Skip to main content
  • Research article
  • Published:

Membrane potential-dependent binding of polysialic acid to lipid monolayers and bilayers

Abstract

Polysialic acids are linear polysaccharides composed of sialic acid monomers. These polyanionic chains are usually membrane-bound, and are expressed on the surfaces of neural, tumor and neuroinvasive bacterial cells. We used toluidine blue spectroscopy, the Langmuir monolayer technique and fluorescence spectroscopy to study the effects of membrane surface potential and transmembrane potential on the binding of polysialic acids to lipid bilayers and monolayers. Polysialic acid free in solution was added to the bathing solution to assess the metachromatic shift in the absorption spectra of toluidine blue, the temperature dependence of the fluorescence anisotropy of DPH in liposomes, the limiting molecular area in lipid monolayers, and the fluorescence spectroscopy of oxonol V in liposomes. Our results show that both a positive surface potential and a positive transmembrane potential inside the vesicles can facilitate the binding of polysialic acid chains to model lipid membranes. These observations suggest that these membrane potentials can also affect the polysialic acid-mediated interaction between cells.

Abbreviations

Δψdiff :

potassium diffusion potential

ψS :

surface potential

DP:

degree of polymerization

ODA:

octadecylamine

polySia:

polysialic acid

OX-V:

oxonol V

TB:

toluidine blue

References

  1. Przybyło, M., Borowik, T. and Langner, M. Fluorescence techniques for determination of the membrane potentials in high throughput screening. J. Fluoresc. 20 (2010) 1139–1157.

    Article  PubMed  Google Scholar 

  2. Rothbard, J.B., Jessop, T.C. and Wender P.A. Adaptive translocation: the role of hydrogen bonding and membrane potential in the uptake of guanidinium-rich transporters into cells. Adv Drug Deliv. Rev. 57 (2005) 495–504.

    Article  CAS  PubMed  Google Scholar 

  3. Troy, F.A., Janas, T., Janas, T. and Merker, R.I. Vectorial translocation of polysialic acid chains across the inner membrane of Escherichia coli K1. FASEB J. 5 (1991) A1548–A1548.

    Google Scholar 

  4. Janas, T., Krajiński, H., Timoszyk, A. and Janas, T. Translocation of polysialic acid across model membranes: kinetic analysis and dynamic studies. Acta Biochim. Polon. 48 (2001) 163–173.

    CAS  PubMed  Google Scholar 

  5. Sundelacruz, S., Levin, M, and Kaplan, D.L. Role of membrane potential in the regulation of cell proliferation and differentiation. Stem Cell Rev. Rep.5 (2009) 231–246.

    Article  Google Scholar 

  6. Kadenbach, B., Ramzan, R., Moosdorf, R. and Vogt, S. The role of mitochondrial membrane potential in ischemic heart failure. Mitochondrion 11 (2009) 700–706.

    Article  Google Scholar 

  7. Brown, G.P. and Douglas, J.G. Influence of transmembrane potential differences of renal tubular epithelial cell on ANG II binding. Am. J. Physiol. 252 (1987) F209–F214.

    CAS  PubMed  Google Scholar 

  8. Mahaut-Smith, M.P., Martinez-Pinna, J. and Gurung, I.S. A role for membrane potential in regulating GPCRs? Trends Pharmacol. Sci. 29 (2008) 421–429.

    Article  CAS  PubMed  Google Scholar 

  9. Janas, T., Kuczera, J. and Chojnacki, T. Voltage-dependent behaviour of dolichyl phosphate-phosphatidylcholine bilayer lipid membranes. Chem. Phys. Lipids 52 (1990) 151–155.

    Article  CAS  PubMed  Google Scholar 

  10. Ferrier, G.R. and Howlett, S.E. Cardiac excitation-contraction coupling: role of membrane potential in regulation of contraction. Am. J. Physiol. Heart Circ. Physiol. 280 (2001) H1928–H1944.

    CAS  PubMed  Google Scholar 

  11. Xu, C. and Loew, L.M. The effect of asymmetric surface potentials on the intramembrane electric field measured with voltage-sensitive dyes. Biophys. J.84 (2003) 2768–2780.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Wojtczak, L., Famulski, K.S., Nalecz, M.J. and Zborowski, J. Influence of the surface potential on the Michaelis constant of membrane-bound enzymes: effect of membrane solubilization. FEBS Lett. 139 (1982) 221–224.

