Concentration dependence of lipopolymer self-diffusion in supported bilayer membranes

Journal of the Royal Society Interface

Volumn 8, Issue 54, 2011, Pages 127-143

  Zhang, Huai Ying ^a   Hill, Reghan J ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Fluorescence recovery after photobleaching; Lipopolymers; Phospholipid bilayer membranes; Self diffusion coefficient

Indexed keywords

AMMONIUM COMPOUNDS; DRAG; ETHYLENE; ETHYLENE GLYCOL; FLUID DYNAMICS; FLUORESCENCE; FRICTION; HYDRODYNAMICS; PHOSPHOLIPIDS; PHOTOBLEACHING; POLYETHYLENE GLYCOLS; POLYETHYLENE OXIDES; RECOVERY;

AMMONIUM SALT; BI-LAYER; BILAYER MEMBRANES; CHAIN SEGMENTS; CONCENTRATION DEPENDENCE; CONTROL EXPERIMENTS; DATA YIELDS; DIFFUSION COEFFICIENTS; DILUTE LIMIT; EXCLUDED VOLUME; FIRST ORDER REACTIONS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FRICTIONAL DRAG; HYDRODYNAMIC INTERACTION; INFINITE DILUTION; LIPO-POLYMER; LIPOPOLYMERS; MOBILE FRACTIONS; MOLE PERCENT; PHOSPHOCHOLINE; PHOSPHOETHANOLAMINE; PHOSPHOLIPID BILAYER; PHOSPHOLIPID BILAYER MEMBRANES; SELF-DIFFUSION; SELF-DIFFUSION COEFFICIENTS; STATISTICAL MECHANICAL THEORY; TRANS-MEMBRANE PROTEINS;

DIFFUSION IN LIQUIDS;

1,2 DIOLEOYL SN GLYCERO 3 PHOSPHOCHOLINE; CHOLINE DERIVATIVE; PHOSPHOLIPID; POLYMER; UNCLASSIFIED DRUG;

ARTICLE; BLEACHING; CHEMICAL REACTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORRELATION ANALYSIS; DIFFUSION; DIFFUSION COEFFICIENT; HYDRODYNAMICS; LIPID BILAYER; STATISTICAL MODEL;

BASIDIOMYCOTA;

EID: 78650807607     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2010.0200     Document Type: Article

References (72)

