046/j.1365-2818.1996.141423.x. [DOI] [PubMed] [Google Scholar]
- Henderson E., Haydon P. G., Sakaguchi D. S. Actin filament dynamics in living glial cells imaged by atomic force microscopy. Science. 1992 Sep 25;257(5078):1944–1946. doi: 10.1126/science.1411511. [DOI] [PubMed] [Google Scholar]
- Huang H. W. Deformation free energy of bilayer membrane and its effect on gramicidin channel lifetime. Biophys J. 1986 Dec;50(6):1061–1070. doi: 10.1016/S0006-3495(86)83550-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Janmey P. A., Euteneuer U., Traub P., Schliwa M. Viscoelastic properties of vimentin compared with other filamentous biopolymer networks. J Cell Biol. 1991 Apr;113(1):155–160. doi: 10.1083/jcb.113.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Janmey P. A., Hvidt S., Käs J., Lerche D., Maggs A., Sackmann E., Schliwa M., Stossel T. P. The mechanical properties of actin gels. Elastic modulus and filament motions. J Biol Chem. 1994 Dec 23;269(51):32503–32513. [PubMed] [Google Scholar]
- Kasas S., Gotzos V., Celio M. R. Observation of living cells using the atomic force microscope. Biophys J. 1993 Feb;64(2):539–544. doi: 10.1016/S0006-3495(93)81396-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Netz RR, Pincus P. Inhomogeneous fluid membranes: Segregation, ordering, and effective rigidity. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 1995 Oct;52(4):4114–4128. doi: 10.1103/physreve.52.4114. [DOI] [PubMed] [Google Scholar]
- Nicot C, Waks M, Ober R, Gulik-Krzywicki T, Urbach W. Squeezing of Oil-Swollen Surfactant Bilayers by a Membrane Protein. Phys Rev Lett. 1996 Oct 14;77(16):3485–3485. doi: 10.1103/PhysRevLett.77.3485. [DOI] [PubMed] [Google Scholar]
- Radmacher M., Fritz M., Kacher C. M., Cleveland J. P., Hansma P. K. Measuring the viscoelastic properties of human platelets with the atomic force microscope. Biophys J. 1996 Jan;70(1):556–567. doi: 10.1016/S0006-3495(96)79602-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rothberg K. G., Heuser J. E., Donzell W. C., Ying Y. S., Glenney J. R., Anderson R. G. Caveolin, a protein component of caveolae membrane coats. Cell. 1992 Feb 21;68(4):673–682. doi: 10.1016/0092-8674(92)90143-z. [DOI] [PubMed] [Google Scholar]
- Schekman R., Orci L. Coat proteins and vesicle budding. Science. 1996 Mar 15;271(5255):1526–1533. doi: 10.1126/science.271.5255.1526. [DOI] [PubMed] [Google Scholar]
- Sheetz M. P., Dai J. Modulation of membrane dynamics and cell motility by membrane tension. Trends Cell Biol. 1996 Mar;6(3):85–89. doi: 10.1016/0962-8924(96)80993-7. [DOI] [PubMed] [Google Scholar]
- Sheetz M. P., Wayne D. B., Pearlman A. L. Extension of filopodia by motor-dependent actin assembly. Cell Motil Cytoskeleton. 1992;22(3):160–169. doi: 10.1002/cm.970220303. [DOI] [PubMed] [Google Scholar]
- Simson R., Yang B., Moore S. E., Doherty P., Walsh F. S., Jacobson K. A. Structural mosaicism on the submicron scale in the plasma membrane. Biophys J. 1998 Jan;74(1):297–308. doi: 10.1016/S0006-3495(98)77787-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thoumine O., Ott A. Time scale dependent viscoelastic and contractile regimes in fibroblasts probed by microplate manipulation. J Cell Sci. 1997 Sep;110(Pt 17):2109–2116. doi: 10.1242/jcs.110.17.2109. [DOI] [PubMed] [Google Scholar]