The aqueous surroundings alter the bending rigidity of lipid membranes

Denitsa MitkovaDenitsa Mitkova, Victoria VitkovaVictoria Vitkova
Российский электрохимический журнал
Abstract / Full Text

The bending elasticity is the mechanical property that characterizes the deformability of lipid bilayers. In the present study the bending elasticity of phosphatidylcholine lipid membranes is reported in aqueous media with various chemical composition and pH. The bending modulus is obtained from analysis of the thermal shape fluctuations, performed on nearly spherical giant lipid vesicles. Lower bending rigidity of phosphatidylcholine bilayers is measured in aqueous media, containing potassium or sodium chlorides, compared to its value in water without salts. The results reported here for the membrane bending elasticity at three acidic values of pH are compared with the literature data from micromanipulation measurements of giant unilamellar vesicles from the same lipid. In accordance with previous results, further evidences are provided for the softening of lipid bilayers in the presence of sucrose in the aqueous surroundings.

Author information
  • Georgi Nadjakov Institute of Solid State Physics, Bulgarian Academy of Sciences, 72 Tzarigradsko Chaussee blvd., Sofia, 1784, BulgariaDenitsa Mitkova & Victoria Vitkova
  1. Zhou, Y. and Raphael, R.M., Solution pH alters mechanical and electrical properties of phosphatidylcholine membranes: Relation between interfacial electrostatics, intramembrane potential, and bending elasticity, Biophys. J., 2007, vol. 92, pp. 2451–2462.
  2. Mitkova, D., Marukovich, N., Ermakov, Y.A., and Vitkova, V., Bending rigidity of phosphatidylserine-containing lipid bilayers in acidic aqueous solutions, Colloids Surf. A: Physicochem. Eng. Aspects, 2014, vol. 460, pp. 71–78.
  3. Allen, T.M. and Cullis, P.R., Drug delivery systems: Entering the mainstream, Science, 2004, vol. 303, pp. 1818–1822.
  4. Carrozzino, J.M. and Khaledi, M.G., pH effects on drug interactions with lipid bilayers by liposome electrokinetic chromatography, J. Chromatogr. A, 2005, vol. 1079, pp. 307–316.
  5. Structure and Dynamics of Membranes, Lipowsky, R. and Sackmann, E., Eds., Amsterdam: Elsevier, 1995.
  6. Giant Vesicles, Luisi, P.L. and Walde, P., Eds., Chichester: John Wiley & Sons, Ltd., 2000.
  7. Dimova, R., Aranda, S., Bezlyepkina, N., Nikolov, V., Riske, K.A., and Lipowsky, R., A practical guide to giant vesicles: Probing the membrane nanoregime via optical microscopy, J. Phys. Condens. Matter, 2006, vol. 18, pp. S1151–S1176.
  8. Bagatolli, L.A., To see or not to see: Lateral organization of biological membranes and fluorescence microscopy, Biochim. Biophys. Acta, 2006, vol. 1758, pp. 1541–1556.
  9. Bloom, M., Evans, E., and Mouritsen, O.G., Physical properties of the fluid lipid-bilayer component of cell membrane: A perspective, Quart. Rev. Biophys., 1991, vol. 24, pp. 293–397.
  10. Gregoriadis, G., Engineering liposomes for drug delivery, Trends Biotechnol., 1995, vol. 13, pp. 527–537.
  11. Harashima, H. and Kiwada, H., Liposomal targeting and drug delivery: Kinetic consideration, Adv. Drug Delivery Rev., 1996, vol. 19, pp. 425–444.
  12. Francis, M.J., Effect of degassing on the electrical conductivity of pure water and potassium chloride solutions, J. Phys. Chem. C, 2008, vol. 112, pp. 14563–14569.
  13. Pashley, R.M., Rzechowicz, M., Pashley, M.L., and Francis, M.J., De-gassed water is a better cleaning agent, J. Phys. Chem. B., 2005, vol. 109, pp. 1231–1238.
  14. Angelova, M. and Dimitrov, D., Liposome electroformation, Faraday Discuss. Chem. Soc., 1986, vol. 81, pp. 303–311.
  15. Vitkova, V., Antonova, K., Popkirov, G., Mitov, M.D., Ermakov, Y.A., and Bivas, I., Electrical resistivity of the liquid phase of vesicular suspensions prepared by different methods, J. Phys.: Conf. Ser., 2010, no. 253, p. 012059.
  16. Mitkova, D., Stoyanova-Ivanova, A., Georgieva, S., Todorov, P., Kozarev, N., Ermakov, Y.A., and Vitkova, V., Charged lipid bilayers in aqueous surroundings with low pH, in Advances in Planar Lipid Bilayers and Liposomes, Iglic, A. and Kulkarni, C.V., Eds., Burlington: Academic Press, 2013, pp. 1–20.
