Abstract
In this paper a two-state, two-component, Ising-type model is used to simulate the lateral distribution of the components and gel/fluid state acyl chains in dimyristoylphosphatidylcholine/distearoylphosphatidylcholine (DMPC/DSPC) lipid bilayers. The same model has been successful in calculating the excess heat capacity curves, the fluorescence recovery after photobleaching (FRAP) threshold temperatures, the most frequent center-to-center distances between DSPC clusters, and the fractal dimensions of gel clusters (Sugar, I. P., T. E. Thompson, and R. L. Biltonen, 1999. Biophys. J. 76:2099-2110). Depending on the temperature and mole fraction the population of the cluster size is either homogeneous or inhomogeneous. In the inhomogeneous population the size of the largest cluster scales with the size of the system, while the rest of the clusters remain small with increasing system size. In a homogeneous population, however, every cluster remains small with increasing system size. For both compositional and fluid/gel state clusters, threshold temperatures-the so-called percolation threshold temperatures-are determined where change in the type of the population takes place. At a given mole fraction, the number of percolation threshold temperatures can be 0, 1, 2, or 3. By plotting these percolation threshold temperatures on the temperature/mole fraction plane, the diagrams of component and state separation of DMPC/DSPC bilayers are constructed. In agreement with the small-angle neutron scattering measurements, the component separation diagram shows nonrandom lateral distribution of the components not only in the gel-fluid mixed phase region, but also in the pure gel and pure fluid regions. A combined diagram of component and state separation is constructed to characterize the lateral distribution of lipid components and gel/fluid state acyl chains in DMPC/DSPC mixtures. While theoretical phase diagrams of two component mixtures can be constructed only in the case of first-order transitions, state and component separation diagrams can be constructed whether or not the system is involved in first-order transition. The effects of interchain interactions on the component and state separation diagrams are demonstrated on three different models. The influences of state and component separation on the in-plane and off-plane membrane reactions are discussed.
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- Bagatolli L. A., Gratton E. A correlation between lipid domain shape and binary phospholipid mixture composition in free standing bilayers: A two-photon fluorescence microscopy study. Biophys J. 2000 Jul;79(1):434–447. doi: 10.1016/S0006-3495(00)76305-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bagatolli L. A., Gratton E. Two photon fluorescence microscopy of coexisting lipid domains in giant unilamellar vesicles of binary phospholipid mixtures. Biophys J. 2000 Jan;78(1):290–305. doi: 10.1016/S0006-3495(00)76592-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown D. A., London E. Structure and origin of ordered lipid domains in biological membranes. J Membr Biol. 1998 Jul 15;164(2):103–114. doi: 10.1007/s002329900397. [DOI] [PubMed] [Google Scholar]
- Brumbaugh E. E., Huang C. Parameter estimation in binary mixtures of phospholipids. Methods Enzymol. 1992;210:521–539. doi: 10.1016/0076-6879(92)10027-b. [DOI] [PubMed] [Google Scholar]
- Brumbaugh E. E., Johnson M. L., Huang C. H. Non-linear least squares analysis of phase diagrams for non-ideal binary mixtures of phospholipids. Chem Phys Lipids. 1990 Jan;52(2):69–78. doi: 10.1016/0009-3084(90)90152-h. [DOI] [PubMed] [Google Scholar]
