Abstract
We examined the consequences of membrane heterogeneity for the association of a simple amphiphilic molecule with phospholipid vesicles with solid-liquid and liquid-liquid phase coexistence. To address this problem we studied the association of a single-chain, fluorescent amphiphile with dimyristoylphosphatidylcholine (DMPC) vesicles containing varying amounts of cholesterol. DMPC bilayers containing 15 mol% cholesterol show a region of solid-liquid-ordered (s-l(o)) coexistence below the T(m) of pure DMPC (23.9 degrees C) and a region of liquid-disordered-liquid-ordered coexistence (l(d)-l(o)) above the T(m). We first examined equilibrium binding and kinetics of amphiphile insertion into single-phase vesicles (s, l(d), and l(o) phase). The data obtained were then used to predict the behavior of the equivalent process in a two-phase system, taking into account the fractions of phases present. Next, the predicted kinetics were compared to experimental kinetics obtained from a two-phase system. We found that association of the amphiphile with lipid vesicles is not influenced by the existence of l(d)-l(o) phase boundaries but occurs much more slowly in the s-l(o) phase coexistence region than expected on the basis of phase composition.
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- Almeida P. F. Lipid transfer between vesicles: effect of high vesicle concentration. Biophys J. 1999 Apr;76(4):1922–1928. doi: 10.1016/S0006-3495(99)77351-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Almeida P. F., Vaz W. L., Thompson T. E. Lateral diffusion and percolation in two-phase, two-component lipid bilayers. Topology of the solid-phase domains in-plane and across the lipid bilayer. Biochemistry. 1992 Aug 11;31(31):7198–7210. doi: 10.1021/bi00146a024. [DOI] [PubMed] [Google Scholar]
- Almeida P. F., Vaz W. L., Thompson T. E. Lateral diffusion in the liquid phases of dimyristoylphosphatidylcholine/cholesterol lipid bilayers: a free volume analysis. Biochemistry. 1992 Jul 28;31(29):6739–6747. doi: 10.1021/bi00144a013. [DOI] [PubMed] [Google Scholar]
- Brown D. A., Rose J. K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 1992 Feb 7;68(3):533–544. doi: 10.1016/0092-8674(92)90189-j. [DOI] [PubMed] [Google Scholar]
- Bäuerle H. D., Seelig J. Interaction of charged and uncharged calcium channel antagonists with phospholipid membranes. Binding equilibrium, binding enthalpy, and membrane location. Biochemistry. 1991 Jul 23;30(29):7203–7211. doi: 10.1021/bi00243a023. [DOI] [PubMed] [Google Scholar]
- Clerc S. G., Thompson T. E. Permeability of dimyristoyl phosphatidylcholine/dipalmitoyl phosphatidylcholine bilayer membranes with coexisting gel and liquid-crystalline phases. Biophys J. 1995 Jun;68(6):2333–2341. doi: 10.1016/S0006-3495(95)80415-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Corvera E., Mouritsen O. G., Singer M. A., Zuckermann M. J. The permeability and the effect of acyl-chain length for phospholipid bilayers containing cholesterol: theory and experiment. Biochim Biophys Acta. 1992 Jun 30;1107(2):261–270. doi: 10.1016/0005-2736(92)90413-g. [DOI] [PubMed] [Google Scholar]
- Cruzeiro-Hansson L., Mouritsen O. G. Passive ion permeability of lipid membranes modelled via lipid-domain interfacial area. Biochim Biophys Acta. 1988 Sep 15;944(1):63–72. doi: 10.1016/0005-2736(88)90316-1. [DOI] [PubMed] [Google Scholar]
- De Young L. R., Dill K. A. Solute partitioning into lipid bilayer membranes. Biochemistry. 1988 Jul 12;27(14):5281–5289. doi: 10.1021/bi00414a050. [DOI] [PubMed] [Google Scholar]
- Duckwitz-peterlein G., Eilenberger G., Overath P. Phospholipid exchange between bilayer membranes. Biochim Biophys Acta. 1977 Sep 19;469(3):311–325. doi: 10.1016/0005-2736(77)90167-5. [DOI] [PubMed] [Google Scholar]