1. Janmey, P. A. & Stossel, T. P. 1989 Gelsolin-polyphosphoinositide interaction - full expression of gelsolin-inhibiting function by polyphosphoinositides in vesicular form and inactivation by dilution, aggregation, or masking of the inositol head group. J. Biol. Chem. 264, 4825-4831.
2. McCloskey, M. A. & Poo, M. 1986 Contact-induced redistribution of specific membrane-components - local accumulation and development of adhesion. J. Cell Biol. 102, 2185-2196. (doi:10.1083/jcb.102.6.2185)
3. Chan, P. Y., Lawrence, M. B., Dustin, M. L., Ferguson, L. M., Golan, D. E. & Springer, T. A. 1991 Influence of receptor lateral mobility on adhesion strengthening between membranes containing lfa-3 and cd2. J. Cell Biol. 115, 245-255. (doi:10.1083/jcb.115.1.245)
4. Saxton, M. J. 1999 Lateral diffusion of lipids and proteins. In Membrane permeability, vol. 48, Current topics in membranes. San Diego, CA: Academic Press.
5. Saffman, P. G. & Delbruck, M. 1975 Brownian motion in biological membranes. Proc. Natl Acad. Sci. USA 72, 3111-3113. (doi:10.1073/pnas.72.8.3111)
6. Peters, R. & Cherry, R. J. 1982 Lateral and rotational diffusion of bacteriorhodopsin in lipid bilayers - experimental test of the Saffman-Delbruck equations. Proc. Natl Acad. Sci. USA 79, 4317-4321. (doi:10.1073/pnas.79.14. 4317)
7. Scalettar, B. A., Abney, J. R. & Owicki, J. C. 1988 Theoretical comparison of the self-diffusion and mutual diffusion of interacting membrane-proteins. Proc. Natl Acad. Sci. USA 85, 6726-6730. (doi:10.1073/pnas. 85.18.6726)
8. Abney, J. R., Scalettar, B. A. & Owicki, J. C. 1989 Self-diffusion of interacting membrane-proteins. Biophys. J. 55, 817-833. (doi:10.1016/S0006- 3495(89)82882-6)
9. Batchelor, G. K. 1976 Brownian diffusion of particles with hydrodynamic interaction. J. Fluid Mech. 74, 1-29. (doi:10.1017/S0022112076001663)
10. Abney, J. R., Scalettar, B. A. & Owicki, J. C. 1989 Mutual diffusion of interacting membrane-proteins. Biophys. J. 56, 315-326. (doi:10.1016/S0006- 3495(89)82678-5)
11. Pink, D. A. 1985 Protein lateral movement in lipid bilayers - stimulation studies of its dependence upon protein-concentration. Biochim. Biophys. Acta 818, 200-204.
12. Saxton, M. J. 1987 Lateral diffusion in an archipelago - the effect of mobile obstacles. Biophys. J. 52, 989-997. (doi:10.1016/S0006-3495(87)83291-5)
13. Bussell, S. J., Koch, D. L. & Hammer, D. A. 1992 The resistivity and mobility functions for a model system of 2 equal-sized proteins in a lipid bilayer. J. Fluid Mech. 243, 679-697. (doi:10.1017/S002211209200288X)
14. Bussell, S. J., Hammer, D. A. & Koch, D. L. 1994 The effect of hydrodynamic interactions on the tracer and gradient diffusion of integral membrane-proteins in lipid bilayers. J. Fluid Mech. 258, 167-190. (doi:10.1017/S0022112094003289)
15. Bussell, S. J., Koch, D. L. & Hammer, D. A. 1995 Effect of hydrodynamic interactions on the diffusion of integral membrane-proteins - tracer diffusion in organelle and reconstituted membranes. Biophys. J. 68, 1828-1835. (doi:10.1016/S0006-3495(95)80359-0)
16. Deverall, M. A., Gindl, E., Sinner, E. K., Besir, H., Ruehe, J., Saxton, M. J. & Naumann, C. A. 2005 Membrane lateral mobility obstructed by polymer-tethered lipids studied at the single molecule level. Biophys. J. 88, 1875-1886. (doi:10.1529/biophysj.104.050559)
17. Soong, R. & Macdonald, P. M. 2005 Lateral diffusion of peg-lipid in magnetically aligned bicelles measured using stimulated echo pulsed field gradient 1 h NMR. Biophys. J. 88, 255-268. (doi:10.1529/biophysj.104.043620)
