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Motion of nanobeads proximate to plasma membranes during single particle tracking

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Abstract

Drag and torque on nanobeads translating within the pericellular layer while attached to glycolipids of the plasma membrane are calculated by a novel hydrodynamic model. The model considers a bead that translates proximate to a rigid planar interface that separates two distinct Brinkman media. The hydrodynamic resistance is calculated numerically by a modified boundary integral equation formulation, where the pertinent boundary conditions result in a hybrid system of Fredholm integrals of the first and second kinds. The hydrodynamic resistance on the translating bead is calculated for different combinations of the Brinkman screening lengths in the two layers, and for different viscosity ratios. Depending on the bead-membrane separation and on the hydrodynamic properties of both the plasma membrane and the pericellular layer, the drag on the bead may be affected by the properties of the plasma membrane. The Stokes-Einstein relation is applied for calculating the diffusivity of probes (colloidal gold nanobeads attached to glycolipids) in the plasma membrane. This approach provides an alternative way for the interpretation of in vitro observations during single particle tracking procedure, and predicts new properties of the plasma membrane structure.

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References

  • Abramowitz, M. and I. A. Stegun (1972). Handbook of Mathematical Functions, New York: Dover.

    MATH  Google Scholar 

  • Adamson, R. H. and G. Clough (1992). Plasma proteins modify the endothelial cell glycocalyx of frog mesenteric microvessels. J. Physiol. (Lond.) 445, 473–486.

    Google Scholar 

  • Broday, D. M. (2000). Diffusion of clusters of transmembrane proteins as a model of focal adhesion remodeling. Bull. Math. Biol. 62, 891–924.

    Article  Google Scholar 

  • Burridge, K., K. Fath, T. Kelly, G. Nuckolls and C. Turner (1988). Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu. Rev. Cell Biol. 4, 487–525.

    Article  Google Scholar 

  • Bussell, S. J., D. L. Koch and D. A. Hammer (1995). Effect of hydrodynamic interactions on the diffusion of integral membrane proteins: diffusion in plasma membrane. Biophys. J. 68, 1836–1849.

    Google Scholar 

  • Cherry, R. J. (1979). Rotational and lateral diffusion of membrane proteins. Biochim. Biophys. Acta. 559, 289–327.

    Google Scholar 

  • Davis, H. T. (1962). Introduction to Nonlinear Differential and Integral Equations, New York: Dover.

    MATH  Google Scholar 

  • Dodd, T. L., D. A. Hammer, A. S. Sangani and D. L. Koch (1995). Numerical simulations of the effect of hydrodynamic interactions on diffusivities of integral membrane proteins. J. Fluid Mech. 293, 147–180.

    Article  MATH  Google Scholar 

  • Doktycz, M. J., H. F. Arlinghaus, R. C. Allen and K. B. Jacobson (1992). Electrophoresis and detection of tin-labeled DNAs on open-faced gels. Electrophoresis 13, 521–528.

    Article  Google Scholar 

  • Edidin, M., S. C. Kuo and M. P. Sheetz (1991). Lateral movements of membrane glycoproteins restricted by dynamic cytoplasmic barriers. Science 254, 1379–1382.

    Google Scholar 

  • Feng, J. and S. Weinbaum (2000). Lubrication theory in highly compressible porous media: the mechanics of skiing, from red cells to humans. J. Fluid Mech. 422, 281–317.

    Article  MathSciNet  MATH  Google Scholar 

  • Feng, J., P. Ganatos and S. Weinbaum (1998). Motion of a sphere near planar confining boundaries in a Brinkman medium. J. Fluid Mech. 375, 265–296.

    Article  MATH  Google Scholar 

  • Goldman, A. J., R. G. Cox and H. Brenner (1966). The slow motion of two identical arbitrary oriented spheres through a viscous fluid. Chem. Eng. Sci. 21, 1151–1170.

    Article  Google Scholar 

  • Goldman, A. J., R. G. Cox and H. Brenner (1967a). Slow viscous motion of a sphere parallel to a plane wall. I. Motion through a quiescent fluid. Chem. Eng. Sci. 22, 637–652.

    Article  Google Scholar 

  • Goldman, A. J., R. G. Cox and H. Brenner (1967b). Slow viscous motion of a sphere parallel to a plane wall. II. Couette flow. Chem. Eng. Sci. 22, 653–660.

    Article  Google Scholar 

  • Gradshteyn, I. S. and I. M. Ryshik (1980). Tables of Integrals, Series, and Products, New York: Academic Press.