- Brumm T., Jørgensen K., Mouritsen O. G., Bayerl T. M. The effect of increasing membrane curvature on the phase transition and mixing behavior of a dimyristoyl-sn-glycero-3-phosphatidylcholine/ distearoyl-sn-glycero-3-phosphatidylcholine lipid mixture as studied by Fourier transform infrared spectroscopy and differential scanning calorimetry. Biophys J. 1996 Mar;70(3):1373–1379. doi: 10.1016/S0006-3495(96)79695-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dibble A. R., Hinderliter A. K., Sando J. J., Biltonen R. L. Lipid lateral heterogeneity in phosphatidylcholine/phosphatidylserine/diacylglycerol vesicles and its influence on protein kinase C activation. Biophys J. 1996 Oct;71(4):1877–1890. doi: 10.1016/S0006-3495(96)79387-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Evans E., Kwok R. Mechanical calorimetry of large dimyristoylphosphatidylcholine vesicles in the phase transition region. Biochemistry. 1982 Sep 28;21(20):4874–4879. doi: 10.1021/bi00263a007. [DOI] [PubMed] [Google Scholar]
- Glaser M., Wanaski S., Buser C. A., Boguslavsky V., Rashidzada W., Morris A., Rebecchi M., Scarlata S. F., Runnels L. W., Prestwich G. D. Myristoylated alanine-rich C kinase substrate (MARCKS) produces reversible inhibition of phospholipase C by sequestering phosphatidylinositol 4,5-bisphosphate in lateral domains. J Biol Chem. 1996 Oct 18;271(42):26187–26193. doi: 10.1074/jbc.271.42.26187. [DOI] [PubMed] [Google Scholar]
- Gliss C., Clausen-Schaumann H., Günther R., Odenbach S., Randl O., Bayerl T. M. Direct detection of domains in phospholipid bilayers by grazing incidence diffraction of neutrons and atomic force microscopy. Biophys J. 1998 May;74(5):2443–2450. doi: 10.1016/S0006-3495(98)77952-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heimburg T. A model for the lipid pretransition: coupling of ripple formation with the chain-melting transition. Biophys J. 2000 Mar;78(3):1154–1165. doi: 10.1016/S0006-3495(00)76673-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hui S. W. The tilting of the hydrocarbon chains in a single bilayer of phospholipid. Chem Phys Lipids. 1976 Feb;16(1):9–18. doi: 10.1016/0009-3084(76)90011-6. [DOI] [PubMed] [Google Scholar]
- Hui S. W., Viswanathan R., Zasadzinski J. A., Israelachvili J. N. The structure and stability of phospholipid bilayers by atomic force microscopy. Biophys J. 1995 Jan;68(1):171–178. doi: 10.1016/S0006-3495(95)80172-4. [DOI] [PMC free article] [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]
- Hønger T., Jørgensen K., Biltonen R. L., Mouritsen O. G. Systematic relationship between phospholipase A2 activity and dynamic lipid bilayer microheterogeneity. Biochemistry. 1996 Jul 16;35(28):9003–9006. doi: 10.1021/bi960866a. [DOI] [PubMed] [Google Scholar]
- Ipsen J. H., Mouritsen O. G. Modelling the phase equilibria in two-component membranes of phospholipids with different acyl-chain lengths. Biochim Biophys Acta. 1988 Oct 6;944(2):121–134. doi: 10.1016/0005-2736(88)90425-7. [DOI] [PubMed] [Google Scholar]
- Jan N., Lookman T., Pink D. A. On computer simulation methods used to study models of two-component lipid bilayers. Biochemistry. 1984 Jul 3;23(14):3227–3231. doi: 10.1021/bi00309a017. [DOI] [PubMed] [Google Scholar]
- Janiak M. J., Small D. M., Shipley G. G. Temperature and compositional dependence of the structure of hydrated dimyristoyl lecithin. J Biol Chem. 1979 Jul 10;254(13):6068–6078. [PubMed] [Google Scholar]
- Jørgensen K., Sperotto M. M., Mouritsen O. G., Ipsen J. H., Zuckermann M. J. Phase equilibria and local structure in binary lipid bilayers. Biochim Biophys Acta. 1993 Oct 10;1152(1):135–145. doi: 10.1016/0005-2736(93)90240-z. [DOI] [PubMed] [Google Scholar]