18. Albertorio, F., Diaz, A. J., Yang, T., Chapa, V. A., Kataoka, S., Castellana, E. T. & Cremer, P. S. 2005 Fluid and air-stable lipopolymer membranes for biosensor applications. Langmuir 21, 7476-7482. (doi:10.1021/la050871s)
19. Low, M. G. & Saltiel, A. R. 1988 Structural and functional roles of glycosyl-phosphatidylinositol in membranes. Science 239, 268-275. (doi:10.1126/science.3276003)
20. Allen, T. M., Hansen, C., Martin, F., Redemann, C. & Yauyoung, A. 1991 Liposomes containing synthetic lipid derivatives of poly(ethylene glycol) show prolonged circulation half-lives in vivo. Biochim. Biophys. Acta 1066, 29-36.
21. Vermette, P. & Meagher, L. 2003 Interactions of phospholipid- and poly(ethylene glycol)-modified surfaces with biological systems: relation to physico-chemical properties and mechanisms. Colloids Surf. B 28, 153-198. (doi:10.1016/S0927-7765(02)00160-1) (Pubitemid 36287176)
22. Albertorio, F., Daniel, S. & Cremer, P. S. 2006 Supported lipopolymer membranes as nanoscale filters: simultaneous protein recognition and size-selection assays. J. Am. Chem. Soc. 128, 7168-7169. (doi:10.1021/ja062010r)
23. Tanakan, M. & Sackmann, E. 2005 Polymer-supported membranes as models of the cell surface. Nature 437, 656-663.
24. Albersdorfer, A., Feder, T. & Sackmann, E. 1997 Adhesion-induced domain formation by interplay of long-range repulsion and short-range attraction force: a model membrane study. Biophys. J. 73, 245-257. (doi:10.1016/S0006- 3495(97)78065-2)
25. Jeppesen, C., Wong, J. Y., Kuhl, T. L., Israelachvili, J. N., Mullah, N., Zalipsky, S. & Marques, C. M. 2001 Impact of polymer tether length on multiple ligand-receptor bond formation. Science 293, 465-468. (doi:10.1126/science.293.5529.465)
26. Chen, Y., Lagerholm, B., Yang, B. & Jacobson, K. 2006 Methods to measure the lateral diffusion of membrane lipids and proteins. Methods 39, 147-153. (doi:10.1016/j.ymeth.2006.05.008)
27. Axelrod, D., Koppel, D. E., Schlessinger, J., Elson, E. & Webb, W. W. 1976 Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys. J. 16, 1055-1069. (doi:10.1016/S0006-3495(76)85755-4)
28. Chary, S. R. & Jain, R. K. 1989 Direct measurement of interstitial convection and diffusion of albumin in normal and neoplastic tissues by fluorescence photobleaching. Proc. Natl Acad. Sci. USA 86, 5385-5389. (doi:10.1073/pnas.86.14.5385)
29. Boxer, S. G. 2000 Molecular transport and organization in supported lipid membranes. Curr. Opin. Chem. Biol. 4, 704-709. (doi:10.1016/S1367-5931(00) 00139-3)
30. Phair, R. D. & Misteli, T. 2000 High mobility of proteins in the mammalian cell nucleus. Nature 404, 604-609.
31. Reits, E. A. J. & Neefjes, J. J. 2001 From fixed to frap: measuring protein mobility and activity in living cells. Nat. Cell Biol. 3, E145-E147. (doi:10.1038/35078615)
32. Lippincott-Schwartz, J., Altan-Bonnet, N. & Patterson, G. H. 2003 Photobleaching and photoactivation: following protein dynamics in living cells. Nat. Rev. Mol. Cell Biol. 5, S7-S14.
33. Owen, M. D., Williamson, D., Rentero, C. & Gaus, K. 2009 Quantitative microscopy: protein dynamics and membrane organisation. Traffic 10, 962-971. (doi:10.1111/j.1600-0854.2009.00908.x)
34. Shav-Tal, Y., Darzacq, X., Shenoy, S. M., Fusco, D., Janicki, S. M., Spector, D. L. & Singer, R. H. 2004 Dynamics of single mrnps in nuclei of living cells. Science 304, 1797-1800. (doi:10.1126/science.1099754)
35. Giese, B. et al. 2003 Long term association of the cytokine receptor gp130 and the janus kinase jak1 revealed by frap analysis. J. Biol. Chem. 278, 39 205-39 213. (doi:10.1074/jbc.M303347200)
36. Dorsch, S., Klotz, K. N., Engelhardt, S., Lohse, M. J. & Bunemann, M. 2009 Analysis of receptor oligomerization by frap microscopy. Nature Methods 6, 225-230. (doi:10.1038/nmeth.1304)
