Skip to main content
Log in

Cell membrane fluidity related to electroporation and resealing

  • Article
  • Published:
European Biophysics Journal Aims and scope Submit manuscript

Abstract

In this paper, we report the results of a systematic attempt to relate the intrinsic plasma membrane fluidity of three different cell lines to their electroporation behaviour, which consists of reversible and irreversible electroporation. Apart from electroporation behaviour of given cell lines the time course required for membrane resealing was determined in order to distinguish the effect of resealing time from the cell’s ability to survive given electric pulse parameters. Reversible, irreversible electroporation and membrane resealing were then related to cell membrane fluidity as determined by electron paramagnetic resonance spectroscopy and computer characterization of membrane domains. We found that cell membrane fluidity does not have significant effect on reversible electroporation although there is a tendency for the voltage required for reversible electroporation to increase with increased membrane fluidity. Cell membrane fluidity, however, may affect irreversible electroporation. Nevertheless, this effect, if present, is masked with different time courses of membrane resealing found for the different cell lines studied. The time course of cell membrane resealing itself could be related to the cell’s ability to survive.

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

Similar content being viewed by others

References

  • Bloom M, Thewalt JL (1995) Time and distance scales of membrane domain organization. Mol Membr Biol 12:9–13

    Article  PubMed  Google Scholar 

  • Canatella PJ, Karr JF, Petros JA, Prausnitz MR (2001) Quantitative study of electroporation mediated uptake and cell viability. Biophys J 80:755–764

    PubMed  Google Scholar 

  • Chen K, Morse PD II, Swartz HM (1988) Kinetics of enzyme-mediated reduction of lipid soluble nitroxide spin labels by living cells. Biochim Biophys Acta 943:477–484

    Article  PubMed  Google Scholar 

  • Chen S-Y, Yang B, Jacobson K, Sulik KK (1996) The membrane disordering effect on ethanol on neural crest cells in vitro and the protective role of GM1 ganglioside. Alcohol 13:589–595

    Article  PubMed  Google Scholar 

  • Chen SY, Periasamy A, Yang B, Herman B, Jacobson K, Sulik KK (2000) Differential sensitivity of mouse neural cells to ethanol-induced toxicity. Alcohol 20:75–81

    Article  PubMed  Google Scholar 

  • Chernomordik LV, Sukharev SI, Popov SV, Pastusenko VF, Sokiroko AV, Abidor IG, Chizmadzev YA (1987) The electrical breakdown of cell and lipid membranes: the similarity of phenomenologies. Biochim Biophys Acta 902:360–373

    Article  PubMed  Google Scholar 

  • Cole KS (1972) Membranes Ions and Impulses. Berkely, Los Angeles, p 15

    Google Scholar 

  • Curtain CC, Gordon LM (1984) ESR spectroscopy of membranes. In: Alan R (ed) Membranes, detergents and receptor solubilization. Liss Inc., New York, pp 177–213

    Google Scholar 

  • Čemazar M, Jarm T, Miklavčič D, Maček-Lebar A, Ihan A, Kopitar NA, Serša G (1998) Effect of electric field induced intensity on electropermeabilization and electro sensitivity of various tumour cell lines in vitro. Electromagnetobiol 17:263–272

    Google Scholar 

  • Danfelter M, Engstrom P, Person B, Salford LG (1998) Effect of high voltage pulses on survival of Chinese hamster V-79 lung fibroblast cells. Bioelectrochem Bioenerg 47:97–101

    Article  Google Scholar 

  • Djuzenova CS, Zimmermann U, Frank H, Sukhorukov VL, Richter E, Fuhr G (1996) Effect of medium conductivity and composition on the uptake of propidium iodide into electropermeabilized myeloma cells. Biochim Biophys Acta 1284:143–152

    Article  PubMed  Google Scholar 

  • Ferber D (2001) Gene therapy: safer and virus free? Science 294:1638–1642

    Article  PubMed  Google Scholar 

  • Filipič B, Štrancar J (2001) Tuning EPR spectral parameters with genetic algorithm. Appl Soft Comput 1:83–90

    Article  Google Scholar 

  • Fromm ME, Taylor LP, Walbot V (1986) Stable transformation of maize after gene transfer by electroporation. Nature 319:791–793

    Article  PubMed  ADS  Google Scholar 

  • Gabriel B, Teissié J (1997) Direct observation in the millisecond time range of fluorescent molecule asymmetrical interaction with the electropermeabilized cell membrane. Biophys J 73:2630–2637

    PubMed  Google Scholar 

  • Gabriel B, Teissié J (1999) Time courses of mammalian cell electropermeabilization observed by milisecond imaging of membrane property changes during the pulse. Biophys J 76:2158–2165

    PubMed  Google Scholar 

  • Gehl J (2003) Electroporation: theory and methods, perspectives for drug delivery, gene therapy and research. Acta Physiol Scand 177:437–447

