Solution pH alters mechanical and electrical properties of phosphatidylcholine membranes: Relation between interfacial electrostatics, intramembrane potential, and bending elasticity

Biophysical Journal

Volumn 92, Issue 7, 2007, Pages 2451-2462

  Zhou, Yong ^a   Raphael, Robert M ^b  

^a RICE UNIVERSITY   (United States)

^b Rice University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 STEAROYL 2 OLEOYL PHOSPHATIDYLCHOLINE; HYDROXIDE; PHOSPHATIDYLCHOLINE; UNCLASSIFIED DRUG;

ARTICLE; DIPOLE; ELASTICITY; ELECTRICAL PARAMETERS; ELECTRICITY; ELECTROPHORETIC MOBILITY; FLUORESCENCE ANALYSIS; LIPID VESICLE; MEMBRANE POTENTIAL; MICROPIPETTE; PH MEASUREMENT; RIGIDITY;

EID: 34047237965     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.096362     Document Type: Article

References (87)

1. Chernomordik, L. V., E. Leikina, V. Frolov, P. Bronk, and J. Zimmerberg. 1997. An early stage of membrane fusion mediated by the low pH conformation of influenza hemagglutinin depends upon membrane lipids. J. Cell Biol. 136:81-93.
2. Redfern, D. A., and A. Gericke. 2004. Domain formation in phosphatidylinositol monophosphate/phosphatidylcholine mixed vesicles. Biophys. J. 86:2980-2992.
3. Redfern, D. A., and A. Gericke. 2005. pH-dependent domain formation in phosphatidylinositol polyphosphate/phosphatidylcholine mixed vesicles. J. Lipid Res. 46:504-515.
4. Carrozzino, J. M., and M. G. Khaledi. 2005. pH effects on drug interactions with lipid bilayers by liposome electrokinetic chromatography. J. Chromatogr. A. 1079:307-316.
5. Cevc, G., A. Watts, and D. Marsh. 1981. Titration of the phase transition of phosphatidylserine bilayer membranes. Effects of pH, surface electrostatics, ion binding, and head-group hydration. Biochemistry. 20:4955-4965.
6. Eibl, H., and A. Blume. 1979. The influence of charge on phosphatidic acid bilayer membranes. Biochim. Biophys. Acta. 553:476-488.
7. Trauble, H., and H. Eibl. 1974. Electrostatic effects on lipid phase transitions: membrane structure and ionic environment. Proc. Natl. Acad. Sci. USA. 71:214-219.
8. Trauble, H., M. Teubner, P. Woolley, and H. Eibl. 1976. Electrostatic interactions at charged lipid membranes. I. Effects of pH and univalent cations on membrane structure. Biophys. Chem. 4:319-342.
9. Stumpel, J., K. Harlos, and H. Eibl. 1980. Charge-induced pretransition in phosphatidylethanolamine multilayers. The occurrence of ripple structures. Biochim. Biophys. Acta. 599:464-472.
10. Smith, B. D., and P. L. La Celle. 1979. Parallel decrease of erythrocyte membrane deformability and spectrin solubility at low pH. Blood. 53:15-18.
11. Heuser, J. 1989. Changes in lysosome shape and distribution correlated with changes in cytoplasmic pH. J. Cell Biol. 108:855-864.
12. Campbell, N. A., and J. B. Reece. 2002. Biology. Benjamin/Cummings, San Francisco, CA.
13. Barreto, J., and L. M. Lichtenberger. 1992. Vesicle acidification driven by a millionfold proton gradient: a model for acid influx through gastric cell membranes. Am. J. Physiol. 262:G30-G34.
14. Lichtenberger, L. M. 1987. Membranes and barriers: with a focus on the gastric mucosal barrier. Clin. Invest. Med. 10:181-188.
15. Nylander-Koski, O., H. Mustonen, I. Vikholm, T. Kiviluoto, and E. Kivilaakso. 2001. HCl causes less intracellular acidification in Necturus gastric mucosa surface epithelial cells than other acids. Am. J. Physiol. Gastrointest. Liver Physiol. 281:G675-G680.
16. Sulkowski, W. W., D. Pentak, K. Nowak, and A. Sulkowska. 2005. The influence of temperature, cholesterol content and pH on liposome stability. J. Mol. Struct. 744:737-747.
17. Smaby, J. M., J. M. Muderhwa, and H. L. Brockman. 1994. Is lateral phase separation required for fatty acid to stimulate lipases in a phosphatidylcholine interface? Biochemistry. 33:1915-1922.
18. Liu, H., R. Z. Lu, J. G. Turcotte, and R. H. Notter. 1994. Dynamic interfacial properties of surface-excess films of phospholipids and phosphonolipids analogs. J. Colloid Interface Sci. 167:378-390.
