Skip to main content
Log in

Boundary Potential and the Energy of Lipid Monolayer Compression at the Liquid Expanded State

  • Published:
Biochemistry (Moscow), Supplement Series A: Membrane and Cell Biology Aims and scope

Abstract

Compression diagrams were obtained and analyzed for monolayers composed from DOPC, POPC, DMPC, DPPC, DPhPC, and DMPS at the surface of solutions containing KCl, CaCl2, or BeCl2 and in the presence of polylysine (PLL) or chlorpromazine (CPZ). Elastic properties of monolayers are characterized by the area of lipid molecules, presented as an incompressible area with a soft shell, the size of which exponentially depends on the lateral pressure and the coefficient of elasticity. This assumption describes well the shape of the lipid compression diagrams, including lipids with saturated hydrocarbon chains (DPPC and DMPS) in the region, where they exhibit liquid crystal properties (liquid expanded state, LE). All lipids show changes in the interfacial Volta potential in this region; these changes linearly depend on the effective value of the work applied to compress the monolayer. Choosing for zero value of the Volta potential its magnitude at the point with a lateral pressure of about 1 mN/m, the slope of linear section of this dependence was estimated. The slope of this dependence makes it possible to identify different types of membrane-active compounds affecting the elastic and electrostatic characteristics of the monolayer. It turned out that this slope is practically independent of the pH and ionic composition of the aqueous subphase but decreases upon adsorption of PLL polypeptides on the surface of the DMPS monolayer. The adsorption of small positively charged CPZ molecules on this monolayer leads to the deviation in the potential vs work dependence from the linear. A quantitative description of this deviation is in a good agreement with the assumption that CPZ molecules are incorporated into the monolayer. Their contribution to the change in the energy of the monolayer and the Volta potential is determined by the amount of incorporated CPZ molecules, the effect of which on lateral pressure can be approximated by a function similar to the Boltzmann relation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.

Similar content being viewed by others

REFERENCES

  1. Laroche G., Carrier D., Pezolet M. 1988. Study of the effect of poly-l-lysine) on phosphatidic acid and phosphatidylcholine/phosphatidic acid bilayers by Raman spectroscopy. Biochemistry. 27, 6220–6228.

    Article  CAS  Google Scholar 

  2. Kim J., Mosior M., Chung L.A., Wu H., McLaughlin S. 1991. Binding of peptides with basic residues to membranes containing acidic phospholipids. Biophys. J. 60 (1), 135–148.

    Article  CAS  Google Scholar 

  3. Rink T., Bartel H., Jung G., Bannwarth W., Boheim G. 1994. Effects of polycations on ion channels formed by neutral and negatively charged alamethicins. Eur. Biophys. J. 23 (3), 155–165.

    Article  CAS  Google Scholar 

  4. Arbuzova A., Wang L., Wang J., Hangyas-Mihalyne G., Murray D., Honig B., McLauglin S. 2000. Membrane binding of peptides containing both basic and aromatic residues. Experimental studies with peptides corresponding to the scaffolding region of caveolin and the effector region of MARCKS. Biochemistry. 39, 10330–10339. https://doi.org/10.1021/bi001039j

    Article  CAS  PubMed  Google Scholar 

  5. Harries D., May S., Ben Shaul A. 2002. Adsorption of charged macromolecules on mixed fluid membranes. Coll. Surfs. A, Physicochem. Eng. Aspects. 208 (1–3), 41–50.

