Dynamics of Pinned Membranes with Application to Protein Diffusion on the Surface of Red Blood Cells

Biophysical Journal

Volumn 86, Issue 2, 2004, Pages 764-780

  Lin, Lawrence C L ^a   Brown, Frank L H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN;

ALGORITHM; ARTICLE; CELL MEMBRANE; DIFFUSION; DYNAMICS; ERYTHROCYTE; HYDRODYNAMICS; PARTICLE SIZE; PROTEIN TRANSPORT; SIMULATION; THEORY;

EID: 1142298541     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(04)74153-3     Document Type: Article

References (101)

1. Arfken, G. B., and H. J. Weber. 2001. Mathematical Methods for Physicists, 5th Ed. Academic Press, San Diego, CA. 90, 93.
2. Ashcroft, N. W., and N. D. Mermin. 1976. Solid State Physics. Holt, Rinehart and Winston, New York.
3. Atkins, P. W. 1990. Physical Chemistry, 4th ed. W. H. Freeman and Co., New York.
4. Ayton, G., S. G. Bardenhagen, P. McMurty, D. Sulsky, and G. A. Voth, 2001. Interfacing continuum and molecular dynamics: an application to lipid bilayers. J. Chem. Phys. 114:6913-6924.
5. Ayton, G., and G. A. Voth. 2002. Bridging microscopic and mesoscopic simulations of lipid bilayers. Biophys. J. 83:3357-3370.
6. Baumgartner, A., and J.-S. Ho. 1990. Crumpling of fluid vesicles. Phys. Rev. A. 41:5747-5750.
7. Boal, D. H. 1994. Computer simulation of a model network for the erythrocyte cytoskeleton. Biophys. J. 67:521-529.
8. Boal, D. H., and S. K. Boey. 1995. Barrier-free paths of directed protein motion in the erythrocyte plasma membrane. Biophys. J. 69:372-379.
9. Brannigan, G., and F. L. H. Brown. 2003. Solvent-free simulations of fluid membrane bilayers. J. Chem. Phys. 120:1059-1071.
10. Brochard, F., and J. F. Lennon. 1975. Frequency spectrum of the flicker phenomenon in erythrocytes. J. Phys. (Paris). 36:1035-1047.
11. Brown, F. L. H. 2003. Regulation of protein mobility via thermal membrane undulations. Biophys. J. 84:842-853.
12. Brown, F. L. H., D. M. Leitner, J. A. McCammon, and K. R. Wilson. 2000. Lateral diffusion of membrane proteins in the presence of static and dynamic corrals: suggestions for appropriate observables. Biophys. J. 78:2257-2269.
13. Byers, T. J., and D. Branton. 1985. Visualization of the protein associations in the erythrocyte membrane skeleton. Proc. Natl. Acad. Sci. USA. 82:6153-6157.
14. Chandler, D. 1987. Introduction to Modern Statistical Mechanics. Oxford Press, New York.
15. Cherry, R. J. 1979. Rotational and lateral diffusion of membrane proteins. Biochim. Biophys. Acta. 559:289-327.
16. Corbett, J. D., P. Agre, J. Palek, and D. E. Golan. 1994. Differential control of band 3 lateral and rotational mobility in intact red cells. J. Clin. Invest. 94:683-688.
17. Dan, N., P. Pincus, and S. A. Safran. 1993. Membrane-induced interactions between inclusions. Langmuir. 9:2768-2771.
18. Doi, M., and S. F. Edwards. 1986. The Theory of Polymer Dynamics. Clarendon Press, Oxford, UK.
19. Drouffe, J.-M., A. C. Maggs, and S. Leibler. 1991. Computer simulations of self-assembled membranes. Science. 254:1353-1356.
20. Edidin, M., S. C. Kuo, and M. P. Sheetz. 1991. Lateral movements of membrane glycoproteins restricted by dynamic cytoplasmic barriers. Science. 254:1379-1382.
21. Ermak, D. L., and J. A. McCammon. 1978. Brownian dynamics with hydrodynamic interactions. J. Chem. Phys. 69:1352-1360.
22. Farago, O. 2003. "Water-free" computer model for fluid bilayer membranes. J. Chem. Phys. 119:596-605.
23. Feller, S. E. 2000. Molecular dynamics simulations of lipid bilayers. Curr. Opin. Colloid. In. 5:217-223.
24. Fleming, T. P. 1987. Trapped by a skeleton-the maintenance of epithelial membrane dynamics. Bioessays. 7:179-181.
25. Gennis, R. B. 1989. Biomembranes: Molecular Structure and Function. Springer-Verlag, Berlin, Germany.
