Lateral clustering of lipids in hydrated bilayers composed of dioleoylphosphatidylcholine and dipalmitoylphosphatidylcholine

  • D. V. Pyrkova
  • N. K. Tarasova
  • N. A. Krylov
  • D. E. Nolde
  • R. G. Efremov
Articles

Abstract

Investigation of lateral heterogeneities (clusters) in cell membranes is an important step toward understanding the physical processes that lead to the formation of lipid domains and rafts. Computer modeling methods represent a powerful tool to solve the problem, since they can detect clusters containing only a few lipid molecules—the situation that still resists characterization with modern experimental techniques. Parameters of clustering depend on lipid composition of a membrane. In this work, we propose a computational method to detect and analyze parts of membrane with different packing densities. Series of one- and two-component fluid systems containing lipids with the same polar heads and different acyl chains, dioleoylphosphatidylcholine (18 : 1) and dipalmitoylphosphatidylcholine (16 : 0), were chosen as the objects under study. The developed algorithm is based on molecular dynamics simulation of hydrated lipid bilayers in all-atom mode. The method is universal and could be applied to any other membrane system with arbitrary lipid composition. Here, we demonstrated that the studied lipid bilayers reveal small lateral dynamic clusters composed of just several (most often, three) lipid molecules. This seems to be one of the most important reasons determining the “mosaic” nature of the membrane-water interface.

Keywords

lipid membranes two-component lipid bilayers molecular dynamics lateral membrane heterogeneities lipid-lipid interactions structural organization of lipid bilayer 