    Article  CAS  PubMed  Google Scholar 

  13. Yeung, T., Gilbert, G.E., Shi, J., Silvius, J., Kapus, A. and Grinstein, S. Membrane phosphatidylserine regulates surface charge and protein localization. Science 319 (2008) 210–213.

    Article  CAS  PubMed  Google Scholar 

  14. Wang, L., Bose, P.S. and Sigworth, F.J. Using cryo-EM to measure the dipole potential of a lipid membrane. Proc. Natl. Ac. Sci. USA 103 (2006) 18528–18533.

    Article  CAS  Google Scholar 

  15. Troy, F.A. Polysialic acid in molecular medicine. Encyclopedia Biol. Chem. 3 (2004) 407–414.

    Article  CAS  Google Scholar 

  16. Bonfanti, L. PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog. Neurobiol. 80 (2006) 129–164.

    Article  CAS  PubMed  Google Scholar 

  17. Gascon, E., Vutskits, L. and Kiss, J.K. Polysialic acid-neural cell adhesion molecule in brain plasticity: from synapses to integration of new neurons. Brain Res. Rev. 56 (2007) 101–118.

    Article  CAS  PubMed  Google Scholar 

  18. Hildebrandt, H., Muhlenhoff, M., Weinhold, B. and Gerardy-Schahn, R. Dissecting polysialic acid and NCAM functions in brain development. J. Neurochem. 103(Suppl 1) (2007) 56–64.

    Article  CAS  PubMed  Google Scholar 

  19. Miyata, S., Sato, C. and Kitajima, K. Glycobiology of polysialic acids on sea urchin gametes. Trends Glycosci. Glycotechnol. 19 (2007) 85–98.

    Article  CAS  Google Scholar 

  20. Rutishauser, U. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nature Rev. Neurosci. 9 (2008) 26–35.

    Article  CAS  Google Scholar 

  21. Janas, T. and Janas, T. Membrane oligo- and polysialic acids. Biochim. Biophys. Acta — Biomembranes 1808 (2011a) 2923–2932.

    Article  CAS  Google Scholar 

  22. Janas, T., Janas, T. and Krajiński, H. Membrane transport of polysialic acid chains: modulation of transmembrane potential. Eur. Biophys. J. 29 (2000a) 507–514.

    Article  CAS  PubMed  Google Scholar 

  23. Janas, T., Nowotarski, K. and Janas, T. Polysialic acid can mediate membrane interactions by interacting with phospholipids. Chem. Phys. Lipids 163 (2010) 286–291.

    Article  CAS  PubMed  Google Scholar 

  24. Hannun, Y.A. and Obeid, L.M. Principles of bioactive lipid signalling: Lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9 (2008) 139–150.

    Article  CAS  PubMed  Google Scholar 

  25. Hengst, J.A., Guilford, J.M., Fox, T.E., Wang, X., Conroy, E.J. and Yun, J.K. Sphingosine kinase 1 localized to the plasma membrane lipid raft microdomain overcomes serum deprivation induced growth inhibition. Arch. Biochem. Biophys. 492 (2009) 62–73.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Janas, T., Nowotarski, K. and Janas, T. The effect of long-chain bases on polysialic acid-mediated membrane interactions. Biochim. Biophys. Acta — Biomembranes 1808 (2011b) 2322–2326.

    Article  CAS  Google Scholar 

  27. Kanato, Y., Kitajima, K. and Sato, C. Direct binding of polysialic acid to a brain-derived neurotrophic factor depends on the degree of polymerization. Glycobiology 18 (2008) 1044–1053.

    Article  CAS  PubMed  Google Scholar 

  28. Janas T., Janas, T. and Yarus, M. Specific RNA binding to ordered phospholipid bilayers. Nucleic Acids Res. 34 (2006) 2128–2136.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Janas, T., Janas, T. and Yarus, M. A membrane transporter for tryptophan composed of RNA. RNA 10 (2004) 1541–1549.

    Article  CAS  PubMed  Google Scholar 

  30. Ohkuma, S., Aoki, E. and Kanehira, M. Interaction of Toluidine Blue and sialoglycopeptides. Proc. Japan Acad. 47 (1971) 587–591.

    CAS  Google Scholar 

  31. Negelmann, L., Pisch, S., Bornscheuer, U. and Schmidt, R. Properties of unusual phospholipids. III: Synthesis, monolayer investigations and DSC studies of hydroxyl octadeca(e)noic acids and diacylglycerophosphocholines derived therefrom. Chem. Phys. Lipids 90 (1997) 117–134.

