Home LiteratureArticle Details
PMID: 15298907 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

The influence of short-chain alcohols on interfacial tension, mechanical properties, area/molecule, and permeability of fluid lipid bilayers.

Biophysical journal ·Vol. 87 ·No. 2 ·2004-08-00 ·Pages 1013-33

Ly HV, Longo ML

Abstract

We used micropipette aspiration to directly measure the area compressibility modulus, bending modulus, lysis tension, lysis strain, and area expansion of fluid phase 1-stearoyl, 2-oleoyl phosphatidylcholine (SOPC) lipid bilayers exposed to aqueous solutions of short-chain alcohols at alcohol concentrations ranging from 0.1 to 9.8 M. The order of effectiveness in decreasing mechanical properties and increasing area per molecule was butanol>propanol>ethanol>methanol, although the lysis strain was invariant to alcohol chain-length. Quantitatively, the trend in area compressibility modulus follows Traube's rule of interfacial tension reduction, i.e., for each additional alcohol CH(2) group, the concentration required to reach the same area compressibility modulus was reduced roughly by a factor of 3. We convert our area compressibility data into interfacial tension values to: confirm that Traube's rule is followed for bilayers; show that alcohols decrease the interfacial tension of bilayer-water interfaces less effectively than oil-water interfaces; determine the partition coefficients and standard Gibbs adsorption energy per CH(2) group for adsorption of alcohol into the lipid headgroup region; and predict the increase in area per headgroup as well as the critical radius and line tension of a membrane pore for each concentration and chain-length of alcohol. The area expansion predictions were confirmed by direct measurements of the area expansion of vesicles exposed to flowing alcohol solutions. These measurements were fitted to a membrane kinetic model to find membrane permeability coefficients of short-chain alcohols. Taken together, the evidence presented here supports a view that alcohol partitioning into the bilayer headgroup region, with enhanced partitioning as the chain-length of the alcohol increases, results in chain-length-dependent interfacial tension reduction with concomitant chain-length-dependent reduction in mechanical moduli and membrane thickness.