- Kapitza H. G., Rüppel D. A., Galla H. J., Sackmann E. Lateral diffusion of lipids and glycophorin in solid phosphatidylcholine bilayers. The role of structural defects. Biophys J. 1984 Mar;45(3):577–587. doi: 10.1016/S0006-3495(84)84195-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knoll W., Ibel K., Sackmann E. Small-angle neutron scattering study of lipid phase diagrams by the contrast variation method. Biochemistry. 1981 Oct 27;20(22):6379–6383. doi: 10.1021/bi00525a015. [DOI] [PubMed] [Google Scholar]
- Koynova R., Caffrey M. Phases and phase transitions of the phosphatidylcholines. Biochim Biophys Acta. 1998 Jun 29;1376(1):91–145. doi: 10.1016/s0304-4157(98)00006-9. [DOI] [PubMed] [Google Scholar]
- Langlet C., Bernard A. M., Drevot P., He H. T. Membrane rafts and signaling by the multichain immune recognition receptors. Curr Opin Immunol. 2000 Jun;12(3):250–255. doi: 10.1016/s0952-7915(00)00084-4. [DOI] [PubMed] [Google Scholar]
- Leidy C., Wolkers W. F., Jørgensen K., Mouritsen O. G., Crowe J. H. Lateral organization and domain formation in a two-component lipid membrane system. Biophys J. 2001 Apr;80(4):1819–1828. doi: 10.1016/S0006-3495(01)76152-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lu D., Vavasour I., Morrow M. R. Smoothed acyl chain orientational order parameter profiles in dimyristoylphosphatidylcholine-distearoylphosphatidylcholine mixtures: a 2H-NMR study. Biophys J. 1995 Feb;68(2):574–583. doi: 10.1016/S0006-3495(95)80219-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mabrey S., Sturtevant J. M. Investigation of phase transitions of lipids and lipid mixtures by sensitivity differential scanning calorimetry. Proc Natl Acad Sci U S A. 1976 Nov;73(11):3862–3866. doi: 10.1073/pnas.73.11.3862. [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]
- Mendelsohn R., Maisano J. Use of deuterated phospholipids in Raman spectroscopic studies of membrane structure. I. Multilayers of dimyristoyl phosphatidylcholine (and its -d54 derivative) with distearoyl phosphatidylcholine. Biochim Biophys Acta. 1978 Jan 19;506(2):192–201. doi: 10.1016/0005-2736(78)90390-5. [DOI] [PubMed] [Google Scholar]
- Mouritsen O. G., Jørgensen K. Small-scale lipid-membrane structure: simulation versus experiment. Curr Opin Struct Biol. 1997 Aug;7(4):518–527. doi: 10.1016/s0959-440x(97)80116-9. [DOI] [PubMed] [Google Scholar]
- Mukherjee S., Soe T. T., Maxfield F. R. Endocytic sorting of lipid analogues differing solely in the chemistry of their hydrophobic tails. J Cell Biol. 1999 Mar 22;144(6):1271–1284. doi: 10.1083/jcb.144.6.1271. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Muresan A. S., Diamant H., Lee K. Y. Effect of temperature and composition on the formation of nanoscale compartments in phospholipid membranes. J Am Chem Soc. 2001 Jul 18;123(28):6951–6952. doi: 10.1021/ja015792r. [DOI] [PubMed] [Google Scholar]
- Norris V., Madsen M. S. Autocatalytic gene expression occurs via transertion and membrane domain formation and underlies differentiation in bacteria: a model. J Mol Biol. 1995 Nov 10;253(5):739–748. doi: 10.1006/jmbi.1995.0587. [DOI] [PubMed] [Google Scholar]
- Pedersen S., Jørgensen K., Baekmark T. R., Mouritsen O. G. Indirect evidence for lipid-domain formation in the transition region of phospholipid bilayers by two-probe fluorescence energy transfer. Biophys J. 1996 Aug;71(2):554–560. doi: 10.1016/S0006-3495(96)79279-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Piknová B., Marsh D., Thompson T. E. Fluorescence-quenching study of percolation and compartmentalization in two-phase lipid bilayers. Biophys J. 1996 Aug;71(2):892–897. doi: 10.1016/S0006-3495(96)79291-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Proceedings of the Fogarty International Center Conference on Domain Organization in Biological Membranes. 2-4 March 1994. Mol Membr Biol. 1995 Jan-Mar;12(1):1–162. [PubMed] [Google Scholar]