26. Goetz, R., and R. Lipowsky. 1998. Computer simulations of bilayer membranes: self assembly and interfacial tension. J. Chem. Phys. 108:7397-7409.
27. Golestanian, R., M. Goulian, and M. Kardar. 1996. Fluctuation-induced interactions between rods on a membrane. Phys. Rev. Lett. 54:6725-6734.
28. Gouliaev, N., and J. F. Nagle. 1998a. Simulations of a single membrane between two walls using a Monte Carlo method. Phys. Rev. E. 58:881-888.
29. Gouliaev, N., and J. F. Nagle. 1998b. Simulations of interacting membranes in the soft confinement regime. Phys. Rev. Lett. 81:2610-2613.
30. Goulian, M., R. Bruinsma, and P. Pincus. 1993. Long-range forces in heterogeneous fluid membranes. Eur. Phys. Lett. 22:145-150.
31. Gov, N., A. G. Zilman, and S. Safran. 2003. Cytoskeleton confinement and tension of red blood cells. Phys. Rev. Lett. 90:228101.
32. Granek, R. 1997. From semi-flexible polymers to membranes: anomalous diffusion and reptation. J. Phys. II (Paris). 7:1761-1788.
33. Groot, R. D., and K. L. Rabone. 2001. Mesoscopic simulation of cell membrane damage, morphology change and rupture by nonionic surfactants. Biophys. J. 81:725-736.
34. Helfrich, W. 1973. Elastic properties of lipid bilayers: theory and possible experiments. Z. Naturforsch. [C]. 28:693-703.
35. Ho, J.-S., and A. Baumgartner. 1990. Simulations of fluid self-avoiding membranes. Eur. Phys. Lett. 12:295-300.
36. Howard, J. 2001. Mechanics of Motor Proteins and the Cytoskeleton. Sinauer, Sunderland, Massachusetts.
37. Jacobson, K., E. D. Sheets, and R. Simson. 1995. Revisiting the fluid mosaic model of membranes. Science. 268:1441-1442.
38. Janmey, P. 1995. Cell membranes and the cytoskeleton. In Structure and Dynamics of Membranes: Part A. From Cells to Vesicles. Elsevier Science, Amsterdam, The Netherlands. 805-849.
39. Kantor, Y., M. Karder, and D. R. Nelson. 1987. Tethered surfaces: statics and dynamics. Phys. Rev. A. 35:3056-3071.
40. Kim, K. S., J. Neu, and G. Oster. 1998. Curvature-mediated interactions between membrane proteins. Biophys. J. 75:2274-2291.
41. Koppel, D. E., M. P. Sheetz, and M. Schindler. 1981. Matrix control of protein diffusion in biological membranes. Proc. Natl. Acad. Sci. USA. 78:3576-3580.
42. Kumar, P. B. S., G. Gompper, and R. Lipowsky. 2001. Budding dynamics of multicomponent membranes. Phys. Rev. Lett. 86:3911-3914.
43. Kumar, P. B. S., and M. Rao. 1998. Shape instabilities in the dynamics of a two-component fluid membrane. Phys. Rev. Lett. 80:2489-2492.
44. Kusumi, A., and Y. Sako. 1996. Cell surface organization by the membrane skeleton. Curr. Opin. Cell Biol. 8:566-574.
45. Kusumi, A., Y. Sako, and M. Yamamoto. 1993. Confined lateral diffusion of membrane receptors as studied by single particle tracking. Effects of calcium-induced differentiation in cultured epithelial cells. Biophys. J. 65:2021-2040.
46. Lague, P., M. J. Zuckermann, and B. Roux. 1998. Protein inclusion in lipid membranes: a theory based on the hypernetted chain integral equation. Faraday Discuss. 111:165-172.
47. Laradji, M. 1999. Polymer adsorption on fluctuating surfaces. Eur. Phys. Lett. 47:694-700.
48. Lee, G. M., F. Zhang, and A. Ishihara. 1993. Unconfined lateral diffusion and an estimate of pericellular matrix viscosity revealed by measuring the mobility of gold-tagged lipids. J. Cell Biol. 120:25-35.
49. Leitner, D. M., F. L. H. Brown, and K. R. Wilson. 2000. Regulation of protein mobility in cell membranes: a dynamic corral model. Biophys. J. 78:125-135.
50. Lipowsky, R. 1991. The conformation of membranes. Nature. 349:475-481.
51. Lipowsky, R., and B. Zielenska. 1989. Binding and unbinding of lipid membranes: a Monte Carlo study. Phys. Rev. Lett. 62:1572-1575.