  17. Bivas, I., Hanusse, P., Bothorel, P., Lalanne, J., and Aguerre-Chariol, O., An application of the optical microscopy to the determination of the curvature elastic modulus of biological and model membranes, J. Phys. (Paris), 1987, vol. 48, pp. 855–867.
  18. Faucon, J.F., Mitov, M.D., Méléard, P., Bivas, I., and Bothorel, P., Bending elasticity and thermal fluctuations of lipid membranes. Theoretical and experimental requirements, J. Phys. (Paris), 1989, vol. 50, pp. 2389–2414.
  19. Mitov, M.D., Faucon, J.F., Meleard, P., and Bothorel, P., Thermal Fluctuations of Membranes, Gokel, G.W., Ed., Greenwich: JAI Press Inc., 1992, pp. 93–139.
  20. Genova, J., Vitkova, V., and Bivas, I., Registration and analysis of the shape fluctuations of nearly spherical lipid vesicles, Phys. Rev. E, 2013, no. 88, p. 022707.
  21. Schneider, M.B., Jenkins, J.T., and Webb, W.W., Thermal fluctuations of large quasi spherical bimolecular phospholipid vesicles, J. Phys. (Paris), 1984, vol. 45, pp. 1457–1472.
  22. Helfrich, W., Size distributions of vesicles: The role of the effective rigidity of membranes, J. Phys. (Paris), 1986, vol. 47, pp. 321–329.
  23. Milner, S.T. and Safran, S.A., Dynamical fluctuations of droplet microemulsions and vesicles, Phys. Rev. A, 1987, vol. 36, pp. 4371–4379.
  24. Helfrich, W., Elastic properties of lipid bilayers: Theory and possible experiments, Z. Naturforsch., 1973, vol. 28c, pp. 693–703.
  25. Helfrich, W., Blocked lipid exchange in bilayers and its possible influence on the shape of vesicles, Z. Naturforsch., 1974, vol. 29c, pp. 510–515.
  26. Engelhardt, H., Duwe, H.-P., and Sackmann, E., Bilayer bending elasticity measured by Fourier analysis of thermally excited surface undulations of flaccid vesicles, J. Phys. Lett., 1985, vol. 46, pp. L-395–L-400.
  27. Genova, J., Vitkova, V., Aladgem, L., and Mitov, M.D., The stroboscopic illumination gives new opportunities and improves the precision of the bending elastic modulus measurement. J. Optoelectron. Adv. Mater., 2005, vol. 7, pp. 257–260.
  28. Vitkova, V. and Misbah, C., Dynamics of lipid vesicles— from thermal fluctuations to rheology, in Advances in Planar Lipid Bilayers and Liposomes, Iglic, A., Ed., Burlington: Academic Press, 2011, vol. 14, ch. 9, pp. 257–292.
  29. Vitkova, V., Genova, J., Finogenova, O., Ermakov, Y., Mitov, M.D., and Bivas, I., Surface charge effect on the lipid bilayer elasticity, C. R. Acad. Bulg. Sci., 2004, vol. 57, pp. 25–30.
  30. Bouvrais, H., Méléard, P., Pott, T., and Ipsen, J.H., Effects of sodium halide solutions of high concentrations on bending elasticity of POPC GUVs, Biophys. J., 2009, no. 96, p. 161a.
  31. Bouvrais, H., Garvik, O.S., Pott, T., Méléard, P., and Ipsen, J.H., Mechanics of POPC bilayers in presence of alkali salts, Biophys. J., 2010. vol. 98, p. 272a.
  32. Vitkova, V., Genova, J., Mitov, M.D., and Bivas, I., Sugars in the aqueous phase change the mechanical properties of lipid mono-and bilayers, Mol. Cryst. Liq. Cryst., 2006, vol. 449, pp. 95–106.
  33. Vitkova, V. and Petrov, A.G., Lipid bilayers and membranes: Material properties, in Advances in Planar Lipid Bilayers and Liposomes, Ales Iglic and Genova, J., Eds., Burlington: Academic Press, 2013, vol. 17, ch. 5, pp. 89–138.
  34. Nagle, J.F., Jablin, M.S., and Tristram-Nagle, S., Sugar does not affect the bending and tilt moduli of simple lipid bilayers, Chem. Phys. Lipids, 2016, vol. 196, pp. 76–80.
  35. Andersen, H.D., Wang, C., Arleth, L., Peters, G.H., and Westh, P., Reconciliation of opposing views on membrane–sugar interactions, Proc. Nat. Acad. Sci. USA, 2011, vol. 108, pp. 1874–1878.
  36. Olbrich, K., Rawicz, W., Needham, D., and Evans, E., Water permeability and mechanical strength of polyunsaturated lipid bilayers, Biophys. J., 2000, vol. 79, pp. 321–327.
  37. Vitkova, V., Genova, J., and Bivas, I., Permeability and the hidden area of lipid bilayers, Eur. Biophys. J., 2004, vol. 33, pp. 706–714.