19. Petriat, F., and S. Giasson. 2005. Study of pH-sensitive copolymer/phospholipid complexes using the Langmuir balance technique: effect of anchoring sequence and copolymer molecular weight. Langmuir. 21:7326-7334.
20. Leonard, M. R., M. A. Bogle, M. C. Carey, and J. M. Donovan. 2000. Spread monomolecular films of monohydroxy bile acids and their salts: influence of hydroxyl position, bulk pH, and association with phosphatidylcholine. Biochemistry. 39:16064-16074.
21. Furuike, S., V. G. Levadny, S. J. Li, and M. Yamazaki. 1999. Low pH induces an interdigitated gel to bilayer gel phase transition in dihexadecylphosphatidylcholine membrane. Biophys. J. 77:2015-2023.
22. Harlos, K., J. Stumpel, and H. Eibl. 1979. Influence of pH on phosphatidic acid multilayers. A rippled structure at high pH values. Biochim. Biophys. Acta. 555:409-416.
23. Blume, A., and H. Eibl. 1979. The influence of charge on bilayer membranes. Calorimetric investigations of phosphatidic acid bilayers. Biochim. Biophys. Acta. 558:13-21.
24. Petelska, A. D., and Z. A. Figaszewski. 1998. Interfacial tension of two-component bilayer lipid membrane modeling of the cell membrane. Bioelectrochem. Bioenerg. 46:199-204.
25. Petelska, A. D., and Z. A. Figaszewski. 2000. Effect of pH on the interfacial tension of lipid bilayer membrane. Biophys. J. 78:812-817.
26. Petelska, A. D., and Z. A. Figaszewski. 2002. Effect of pH on the interfacial tension of bilayer lipid membrane formed from phosphatidylcholine or phosphatidylserine. Biochim. Biophys. Acta. 1561:135-146.
27. Gennis, R. B. 1989. Biomembrane Molecular Structure and Function. C. R. Cantor, editor. Springer-Verlag, New York.
28. Cevc, G., and D. Marsh. 1987. Phospholipid Bilayers: Physical Principles and Models. E. E. Bittar, editor. John Wiley & Sons, New York, NY.
29. Israelachvili, J. N., D. J. Mitchell, and B. W. Ninham. 1976. Theory of self-assembly of hydrocarbon amphiphiles into micelles and bilayers. J. Chem. Soc. Faraday Trans. II. 72:1525-1568.
30. Israelachvili, J. N., S. Marcelja, and R. G. Horn. 1980. Physical principles of membrane organization. Q. Rev. Biophys. 13:121-200.
31. Evans, E. A., and R. Skalak. 1980. Mechanics and Thermodynamics of Biomembranes. CRC Press, Boca Raton, FL.
32. Rawicz, W., K. C. Olbrich, T. McIntosh, D. Needham, and E. Evans. 2000. Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys. J. 79:328-339.
33. Glassinger, E., A. C. Lee, and R. M. Raphael. 2005. Electromechanical effects on tether formation from lipid membranes: a theoretical analysis. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 72:041926.
34. Zhou, Y., and R. M. Raphael. 2005. Effect of salicylate on the elasticity, bending stiffness, and strength of SOPC membranes. Biophys. J. 89:1789-1801.
35. Shoemaker, S. D., and T. K. Vanderlick. 2002. Intramembrane electrostatic interactions destabilize lipid vesicles. Biophys. J. 83:2007-2014.
36. Needham, D., and R. S. Nunn. 1990. Elastic deformation and failure of lipid bilayer membranes containing cholesterol. Biophys. J. 58:997-1009.
37. Needham, D., and D. V. Zhelev. 1995. Lysolipid exchange with lipid vesicle membranes. Ann. Biomed. Eng. 23:287-298.
38. Ly, H. V., and M. L. Longo. 2004. The influence of short-chain alcohols on interfacial tension, mechanical properties, area/molecule, and permeability of fluid lipid bilayers. Biophys. J. 87:1013-1033.
39. Kwok, R., and E. Evans. 1981. Thermoelasticity of large lecithin bilayer vesicles. Biophys. J. 35:637-652.
40. Hung, V. L., D. E. Block, and M. L. Longo. 2002. Interfacial tension effect of ethanol on lipid bilayer rigidity, stability, and area/molecule: a micropipette aspiration approach. Langmuir. 18:8988-8995.