52. Liu, S., L. Derick, and J. Palek. 1987. Visualization of the hexagonal lattice in the erythrocyte membrane skeleton. J. Cell Biol. 104:527-536.
53. Lodish, H., D. Baltimore, A. Berk, S. L. Zipursky, P. Matsudaira, and J. Darnell. 1995. Molecular Cell Biology, 3rd Ed. Scientific American Books, New York.
54. Lopez, C. F., P. B. Moore, J. C. Shelley, M. Y. Shelley, and L. M. Klein. 2002. Computer simulation studies of biomembranes using a coarse grain model. Comp. Phys. Commun. 147:1-6.
55. Luna, E. J., and A. L. Hitt. 1992. Cytoskeleton-plasma membrane interactions. Science. 258:955-964.
56. Marcelja, S. 1976. Lipid-mediated protein interactions in membranes. Biochim. Biophys. Acta. 455:1-7.
57. Marrink, S. J., E. Lindahl, O. Edholm, and A. E. Mark. 2001. Simulation of the spontaneous aggregation of phospholipids into bilayers. J. Am. Chem. Soc. 123:8638-8639.
58. Milner, S. T., and S. A. Safran. 1987. Dynamical fluctuations of droplet microemulsions and vesicles. Phys. Rev. A. 36:4371-4379.
59. Noguchi, H., and M. Takasu. 2001. Fusion pathways of vesicles: a Brownian dynamics simulation. J. Chem. Phys. 115:9547-9551.
60. Owicki, J. C., M. W. Springgate, and H. M. McConnell. 1978. Theoretical study of protein-lipid interactions in bilayer membranes. Proc. Natl. Acad. Sci. USA. 75:1616-1619.
61. Pastor, R. W. 1994. Molecular-dynamics and Monte Carlo simulations of lipid bilayers. Curr. Opin. Struct. Biol. 4:486-492.
62. Pollard, T. D., L. Blanchoin, and R. D. Mullins. 2000. Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu. Rev. Biophys. Biomol. Struct. 29:545-576.
63. Press, W. H., S. A. Teukolsky, W. T. Vetterling, and B. P. Flannery. 1994. Numerical Recipes in C. Cambridge University Press, Cambridge, UK.
64. Purcell, E. M. 1977. Life at low Reynolds number. Am. J. Phys. 45:3-10.
65. Qi, S. Y., J. T. Groves, and A. K. Chakraborty. 2001. Synaptic pattern formation during cellular recognition. Proc. Natl. Acad. Sci. USA. 98:6548-6553.
66. Sackmann, E. 1995. Biological membranes architecture and function. In Structure and Dynamics of Membranes: Part A. From Cells to Vesicles. Elsevier Science, Amsterdam, The Netherlands. 1-62.
67. Saffman, P. G., and M. Delbruck. 1975. Brownian motion in biological membranes. Proc. Natl. Acad. Sci. USA. 73:3111-3113.
68. Safran, S. A. 1994. Statistical Thermodynamics of Surfaces, Interfaces and Membranes. Westview Press, Boulder, CO.
69. Saxton, M. J. 1989. The spectrin network as a barrier to lateral diffusion in erythrocytes: a percolation analysis. Biophys. J. 55:21-28.
70. Saxton, M. J. 1990a. The membrane skeleton of erythrocytes: a percolation model. Biophys. J. 57:1167-1177.
71. Saxton, M. J. 1990b. The membrane skeleton of erythrocytes: models of its effect on lateral diffusion. Int. J. Biochem. 22:801-809.
72. Saxton, M. J. 1995. Single-particle tracking: effects of corrals. Biophys. J. 69:389-398.
73. Saxton, M. J., and K. Jacobson. 1997. Single particle tracking: applications to membrane dynamics. Annu. Rev. Biophys. Biomol. Struct. 26:373-399.
74. Schindler, M., D. E. Koppel, and M. P. Sheetz. 1980. Modulation of protein lateral mobility by polyphosphates and polyamines. Proc. Natl. Acad. Sci. USA. 77:1457-1461.
75. Schneider, M. B., J. T. Jenkins, and W. W. Webb. 1984. Thermal fluctuations of large quasi-spherical bimolecular phospholipid vesicles. J. Phys. (Paris). 45:1457-1472.
76. Sheets, E. D., R. Simson, and K. Jacobson. 1995. New insights into membrane dynamics from the analysis of cell-surface interactions by physical methods. Curr. Opin. Cell Biol. 7:707-714.
77. Sheetz, M. P. 1983. Membrane skeletal dynamics: role in modulation of red blood deformability, mobility of transmembrane proteins and shape. Semin. Hematol. 20:175-188.