    Article  CAS  Google Scholar 

  32. Janas, T., Nowotarski, K., Gruszecki, W.I. and Janas, T. The effect of hexadecaprenol on molecular organisation and transport properties of model membranes. Acta Biochim. Polon. 47 (2000c) 661–673.

    CAS  PubMed  Google Scholar 

  33. Van Damme, M.P.I., Tiglias, J., Nemet, N. and Preston, B.N. Determination of the charge content at the surface of cells using a colloid titration technique. Anal. Biochem. 223 (1994) 62–70.

    Article  PubMed  Google Scholar 

  34. Yun, S., Ahn, K. and Kim, M.W. Polyelectrolyte flexibility effect on the morphology of charged lipid multilayers. Europhys. Lett. 70 (2005) 555–561.

    Article  CAS  Google Scholar 

  35. Smith, J.C., Russ, P., Cooperman, S. and Chance, B. Synthesis, structure determination, spectral properties, and energy-linked spectral responses of the extrinsic probe oxonol V in membranes. Biochemistry 15 (1976) 50794–5105.

    Google Scholar 

  36. Bashford, C.L., Chance, B., Smith, J.C. and Yoshida, T. The behavior of Oxonol dyes in phospholipid dispersions. Biophys. J. 25 (1979) 63–85.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Clarke, R.J. and Apell, H.J. A stopped-flow kinetic study of the interaction of potential-sensitive oxonol dyes with lipid vesicles. Biophys. Chem. 34 (1989) 225–237.

    Article  CAS  PubMed  Google Scholar 

  38. Holoubek, A., Vecer, J. and Sigler, K. Monitoring of the proton electrochemical gradient in reconstituted vesicles: quantitative measurements of both transmembrane potential and intravesicular pH by ratiometric fluorescent probes. J. Fluoresc. 17 (2007) 201–213.

    Article  CAS  PubMed  Google Scholar 

  39. Janas, T. and Janas, T. Polysialic acid: structure and properties. in: Polysaccharides: Structural Diversity and Functional Versality (Dumitriu, S. Ed.), 2nd edition, Marcel Dekker, New York, NY, 2005a, 707–727.

    Google Scholar 

  40. Janas, T., Krajiński, H. and Janas, T. Electromigration of polyion homopolymers across biomembranes: a biophysical model. Biophys. Chem.87 (2000b) 167–178.

    Article  CAS  PubMed  Google Scholar 

  41. Koiv, A., Mustonen, P. and Kinnunen, P.K.J. Differential scanning calorimetry study on the binding of nucleic-acids to dimyristoylphosphatidylcholine-sphingosine liposomes. Chem. Phys. Lipids 70 (1994) 1–10.

    Article  CAS  PubMed  Google Scholar 

  42. Fang, Y. and Yang, J. Two-dimensional condensation of DNA molecules on cationic lipid membranes. J. Phys. Chem. B 101 (1997) 441–449.

    Article  CAS  Google Scholar 

  43. Jurkiewicz, P., Okruszek, A., Hof, M. and Langner M. Associating oligonucleotides with positively charged liposomes. Cell. Mol. Biol. Lett. 8 (2003) 77–84.

    CAS  PubMed  Google Scholar 

  44. Koltover, I., Salditt, T. and Safinya, C.R. Phase diagram, stability, and overcharging of lamellar cationic lipid-DNA self-assembled complexes. Biophys. J. 77 (1999) 915–924.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Bordi, F., Cametti, C. and Sennato, S. Does a cluster phase in polyionliposome colloidal suspensions exist? An integrated experimental overview. Colloids Surf. A 306 (2007) 102–110.

    Article  CAS  Google Scholar 

  46. Michanek, A., Kristen, N., Höök, F., Nylander, T. and Sparr, E. RNA and DNA interactions with zwitterionic and charged lipid membranes — a DSC and QCM-D study. Biochim. Biophys. Acta 1798 (2010) 829–838.

    Article  CAS  PubMed  Google Scholar 

  47. Even-Chen, S., Cohen, R. and Barenholz, Y. Factors affecting DNA binding and stability of association to cationic liposomes. Chem. Phys. Lipids 165 (2012) 414–423.

    Article  CAS  PubMed  Google Scholar 

  48. Diederich, A., Bahr, G. and Winterhalter, M. Influence of polylysine on the rupture of negatively charged membranes. Langmuir 14 (1998) 4597–4605.

