AIMS Biophysics, 2017, 4(4): 528-542. doi: 10.3934/biophy.2017.4.528.

Research article

Export file:

Format

  • RIS(for EndNote,Reference Manager,ProCite)
  • BibTex
  • Text

Content

  • Citation Only
  • Citation and Abstract

Lipid phase separation in the presence of hydrocarbons in giant unilamellar vesicles

Groningen Biomolecular Sciences and Biotechnology Institute and Zernike Institute for Advanced Materials, University of Groningen, Nijenborgh 7, 9747 AG Groningen, The Netherlands

Hydrophobic hydrocarbons are absorbed by cell membranes. The effects of hydrocarbons on biological membranes have been studied extensively, but less is known how these compounds affect lipid phase separation. Here, we show that pyrene and pyrene-like hydrocarbons can dissipate lipid domains in phase separating giant unilamellar vesicles at room temperature. In contrast, related aromatic compounds left the phase separation intact, even at high concentration. We hypothesize that this behavior is because pyrene and related compounds lack preference for either the liquid-ordered (Lo) or liquid-disordered (Ld) phase, while larger molecules prefer Lo, and smaller, less hydrophobic molecules prefer Ld. In addition, our data suggest that localization in the bilayer (depth) and the shape of the molecules might contribute to the effects of the aromatic compounds. Localization and shape of pyrene and related compounds are similar to cholesterol and therefore these molecules could behave as such.
  Figure/Table
  Supplementary
  Article Metrics

Keywords biological membranes; lipid phase separation; unilamellar vesicles; hydrocarbons; membrane partitioning; polycyclic aromatic hydrocarbons; fluorescence microscopy

Citation: Rianne Bartelds, Jonathan Barnoud, Arnold J. Boersma, Siewert J. Marrink, Bert Poolman. Lipid phase separation in the presence of hydrocarbons in giant unilamellar vesicles. AIMS Biophysics, 2017, 4(4): 528-542. doi: 10.3934/biophy.2017.4.528