    Article  CAS  Google Scholar 

  6. Wu Z., Cui Q., Yethira A. 2013. Why do arginine and lysine organize lipids differently? Insights from coarse grained and atomistic simulations. J. Phys Chem. B. 117, 12145–12156. https://doi.org/10.1021/jp4068729

    Article  CAS  PubMed  Google Scholar 

  7. Vorobyov I., Allen T.W. 2010. On the role of anionic lipids in charged protein interactions with membranes. Biochim. Biophys. Acta. 1808, 1673–1683. https://doi.org/10.1016/j.bbamem.2010.11.009

    Article  CAS  PubMed  Google Scholar 

  8. Doltchinkova V., Vitkova V. 2020. Polylysine effect on thylakoid membranes. Biophys. Chem. 266, 106440. https://doi.org/10.1016/j.bpc.2020.106440

    Article  CAS  PubMed  Google Scholar 

  9. Alvares D.S., Cabrera M.P.S., Neto J.R. 2016. Strategies for exploring electrostatic and nonelectrostatic contributions to the interaction of helical antimicrobial peptides with model membranes. In: Advances in biomembranes and lipid self-assembly. London, UK: Elsevier Inc., p. 43–73. https://doi.org/10.1016/j.bpc.2020.106440

    Book  Google Scholar 

  10. Ermakov Yu. A., Averbakh A. Z., Arbuzova A. B., Sukharev S.I. 1998. Lipid and cell membranes in the presence of gadolinium and other ions with high affinity to lipids. 2. A dipole component of the boundary potential on membranes with different surface charge. Biochemistry (Moscow) Suppl. Series A, Membr. Cell Biol. 12, 411–426.

    PubMed  Google Scholar 

  11. Ermakov Yu.A. 2005. Bioelectrochemistry of bilayer lipid membranes. Rossiiskii Khimicheskii Zhurnal (Rus.). 49 (5), 114–121.

    CAS  Google Scholar 

  12. Ermakov Y.A., Averbakh A.Z., Yusipovich A.I., Sukharev S. 2001. Dipole potentials indicate restructuring of the membrane interface induced by gadolinium and beryllium ions. Biophys. J. 80 (4), 1851–1862. https://doi.org/10.1016/S0006-3495(01)76155-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ermakov Yu., Kamaraju K., Dunina-Barkovskaya A., Vishnyakova K., Egorov Y., Anishkin A., Sukharev S. 2017. High-affinity interactions of beryllium (2+) with phosphatidylserine result in a cross-linking effect reducing surface recognition of the lipid. Biochemistry. 56, 5457–5470. https://doi.org/10.1021/acs.biochem.7b00644

    Article  CAS  PubMed  Google Scholar 

  14. Hammoudah M.M., Nir S., Isac T., Kornhouser R., Stewart T.P., Hui S.W., Vaz W.L.C. 1979. Intreraction of La3+ with phosphatidylserine vesicles: Binding, phase transition, leakage and fusion. Biochim. Biophys. Acta. 558, 338–343.

    Article  CAS  Google Scholar 

  15. Han K.-H., Tong Y., Huang W., Wang E. 2002. Study of the interaction between lanthanide ions and a supported bilayer lipid membrane by cyclic voltammetry and ac impedance. J. Electroanal. Chem. 523, 136–141.

    Article  CAS  Google Scholar 

  16. Li X., Zhang Y., Ni J., Chen J., Hwang F. 1994. Effect of lanthanide ions on the phase behaviour of dipalmitoylphosphatidylcholine multilamellar liposomes. J. Inorg. Biochem. 53, 139–149.

    Article  CAS  Google Scholar 

  17. Ermakov Y.A., Makhmudova S.S., Averbakh A.Z. 1998. Two components of boundary potentials at the lipid membrane surface: Electrokinetic and complementary methods studies. Coll. Surf. A. Physicochem. Eng. Aspects. 140 (1–3), 13–22.

    Article  CAS  Google Scholar 

  18. Barthel D., Zschoernig O., Lange K., Lenk R., Arnold K. 1988. Interaction of electrically charged drug molecules with phospholipid membranes. Biochim. Biophys. Acta. 945 (2), 361–366.

    Article  CAS  Google Scholar 

  19. Jutila A., Soderlund T., Pakkanen A.L., Huttunen M., Kinnunen P.K. 2001. Comparison of the effects of clozapine, chlorpromazine, and haloperidol on membrane lateral heterogeneity. Chem. Phys. Lipids. 112(2), 151–163.