    Article  PubMed  Google Scholar 

  • Gaškova D, Sigler K, Janderova B, Plašek J (1996) Effect of high voltage electric pulses on yeast cells: factors influencing the killing efficiency. Bioelectrochem Bioenerg 39:195–202

    Article  Google Scholar 

  • Hamilton WA, Sale JH (1967) Effects of high electric fields on micro organism II. Mechanism of action of the lethal effect. Biochim Biophys Acta 148:789–800

    Google Scholar 

  • Golzio M, Mora MP, Raynaud C, Delteil C, Teissié J, Rols MP (1998) Control by osmotic pressure of voltage induced permeabilization and gene transfer in mammalian cells. Biophys J 74:3015–3022

    PubMed  Google Scholar 

  • Jordão AA, Chiarello PG, Arantes MR, Meirelles M, Vannucchi H (2004) Effect of an dose of ethanol on lipid peroxidation in rats: action of vitamin E. Food Chem Toxicol 42:459–464

    Article  PubMed  Google Scholar 

  • Kandušer M, Fošnarič M, Šentjurc M, Kralj-Iglič V, Hagerstrand H, Iglič A, Miklavčič D (2003) Effect of surfactant polyoxyethylene glycol (C12E8) on electroporation of cell line DC-3F. Colloid Surf A 214:205–217

    Article  Google Scholar 

  • Kinoshita K, Tsong TY (1977) Formation and resealing of pores of controlled sizes in human erythrocyte membrane. Nature 268:438–440

    Article  PubMed  ADS  Google Scholar 

  • Kinoshita K, Tsong TY (1979) Voltage induced conductance in human erythrocyte membranes. Biochim Biophys Acta 554:479–497

    Article  PubMed  Google Scholar 

  • Kotnik T, Maček-Lebar A, Miklavčič D, Mir LM (2000) Evaluation of cell membrane electropermeabilization by means of non-permeant cytotoxic agent. Biotechniques 28:921–926

    PubMed  Google Scholar 

  • Kotnik T, Bobanović F, Miklavčič D (1997) Sensitivity of transmembrane voltage induced by applied electric fields—a theoretical analysis. Bioelectrochem Bioenerg 43:285–291

    Article  Google Scholar 

  • Leontiadou H, Mark AE, Marrink SJ (2004) Molecular dynamics simulations of hydrophilic pores in lipid bilayers. Biophys J 86:2156–2164

    Article  PubMed  Google Scholar 

  • Li Y, King MA, Meyer MM (2000) ά/nicotinic recetpor-mediated protection against ethanol-induced oxidative stress and cytotoxicity in PC12 cells. Brain Res 861:165–167

    Article  PubMed  Google Scholar 

  • Marsh D (1981) Electron spin resonance: spin labels. In: Grell E (ed) Membrane spectroscopy. Springer-Verlang, Berlin, pp 51–142

    Google Scholar 

  • Meaking WS, Edgerton J, Wharton CW, Meldrum RA (1995) Electroporation induced damage in mammalian cell DNA. Biochim Biophys Acta 1264:357–362

    PubMed  Google Scholar 

  • Marszalek P, Liu DS, Tsong TY (1990) Schwan equation and transmembrane potential induced by alternating electric field. Biophys J 58:1053–1058

    PubMed  Google Scholar 

  • Meshar A, Holownia A, Bardou LG, Menez J-F (1996) Effect of acetaldehyde generated from ethanol by ADH-transfected CHO cells on their membrane fatty acid profiles. Alcohol 13:611–616

    Article  PubMed  Google Scholar 

  • Mir LM (2000) Therapeutic perspectives of in vivo electropermeabilization. Bioelectrochemistry 53:1–10

    Article  Google Scholar 

  • Mir LM, Tounekti O, Orlowski S (1996) Bleomycin: revival of an old drug. Gen Pharmacol 27:745–748

    PubMed  Google Scholar 

  • Neuman MG (2002) Synergetic signaling of apoptosis in vitro by ethanol and acetaminophen. Alcohol 27:89–98

    Article  PubMed  Google Scholar 

  • Neuman MG, Haber JA, Malkiewicz IM, Cameron RG, Katz GG, Shear NH (2002) Ethanol signals for apoptosis in cultured skin cells. Alcohol 26:179–190

    Article  PubMed  Google Scholar 

  • Neumann E (1989) The relaxation hysteresis of membrane electroporation. In: Neumann E, Sowers AE, Jordan CA (eds) Electroporation and electrofusion in cell biology. Plenium Press, New York, pp 61–82

    Google Scholar 

  • Neumann E (1992) Membrane electroporation and direct gene transfer. Bioelectrochem Bioenerg 28:247–267

    Article  Google Scholar 

  • Neumann E, Schaefer-Ridder M, Wang Y, Holschneider PH (1982) Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J 1:841–845