    Article  CAS  Google Scholar 

  49. de Kroon, A.I.P.M., de Gier, J. and de Kruijff, B. Association of synthetic model peptides with phospholipid vesicles induced by a membrane potential. Biochim. Biophys. Acta 981 (1989) 371–373.

    Article  PubMed  Google Scholar 

  50. Janas, T., Kotowski, J. and Tien, H.T. Polymer-modified bilayer lipid membranes: the polypyrrole-lecithin system. Bioelectrochem. Bioenerg. 19 (1988) 405–412.

    Article  CAS  Google Scholar 

  51. Jennings, M.L., Schulz, R.K. and Allen, M. Effects of membrane potential on electrically silent transport. J. Gen. Physiol. 96 (1990) 991–1012.

    Article  CAS  PubMed  Google Scholar 

  52. Janas, T. and Janas, T. Involvement of carboxyl groups in chloride transport and reversible DIDS binding to Band 3 protein in human erythrocytes. Cell. Mol. Biol. Lett. 16 (2011) 342–358.

    Article  CAS  PubMed  Google Scholar 

  53. Berkovich, A.K., Lukashev, E.P. and Melik-Nubarov, N.S. Dipole potential as a driving force for the membrane insertion of polyacrylic acid in slightly acidic milieu. Biochim. Biophys. Acta 1818 (2012) 375–383.

    Article  CAS  PubMed  Google Scholar 

  54. Janas, T. and Yarus, M. Visualization of membrane RNAs. RNA 9 (2003) 1353–1361.

    Article  CAS  PubMed  Google Scholar 

  55. Janas, T., Janas, T. and Yarus, M. RNA, lipids and membranes. in: The RNA World III (Gesteland, R., Cech, T.R., Atkins, J., Eds), Cold Spring Harbor Laboratory Press, New York, NY, 2005b, 207–225.

    Google Scholar 

  56. Janas, T. and Janas, T. The selection of aptamers specific for membrane molecular targets. Cell. Mol. Biol. Lett. 16 (2011) 25–39.

    Article  CAS  PubMed  Google Scholar 

  57. Gabrielska, J., Gagos, M., Gubernator, J. and Gruszecki, W.I. Binding of antibiotic amphotericin B to lipid membranes: A 1H NMR study. FEBS Lett. 580 (2006) 2677–2685.

    Article  CAS  PubMed  Google Scholar 

  58. Müller, E., Giehl, A., Schwarzmann, G., Sandhoff, K. and Blume, A. Oriented I,2-dimyristoyl-sn-glycero-3-phosphorylcholine/ganglioside membranes: a Fourier transform infrared attenuated total reflection spectroscopic study. Band assignments; orientational, hydrational, and phase behavior; and effects of Ca2+ binding. Biophys. J. 71 (1996) 1400–1421.

    Article  PubMed Central  PubMed  Google Scholar 

  59. Khalil, M.B., Kates, M. and Carrier, D. FTIR study of the monosialoganglioside GM1 in perdeuterated dimyristoylglycerophosphocholine (DMPCd54) multilamellar bilayers: spectroscopic evidence of a significant interaction between Ca2+ ions and the sialic acid moiety of GM1. Biochemistry 39 (2000) 2980–2988.

    Article  CAS  Google Scholar 

  60. Theis, T., Mishra, B., von der Ohe, M., Loers, G., Prondzynski, M., Pless, O., Blackshear, P.J., Schachner, M. and Kleene, R. Functional role of the interaction between polysialic acid and myristoylated alanine-rich C kinase substrate at the plasma membrane. J. Biol. Chem. 288 (2013) 6726–6742.

    Article  CAS  PubMed  Google Scholar 

  61. Azurmendi, H.F., Vionnet, J., Wrightson, L., Trinh, L.B., Shiloach, J. and Freedberg, D.I. Extracellular structure of polysialic acid explored by on cell solution NMR. Proc. Natl. Ac. Sci. USA 104 (2007) 11557–11561.

    Article  CAS  Google Scholar 

  62. Brisson, J.R., Baumann, H., Imberty, A., Perez, S. and Jennings, H.J. Helical epitope of the group B meningococcal α(2–8)-linked sialic acid polysaccharide. Biochemistry 31 (1992) 4996–5004.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Teresa Janas.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nowotarski, K., Sapoń, K., Kowalska, M. et al. Membrane potential-dependent binding of polysialic acid to lipid monolayers and bilayers. Cell Mol Biol Lett 18, 579–594 (2013). https://doi.org/10.2478/s11658-013-0108-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11658-013-0108-x

Key words