    Article  CAS  Google Scholar 

  20. Nussio M.R., Sykes M.J., Miners J.O., Shapter J.G. 2009. Kinetics membrane disruption due to drug interactions of chlorpromazine hydrochloride. Langmuir. 25 (2), 1086–1090. https://doi.org/10.1021/la803288s

    Article  CAS  PubMed  Google Scholar 

  21. Steinkopf S., Simeunovic A., Bustad H.J., Ngo T.H., Sveaass H., Gjerde A.U., Holmsen H. 2010. pH-dependent interaction of psychotropic drug with glycerophospholipid monolayers studied by the Langmuir technique. Biophys. Chem. 152 (1–3), 65–73. https://doi.org/10.1016/j.bpc.2010.08.001

    Article  CAS  PubMed  Google Scholar 

  22. Agasosler A.V., Holmsen H. 2001. Chlorpromazine associates with phosphatidylserines to cause an increase in the lipid’s own interfacial molecular area role of the fatty acyl composition. Biophys. Chem. 19, 37–47.

    Google Scholar 

  23. Agasosler A.V., Tungodden L.M., Cejka D., Bakstad E., Sydnes L.K., Holmsen H. 2001. Chlorpromazine-induced increase in dipalmitoylphosphatidylserine surface area in monolayers at room temperature. Biochem. Pharmacol. 61, 817–825.

    Article  CAS  Google Scholar 

  24. Ermakov Yu. A. 2011. Relationships between electrostatic and mechanical characteristics of dimyristoylphosphatidylserine monolayer. Biochemistry (Moscow) Suppl. Series A, Membr. Cell Biol. 5, 379–384. https://doi.org/10.1134/S1990747811050059

    Article  Google Scholar 

  25. Ermakov Yu.A., Asadchikov V.E., Roshchin B.S., Volkov Yu.O., Khomich D.A., Nesterenko A.M., Tikhonov A.M. 2019. Comprehensive study of the LE–LC phase transition in DMPS monolayers: Surface pressure, Volta potential, X-ray reflectivity and MD modeling. Langmuir. 35, 12326–12338. https://doi.org/10.1021/acs.langmuir.9b01450

    Article  CAS  PubMed  Google Scholar 

  26. Ermakov Y.A., Kamaraju K., Sengupta K., Sukharev S. 2010. Gadolinium ions block mechanosensitive channels by altering the packing and lateral pressure of anionic lipids. Biophys. J. 98 (6), 1018–1027. https://doi.org/10.1016/j.bpj.2009.11.044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Shapovalov V.L. 1998. Interaction of DPPC monolayer at air–water interface with hydrophobic ions. Thin Solid Films. 327–329, 599–602.

    Article  Google Scholar 

  28. Molotkovsky R.J. Ermakov Yu.A. 2015. Two possible approaches to quantitative analysis of compression diagrams of lipid monolayers. Biochemistry (Moscow) Suppl. Series A, Membr. Cell Biol. 9, 48–52. https://doi.org/10.1134/S199074781406004X

    Article  Google Scholar 

  29. Cevc G., Marsh D. 1987. Cell biology. A series of monographs. New York: Willey-Interscience Publ. Vol. 5.

  30. Marukovich N., McMurray M., Finogenova O., Nesterenko A., Batishchev O., Ermakov Yu. 2013. Interaction of polylysines with the surface of lipid membranes: The electrostatic and structural aspects. In: Advances in planar lipid bilayers and liposomes. Ed. Iglic A. Amsterdam, London, San Diego: Elsevier Acad. Press, p. 139–166.