    Google Scholar 

  • Happel, J. (1959). Viscous flow relative to arrays of cylinders. AIChE J. 5, 174–177.

    Article  Google Scholar 

  • Higdon, J. J. L. (1995). Stokes flow in arbitrary two-dimensional domains: shear flow over ridges and cavities. J. Fluid Mech. 159, 195–226.

    Article  MathSciNet  Google Scholar 

  • Howells, I. D. (1974). Drag due to the motion of a Newtonian fluid through a sparse random array of small fixed rigid objects. J. Fluid Mech. 64, 449–475.

    Article  MATH  Google Scholar 

  • Jackson, G. W. and D. F. James (1986). The permeability of fibrous porous media. Can. J. Chem. Eng. 64, 364–374.

    Article  Google Scholar 

  • James, D. F. and A. M. J. Davis (2001). Flow at the interface of a model fibrous porous medium. J. Fluid Mech. 426, 47–72.

    Article  MathSciNet  MATH  Google Scholar 

  • Janson, L. W., K. Ragsdale and K. Luby-Phelps (1996). Mechanism and size cutoff for steric exclusion from actin-rich cytoplasmic domains. Biophys. J. 71, 1228–1234.

    Google Scholar 

  • Kim, S. and W. B. Russel (1985). The hydrodynamic interactions between two spheres in a Brinkman medium. J. Fluid Mech. 154, 253–268.

    Article  MATH  Google Scholar 

  • Koch, D. L. and A. J. C. Ladd (1997). Moderate Reynolds number flows through periodic and random arrays of aligned cylinders. J. Fluid Mech. 349, 31–66.

    Article  MathSciNet  MATH  Google Scholar 

  • Kucik, D. F., E. L. Elson and M. P. Sheetz (1999). Weak dependence of mobility of membrane protein aggregates on aggregate size supports a viscous model of retardation of diffusion. Biophys. J. 76, 314–322.

    Article  Google Scholar 

  • Kusumi, A. and Y. Sako (1996). Cell surface organization by the membrane skeleton. Curr. Opin. Cell Biol. 8, 566–574.

    Article  Google Scholar 

  • Ladyzhenskaya, O. A. (1969). The Mathematical Theory of Viscous Incompressible Flow, New York: Gordon and Breach.

    MATH  Google Scholar 

  • Lee, G. M., F. Zhang, A. Ishihara, C. L. McNeil and K. A. Jacobson (1993). Unconfined lateral diffusion and estimate of pericellular matrix viscosity revealed by measuring the mobility of gold-tagged lipids. J. Cell Biol. 120, 25–35.

    Article  Google Scholar 

  • Loewenberg, M (1994a). Asymmetric oscillatory motion of a finite-length cylinder: the macroscopic effect of particle edges. Phys. Fluids 6, 1095–1107.

    Article  MATH  Google Scholar 

  • Loewenberg, M. (1994b). Axisymmetric unsteady Stokes flow past an oscillating finite-length cylinder. J. Fluid Mech. 265, 265–288.

    Article  MATH  Google Scholar 

  • Muldowney, G. P. and J. J. L. Higdon (1995). A spectral boundary element approach to three-dimensional Stokes flow. J. Fluid Mech. 298, 167–192.

    Article  MATH  Google Scholar 

  • O’Neill, M. E. and K. Stewartson (1967). On the slow motion of a sphere parallel to a nearby wall. J. Fluid Mech. 27, 705–724.

    Article  MathSciNet  MATH  Google Scholar 

  • Pozrikidis, C. (1988). A study of linearized oscillatory flow past particles by the boundary-integral method. J. Fluid Mech. 202, 17–41.

    Article  MathSciNet  Google Scholar 

  • Pozrikidis, C. (1992). Boundary Integral and Singularity Method for Linearized Viscous Flow, Cambridge: Cambridge University Press.

    Google Scholar 

  • Pozrikidis, C. (1994). The motion of particles in the Hele-Shaw cell. J. Fluid Mech. 261, 199–222.

    Article  MATH  MathSciNet  Google Scholar 

  • Pries, A. R., T. W. Secomb and P. Gaehtgens (2000). The endothelial surface layer. Pflugers Arch. 440, 653–666.

    Article  Google Scholar 

  • Rallison, J. M. and A. Acrivos (1978). A numerical study of the deformation and burst of a viscous drop in an extensional flow. J. Fluid Mech. 89, 191–200.

    Article  MATH  Google Scholar 

  • Saffman, P. G. (1976). Brownian motion in thin sheets of viscous fluid. J. Fluid Mech. 73, 593–602.