References

  • 1. Levental I, Lingwood D, Grzybek M, et al. (2010) Palmitoylation regulates raft affinity for the majority of integral raft proteins. Proc Natl Acad Sci 107: 22050–22054.    
  • 2. Bryant DM, Mostov KE (2008) From cells to organs: building polarized tissue. Nat Rev Mol Cell Biol 9: 887–901.
  • 3. Hashimoto-Tane A, Yokosuka T, Ishihara C, et al. (2010) T-cell receptor microclusters critical for T-cell activation are formed independently of lipid raft clustering. Mol Cell Biol 30: 3421–3429.    
  • 4. Levental I, Veatch SL (2016) The continuing mystery of lipid rafts. J Mol Biol 428: 4749–4764.    
  • 5. Gray E, Karslake J, Machta B, et al. (2013) Liquid general anesthetics lower critical temperatures in plasma membrane vesicles. Biophys J 105: 2751–2759.    
  • 6. Ingólfsson HI, Thakur P, Herold KF, et al. (2014) Phytochemicals perturb membranes and promiscuously alter protein function. ACS Chem Biol 9: 1788–1798.    
  • 7. Sikkema J, De Bont JA, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59: 201–222.
  • 8. Sikkema J, De Bont JAM, Poolman B (1994) Interactions of cyclic hydrocarbons with biological membranes. J Biol Chem 269: 8022–8028.
  • 9. McKarns SC, Hansch C, Caldwell WS, et al. (1997) Correlation between hydrophobicity of short-chain aliphatic alcohols and their ability to alter plasma membrane integrity. Fundam Appl Toxicol 36: 62–70.    
  • 10. Stegeman JJ, Teal JM (1973) Accumulation, release and retention of petroleum hydrocarbons by the oyster Crassostrea virginica. Mar Biol 22: 37–44.    
  • 11. Wagrowski DM, Hites RA (1996) Polycyclic aromatic hydrocarbon accumulation in urban, suburban, and rural vegetation. Environ Sci Technol 31: 279–282.
  • 12. Hearn EM, Dennis JJ, Gray MR, et al. (2003) Identification and characterization of the emhABC efflux system for polycyclic aromatic hydrocarbons in Pseudomonas fluorescens cLP6a. J Bacteriol 185: 6233–6240.    
  • 13. Bugg T, Foght JM, Pickard MA, et al. (2000) Uptake and active efflux of polycyclic aromatic hydrocarbons by Pseudomonas uptake and active efflux of polycyclic aromatic hydrocarbons by Pseudomonas fluorescens LP6a. Appl Environ Microbiol 66: 5387–5392.    
  • 14. Keweloh H, Diefenbach R, Rehm HJ (1991) Increase of phenol tolerance of Escherichia coli by alterations of the fatty acid composition of the membrane lipids. Arch Microbiol 157: 49–53.
  • 15. Kim IS, Lee H, Trevors JT (2001) Effects of 2,2',5,5'-tetrachlorobiphenyl and biphenyl on cell membranes of Ralstonia eutropha H850. FEMS Microbiol Lett 200: 17–24.
  • 16. McIntosh TJ, Simon SA, MacDonald RC (1980) The organization of n-alkanes in lipid bilayers. BBA-Biomembranes 597: 445–463.    
  • 17. White SH, King GI, Cain JE (1981) Location of hexane in lipid bilayers determined by neutron diffraction. Nature 290: 161–163.    
  • 18. MacCallum JL, Tieleman DP (2006) Computer simulation of the distribution of hexane in a lipid bilayer: Spatially resolved free energy, entropy, and enthalpy profiles. J Am Chem Soc 128: 125–130.    
  • 19. Bemporad D, Essex JW, Luttmann C (2004) Permeation of small molecules through a lipid bilayer: A computer simulation study. J Phys Chem B 108: 4875–4884.    
  • 20. Cornell BA, Separovic F (1983) Membrane thickness and acyl chain length. BBA-Biomembranes 733: 189–193.    
  • 21. Norman KE, Nymeyer H (2006) Indole localization in lipid membranes revealed by molecular simulation. Biophys J 91: 2046–2054.    
  • 22. Bassolino-klimas D, Alper HE, Stouch TR (1995) Mechanism of solute diffusion through lipid bilayer membranes by molecular dynamics simulation. J Am Chem Soc 117: 4118–4129.    
  • 23. Čurdová J, Čapková P, Plášek J, et al. (2007) Free pyrene probes in gel and fluid membranes: Perspective through atomistic simulations. J Phys Chem B 111: 3640–3650.    
  • 24. Hoff B, Strandberg E, Ulrich AS, et al. (2005) 2H-NMR study and molecular dynamics simulation of the location, alignment, and mobility of pyrene in POPC bilayers. Biophys J 88: 1818–1827.    
  • 25. do Canto AMTM, Santos PD, Martins J, et al. (2015) Behavior of pyrene as a polarity probe in palmitoylsphingomyelin and palmitoylsphingomyelin/cholesterol bilayers : A molecular dynamics simulation study. Colloid Surface A 480: 296–306.    
  • 26. Kopeć W, Telenius J, Khandelia H, et al. (2013) Molecular dynamics simulations of the interactions of medicinal plant extracts and drugs with lipid bilayer membranes. FEBS J 280: 2785–2805.    
  • 27. Luch A (2005) The Carcinogenic Effects of Polycyclic Aromatic Hydrocarbons, 1Eds., London: Imperial college press.
  • 28. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387: 569–572.    
  • 29. Pike LJ (2006) Rafts defined: a report on the Keystone symposium on lipid rafts and cell function. J Lipid Res 47: 1597–1598.    
  • 30. Veatch SL, Keller SL (2003) Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol. Biophys J 85: 3074–3083.    
  • 31. Kahya N, Scherfeld D, Bacia K, et al. (2003) Probing lipid mobility of raft-exhibiting model membranes by fluorescence correlation spectroscopy. J Biol Chem 278: 28109–28115.    