    Google Scholar 

  31. Finogenova O.A., Batishchev O.V., Indenbom A.V., Zolotarevsky V.I., Ermakov Yu.A. 2009. Molecular distribution and charge of polylysine layers at the surface of lipid membranes and mica. Biochemistry (Moscow) Suppl. Series A, Membr. Cell Biol. 3, 496–503. https://doi.org/10.1134/S1990747809040187

    Article  Google Scholar 

  32. Finogenova O., Filinsky D., Ermakov Y. 2008. Electrostatic effects upon adsorption and desorption of polylysines on the surface of lipid membranes of different composition. Biochemistry (Moscow) Suppl. Series A, Membr. Cell Biol. 2, 181–188. https://doi.org/10.1134/S1990747808020128

    Article  Google Scholar 

  33. Marukovich N., Nesterenko A., Ermakov Yu.A. 2015. Structural factors of lysine and polylysine interaction with lipid membranes. Biochemistry (Moscow) Suppl. Series A, Membr. Cell Biol. 9, 40–47.

    Google Scholar 

  34. Asadchikov V.E., Tikhonov A.M., Volkov Yu.O., Roshchin B.S., Ermakov Y.A., Rudakova E.B., D’yachkova I.G., Nuzhdin A.D. 2017. X-Ray study of the structure of phospholipid monolayers on the water surface. JETP Letters. 106, 534–539. https://doi.org/10.1134/S0021364017200061

    Article  CAS  Google Scholar 

  35. Tikhonov A.M., Asadchikov V.E., Volkov Yu.O., Roshchin B.S., Ermakov Yu.A. 2017. X-Ray reflectometry of DMPS monolayers on a water substrate. JETP. 125, 1051–1057. https://doi.org/10.1134/S1063776117120093

    Article  CAS  Google Scholar 

  36. Ermakov Yu.A., Asadchikov V.E., Volkov Yu.O., Nuzhdin A.D., Roshchin B.S., Honkimaki V., Tikho-nov A.M. 2019. Electrostatic and structural effects at the adsorption of polylysine on the surface of the DMPS monolayer. JETP Letters. 109, 334–339. https://doi.org/10.1134/S0021364019050060

    Article  CAS  Google Scholar 

  37. Steinkopf S., Simeunovic A., Bustad H.J., Ngo T.H., Sveaass H., Gjerde A.U., Holmsen H. 2010. pH-dependent interaction of psychotropic drug with glycerophospholipid monolayers studied by the Langmuir technique. Biophys. Chem. 152 (1–3), 65–73. https://doi.org/10.1016/j.bpc.2010.08.001

    Article  CAS  PubMed  Google Scholar 

  38. Wajnberg E., Tabak M., Nussenzveig P.A., Lopes C.M.B., Louro S.R.W. 1988. pH dependent phase transition of chlorpromazine micellat solutions in the physiological range. Biochim. Biophys. Acta. 944, 185–190.

    Article  CAS  Google Scholar 

  39. Eisenberg M., Gresalfi T., Riccio T., McLaughlin S. 1979. adsorption of monovalent cations to bilayer membranes containing negative phospholipids. Biochemistry. 18 (23), 5213–5223.

    Article  CAS  Google Scholar 

  40. Bennouna M., FerreiraMarques J., Banerjee S., Caspers J., Ruysschaert J.M. 1997. Interaction of chlorpromazine with phospholipid membranes: A monolayer and a microelectrophoresis approach. Langmuir. 13 (24), 6533–6539.

    Article  CAS  Google Scholar 

  41. Ermakov Yu.A. 2000. Ion equilibrium near lipid membranes: Empirical analysis of the simplest model. Colloid J. 62, 389–400.

    CAS  Google Scholar 

Download references

ACKNOWLEDGMENTS

This work supported by the Ministry of Science and Higher Education of the Russian Federation (project no. AAAA-A19-119010990119-9) and by the Russian Foundation for Basic Research (project no. 19-04-00242a).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yu. A. Ermakov.

Ethics declarations

The author declares that he has no conflict of interest.

This article does not contain any studies involving animals or human participants performed by the author.

Additional information

Translated by Yu. Ermakov

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ermakov, Y.A. Boundary Potential and the Energy of Lipid Monolayer Compression at the Liquid Expanded State. Biochem. Moscow Suppl. Ser. A 15, 130–141 (2021). https://doi.org/10.1134/S1990747821020057

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990747821020057

Keywords:

Navigation