    PubMed  Google Scholar 

  • Neumann E, Kakorin S, Toesing K (1999) Fundamentals of electroporative delivery of drugs and genes. Bioelectrochem Bioenerg 48:3–16

    Article  PubMed  Google Scholar 

  • O’Hare MJ, Ormerod MG, Imrie PR, Peacock JH, Asche W (1989) Electropermeabilization and electrosensitivity of different types of mammalian cells. In: Neumann E, Sowers AE, Jordan CA (eds) Electroporation and electrofusion in cell biology. Plenium Press, New York, pp 319–330

    Google Scholar 

  • Puc M, Flisar K, Reberšek S, Miklavčič D (2001) Electroporator for in vitro cell permeabilization. Radiol Oncol 35:203–207

    Google Scholar 

  • Puc M, Kotnik T, Mir L, Miklavčič D (2003) Quantitative model of small molecules uptake after in vitro cell electropermeabilization. Bioelectrochemistry 60:1–10

    Article  PubMed  Google Scholar 

  • Pucihar G, Kotnik T, Kandušer M, Miklavčič D (2001) The influence of medium conductivity on electropermeabilization and survival of cells in vitro. Bioelectrochemistry 54:107–115

    Article  PubMed  Google Scholar 

  • Rols MP, Teissié J (1989) Ionic strength modulation of electrically induced permeabilization and associated fusion of mammalian cells. Eur J Biochem 179:109–115

    Article  PubMed  Google Scholar 

  • Rols MP, Teissié J (1990a) Electropermeabilization of mammalian cells. Quantitative analysis of the phenomenaon. Biophys J 58:1089–1098

    PubMed  Google Scholar 

  • Rols MP, Teissié J (1990b) Modulation of electrically induced permeabilization and fusion of Chinese hamster ovary cells by osmotic pressure. Biochemistry 29:4561–4567

    Article  PubMed  Google Scholar 

  • Rols MP, Teissié J (1992) Experimental evidence for the involvememnt of the cytoskeleton in mammalian cell electropermeabilization. Biochim Biophys Acta 1111:45–50

    Article  PubMed  Google Scholar 

  • Rols MP, Dahhou F, Mishra KP, Teissié J (1990) Control of electric field induced cell membrane permeabilization by membrane order. Biochemistry 29:2960–2966

    Article  PubMed  Google Scholar 

  • Sale AJH, Hamilton WA (1967) Effect of high electric field on micro organisms. I. Killing of bacteria and yeasts. Biochim Biophys Acta 148:781–788

    Google Scholar 

  • Serša G, Čemažar M, Rudolf Z (2003) Electrochemotherapy: adventages and drawbacks in treatment of cancer patient. Cancer Ther 1:133–142

    Google Scholar 

  • Šentjurc M, Štrancar J, Koklič T (2002) Membrane domain alteration under the action of biologically active substances: an EPR study. Curr Top Biophys 26:65–73

    Google Scholar 

  • Štrancar J, Šentjurc M, Schara M (2000) Fast and accurate characterization of biological membranes by EPR spectral simulation of nitroxides. J Magn Reson 142:254–265

    Article  PubMed  ADS  Google Scholar 

  • Teissié J, Eynord N, Gabriel B, Rols MP (1999) Electropermeabilization of cell membranes. Adv Drug Deliv Rev 35:3–19

    Article  PubMed  Google Scholar 

  • Tounekti O, Kenani A, Foray N, Orlowski S, Mir LM (2001) The ratio of single to double strand DNA brakes and their absolute values determine cell death pathway. Br J Cancer 84:1272–1279

    Article  PubMed  Google Scholar 

  • Valič B, Golzio M, Pavlin M, Schatz A, Faurie C, Gabriel B, Teissié J, Rols M-P, Miklavčič D (2003) Effect of electric field induced transmembrane potential on spheroidal cells: theory and experiment. Eur Biophys J Biophy 32:519–528

    Article  Google Scholar 

  • Vernhes MC, Cabanes PA, Teissié J (1999) Chinese hamster ovary cells sensitivity to localized electrical stress. Bioelectrochem Bioenerg 48:17–25

    Article  PubMed  Google Scholar 

  • Zimmermann U (1982) Electric field mediated fusion and related electrical phenomena. Biochem Biophys Acta 694:227–277

    PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by the Ministry of Education, Science and Sport of the Republic of Slovenia. The authors wish to express their thanks to Zorka Stolič from the J. Stefan Institute, Ljubljana, Slovenia, for technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Damijan Miklavčič.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kandušer, M., Šentjurc, M. & Miklavčič, D. Cell membrane fluidity related to electroporation and resealing. Eur Biophys J 35, 196–204 (2006). https://doi.org/10.1007/s00249-005-0021-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00249-005-0021-y

Key words

Navigation