41. Evans, E. A., W. Rawicz, and A. Hoffmann. 1994. Lipid Bilayer Expansion and Mechanical Degradation in Solutions of Water-Soluble Bile Acids. A. Hoffmann, G. Baumgartner, and A. Stiehl, editors. San Diego, CA.
42. Silvander, M., P. Hansson, and K. Edwards. 2000. Liposomal surface potential and bilayer packing as affected by PEG-lipid inclusion. Langmuir. 16:3696-3702.
43. Tatulian, S. A. 1983. Effect of lipid phase transition on the binding of anions to dimyristoylphosphatidylcholine liposomes. Biochim. Biophys. Acta. 736:189-195.
44. Petrache, H. I., T. Zemb, L. Belloni, and V. A. Parsegian. 2006. Salt screening and specific ion adsorption determine neutral-lipid membrane interactions. Proc. Natl. Acad. Sci. USA. 103:7982-7987.
45. Petrache, H. I., S. Tristram-Nagle, D. Harries, N. Kucerka, J. F. Nagle, and V. A. Parsegian. 2006. Swelling of phospholipids by monovalent salt. J. Lipid Res. 47:302-309.
46. Winterhalter, M., and W. Helfrich. 1988. Effect of surface charge on the curvature elasticity membranes. J. Phys. Chem. 92:6865-6867.
47. Winterhalter, M., and W. Helfrich. 1992. Bending elasticity of electrical charged bilayers: coupled monolayers, neutral surfaces, and balancing stresses. J. Phys. Chem. 96:327-330.
48. Lekkerkerker, H. N. W. 1989. Contribution of the electric double layer to the curvature elasticity of charged amphiphilic monolayers. Physica A. 159:319-328.
49. Mitchell, D. J., and B. W. Ninham. 1989. Curvature elasticity of charged membranes. Langmuir. 5:1121-1123.
50. Duplantier, B., R. E. Goldstein, V. Romero-Rochn, and A. I. Pesci. 1990. Geometrical and topological aspects of electric double layers near curved surfaces. Phys. Rev. Lett. 65:508-511.
51. Clarke, R. J., and C. Lupfert. 1999. Influence of anions and cations on the dipole potential of phosphatidylcholine vesicles: a basis for the Hofmeister effect. Biophys. J. 76:2614-2624.
52. Brockman, H. 1994. Dipole potential of lipid membranes. Chem. Phys. Lipids. 73:57-79.
53. Clarke, R. J. 2001. The dipole potential of phospholipid membranes and methods for its detection. Adv. Colloid Interface Sci. 89-90:263-281.
54. Honig, B. H., W. L. Hubbell, and R. F. Flewelling. 1986. Electrostatic interactions in membranes and proteins. Annu. Rev. Biophys. Biophys. Chem. 15:163-193.
55. Franklin, J. C., and D. S. Cafiso. 1993. Internal electrostatic potentials in bilayers: measuring and controlling dipole potentials in lipid vesicles. Biophys. J. 65:289-299.
56. Xu, C., and L. M. Loew. 2003. The effect of asymmetric surface potentials on the intramembrane electric field measured with voltage-sensitive dyes. Biophys. J. 84:2768-2780.
57. Clarke, R. J. 1997. Effect of lipid structure on the dipole potential of phosphatidylcholine bilayers. Biochim. Biophys. Acta. 1327:269-278.
58. Starke-Peterkovic, T., N. Turner, M. F. Vitha, M. P. Waller, D. E. Hibbs, and R. J. Clarke. 2006. Cholesterol effect on the dipole potential of lipid membranes. Biophys. J. 90:4060-4070.
59. Angelova, M. J., S. Soleau, P. Melaeard, J. F. Faucon, and P. Bothorel. 1992. Preparation of giant vesicles by AC electric fields. kinetic and applications. Prog. Colloid Polym. Sci. 89:127-131.
60. Evans, E., V. Heinrich, F. Ludwig, and W. Rawicz. 2003. Dynamic tension spectroscopy and strength of biomembranes. Biophys. J. 85:2342-2350.
61. Evans, E., and W. Rawicz. 1990. Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys. Rev. Lett. 64:2094-2097.
62. McLaughlin, S. 1989. The electrostatic properties of membranes. Annu. Rev. Biophys. Biophys. Chem. 18:113-136.
63. Parasassi, T., E. de Felip, F. Lepore, and F. Conti. 1986. Calcium-induced phase separation in phospholipid bilayers. A fluorescence anisotropy study. Cell. Mol. Biol. 32:261-266.
64. Parasassi, T., G. De Stasio, A. d'Ubaldo, and E. Gratton. 1990. Phase fluctuation in phospholipid membranes revealed by Laurdan fluorescence. Biophys. J. 57:1179-1186.
65. Bagatolli, L. A., E. Gratton, and G. D. Fidelio. 1998. Water dynamics in glycosphingolipid aggregates studied by LAURDAN fluorescence. Biophys. J. 75:331-341.