- Edidin M. Lipid microdomains in cell surface membranes. Curr Opin Struct Biol. 1997 Aug;7(4):528–532. doi: 10.1016/s0959-440x(97)80117-0. [DOI] [PubMed] [Google Scholar]
- Hong-wei S., McConnell H. Phase separations in phospholipd membranes. Biochemistry. 1975 Feb 25;14(4):847–854. doi: 10.1021/bi00675a032. [DOI] [PubMed] [Google Scholar]
- Huang C. H., Charlton J. P. Interactions of phosphatidylcholine vesicles with 2-p-toluidinylnaphthalene-6-sulfonate. Biochemistry. 1972 Feb 29;11(5):735–740. doi: 10.1021/bi00755a010. [DOI] [PubMed] [Google Scholar]
- Hwang J., Gheber L. A., Margolis L., Edidin M. Domains in cell plasma membranes investigated by near-field scanning optical microscopy. Biophys J. 1998 May;74(5):2184–2190. doi: 10.1016/S0006-3495(98)77927-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ipsen J. H., Karlström G., Mouritsen O. G., Wennerström H., Zuckermann M. J. Phase equilibria in the phosphatidylcholine-cholesterol system. Biochim Biophys Acta. 1987 Nov 27;905(1):162–172. doi: 10.1016/0005-2736(87)90020-4. [DOI] [PubMed] [Google Scholar]
- Jacobs R. E., White S. H. The nature of the hydrophobic binding of small peptides at the bilayer interface: implications for the insertion of transbilayer helices. Biochemistry. 1989 Apr 18;28(8):3421–3437. doi: 10.1021/bi00434a042. [DOI] [PubMed] [Google Scholar]
- Jones J. D., Thompson T. E. Mechanism of spontaneous, concentration-dependent phospholipid transfer between bilayers. Biochemistry. 1990 Feb 13;29(6):1593–1600. doi: 10.1021/bi00458a034. [DOI] [PubMed] [Google Scholar]
- KAUZMANN W. Some factors in the interpretation of protein denaturation. Adv Protein Chem. 1959;14:1–63. doi: 10.1016/s0065-3233(08)60608-7. [DOI] [PubMed] [Google Scholar]
- Kenworthy A. K., Edidin M. Distribution of a glycosylphosphatidylinositol-anchored protein at the apical surface of MDCK cells examined at a resolution of <100 A using imaging fluorescence resonance energy transfer. J Cell Biol. 1998 Jul 13;142(1):69–84. doi: 10.1083/jcb.142.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kraayenhof R., Sterk G. J., Sang H. W. Probing biomembrane interfacial potential and pH profiles with a new type of float-like fluorophores positioned at varying distance from the membrane surface. Biochemistry. 1993 Sep 28;32(38):10057–10066. doi: 10.1021/bi00089a022. [DOI] [PubMed] [Google Scholar]
- Kurzchalia T. V., Hartmann E., Dupree P. Guilty by insolubility--does a protein's detergent insolubility reflect a caveolar location? Trends Cell Biol. 1995 May;5(5):187–189. doi: 10.1016/s0962-8924(00)88990-4. [DOI] [PubMed] [Google Scholar]
- Leikin S., Parsegian V. A., Rau D. C., Rand R. P. Hydration forces. Annu Rev Phys Chem. 1993;44:369–395. doi: 10.1146/annurev.pc.44.100193.002101. [DOI] [PubMed] [Google Scholar]
- Lisanti M. P., Scherer P. E., Tang Z., Sargiacomo M. Caveolae, caveolin and caveolin-rich membrane domains: a signalling hypothesis. Trends Cell Biol. 1994 Jul;4(7):231–235. doi: 10.1016/0962-8924(94)90114-7. [DOI] [PubMed] [Google Scholar]
- Marsh D., Watts A., Knowles P. F. Evidence for phase boundary lipid. Permeability of Tempo-choline into dimyristoylphosphatidylcholine vesicles at the phase transition. Biochemistry. 1976 Aug 10;15(16):3570–3578. doi: 10.1021/bi00661a027. [DOI] [PubMed] [Google Scholar]