MeSH Terms
Adsorption Alcohols/chemistry Elasticity Lipid Bilayers/chemistry Liposomes/chemistry Membrane Fluidity Membranes, Artificial Micromanipulation/methods Permeability Phosphatidylcholines/chemistry Physical Stimulation/methods Porosity Surface Tension
Chemicals
Alcohols Lipid Bilayers Liposomes Membranes, Artificial Phosphatidylcholines 1-stearoyl-2-oleoyl-sn-glycero-3-phosphocholine
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Ly Hung V
Department of Chemical Engineering and Material Science, University of California, Davis, California, USA.
Longo Marjorie L
References (61)
61 references, click to expand
  1. Short-chain alcohols promote an early stage of membrane hemifusion.
    Biophys J. 1999 Oct;77(4):2035-45 PMID: 10512823
  2. Water permeability and mechanical strength of polyunsaturated lipid bilayers.
    Biophys J. 2000 Jul;79(1):321-7 PMID: 10866958
  3. Intrinsic perturbing ability of alkanols in lipid bilayers.
    Biochim Biophys Acta. 1978 May 4;509(1):1-8 PMID: 647001
  4. Nuclear Overhauser enhancement spectroscopy cross-relaxation rates and ethanol distribution across membranes.
    Biophys J. 2002 Mar;82(3):1396-404 PMID: 11867455
  5. Effect of chain length and unsaturation on elasticity of lipid bilayers.
    Biophys J. 2000 Jul;79(1):328-39 PMID: 10866959
  6. Tension-stabilized pores in giant vesicles: determination of pore size and pore line tension.
    Biochim Biophys Acta. 1993 Apr 8;1147(1):89-104 PMID: 8466935
  7. Interaction of GM(1) glycolipid in phospholipid monolayers with wheat germ agglutinin: effect of phospholipidic environment and subphase.
    Chem Phys Lipids. 2001 Nov;113(1-2):41-53 PMID: 11687226
  8. Lysolipid exchange with lipid vesicle membranes.
    Ann Biomed Eng. 1995 May-Jun;23(3):287-98 PMID: 7631982
  9. Gramicidin channel kinetics under tension.
    Biophys J. 1998 Jan;74(1):328-37 PMID: 9449333
  10. Determining ethanol distribution in phospholipid multilayers with MAS-NOESY spectra.
    Biochemistry. 1997 Apr 15;36(15):4669-74 PMID: 9109678
  11. Direct NMR evidence for ethanol binding to the lipid-water interface of phospholipid bilayers.
    Biochemistry. 1994 Jul 5;33(26):8082-8 PMID: 8025114
  12. Hydration of lipid membranes and the action mechanisms of anesthetics and alcohols.
    Chem Phys Lipids. 1999 Aug;101(1):65-79 PMID: 10810926
  13. Entropy-driven tension and bending elasticity in condensed-fluid membranes.
    Phys Rev Lett. 1990 Apr 23;64(17):2094-2097 PMID: 10041575
  14. Is lateral phase separation required for fatty acid to stimulate lipases in a phosphatidylcholine interface?
    Biochemistry. 1994 Feb 22;33(7):1915-22 PMID: 8110796
  15. Probing the interactions of alcohols with biological membranes with the fluorescent probe Prodan.
    Biochemistry. 1992 Oct 6;31(39):9473-81 PMID: 1390730
  16. Thermodynamic constants for nonelectrolyte partition between dimyristoyl lecithin and water.
    J Membr Biol. 1974;17(2):101-20 PMID: 4407659
  17. Permeability of human red cells to a homologous series of aliphatic alcohols. Limitations of the continuous flow-tube method.
    J Gen Physiol. 1983 Feb;81(2):283-304 PMID: 6842175
  18. Effects of low concentrations of ethanol on the fluidity of spin-labeled erythrocyte and brain membranes.
    Mol Pharmacol. 1977 May;13(3):435-41 PMID: 876032
  19. Commentary: surface tension of biomembranes.
    Biophys J. 1996 Sep;71(3):1346-7 PMID: 8874008
  20. Universality in interacting membranes: The effect of cosurfactants on the interfacial rigidity.
    Phys Rev Lett. 1989 Mar 6;62(10):1134-1137 PMID: 10039585
  21. Intracellular ethanol--accumulation and exit from yeast and other cells.
    FEMS Microbiol Rev. 1988 Sep;4(3):239-58 PMID: 3078745
  22. Increased permeability of phase-separated liposomal membranes with mixtures of ethanol-induced interdigitated and non-interdigitated structures.
    Biochim Biophys Acta. 1995 Jul 26;1237(2):169-75 PMID: 7632710
  23. Ethanol transport in Zymomonas mobilis measured by using in vivo nuclear magnetic resonance spin transfer.
    J Bacteriol. 1996 Mar;178(6):1756-61 PMID: 8626306
  24. What is the surface tension of a lipid bilayer membrane?
    Biophys J. 1996 Sep;71(3):1348-9 PMID: 8874009
  25. Thermodynamics of alcohol-lipid bilayer interactions: application of a binding model.
    Biochim Biophys Acta. 1999 Oct 15;1421(2):261-72 PMID: 10518696
  26. Alcohols dehydrate lipid membranes: an infrared study on hydrogen bonding.
    Biochim Biophys Acta. 1992 Oct 5;1110(2):225-33 PMID: 1390852
  27. The lateral pressure profile in membranes: a physical mechanism of general anesthesia.
    Biochemistry. 1997 Mar 4;36(9):2339-44 PMID: 9054538
  28. Effect of lipid characteristics on the structure of transmembrane proteins.
    Biophys J. 1998 Sep;75(3):1410-4 PMID: 9726942
  29. Interdigitated bilayer membranes.
    Prog Lipid Res. 1988;27(4):325-59 PMID: 3076241
  30. Mechanosensitive channels of Escherichia coli: the MscL gene, protein, and activities.