- Sankaram M. B., Marsh D., Thompson T. E. Determination of fluid and gel domain sizes in two-component, two-phase lipid bilayers. An electron spin resonance spin label study. Biophys J. 1992 Aug;63(2):340–349. doi: 10.1016/S0006-3495(92)81619-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sankaram M. B., Thompson T. E. Deuterium magnetic resonance study of phase equilibria and membrane thickness in binary phospholipid mixed bilayers. Biochemistry. 1992 Sep 8;31(35):8258–8268. doi: 10.1021/bi00150a020. [DOI] [PubMed] [Google Scholar]
- Scheiffele P., Rietveld A., Wilk T., Simons K. Influenza viruses select ordered lipid domains during budding from the plasma membrane. J Biol Chem. 1999 Jan 22;274(4):2038–2044. doi: 10.1074/jbc.274.4.2038. [DOI] [PubMed] [Google Scholar]
- Schram V., Lin H. N., Thompson T. E. Topology of gel-phase domains and lipid mixing properties in phase-separated two-component phosphatidylcholine bilayers. Biophys J. 1996 Oct;71(4):1811–1822. doi: 10.1016/S0006-3495(96)79382-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simons K., Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol. 2000 Oct;1(1):31–39. doi: 10.1038/35036052. [DOI] [PubMed] [Google Scholar]
- Sugár I. P., Biltonen R. L. Structure-function relationships in two-component phospholipid bilayers: Monte Carlo simulation approach using a two-state model. Methods Enzymol. 2000;323:340–372. doi: 10.1016/s0076-6879(00)23373-9. [DOI] [PubMed] [Google Scholar]
- Sugár I. P., Michonova-Alexova E., Chong P. L. Geometrical properties of gel and fluid clusters in DMPC/DSPC bilayers: Monte Carlo simulation approach using a two-state model. Biophys J. 2001 Nov;81(5):2425–2441. doi: 10.1016/s0006-3495(01)75890-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sugár I. P., Monticelli G. Interrelationships between the phase diagrams of the two-component phospholipid bilayers. Biophys J. 1985 Aug;48(2):283–288. doi: 10.1016/S0006-3495(85)83781-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sugár I. P., Thompson T. E., Biltonen R. L. Monte Carlo simulation of two-component bilayers: DMPC/DSPC mixtures. Biophys J. 1999 Apr;76(4):2099–2110. doi: 10.1016/S0006-3495(99)77366-2. [DOI] [PMC free article] [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., Melo E. C., Thompson T. E. Translational diffusion and fluid domain connectivity in a two-component, two-phase phospholipid bilayer. Biophys J. 1989 Nov;56(5):869–876. doi: 10.1016/S0006-3495(89)82733-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Verkade P., Simons K. Robert Feulgen Lecture 1997. Lipid microdomains and membrane trafficking in mammalian cells. Histochem Cell Biol. 1997 Sep;108(3):211–220. doi: 10.1007/s004180050161. [DOI] [PubMed] [Google Scholar]
- Welby M., Poquet Y., Tocanne J. F. The spatial distribution of phospholipids and glycolipids in the membrane of the bacterium Micrococcus luteus varies during the cell cycle. FEBS Lett. 1996 Apr 15;384(2):107–111. doi: 10.1016/0014-5793(96)00278-5. [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]
- Wilkinson D. A., Nagle J. F. Dilatometric study of binary mixtures of phosphatidylcholines. Biochemistry. 1979 Sep 18;18(19):4244–4249. doi: 10.1021/bi00586a032. [DOI] [PubMed] [Google Scholar]
- Yang L., Glaser M. Formation of membrane domains during the activation of protein kinase C. Biochemistry. 1996 Nov 5;35(44):13966–13974. doi: 10.1021/bi9610008. [DOI] [PubMed] [Google Scholar]
- van Dijck P. W., Kaper A. J., Oonk H. A., de Gier J. Miscibility properties of binary phosphatidylcholine mixtures. A calorimetric study. Biochim Biophys Acta. 1977 Oct 3;470(1):58–69. doi: 10.1016/0005-2736(77)90061-x. [DOI] [PubMed] [Google Scholar]
- von Dreele P. H. Estimation of lateral species separation from phase transitions in nonideal two-dimensional lipid mixtures. Biochemistry. 1978 Sep 19;17(19):3939–3943. doi: 10.1021/bi00612a009. [DOI] [PubMed] [Google Scholar]