- Mayor S., Maxfield F. R. Insolubility and redistribution of GPI-anchored proteins at the cell surface after detergent treatment. Mol Biol Cell. 1995 Jul;6(7):929–944. doi: 10.1091/mbc.6.7.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Melo E. C., Lourtie I. M., Sankaram M. B., Thompson T. E., Vaz W. L. Effects of domain connection and disconnection on the yields of in-plane bimolecular reactions in membranes. Biophys J. 1992 Dec;63(6):1506–1512. doi: 10.1016/S0006-3495(92)81735-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nichols J. W. Thermodynamics and kinetics of phospholipid monomer-vesicle interaction. Biochemistry. 1985 Nov 5;24(23):6390–6398. doi: 10.1021/bi00344a011. [DOI] [PubMed] [Google Scholar]
- Papahadjopoulos D., Jacobson K., Nir S., Isac T. Phase transitions in phospholipid vesicles. Fluorescence polarization and permeability measurements concerning the effect of temperature and cholesterol. Biochim Biophys Acta. 1973 Jul 6;311(3):330–348. doi: 10.1016/0005-2736(73)90314-3. [DOI] [PubMed] [Google Scholar]
- Sankaram M. B., Thompson T. E. Cholesterol-induced fluid-phase immiscibility in membranes. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8686–8690. doi: 10.1073/pnas.88.19.8686. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sankaram M. B., Thompson T. E. Interaction of cholesterol with various glycerophospholipids and sphingomyelin. Biochemistry. 1990 Nov 27;29(47):10670–10675. doi: 10.1021/bi00499a014. [DOI] [PubMed] [Google Scholar]
- Seelig J., Ganz P. Nonclassical hydrophobic effect in membrane binding equilibria. Biochemistry. 1991 Sep 24;30(38):9354–9359. doi: 10.1021/bi00102a031. [DOI] [PubMed] [Google Scholar]
- Simons K., Ikonen E. Functional rafts in cell membranes. Nature. 1997 Jun 5;387(6633):569–572. doi: 10.1038/42408. [DOI] [PubMed] [Google Scholar]
- Thompson T. E., Sankaram M. B., Biltonen R. L., Marsh D., Vaz W. L. Effects of domain structure on in-plane reactions and interactions. Mol Membr Biol. 1995 Jan-Mar;12(1):157–162. doi: 10.3109/09687689509038512. [DOI] [PubMed] [Google Scholar]
- Vaz W. L. Diffusion and chemical reactions in phase-separated membranes. Biophys Chem. 1994 May;50(1-2):139–145. doi: 10.1016/0301-4622(94)85026-7. [DOI] [PubMed] [Google Scholar]
- Vaz W. L. Percolation properties of two-component, two-phase phospholipid bilayers. Mol Membr Biol. 1995 Jan-Mar;12(1):39–43. doi: 10.3109/09687689509038493. [DOI] [PubMed] [Google Scholar]
- Vist M. R., Davis J. H. Phase equilibria of cholesterol/dipalmitoylphosphatidylcholine mixtures: 2H nuclear magnetic resonance and differential scanning calorimetry. Biochemistry. 1990 Jan 16;29(2):451–464. doi: 10.1021/bi00454a021. [DOI] [PubMed] [Google Scholar]
- Welti R., Glaser M. Lipid domains in model and biological membranes. Chem Phys Lipids. 1994 Sep 6;73(1-2):121–137. doi: 10.1016/0009-3084(94)90178-3. [DOI] [PubMed] [Google Scholar]
- White S. H., Wimley W. C., Ladokhin A. S., Hristova K. Protein folding in membranes: determining energetics of peptide-bilayer interactions. Methods Enzymol. 1998;295:62–87. doi: 10.1016/s0076-6879(98)95035-2. [DOI] [PubMed] [Google Scholar]
- Wimley W. C., Thompson T. E. Exchange and flip-flop of dimyristoylphosphatidylcholine in liquid-crystalline, gel, and two-component, two-phase large unilamellar vesicles. Biochemistry. 1990 Feb 6;29(5):1296–1303. doi: 10.1021/bi00457a027. [DOI] [PubMed] [Google Scholar]
- Wimley W. C., Thompson T. E. Transbilayer and interbilayer phospholipid exchange in dimyristoylphosphatidylcholine/dimyristoylphosphatidylethanolamine large unilamellar vesicles. Biochemistry. 1991 Feb 12;30(6):1702–1709. doi: 10.1021/bi00220a036. [DOI] [PubMed] [Google Scholar]
- Xiang T. X., Anderson B. D. Phase structures of binary lipid bilayers as revealed by permeability of small molecules. Biochim Biophys Acta. 1998 Mar 6;1370(1):64–76. doi: 10.1016/s0005-2736(97)00244-7. [DOI] [PubMed] [Google Scholar]