37. Phair, R. D. & Misteli, T. 2001 Kinetic modelling approaches to in vivo imaging. Nat. Rev. Mol. Cell Biol. 2, 898-907. (doi:10.1038/35103000)
38. Sprague, B. L. & McNally, J. G. 2005 Frap analysis of binding: proper and fitting. Trends Cell Biol. 15, 84-91. (doi:10.1016/j.tcb.2004.12.001)
39. Mueller, F., Wach, P. & McNally, J. G. 2008 Evidence for a common mode of transcription factor interaction with chromatin as revealed by improved quantitative fluorescence recovery after photobleaching. Biophys. J. 94, 3323-3339. (doi:10.1529/biophysj.107.123182)
40. Weiss, M. 2004 Challenges and artifacts in quantitative photobleaching experiments. Traffic 5, 662-671. (doi:10.1111/j.1600-0854.2004.00215.x) (Pubitemid 39199130)
41. Dushek, O. & Coombs, D. 2008 Improving parameter estimation for cell surface frap data. J. Biochem. Biophys. Meth. 70, 1224-1231. (doi:10.1016/j.jbbm.2007.07.002)
42. Soumpasis, D. M. 1983 Theoretical analysis of fluorescence photobleaching recovery experiments. Biophys. J. 41, 95-97. (doi:10.1016/S0006-3495(83)84410- 5)
43. Seiffert, S. & Oppermann, W. 2005 Systematic evaluation of frap experiments performed in a confocal laser scanning microscope. J. Microscopy 220, 20-30. (doi:10.1111/j.1365-2818.2005.01512.x)
44. Ellenberg, J., Siggia, E. D., Moreira, J. E., Smith, C. L., Presley, J. F., Worman, H. J. & Lippincott-Schwartz, J. 1997 Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis. J. Cell Biol. 138, 1193-1206. (doi:10.1083/jcb.138.6. 1193)
45. Jonsson, P., Jonsson, M. P., Tegenfeldt, J. O. & Hook, F. 2008 A method improving the accuracy of fluorescence recovery after photobleaching analysis. Biophys. J. 95, 5334-5348. (doi:10.1529/biophysj.108.134874)
46. Phair, R. D., Gorski, S. A. & Misteli, T. 2004 Measurement of dynamic protein binding to chromatin in vivo, using photobleaching microscopy. In Chromatin and chromatin remodeling enzymes, Pt A, vol. 375, Methods in enzymology, pp. 393-414. San Diego, CA: Academic Press.
47. Endress, E., Weigelt, S., Reents, G. & Bayerl, T. M. 2005 Derivation of a closed form analytical expression for fluorescence recovery after photo bleaching in the case of continuous bleaching during read out. Eur. Phys. J. E 16, 81-87. (doi:10.1140/epje/e2005-00010-5)
48. Ren, C. L., Nap, R. J. & Szleifer, I. 2008 The role of hydrogen bonding in tethered polymer layers. J. Phys. Chem. B 112, 16 238-16 248. (doi:10.1021/jp8080904)
49. Groves, J. T. & Boxer, S. G. 1995 Electric field-induced concentration gradients in planar supported bilayers. Biophys. J. 69, 1972-1975. (doi:10.1016/S0006-3495(95)80067-6)
50. van Oostveldt, P. & Bauwens, S. 1990 Quantitative fluorescence in confocal microscopy: the effect of the detection pinhole aperture on the re-absorption and inner filter phenomena. J. Microscopy 158, 121-132.
51. Herman, B. 1998 Fluorescence microscopy. Oxford, UK: Bios Scientific Publishers.
52. Kang, M., Day, C. A., Drake, K., Kenworthy, A. K. & DiBenedetto, E. 2009 A generalization of theory for two-dimensional fluorescence recovery after photobleaching applicable to confocal laser scanning microscopes. Biophys. J. 97, 1501-1511. (doi:10.1016/j.bpj.2009.06.017)
53. Widengreny, J. & Rigler, R. 1996 Mechanisms of photo-bleaching investigated by fluorescence correlation spectroscopy. Bioimaging 4, 149-157.
54. Rabut, G. & Ellenberg, J. 2004 Live cell imaging, a laboratory manual: photobleaching techniques to study mobility and molecular dynamics of proteins in live cells: FRAP, iFRAP and FLIP. Ann Arbor, MI: Cold Spring Harbor Laboratory Press.
