Share This Article:

Curvature-driven lipid sorting: coarse-grained dynamics simulations of a membrane mimicking a hemifusion intermediate

Full-Text HTML Download Download as PDF (Size:3136KB) PP. 86-95
DOI: 10.4236/jbpc.2010.12011    3,660 Downloads   8,029 Views   Citations

ABSTRACT

How membrane curvature influences lipid distribution is under intensive research. In this short report, after a brief review of recent studies, the results of our coarse-grained (CG) molecular dynamics simulations of membranes with “hemifused ribbons” geometry are discussed. When membranes of a binary mixture of (dipalmitoyl-phosphatidylcholine (DPPC) / diol-eoyl-phosphatidylethanolamine (DOPE) were used, DOPE accumulated in the negatively curved region of the monolayer that formed as the proximal monolayers fused (i.e., cis leaflets). However, the enrichment was dependent on the presence of tethering molecules which kept the curvature high (the curvature radius of ~1 nm), placing the cis monolayers ~2-2.5 nm from each other. Simulations in which DOPE was replaced with dioleoyl-phosphatidylcholine (DOPC) showed an insignificant degree of DOPC accumulation, suggesting the importance of lateral interaction among DOPE molecules for the curvature sorting. The above composition was not close to a demixing point and our radial distribution function analysis suggested that the DOPE accumulation was not assisted by the lipid phase separation which has been shown to promote curvature-driven lipid sorting. Relevance of curvature-driven lipid sorting to biological membrane fusion is discussed.

Cite this paper

Nishizawa, M. and Nishizawa, K. (2010) Curvature-driven lipid sorting: coarse-grained dynamics simulations of a membrane mimicking a hemifusion intermediate. Journal of Biophysical Chemistry, 1, 86-95. doi: 10.4236/jbpc.2010.12011.