  • 32. Schroeder R, London E, Brown D (1994) Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior. Proc Natl Acad Sci 91: 12130–12134.    
  • 33. Ahmed S, Brown D, London E (1997) On the origin of sphingolipid/cholesterol-rich detergent-insoluble cell membranes: physiological concentrations of cholesterol and sphingolipid induce formation of a detergent-insoluble, liquid-ordered lipid phase in model membranes. Biochemistry 36: 10944–10953.    
  • 34. Schroeder RJ, Ahmed SN, Zhu Y, et al. (1998) Cholesterol and sphingolipid enhance the Triton X-100 insolubility of glycosylphosphatidylinositol-anchored proteins by promoting the formation of detergent-insoluble ordered membrane domains. J Biol Chem 273: 1150–1157.    
  • 35. Rinia HA, Snel MM, Van der EJP, et al. (2001) Imaging domains in model membranes with atomic force microscopy. FEBS Lett 501: 92–96.    
  • 36. Klose C, Ejsing CS, García-Sáez AJ, et al. (2010) Yeast lipids can phase-separate into micrometer-scale membrane domains. J Biol Chem 285: 30224–30232.    
  • 37. Kaiser H, Lingwood D, Levental I, et al. (2009) Order of lipid phases in model and plasma membranes. Proc Natl Acad Sci 106: 16645–16650.    
  • 38. Sezgin E, Kaiser HJ, Baumgart T, et al. (2012) Elucidating membrane structure and protein behavior using giant plasma membrane vesicles. Nat Protoc 7: 1042–1051.    
  • 39. Baumgart T, Hammond AT, Sengupta P, et al. (2007) Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles. Proc Natl Acad Sci 104: 3165–3170.    
  • 40. Leung SSW, Thewalt J (2017) Link between fluorescent probe partitioning and molecular order of liquid ordered-liquid disordered membranes. J Phys Chem B 121: 1176–1185.    
  • 41. Barnoud J, Rossi G, Marrink S, et al. (2014) Hydrophobic compounds reshape membrane domains. PLoS Comput Biol 10: e1003873.    
  • 42. Van Duyl BY, Rijkers DTS, De KB, et al. (2002) Influence of hydrophobic mismatch and palmitoylation on the association of transmembrane ɑ-helical peptides with detergent-resistant membranes. FEBS Lett 523: 79–84.    
  • 43. Veatch SL, Leung SSW, Hancock REW, et al. (2007) Fluorescent probes alter miscibility phase boundaries in ternary vesicles. J Phys Chem B 111: 502–504.    
  • 44. Skaug MJ, Longo ML, Faller R (2011) The impact of texas red on lipid bilayer properties. J Phys Chem B 115: 8500–8505.    
  • 45. Bouvrais H, Pott T, Bagatolli LA, et al. (2010) Impact of membrane-anchored fluorescent probes on the mechanical properties of lipid bilayers. BBA-Biomembranes 1798: 1333–1337.    
  • 46. Van Duyl BY, Ganchev D, Chupin V, et al. (2003) Sphingomyelin is much more effective than saturated phosphatidylcholine in excluding unsaturated phosphatidylcholine from domains formed with cholesterol. FEBS Lett 547: 101–106.    
  • 47. Lönnfors M, Doux JPF, Killian JA, et al. (2011) Sterols have higher affinity for sphingomyelin than for phosphatidylcholine bilayers even at equal Acyl-chain order. Biophys J 100: 2633–2641.    
  • 48. Fritzsching KJ, Kim J, Holland GP (2013) Probing lipid-cholesterol interactions in DOPC/eSM/Chol and DOPC/DPPC/Chol model lipid rafts with DSC and 13C solid-state NMR. BBA -Biomembranes 1828: 1889–1898.    
  • 49. Engberg O, Yasuda T, Hautala V, et al. (2016) Lipid interactions and organization in complex bilayer membranes. Biophys J 110: 1563–1573.    
  • 50. Loura LMS, Do Canto AMTM, Martins J (2013) Sensing hydration and behavior of pyrene in POPC and POPC/cholesterol bilayers: A molecular dynamics study. BBA-Biomembranes 1828: 1094–1101.    
  • 51. Vist MR, Davis JH (1990) Phase equilibria of cholesterol/dipalmitoylphosphatidylcholine mixtures: deuterium nuclear magnetic resonance and differential scanning calorimetry. Biochemistry 29: 451–464.    
  • 52. Baumgart T, Hunt G, Farkas ER, et al. (2007) Fluorescence probe partitioning between Lo membranes /Ld phases in lipid. BBA-Biomembranes 1768: 2182–2194.    
  • 53. Juhasz J, Davis JH, Sharom FJ (2010) Fluorescent probe partitioning in giant unilamellar vesicles of 'lipid raft' mixtures. Biochem J 430: 415–423.    
  • 54. Baumgart T, Hess ST, Webb WW (2003) Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425: 821–824.    
  • 55. Ramstedt B, Slotte JP (2006) Sphingolipids and the formation of sterol-enriched ordered membrane domains. BBA -Biomembranes 1758: 1945–1956.    
  • 56. Engelke M, Tähti H, Vaalavirta L (1996) Perturbation of artificial and biological membranes by organic compounds of aliphatic, alicyclic and aromatic structure. Toxicol In Vitro 10: 111–115.    
  • 57. Cheng T, Zhao Y, Li X, et al. (2012) Computation of octanol-water partition coefficients by guiding an additive model with knowledge. J Chem Inf Model 47: 2140–2148.

 

Reader Comments

your name: *   your email: *  

Copyright Info: © 2017, Bert Poolman, et al., licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution Licese (http://creativecommons.org/licenses/by/4.0)

Download full text in PDF

Export Citation

Copyright © AIMS Press All Rights Reserved