55. Peters, R., Brunger, A. & Schulten, K. 1981 Continuous fluorescence microphotolysis - a sensitive method for study of diffusion-processes in single cells. Proc. Natl Acad. Sci. USA 78, 962-966. (doi:10.1073/pnas.78.2.962)
56. Kam, L. & Boxer, S. G. 2001 Cell adhesion to protein-micropatterned- supported lipid bilayer membranes. J. Biomed. Mater. Res. 55, 487-495. (doi:10.1002/1097-4636(20010615)55:4〈487::AID-JBM1041〉3.0.CO;2-7)
57. Kaufmann, S., Papastavrou, G., Kumar, K., Textor, M. & Reimhult, E. 2009 A detailed investigation of the formation kinetics and layer structure of poly(ethylene glycol) tether supported lipid bilayers. Soft Matter 5, 2804-2814. (doi:10.1039/b901874c)
58. Irrechukwu, O. N. & Levenston, M. E. 2009 Improved estimation of solute diffusivity through numerical analysis of frap experiments. Cell. Mol. Bioeng. 2, 104-117. (doi:10.1007/s12195-009-0042-1)
59. Bevington, P. R. & Robinson, D. K. 2002 Data reduction and error analysis for the physical sciences, 3rd edn. London, UK: McGraw-Hill.
60. de Gennes, P. G. 1980 Conformations of polymers attached to an interface. Macromolecules 13, 1069-1075. (doi:10.1021/ma60077a009)
61. Hristova, K., Kenworthy, A. & McIntosh, T. 1995 Effect of bilayer composition on the phase behavior of liposomal suspensions containing poly(ethylene glycol)-lipids. Macromolecules 28, 7693-7699. (doi:10.1021/ ma00127a015)
62. Nagle, J. F. & Tristram-Nagle, S. 2000 Lipid bilayer structure. Curr. Opin. Struct. Biol. 10, 474-480. (doi:10.1016/S0959-440X(00)00117-2)
63. Przybylo, M., Sykora, J., Humpolickova, J., Benda, A., Zan, A. & Hof, M. 2006 Lipid diffusion in giant unilamellar vesicles is more than 2 times faster than in supported phospholipid bilayers under identical conditions. Langmuir 22, 9096-9099. (doi:10.1021/la061934p)
64. Scomparin, C., Lecuyer, S., Ferreira, M., Charitat, T. & Tinland, B. 2009 Diffusion in supported lipid bilayers: influence of substrate and preparation technique on the internal dynamics. Eur. Phys. J. E 28, 211-220. (doi:10.1140/epje/i2008-10407-3)
65. Seu, K. J., Cambrea, L. R., Everly, R. M. & Hovis, J. S. 2006 Influence of lipid chemistry on membrane fluidity: tail and headgroup interactions. Biophys. J. 91, 3727-3735. (doi:10.1529/biophysj.106.084590)
66. Seu, K. J., Pandey, A. P., Haque, F., Proctor, E. A., Ribbe, A. E. & Hovis, J. S. 2007 Effect of surface treatment on diffusion and domain formation in supported lipid bilayers. Biophys. J. 92, 2445-2450. (doi:10.1529/biophysj. 106.099721)
67. Lis, L. J., Mcalister, M., Fuller, N., Rand, R. P. & Parsegian, V. A. 1982 Interactions between neutral phospholipid-bilayer membranes. Biophys. J. 37, 657-665.
68. Marsh, D. 1990 Handbook of lipid bilayers. Boca Raton, FL: CRC Press.
69. Ishii, C. Y. & Boxer, S. G. 2006 Controlling two-dimensional tethered vesicle motion using an electric field: interplay of electrophoresis and electro-osmosis. Langmuir 22, 2384-2391.
70. Evans, E. & Sackmann, E. 1988 Translational and rotational drag coefficients for a disk moving in a liquid membrane-associated with a rigid substrate. J. Fluid Mech. 194, 553-561. (doi:10.1017/S0022112088003106)
71. Kuhner, M., Tampe, R. & Sackmann, E. 1994 Lipid monolayer and bilayer supported on polymer-films - composite polymer-lipid films on solid substrates. Biophys. J. 67, 217-226. (doi:10.1016/S0006-3495(94)80472-2)
72. Tanaka, M., Hermann, J., Haase, I., Fischer, M. & Boxer, S. G. 2007 Frictional drag and electrical manipulation of recombinant proteins in polymer-supported membranes. Langmuir 23, 5638-5644. (doi:10.1021/la0628219)