References

  1. 1.
    Bagatolli L.A., Ipsen J.H., Simonsen A.C., Mouritsen O.G. 2010. An outlook on organization of lipids in membranes: Searching for a realistic connection with the organization of biological membranes. Prog. Lipid Res. 49, 378–389.PubMedCrossRefGoogle Scholar
  2. 2.
    Brown D.A., London E. 1998. Structure and origin of ordered lipid domains in biological membranes. J. Membrane Biol. 164, 103–114.CrossRefGoogle Scholar
  3. 3.
    Lingwood D., Kaiser H.-J., Levental I., Simons K. 2009. Lipid rafts as functional heterogeneity in cell membranes. Biochem. Soc. Trans. 37, 955–960.PubMedCrossRefGoogle Scholar
  4. 4.
    Honerkamp-Smith A.R., Veatch S.L., Keller S.L. 2009. An introduction to critical points for biophysicists; Observations of compositional heterogeneity in lipid membranes. Biochim. Biophys. Acta. 1788, 53–63.PubMedCrossRefGoogle Scholar
  5. 5.
    Mouritsen O.G. 2010. The liquid-ordered state comes of age. Biochim. Biophys. Acta. 1798, 1286–1288.PubMedCrossRefGoogle Scholar
  6. 6.
    Lingwood D., Simons K. 2010. Lipid rafts as a membrane-organizing principle. Science. 327, 46–50.PubMedCrossRefGoogle Scholar
  7. 7.
    London E. 2002. Insights into lipid raft structure and formation from experiments in model membranes. Curr. Opin. Struct. Biol. 12, 480–486.PubMedCrossRefGoogle Scholar
  8. 8.
    Freire E., Snyder B. 1980. Estimation of the lateral distribution of molecules in two-component lipid bilayers. Biochemistry. 19, 88–94.PubMedCrossRefGoogle Scholar
  9. 9.
    Chiu S.W., Jakobsson E., Mashl R.J., Scott H.L. 2002. Cholesterol-induced modifications in lipid bilayers: A simulation study. Biophys. J. 83, 1842–1853.PubMedCrossRefGoogle Scholar
  10. 10.
    Khelashvili G.A., Scott H.L. 2004. Combined Monte Carlo and molecular dynamics simulation of hydrated 18: 0 sphingomyelin-cholesterol lipid bilayers. J. Chem. Phys. 120, 9841–9847.PubMedCrossRefGoogle Scholar
  11. 11.
    Nicolini C., Kraineva J., Khurana M., Periasamy N., Funari S.S., Winter R. 2006. Temperature and pressure effects on structural and conformational properties of POPC/SM/cholesterol model raft mixtures — a FT-IR, SAXS, DSC, PPC and Laurdan fluorescence spectroscopy study. Biochim. Biophys. Acta. 1758, 248–258.PubMedCrossRefGoogle Scholar
  12. 12.
    Dewa T., Vigmond S.J., Regen S.L. 1996. Lateral heterogeneity in fluid bilayers composed of saturated and unsaturated phospholipids. J. Am. Chem. Soc. 118, 3435–3440.CrossRefGoogle Scholar
  13. 13.
    Almeida P.F.F. 2009. Thermodynamics of lipid interactions in complex bilayers. Biochim. Biophys. Acta. 1788, 72–85.PubMedCrossRefGoogle Scholar
  14. 14.
    Bennun S.V., Hoopes M.I., Xing C., Faller R. 2009. Coarse-grained modeling of lipids. Chem. Phys. Lipids. 159, 59–66.PubMedCrossRefGoogle Scholar
  15. 15.
    Efremov R.G., Nolde D.E., Konshina A.G., Syrtcev N.P., Arseniev A.S. 2004. Peptides and proteins in membranes: What can we learn via computer simulations? Curr. Med. Chem. 11, 2421–2442.PubMedGoogle Scholar
  16. 16.
    de Joannis J., Jiang Y., Yin F., Kindt J.T. 2006. Equilibrium distributions of dipalmitoyl phosphatidylcholine and dilauroyl phosphatidylcholine in mixed lipid bilayer: Atomistic semigrand canonical ensemble simulations. J. Phys. Chem. B. 110, 25875–25882.PubMedCrossRefGoogle Scholar
  17. 17.
    Faller R., Marrink S.J. 2004. Simulaion of domain formation in DLPC-DSPC mixed bilayers. Langmuir. 20, 7686–7693.PubMedCrossRefGoogle Scholar
  18. 18.
    Bennun S.V., Longo M., Faller R. 2007. Phase and mixing behavior in two-component lipid bilayers: A molecular dynamics study in DLPC/DSPC mixtures. J. Phys. Chem. B. 111, 9504–9512.PubMedCrossRefGoogle Scholar
  19. 19.
    Wang H., de Joannis J., Jiang Y., Gaulding J.C., Albrecht B., Yin F., Khanna K., Knidt J.T. 2008. Bilayer edge and curvature effects on partitioning of lipids by tail length: Atomistic simulations. Biophys. J. 95, 2647–2657.PubMedCrossRefGoogle Scholar
  20. 20.
    Berger O., Edholm O., Jahning F. 1997. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 72, 2002–2013.PubMedCrossRefGoogle Scholar
  21. 21.
    Pandit S.A., Bostick D., Berkowitz M.L. 2003. Mixed bilayer containing dopalmitoylphosphatidylcholine and dipalmitoylphosphatidylserine: Lipid complexation, ion binding, and electrostatics. Biophys. J. 85, 3120–3131.PubMedCrossRefGoogle Scholar
  22. 22.
    Murzyn K., Rog T., Pasenkiwicz-Gierula M. 2005. Phosphatidylethanolamine-phosphatidylglycerol bilayer as a model of the inner bacterial membrane. Biophys. J. 88, 1091–1103.PubMedCrossRefGoogle Scholar
  23. 23.