    Annu Rev Physiol. 1997;59:633-57 PMID: 9074781
  31. Influence of chain ordering on the selectivity of dipalmitoylphosphatidylcholine bilayer membranes for permeant size and shape.
    Biophys J. 1998 Dec;75(6):2658-71 PMID: 9826590
  32. Ethanol tolerance in bacteria.
    Crit Rev Biotechnol. 1990;9(4):305-19 PMID: 2178781
  33. Monocarboxylic acid permeation through lipid bilayer membranes.
    J Membr Biol. 1984;77(3):255-64 PMID: 6699907
  34. Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness.
    Biophys J. 1996 Jan;70(1):339-48 PMID: 8770210
  35. Structure and deformation properties of red blood cells: concepts and quantitative methods.
    Methods Enzymol. 1989;173:3-35 PMID: 2674613
  36. Structure of lipid bilayers.
    Biochim Biophys Acta. 2000 Nov 10;1469(3):159-95 PMID: 11063882
  37. Dynamics of pore growth in membranes and membrane stability.
    Biophys J. 1997 Oct;73(4):1797-804 PMID: 9336175
  38. The membrane disordering effect of ethanol on neural crest cells in vitro and the protective role of GM1 ganglioside.
    Alcohol. 1996 Nov-Dec;13(6):589-95 PMID: 8949954
  39. Effect of ethanol and osmotic stress on receptor conformation. Reduced water activity amplifies the effect of ethanol on metarhodopsin II formation.
    J Biol Chem. 2000 Feb 25;275(8):5355-60 PMID: 10681509
  40. Trehalose inhibits ethanol effects on intact yeast cells and liposomes.
    Biochim Biophys Acta. 1994 May 11;1191(2):309-16 PMID: 8172916
  41. Dynamic tension spectroscopy and strength of biomembranes.
    Biophys J. 2003 Oct;85(4):2342-50 PMID: 14507698
  42. Material property characteristics for lipid bilayers containing lysolipid.
    Biophys J. 1998 Jul;75(1):321-30 PMID: 9649389
  43. Interpretation of nonelectrolyte partition coefficients between dimyristoyl lecithin and water.
    J Membr Biol. 1974;17(2):121-54 PMID: 4407798
  44. Binding of small alcohols to a lipid bilayer membrane: does the partitioning coefficient express the net affinity?
    Biophys Chem. 2001 Jan 31;89(1):53-63 PMID: 11246745
  45. Passive mechanical behavior of human neutrophils: power-law fluid.
    Biophys J. 1993 Nov;65(5):2078-88 PMID: 8298037
  46. Permeability of small nonelectrolytes through lipid bilayer membranes.
    J Membr Biol. 1986;90(3):207-17 PMID: 3735402
  47. The seventh Datta Lecture. Membrane bending energy concept of vesicle- and cell-shapes and shape-transitions.
    FEBS Lett. 1994 Jun 6;346(1):3-16 PMID: 8206154
  48. Physical principles of membrane organization.
    Q Rev Biophys. 1980 May;13(2):121-200 PMID: 7015403
  49. Alcohol interactions with lipids: a carbon-13 nuclear magnetic resonance study using butanol labeled at C-1.
    Biochim Biophys Acta. 1987 Nov 27;905(1):151-61 PMID: 3676306
  50. Diffusional water permeability of human erythrocytes and their ghosts.
    J Gen Physiol. 1982 May;79(5):791-819 PMID: 7097244
  51. Saccharomyces cerevisiae does not accumulate ethanol against a concentration gradient.
    J Bacteriol. 1984 Dec;160(3):874-8 PMID: 6389514
  52. Membrane lateral compressibility determined by NMR and x-ray diffraction: effect of acyl chain polyunsaturation.
    Biophys J. 1997 Oct;73(4):1954-66 PMID: 9336191
  53. A thermodynamic study of the effects of cholesterol on the interaction between liposomes and ethanol.
    Biophys J. 2000 May;78(5):2486-92 PMID: 10777745
  54. Material studies of lipid vesicles in the L(alpha) and L(alpha)-gel coexistence regimes.
    Biophys J. 2003 Feb;84(2 Pt 1):998-1009 PMID: 12547781
  55. Effect of protein hydration on receptor conformation: decreased levels of bound water promote metarhodopsin II formation.
    Biochemistry. 1999 Jun 15;38(24):7617-23 PMID: 10387000
  56. Thermodynamic reversibility of phase transitions. Specific effects of alcohols on phosphatidylcholines.
    Biochim Biophys Acta. 1985 Mar 14;813(2):321-30 PMID: 3970925
  57. Molecular simulations of liquid-liquid interfacial properties: water-n-alkane and water-methanol-n-alkane systems.
    Phys Rev E Stat Nonlin Soft Matter Phys. 2003 Jan;67(1 Pt 1):011603 PMID: 12636510
  58. Interaction of the influenza hemagglutinin fusion peptide with lipid bilayers: area expansion and permeation.
    Biophys J. 1997 Sep;73(3):1430-9 PMID: 9284310
  59. Titration calorimetric and differential scanning calorimetric studies of the interactions of n-butanol with several phases of dipalmitoylphosphatidylcholine.
    Biochemistry. 1992 Feb 25;31(7):2005-11 PMID: 1536843
  60. Thermodynamics of membrane partitioning for a series of n-alcohols determined by titration calorimetry: role of hydrophobic effects.
    Biochemistry. 1998 Feb 24;37(8):2430-40 PMID: 9485391
  61. Lateral diffusion in the liquid phases of dimyristoylphosphatidylcholine/cholesterol lipid bilayers: a free volume analysis.
    Biochemistry. 1992 Jul 28;31(29):6739-47 PMID: 1637810
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
2004-08-00
Pages
1013-33
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1304443
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]