78. Sheetz, M. P., M. Schindler, and D. E. Koppel. 1980. The lateral mobility of integral membrane proteins is increased in spherocytic erythrocytes. Nature. 285:510-512.
79. Shillcock, J., and R. Lipowsky. 2002. Equilibrium structure and lateral stress distribution of amphiphilic bilayers from dissipative particle dynamics simulations. J. Chem. Phys. 117:5048-5061.
80. Simons, K., and E. Ikonen. 2000. Cell biology - how cells handle cholesterol. Science. 290:1721-1726.
81. Singer, S. J., and G. L. Nicolson. 1972. The fluid mosaic model of the structure of cell membranes. Science. 175:720-731.
82. Smit, B., K. Esselink, P. Hilbers, N. van Os, L. Rupert, and I. Szleifer. 1993. Computer simulations of surfactant self-assembly. Langmuir. 9:9-11.
83. Soddemann, T., B. Dunweg, and K. Kremer. 2001. A generic computer model for amphiphilic systems. Eur. Phys. J. E. 6:409-419.
84. Steck, T. L. 1989. Red cell shape. In Cell Shape: Determinants, Regulation and Regulatory Role. W. Stein and F. Bronner, editors. Academic Press, New York. 205-246.
85. Stossel, T. P. 1993. On the crawling of animal cells. Science. 260:1086-1094.
86. Theriot, J. A., and T. J. Mitchison. 1991. Actin microfilament dynamics in locomoting cells. Nature. 352:126-131.
87. Tieleman, D. P., S. J. Marrink, and H. J. C. Berendsen. 1997. A computer perspective of membranes: molecular dynamics studies of lipid bilayer systems. Biochim. Biophys. Acta. 1331:235-270.
88. Tobias, D. J., K. C. Tu, and M. L. Klein. 1997. Atomic-scale molecular dynamics simulations of lipid membranes. Curr. Opin. Coll. Interf. 2:15-26.
89. Tomishige, M. 1997. Regulation mechanism of the lateral diffusion of band 3 in erythrocyte membranes: corralling and binding effects of the membrane skeleton. PhD thesis. The University of Tokyo.
90. Tomishige, M., Y. Sako, and A. Kusumi. 1998. Regulation mechanism of the lateral diffusion of band 3 in erythrocyte membranes by the membrane skeleton. J. Cell Biol. 142:989-1000.
91. Tsuji, A., K. Kawasaki, S. Ohnishi, H. Merkle, and A. Kusumi. 1988. Regulation of band 3 mobilities in erythrocyte ghost membranes by protein association and cytoskeletal meshwork. Biochemistry. 27:7447-7452.
92. Tsuji, A., and S. Ohnishi. 1986. Restriction of the lateral motion of band 3 in the erythrocyte membrane by the cytoskeletal network: dependence on spectrin association state. Biochemistry. 25:6133-6139.
93. van Kampen, N. G. 1992. Stochastic Processes in Physics and Chemistry. North-Holland, Amsterdam, The Netherlands.
94. Weikl, T. R. 2002. Dynamic phase separation of fluid membranes with rigid inclusions. Phys. Rev. E. 66:061915.
95. Weikl, T. R., and R. Lipowsky. 2000. Local adhesion of membranes to striped surface domains. Langmuir. 16:9338-9346.
96. Winckler, B., P. Forscher, and I. Mellman. 1999. A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature. 397:698-701.
97. Yamamoto, S., Maruyama, Y., and S.-A. Hyodo. 2002. Dissipative particle dynamics study of spontaneous vesicle formation of amphiphilic molecules. J. Chem. Phys. 116:5842-5849.
98. Zhang, D., A. Klyatkin, J. T. Bolin, and P. S. Low. 2000. Crystallographic structure and functional interpretation of the cytoplasmic domain of erythrocyte membrane band 3. Blood. 96:2925-2933.
99. Zhou, H.-X., S. T. Wlodek, and J. A. McCammon. 1998. Conformation gating as a mechanism for enzyme specificity. Proc. Natl. Acad. Sci. USA. 95:9280-9283.
100. -1 regime by microinterferometry combined with fast image processing. Phys. Rev. A. 46:7998-8001.
101. Zilman, A. G., and R. Granek. 1996. Undulations and dynamic structure factor of membranes. Phys. Rev. Lett. 77:4788-4791.