    Leekumjorn S., Sum A.K. 2006. Molecular simulation study of structural and dynamic properties of mixed DPPC/DPPE bilayers. Biophys. J. 90, 3951–3965.PubMedCrossRefGoogle Scholar
  24. 24.
    Jusoh S.A., Helms V. 2011. Helical integrity and microsolvation of transmembrane domains from Flaviviridae envelope glycoproteins. Biochim. Biophys. Acta. 1808, 1040–1049.PubMedCrossRefGoogle Scholar
  25. 25.
    Mojumdar E.H., Lyubartsev A.P. 2010. Molecular dynamics simulations of local anesthetic articine in a lipid bilayer. Biophys. Chem. 153, 27–35.PubMedCrossRefGoogle Scholar
  26. 26.
    Pasenkiewicz-Gierula M., Takaoka Y., Miyagawa H., Kitamura K., Kusumi A. 1997. Hydrogen bonding of water to phosphatidylcholine in the membrane as studied by a molecular dynamics simulation: Location, geometry, and lipid-lipid bridging via hydrogen bonded water. J. Phys. Chem. A. 101, 3677–3691.CrossRefGoogle Scholar
  27. 27.
    Pyrkova D.V., Tarasova N.K., Pyrkov T.V., Krylov N.A., Efremov R.G. 2011. Atomic-scale lateral heterogeneity and dynamics of two-component lipid bilayers composed of saturated and unsaturated phosphatidylcholines. Soft Matter. 7, 2569–2579.CrossRefGoogle Scholar
  28. 28.
    Polyansky A.A., Ramaswamy R., Volynsky P.E., Sbalzarini I.F., Marrink S.J., Efremov R.G. 2010. Antimicrobial peptides induce growth of phosphatidylglycerol domains in a model bacterial membrane. J. Phys. Chem. Lett. 20, 3108–3111.CrossRefGoogle Scholar
  29. 29.
    Risselada H.J., Marrink S.J. 2008. The molecular face of lipid rafts in model membranes. Proc. Natl. Acad. Sci. USA. 105, 17367–17372.PubMedCrossRefGoogle Scholar
  30. 30.
    Nagle J.F., Tristram-Nagle S. 2000. Structure of lipid bilayers. Biochim. Biophys. Acta. 1469, 159–195.PubMedGoogle Scholar
  31. 31.
    Polyansky A.A., Volynsky P.E., Nolde D.E., Arseniev A.S., Efremov R.G. 2005. Role of lipid charge in organization of water/lipid bilayer interface: Insights via computer simulations. J. Phys. Chem. B. 109, 15052–15059.PubMedCrossRefGoogle Scholar
  32. 32.
    Berendsen H.J.C., Postma J.P.M., van Gunsteren W.F., Hermans J. 1981. Interaction Models for Water in Relation to Protein Hydration. Dordrecht: Pullman, p. 331–342.Google Scholar
  33. 33.
    Lindahl E., Hess B., van der Spole D. 2001. Gromacs 3.0: A package for molecular simulation and trajectory analysis. J. Mol. Mod. 7, 306–317.Google Scholar
  34. 34.
    Berendsen H.J.C., Postma J.P.M., van Gunsteren W.F., DiNola A., Haak J.R. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684–3690.CrossRefGoogle Scholar
  35. 35.
    Schmidt M.L., Ziani L., Boureau M., Davis J.H. 2009. Phase equilibria in DOPC/DPPC: Conversion from gel to subgel in two component mixtures. J. Chem. Phys. 131, 175103PubMedCrossRefGoogle Scholar
  36. 36.
    Essmann U., Perera L., Berkowitz M.L., Darden T., Lee H., Pedersen L.G. 1995. A smooth particle mesh ewald method. J. Chem. Phys. 103, 8577–8592.CrossRefGoogle Scholar
  37. 37.
    Pyrkov T.V., Chugunov A.O., Krylov N.A., Nolde D.E., Efremov R.G. 2009. PLATINUM: A web tool for analysis of hydrophobic/hydrophilic organization of biomolecular complexes. Bioinformatics. 25, 1201–1202.PubMedCrossRefGoogle Scholar
  38. 38.
    Efremov R.G., Gulyaev D.I., Vergoten G., Modyanov N.N. 1992. Application of 3D molecular hydrophobicity potential to the analysis of spatial organization of membrane domains in proteins. I. Hydrophobic properties of transmembrane segments of Na,K-ATPase. J. Protein Chemistry. 11, 665–675.CrossRefGoogle Scholar
  39. 39.
    Polyansky A.A., Volynsky P.E., Arseniev A.S., Efremov R.G. 2009. Adaptation of a membrane-active peptide to heterogeneous environment. II. The role of mosaic nature of the membrane surface. J. Phys. Chem. B. 113, 1120–1126.PubMedCrossRefGoogle Scholar
  40. 40.
    Roark M., Feller S.E. 2009. Molecular dynamics simulation study of correlated motions in phospholipid bilayer membranes. J. Phys. Chem. B. 113, 13229–13234.PubMedCrossRefGoogle Scholar
  41. 41.
    Volynsky P.E., Polyansky A.A., Simakov N.A., Arseniev A.S., Efremov R.G. 2005. Effect of lipid composition on the “membrane response” induced by a fusion peptide. Biochemistry. 44, 14626–14637.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2011

Authors and Affiliations

  • D. V. Pyrkova
    • 1
  • N. K. Tarasova
    • 2
  • N. A. Krylov
    • 1
  • D. E. Nolde
    • 1
  • R. G. Efremov
    • 1
  1. 1.Shemyakin-Ovchinnikov Institute of Bioorganic ChemistryRussian Academy of SciencesMoscowRussia
  2. 2.Biological Faculty, Department of BioengineeringMoscow Lomonosov State UniversityMoscowRussia

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