Selective field effects on intracellular vacuoles and vesicle membranes with nanosecond electric pulses

Biophysical Journal

Volumn 89, Issue 1, 2005, Pages 274-284

  Tekle, Ephrem ^a   Oubrahim, Hammou ^a   Dzekunov, Sergey M ^b   Kolb, Juergen F ^c   Schoenbach, Karl H ^c   Chock, P B ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b MAXCYTE INC   (United States)

^c Old Dominion University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIOLEOYLPHOSPHATIDYLCHOLINE;

ANIMAL CELL; ARTICLE; CELL ORGANELLE; CELL PERMEABILIZATION; CELL STRAIN COS7; CELL VACUOLE; ELECTRIC CURRENT; ELECTRIC FIELD; ENDOCYTOSIS; ENDOSOME; MEMBRANE PERMEABILITY; MEMBRANE VESICLE; MODEL; NANOSECOND ELECTRIC PULSE; NONHUMAN; OUTER MEMBRANE; PHOSPHOLIPID VESICLE;

EID: 23244454422     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.054494     Document Type: Article

References (46)

1. Bullock, T. H., and W. Heiligenberg (editors). 1986. Electroreception. John Wiley, New York.
2. Song, B., M. Zhao, J. V. Forrester, and C. D. McCaig. 2002. Electrical cues regulate the orientation and frequency of cell division and the rate of wound healing in vivo. Proc. Natl. Acad. Sci. USA. 99:13577-13582.
3. Wang, E., Y. Yin, M. Zhao, J. V. Forrester, and C. D. McCaig. 2003. Physiological electric fields inhibit proliferation of vascular endothelial cells by block at G1. FASEB J. 17:458-460.
4. Astumian, R. D., P. B. Chock, and T. Y. Tsong. 1987. Absorption and conversion from dynamic electric fields by membrane proteins- electroconformational coupling. Studies Biophys. 119:123-130.
5. Potter, H. 1988. Electroporation in biology: methods, applications, and instrumentation. Anal. Biochem. 174:361-373.
6. Neumann, E., A. E. Sowers, and C. A. Jordan, eds. 1989. Electroporation and Electrofusion in Cell Biology. Plenum Press, New York.
7. Tekle, E., R. D. Astumian, and P. B. Chock. 1991. Electroporation by using bipolar oscillating electric fields: an improved method for DNA transfection of NIH3T3 cells. Proc. Natl. Acad. Sci. USA. 88:4230-4234.
8. Chang, D. C., P. Q. Gao, and B. L. Maxwell. 1991. High-efficiency gene transfection by electroporation using a radiofrequency electric-field. Biochim. Biophys. Acta. 1092:153-160.
9. Al-Atabee, J. S., B. J. Mulligan, and J. B. Powers. 1990. Interspecific somatic hybrids of Rudbeckia hirta and R. laciniata (compositae). Plant Cell Rep. 8:517-520.
10. Karsten, U., P. Stolley, I. Walther, G. Papsdorf, S. Weber, K. Conard, L. Pasternak, and J. Kopp. 1988. Direct comparison of electric field-mediated and PEG-mediated cell fusion for the generation of antibody producing hybridomas. Hybridoma. 7:627-633.
11. Mouneimne, Y., P. F. Tosi, R. Barhoumi, and C. Nicolau. 1991. Electroinsertion of xeno-proteins in red blood cell membranes yields a long lived protein carrier in circulation. Biochim. Biophys. Acta. 1066:83-89.
12. Prausnitz, M. R., V. G. Bose, R. Langer, and J. C. Weaver. 1993. Electroporation of mammalian skin- mechanism to enhance transdermal drug delivery. Proc. Natl. Acad. Sci. USA. 90:10504-10508.
13. Heller, R., M. J. Jaroszeski, L. F. Glass, J. L. Messina, D. P. Rapaport, R. C. DeConti, N. A. Fenske, R. A. Gilbert, L. M. Mir, and D. S. Reintgen. 1996. Phase I/II trial for the treatment of cutaneous and subcutaneous tumors using electrochemotherapy. Cancer. 77:964-971.
14. Mir, L. M., N. Marsili, J. R. Garbay, V. Billard, C. Robert, and M. Marty. 2003. Electrochemotherapy: a new treatment of solid tumors. J. Exp. Clin. Canc. Res. 22:145-148.
15. Teissie, J., and T. Y. Tsong. 1981. Electric field induced transient pores in phospholipid bilayer vesicles. Biochemistry. 20:1548-1554.
16. Zhelev, D. V., and D. Needham. 1993. Tension-stabilized pores in giant vesicles: determination of pore size and pore line tension. Biochim. Biophys. Acta. 1147:89-104.
17. Kakorin, S., and E. Neumann. 1998. Kinetics of the electroporative deformation of lipid vesicles and biological cells in an electric field Ber. Bunsenges Phys. Chem. 102:670-675.
18. Tekle, E., R. D. Astumian, W. A. Friauf, and P. B. Chock. 2001. