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On the diffusion of circular domains on a spherical vesicle

Published online by Cambridge University Press:  11 May 2010

S. ALIASKARISOHI
Affiliation:
Institut für Experimentalphysik, Universität Bayreuth, 95440 Bayreuth, Germany
P. TIERNO
Affiliation:
Departament de Química Física, Universitat de Barcelona, Marti i Franqes 1, 08028 Barcelona, Spain
P. DHAR
Affiliation:
Department of Chemical Engineering, University of California Santa Barbara, Santa Barbara, CA 93106, USA
Z. KHATTARI
Affiliation:
Department of Physics, Hashemite University, 13115 Zarqa, Jordan
M. BLASZCZYNSKI
Affiliation:
Institut für Experimentalphysik, Universität Bayreuth, 95440 Bayreuth, Germany
TH. M. FISCHER*
Affiliation:
Institut für Experimentalphysik, Universität Bayreuth, 95440 Bayreuth, Germany
*
Email address for correspondence: thomas.fischer@uni-bayreuth.de

Abstract

Tracking the motion of lipid domains on a vesicle is a rheological technique allowing the measurement of surface shear viscosities of vesicular lipid phases. The ratio of surface to bulk viscosity defines a viscous length scale. Hydrodynamic interactions split the motion of the domains into different modes of diffusion. The measurability of surface shear viscosities from any mode of diffusion is limited to viscous length scales between the radius of the domains and the radius of the vesicle. The measurability of the surface shear viscosity results from the sensitivity of the diffusion to surface shear viscosities and from sufficient spatial resolution to resolve the diffusive motion. Switching between the various modes of diffusion is a trade between sensitivity gained and resolution lost by the hydrodynamic interactions leaving the measurability unchanged. Measurability drops with the number of domains making single-domain rheology the best technique to measure surface shear viscosities. Ultimately confinement of the domains to small vesicles renders measurements of surface rheological properties with domain-tracking rheology impossible. Experiments on domains in vesicles of a mixture of dioleoylphosphatidylcholine (DOPC), dipalmytoylphosphatidylcholin (DPPC) and cholesterol (Chol) exhibit diffusion that is entirely controlled by dissipation into the water. The diffusion is suppressed compared to the diffusion of isolated domains in a flat membrane due to confinement to the curved vesicle and by hydrodynamic interactions between the domains. Effects of surface shear viscosity can be neglected.

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Papers
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Angelova, M. I., Soléau, S., Méléard, Ph., Faucon, J. F. & Bothorel, P. 1992 Preparation of giant vesicles by external AC electric-fields – kinetics and applications. Program. Colloid Polym. Sci. 89, 127131.Google Scholar
Bagatolli, L. A. & Gratton, E. 2000 Two photon fluorescence microscopy of coexisting lipid domains in giant unilamellar vesicles of binary phospholipid mixtures. Biophys. J. 78, 290305.Google Scholar
Baumgart, T., Hess, S. T. & Webb, W. W. 2003 Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425, 821824.CrossRefGoogle ScholarPubMed
Beattie, M. E., Veatch, S. L., Stottrup, B. L. & Keller, S. L. 2005 Sterol structure determines miscibility versus melting transitions in lipid vesicles. Biophys. J. 89, 17601768.CrossRefGoogle ScholarPubMed
Berne, B. J. & Precora, R. 2000 Dynamic Light Scattering with Applications to Chemistry, Biology and Physics. Dover.Google Scholar
Brown, D. A. & London, E. 1998 Functions of lipid rafts in biological membranes. Annu. Rev. Cell Devel. Biol. 14, 111136.CrossRefGoogle ScholarPubMed
Cicuta, P., Keller, S. L. & Veatch, S. L. 2007 Diffusion of liquid domains in lipid bilayer membranes. J. Phys. Chem. B 111, 33283331.Google Scholar
Daniels, D. R. & Turner, M. S. 2002 Diffusion on membrane tubes: a highly discriminatory test of the Saffman–Delbrück theory. Langmuir 23, 66676670.Google Scholar
Danov, K., Dimova, R. & Pouligny, B. 2000 Viscous drag of a solid sphere straddling a spherical or flat surface. Phys. Fluids 12, 27112722.Google Scholar
De Koker, R. 1996 Domain structures and hydrodynamics in lipid monolayers. PhD dissertation, Stanford University.CrossRefGoogle Scholar
Dimova, R., Dietrich, C., Hadjiisky, A., Danov, K. & Pouligny, B. 1999 a Falling ball viscosimetry of giant vesicle membranes: finite-size effects. Eur. Phys. J. B 12, 589598.Google Scholar
Dimova, R., Dietrich, C. & Pouligny, B. 1999 b Motion of particles attached to giant vesicles: falling ball viscosimetry and elasticity measurements on lipid membranes. In Giant Vesicles (ed. Walde, P. & Luisi, P.), chap. 15, p. 221. John Willey & Sons.Google Scholar
Edwards, D. A., Brenner, H. & Wasan, D. T. 1991 Interfacial transport and rheology. Butterworth–Heinemann Ser. Chem. Engng Boston, pp. 104–111.Google Scholar
Engelman, D. M. 2005 Membranes are more mosaic than fluid. Nature 438, 578580.CrossRefGoogle ScholarPubMed
Fischer, Th. M. 2003 The drag on needles moving in a Langmuir monolayer. J. Fluid Mech. 498, 123137.CrossRefGoogle Scholar
Fischer, T. M., Dhar, P. & Heinig, P. 2006 The viscous drag of spheres and filaments moving in membranes or monolayers. J. Fluid. Mech. 558, 451475.CrossRefGoogle Scholar
Fischer, T. M. & Lösche, M. 2004 Pattern formation in Langmuir monolayers due to long range electrostatic interactions. In Lecture Notes in Physics, Molecules in Interaction with Surfaces and Interfaces (ed. Haberlandt, R., Michel, D., Pöppl, A. & Stannarius, R.), vol. 634, pp. 383394. Springer.Google Scholar
Filippov, A., Orädd, G. & Lindblom, G. 2004 Lipid lateral diffusion in ordered and disordered phases in raft mixtures. Biophys. J. 86, 891896.CrossRefGoogle ScholarPubMed
Gaus, K., Gratton, E., Kable, E. P. W., Jones, A. S., Gelissen, I., Kritharides, L. & Jessup, W. 2003 Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc. Nat. Acad. Sci. 100, 1555415559.CrossRefGoogle ScholarPubMed
Heinig, P., Wurlitzer, S., John, t. & Fischer, Th. M. 2002 Stability criterion for three phase intersection points in monolayers. J. Phys. Chem. B 106, 1195111960.Google Scholar
Honerkamp-Smith, A. R., Cicuta, P., Collins, M. D., Veatch, S. L., den Nijs, M., Schick, M. & Keller, S. L. 2008 Line tensions, correlation lengths and critical exponents in lipid membranes near critical points. Biophys. J. 95, 236246.Google Scholar
Hughes, B. D., Pailthorpe, B. A. & White, L. R. 1981 The translational and rotational drag on a cylinder moving in a membrane. J. Fluid Mech. 110, 349372.Google Scholar
Kahya, N. & Schwille, P. 2006 How phospholipid-cholesterol interactions modulate lipid lateral diffusion, as revealed by fluorescence correlation spectroscopy. J. Fluoresc. 16, 671678.CrossRefGoogle ScholarPubMed
Khattari, Z., Heinig, P., Wurlitzer, S., Steffen, P., Lösche, M. & Fischer, Th. M. 2002 Wetting in asymmetric quasi-2d-systems. Langmuir 18, 22732279.CrossRefGoogle Scholar
Klingler, J. F. & McConnell, H. 1993 Brownian-motion and fluid-mechanis of lipid monolayer domains. J. Phys. Chem. 97, 60966100.Google Scholar
Korlach, J., Schwille, P., Webb, W. W. & Feigenson, G. W. 1999 Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. Proc. Nat. Acad. Sci. 96, 84618466.Google Scholar
Kubo, R. 1957 Statistical-mechanical theory of irreversible processes 1. General theory and simple applications to magnetic and conduction problems. J. Phys. Soc. Japan 12, 570586.CrossRefGoogle Scholar
Levine, A. J. & MacKintosh, F. C. 2002 Dynamics of viscoelastic membranes. Phys. Rev. E 66, 061606.Google Scholar
Misner, C. W., Thorne, K. P. & Wheeler, J. A. 1973 Gravitation. W. H. Freeman and Company.Google Scholar
Mukherjee, S. & Maxfield, F. R. 2000 Role of membrane organization and membrane domains in endocytic lipid trafficking. Traffic 1, 203211.CrossRefGoogle ScholarPubMed
Naji, A., Levine, A. J. & Pincus, P. A. 2007 Corrections to the Saffman–Delbrück mobility for membrane bound proteins. Biophys. J. 93, L49–L51.Google Scholar
Peters, R. & Cherry, R. J. 1982 Lateral and rotational diffusion of bacteriorhodopsin in lipid bilayers: experimental test of Saffman–Delbrck equations. Proc. Nat. Acad. Sci. USA 79, 43174321.CrossRefGoogle ScholarPubMed
Petrov, E. P. & Schwille, P. 2008 Translational diffusion in lipid membranes beyond the Saffman–Delbrück approximation. Biophys. J. 94, L41–L43.Google Scholar
Prasad, V., Koehler, S. A. & Weeks, E. R. 2006 Two-particle microrheology of quasi-2D viscous systems. Phys. Rev. Lett. 97, 176001176004.Google Scholar
Radhakrishnan, H. A. & McConnell, H. M. 1999 Cholesterol-phospholipid complexes in membranes. J. Am. Chem. Soc. 121, 486487.CrossRefGoogle Scholar
Reichl, L. E. 1980 A Modern Course in Statistical Physics. Edward Arnold, pp. 545595.Google Scholar
Riess, J. G. 2002 Fluorous micro- and nanophases with a biomedical perspective. Tetrahedron 58, 41134131.CrossRefGoogle Scholar
Russel, W. B., Saville, D. A. & Schowalter, W. R. 1989 Colloidal dispersions. In Cambridge Monographs on Mechanics and Applied Mathematics (ed. Batchelor, G. K.), pp. 3135. Cambridge University Press.Google Scholar
Saffman, P. G. & Delbrück, M. 1975 Brownian-motion in biological-membranes. Proc. Nat. Acad. Sci. (USA) 72, 31113113.Google Scholar
Sickert, M., Rondelez, F. & Stone, H. A. 2007 Single-particle Brownian dynamics for characterizing the rheology of fluid Langmuir monolayers. Eur. Phys. Lett. 79, 6600566010.Google Scholar
Simons, K. & Ikonen, E. 1997 Functional rafts in cell membranes. Science 387, 569572.Google Scholar
Singer, S. J. & Nicholson, G. L. 1972 The fluid mosaic model of the structure of cell membranes. Science 175, 720731.CrossRefGoogle ScholarPubMed
Trabelsi, S., Zhang, S., Lee, T. R. & Schwartz, D. K. 2006 Linactants: surfactant analogues in two dimensions. Phys. Rev. Lett 18, 037802.Google Scholar
Veatch, S. L., Gawrisch, K. & Keller, S. L. 2006 Closed-loop miscibility gap and quantitative tie-lines in ternary membranes containing diphytanoyl PC. Biophys. J. 90, 44284436.Google Scholar
Veatch, S. L. & Keller, S. L. 2002 Organization in lipid membranes containing cholesterol. Phys. Rev. Lett. 89, 268101268104.Google Scholar
Veatch, S. L. & Keller, S. L. 2003 Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol. Biophys. J. 85, 30743083.CrossRefGoogle Scholar