    Article  MATH  MathSciNet  Google Scholar 

  • Sako, Y. and A. Kusumi (1995). Barriers for lateral diffusion of transferrin receptors in the plasma membranes as characterized by receptor dragging by laser tweezers: fence versus tether. J. Cell Biol. 129, 1559–1574.

    Article  Google Scholar 

  • Sako, Y., A. Nagafuchi, S. Tsukita, M. Takeichi and A. Kusumi (1998). Cytoplasmic regulation of the movement of E-cadherin on the free cell surface as studied by optical tweezers and single particle tracking: corralling and tethering by membrane skeleton. J. Cell Biol. 140, 1227–1240.

    Article  Google Scholar 

  • Sangani, S. A. and C. Yao (1988a). Transport processes in random arrays of cylinders. I Thermal conduction. Phys. Fluids 31, 2426–2434.

    Article  MATH  Google Scholar 

  • Sangani, S. A. and C. Yao (1988b). Transport processes in random arrays of cylinders. II Viscous flow. Phys. Fluids 31, 2435–2444.

    Article  MATH  Google Scholar 

  • Sangani, S. A. and G. Mo (1994). Inclusion of lubrication forces in dynamic simulations. Phys. Fluids 6, 1653–1662.

    Article  MATH  Google Scholar 

  • Schmidt, C. E., A. F. Horwitz, D. A. Lauffenburger and M. P. Sheetz (1993). Integrin-cytoskeletal interactions in migrating fibroblasts are dynamic, asymmetric, and regulated. J. Cell Biol. 123, 977–991.

    Article  Google Scholar 

  • Secomb, T. W., R. Hsu and A. R. Pries (2001). Motion of red blood cells in a capillary with an endothelial surface layer: effect of flow velocity. Am. J. Physiol. Heart Circ. Physiol. 281, H629–H636.

    Google Scholar 

  • Sheetz, M. P. (1993). Glycoprotein motility and dynamic domains in fluid plasma membranes. Ann. Rev. Biophys. Biomol. Struct. 22, 417–431.

    Article  Google Scholar 

  • Sheetz, M. P., S. Turney, H. Qian and E. L. Elson (1989). Nanometer-level analysis demonstrates that lipid flow does not drive membrane glycoprotein movements. Nature 340, 284–288.

    Article  Google Scholar 

  • Solomentsev, Y. E. and J. L. Anderson (1996). Rotation of a sphere in Brinkman fluids. Phys. Fluids 8, 1119–1121.

    Article  MATH  Google Scholar 

  • Vink, H. and B. R. Duling (1996). Identification of distinct luminal domains for macromolecules, erythrocytes and leukocytes within mammalian capillaries. Circ. Res. 71, 581–589.

    Google Scholar 

  • Wang, W. and S. A. Sangani (1997). Nusselt number for flow perpendicular to arrays of cylinders in the limit of small Reynolds and large Peclet numbers. Phys. Fluids 9, 1529–1539.

    Article  Google Scholar 

  • Weinbaum, S. (1998). Models to solve mysteries in biomechanics at the cellular level; a new view of fiber matrix layers. Ann. Biomed. Eng. 26, 1–17.

    Article  Google Scholar 

  • Williams, W. E. (1966). A note on slow vibrations in a viscous fluid. J. Fluid Mech. 25, 589–590.

    Article  Google Scholar 

  • Yechiel, E. and M. Edidin (1987). Micrometer-scale domains in fibroblast plasma membranes. J. Cell Biol. 105, 755–760.

    Article  Google Scholar 

  • Youngren, G. K. and A. Acrivos (1975). Stokes flow past a particle of arbitrary shape: a numerical method of solution. J. Fluid Mech. 69, 377–403.

    Article  MathSciNet  MATH  Google Scholar 

  • Youngren, G. K. and A. Acrivos (1976). On the shape of a gas bubble in a viscous extensional flow. J. Fluid Mech. 76, 433–442.

    Article  MathSciNet  MATH  Google Scholar 

  • Zhang, F., B. Crise, B. Su, Y. Hou, J. K. Rose, A. Bothwell and K. Jacobson (1991). Lateral diffusion of membrane-spanning and glycosylphosphatidylinositol-link proteins: toward establishing rules governing the lateral mobility of membrane proteins. J. Cell Biol. 115, 75–84.

    Article  Google Scholar 

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Broday, D.M. Motion of nanobeads proximate to plasma membranes during single particle tracking. Bull. Math. Biol. 64, 531–563 (2002). https://doi.org/10.1006/bulm.2002.0289

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