References

[1] Holthuis, J.C. and Levine, T.P. (2005) Lipid traffic: Floppy drives and a superhighway. Nature Reviews Molecular Cell Biology, 6(3), 209-220.
[2] Van Meer, G., Voelker, D.R. and Feigenson, G.W. (2008) Membrane lipids: Where they are and how they behave. Nature Reviews Molecular Cell Biology, 9(2), 112-124.
[3] De Matteis, M.A. and Luini, A. (2008) Exiting the Golgi complex. Nature Reviews Molecular Cell Biology, 9(4), 273-284.
[4] Mukherjee, S., Soe, T.T. and Maxfield, F.R. (1999) Endocytic sorting of lipid analogues differing solely in the chemistry of their hydrophobic tails. Journal of Cell Biology, 144(6), 1271-1284.
[5] Van Meer, G. and Lisman, Q. (2002) Sphingolipid trans- port: Rafts and translocators. Journal of Biological Che- mistry, 277(29), 25855-25858.
[6] Ostrowski, S.G., Van Bell, C.T., Winograd, N. and Ewing, A.G. (2004) Mass spectrometric imaging of highly curved membranes during Tetrahymena mating. Science, 305(5680), 71-73.
[7] Fratti, R.A., Jun, Y., Merz, A.J., Margolis, N. and Wickner, W. (2004) Interdependent assembly of specific re- gulatory lipids and membrane fusion proteins into the vertex ring domain of docked vacuoles. Journal of Cell Biology, 167(6), 1087-1098.
[8] Helfrich, W. (1973) Elastic properties of lipid bilayers: Theory and possible experiments. Zeitschrift fur Naturforschung C, 28(11), 693-703.
[9] Markin, V.S. (1981) Lateral organization of membranes and cell shapes. Biophysical Journal, 36(1), 1-19.
[10] Kozlov, M.M. and Helfrich, W. (1992) Effects of a cosurfactant on the stretching and bending elasticities of a surfactant monolayer. Langmuir, 8(11), 2792-2797.
[11] Seifert, U. (1993) Curvature-induced lateral phase segregation in two-component vesicles. Physical Review Letters, 7(9), 1335-1338.
[12] Iglic, A., H?gerstrand, H., Veranic, P., Plemenitas, A. and Kralj-Iglic, V. (2006) Curvature-induced accumulation of anisotropic membrane components and raft formation in cylindrical membrane protrusions. Journal of Theoretical Biology, 240(3), 368-373.
[13] Derganc, J. (2007) Curvature-driven lateral segregation of membrane constituents in Golgi cisternae. Physical Biology, 4(4), 317-324.
[14] Baumgart, T., Hess, S.T. and Webb, W.W. (2003) Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature, 425(6960), 821-824.
[15] Radhakrishnan, A. and McConnell, H. (2005) Condensed complexes in vesicles containing cholesterol and phospholipids. Proceedings of the National Academy of Sciences of the United States of America, 102(36), 12662- 12666.
[16] Parthasarathy, R., Yu, C.H. and Groves, J.T. (2006) Curvature-modulated phase separation in lipid bilayer membranes. Langmuir, 22(11), 5095-5099.
[17] Bo, L. and Waugh, R.E. (1989) Determination of bilayer membrane bending stiffness by tether formation from giant, thin-walled vesicles. Biophysical Journal, 55(3), 509-517.
[18] Roux, A., Cuvelier, D., Nassoy, P., Prost, J., Bassereau, P. and Goud, B. (2005) Role of curvature and phase transition in lipid sorting and fission of membrane tubules. European Molecular Biology Organization Journal, 24(8), 1537-1545.
[19] Tian, A. and Baumgart, T. (2009) Sorting of lipids and proteins in membrane curvature gradients. Biophysical Journal, 96(7), 2676-2688.
[20] Kamal, M.M., Mills, D., Grzybek, M. and Howard, J. (2009) Measurement of the membrane curvature preference of phospholipids reveals only weak coupling between lipid shape and leaflet curvature. Proceedings of the National Academy of Sciences of the United States of America, 106(52), 22245-22250.
[21] Cooke, I.R. and Deserno, M. (2006) Coupling between lipid shape and membrane curvature. Biophysical Journal, 91(2), 487-495.
[22] Chernomordik, L.V., Melikyan, G.B. and Chizmadzhev, Y.A. (1987) Biomembrane fusion: A new concept derived from model studies using two interacting planar lipid bilayers. Biochimica et Biophysica Acta, 906(3), 309- 352.
[23] Tamm, L.K., Crane, J. and Kiessling, V. (2003) Membrane fusion: A structural perspective on the interplay of lipids and proteins. Current Opinion in Structural Biology, 13(4), 453-466.
[24] Chernomordik, L.V. and Kozlov, M.M. (2008) Mechanics of membrane fusion. Nature Structural & Molecular Biology, 15(7), 675-683.
[25] Marsh, D. (2006) Elastic curvature constants of lipid monolayers and bilayers. Chemistry and Physics of Lipids, 144(2), 146-159.
[26] Fuller, N. and Rand, R.P. (2001) The influence of lysolipids on the spontaneous curvature and bending elasticity of phospholipid membranes. Biophysical Journal, 81(1), 243-254.
[27] Marrink, S.J. and Mark, A.E. (2003) The mechanism of vesicle fusion as revealed by molecular dynamics simulations. Journal of American Chemical Society, 125(37), 11144-11145.
[28] Kasson, P.M., Kelley, N.W., Singhal, N., Vrljic, M., Brunger, A.T. and Pande, V.S. (2006) Ensemble molecular dynamics yields submillisecond kinetics and intermediates of membrane fusion. Proceedings of the National Academy of Sciences of the United States of America, 103(32), 11916-11921.