66. Bagatolli, L. A., and E. Gratton. 2000. Two photon fluorescence microscopy of coexisting lipid domains in giant unilamellar vesicles of binary phospholipid mixtures. Biophys. J. 78:290-305.
67. Bagatolli, L. A., and E. Gratton. 1999. Two-photon fluorescence microscopy observation of shape changes at the phase transition in phospholipid giant unilamellar vesicles. Biophys. J. 77:2090-2101.
68. Smejtek, P., A. Blochel, and S. Wang. 1996. Hydrophobicity and adsorption of chlorophenolates to lipid membranes. Chemosphere. 33:177-201.
69. Kinraide, T. B., U. Yermiyahu, and G. Rytwo. 1998. Computation of surface electrical potentials of plant cell membranes. Correspondence to published z-potentials from diverse plant sources. Plant Physiol. 118:505-512.
70. Tocanne, J. F., and J. Teissie. 1990. Ionization of phospholipids and phospholipid-supported interfacial lateral diffusion of protons in membrane model systems. Biochim. Biophys. Acta. 1031:111-142.
71. Loundon, G. M. 1995. Organic Chemistry. A. Scanlan-Rohrer, editor. Benjamin/Cummings, Redwood City, CA.
72. Heinz, W. F., and J. H. Hoh. 1999. Relative surface charge density mapping with the atomic force microscope. Biophys. J. 76:528-538.
73. Gilbert, D. L., and G. Ehrenstein. 1969. Effect of divalent cations on potassium conductance of squid axons: determination of surface charge. Biophys. J. 9:447-463.
74. Cole, K. S. 1969. Zeta potential and discrete versus uniform surface charges. Biophys. J. 9:465-469.
75. Lau, A., A. McLaughlin, and S. McLaughlin. 1981. The adsorption of divalent cations to phosphatidylglycerol bilayer membranes. Biochim. Biophys. Acta. 645:279-292.
76. Song, J., and R. Waugh. 1990. Bilayer membrane bending stiffness by tether formation from mixed PC-PS lipid vesicles. J. Biomech. Eng. 112:235-240.
77. Tawa, G. J., I. A. Topol, S. K. Burt, R. A. Calwell, and A. A. Rashin. 1998. Calculation of the aqueous solvation free energy of the proton. J. Chem. Phys. 109:4852-4863.
78. Bostrom, M., D. R. Williams, and B. W. Ninham. 2001. Specific ion effects: why DLVO theory fails for biology and colloid systems. Phys. Rev. Lett. 87:168103.
79. Bostrom, M., D. R. Williams, P. R. Stewart, and B. W. Ninham. 2003. Hofmeister effects in membrane biology: the role of ionic dispersion potentials. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 68:041902.
80. Nagle, J. F. 1987. Theory of passive proton conductance in lipid bilayers. J. Bioenerg. Biomembr. 19:413-426.
81. Nichols, J. W., and D. W. Deamer. 1980. Net proton-hydroxyl permeability of large unilamellar liposomes measured by an acid-base titration technique. Proc. Natl. Acad. Sci. USA. 77:2038-2042.
82. Nichols, J. W., M. W. Hill, A. D. Bangham, and D. W. Deamer. 1980. Measurement of net proton-hydroxyl permeability of large unilamellar liposomes with the fluorescent pH probe, 9-aminoacridine. Biochim. Biophys. Acta. 596:393-403.
83. Mouritsen, O. G., and M. J. Zuckermann. 1985. Softening of lipid bilayers. Eur. Biophys. J. 12:75-86.
84. Nagle, J. F., and H. L. Scott, Jr. 1978. Lateral compressibility of lipid mono- and bilayers. Theory of membrane permeability. Biochim. Biophys. Acta. 513:236-243.
85. Evans, E., and R. Kwok. 1982. Mechanical calorimetry of large dimyristoylphosphatidylcholine vesicles in the phase transition region. Biochemistry. 21:4874-4879.
86. Mills, J. K., and D. Needham. 2005. Lysolipid incorporation in dipalmitoylphosphatidylcholine bilayer membranes enhances the ion permeability and drug release rates at the membrane phase transition. Biochim. Biophys. Acta. 1716:77-96.
87. Papahadjopoulos, D., K. Jacobson, S. Nir, and T. Isac. 1973. Phase transitions in phospholipid vesicles. Fluorescence polarization and permeability measurements concerning the effect of temperature and cholesterol. Biochim. Biophys. Acta. 311:330-348.