[29] Marrink, S.J., Risselada, H.J., Yefimov, S., Tieleman, D.P. and De Vries, A.H. (2007) The MARTINI force field: Coarse grained model for biomolecular simulations. Journal of Physical Chemistry B, 111(27), 7812-7824.
[30] Bond, P.J. and Sansom, M.S.P. (2006) Insertion and assembly of membrane proteins via simulation. Journal of the American Chemical Society, 128(8), 2697-2704.
[31] Bond, P.J., Holyoake, J., Ivetac, A., Khalid, S. and Sansom, M.S.P. (2007) Coarse-grained molecular dynamics simulations of membrane proteins and peptides. Journal of Structural Biology, 157(3), 593-605.
[32] Lindahl, E., Hess, B. and Van der Spoel, D. (2001) GROMACS 3.0: A package for molecular simulation and trajectory analysis. Journal of Molecular Modeling, 7(8), 306-317.
[33] Weissenhorn, W., Hinz, A. and Gaudin, Y. (2007) Virus membrane fusion. FEBS Letters, 581(11), 2150-2155.
[34] Wickner, W. and Schekman, R. (2008) Membrane fusion. Nature Structural & Molecular Biology, 15(7), 658-664.
[35] Giraudo, C.G., Hu, C., You, D., Slovic, A.M., Mosharov, E.V., Sulzer, D., Melia, T.J. and Rothman, J.E. (2005) SNAREs can promote complete fusion and hemifusion as alternative outcomes. Journal of Cell Biology, 170(2), 249- 260.
[36] Liu, T., Wang, T., Chapman, E.R. and Weisshaar, J.C. (2008) Productive hemifusion intermediates in fast vesicle fusion driven by neuronal SNAREs. Biophysical Journal, 94(4), 1303-1314.
[37] Kasson, P.M. and Pande, V.S. (2007) Control of membrane fusion mechanism by lipid composition: Predictions from ensemble molecular dynamics. PLoS Computational Biology, 3(11), 2228-2238.
[38] Van Meer, G. and Sprong, H. (2004) Membrane lipids and vesicular traffic. Current Opinion in Cell Biology, 16(4), 373-378.
[39] Tian, A., Capraro, B.R., Esposito, C. and Baumgart, T. (2009) Bending stiffness depends on curvature of ternary lipid mixture tubular membranes. Biophysical Journal, 97(6), 1636-1646.
[40] Edidin, M. (2003) The state of lipid rafts: From model membranes to cells. Annual Review of Biophysics and Biomolecular Structure, 32(1), 257-283.
[41] Jacobson, K., Mouritsen, O.G. and Anderson, R.G. (2007) Lipid rafts: At a crossroad between cell biology and physics. Nature Cell Biology, 9(1), 7-14.
[42] Mannock, D.A., Lewis, R.N., McMullen, T.P. and McEl- haney, R.N. (2010) The effect of variations in phospholipid and sterol structure on the nature of lipid-sterol interactions in lipid bilayer model membranes. Chemistry and Physics of Lipids, 163(6), 403-448.
[43] Wang, W., Yang, L. and Huang, H.W. (2007) Evidence of cholesterol accumulated in high curvature regions: Implication to the curvature elastic energy for lipid mixtures. Biophysical Journal, 92(8), 2819-2830.
[44] Chiu, S.W., Jakobsson, E., Mashl, R.J. and Scott, H.L. (2002) Cholesterol-induced modifications in lipid bilayers: A simulation study. Biophysical Journal, 83(4), 1842- 1853.
[45] Hofs?ss, C., Lindahl, E. and Edholm, O. (2003) Molecular dynamics simulations of phospholipid bilayers with cholesterol. Biophysical Journal, 84(4), 2192-2206.
[46] Pandit, S.A., Khelashvili, G., Jakobsson, E., Grama, A. and Scott, H.L. (2007) Lateral organization in lipid-cho- lesterol mixed bilayers. Biophysical Journal, 92(2), 440- 447.
[47] McMullen, T.P. and McElhaney, R.N. (1995) New aspects of the interaction of cholesterol with dipalmitoylphosphatidylcholine bilayers as revealed by high-sensi- tivity differential scanning calorimetry. Biochimica et Bio- physica Acta, 1234(1), 90-98.
[48] Murtola, T., Falck, E., Patra, M., Karttunen, M. and Vattulainen, I. (2004) Coarse-grained model for phospholipid/ cholesterol bilayer. Journal of Chemical Physics, 121(18), 9156-9165.
[49] Murtola, T., Karttunen, M. and Vattulainen, I. (2009) Systematic coarse graining from structure using internal states: Application to phospholipid/cholesterol bilayer. Journal of Chemical Physics, 131(5), (055101)1-15.
[50] Risselada, H.J. and Marrink, S.J. (2008) The molecular face of lipid rafts in model membranes. Proceedings of the National Academy of Sciences of the United States of America, 105(45), 17367-17372.
[51] Niemel?, P.S., Ollila, S., Hyv?nen, M.T., Karttunen, M. and Vattulainen, I. (2007) Assessing the nature of lipid raft membranes. PLoS Computational Biology, 3(2), 304- 312.
[52] Nishizawa, M. and Nishizawa, K. (2010) Molecular dynamics simulation analyses of viral fusion peptides in membranes prone to phase transition: Effects on membrane curvature, phase behavior and lipid-water interface destabilization Journal of Biophysical Chemistry, 1(1), 19-32.
[53] Kasson, P.M., Lindahl, E. and Pande, V.S. (2010) Atomic- resolution simulations predict a transition state for vesicle fusion defined by contact of a few lipid tails. PLoS Computational Biology, 6(6), e1000829.
[54] Langosch, D., Hofmann, M. and Ungermann, C. (2007) The role of transmembrane domain in membrane fusion. Cellular and Molecular Life Sciences, 64(7-8), 850-864.

  
comments powered by Disqus

Copyright © 2017 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.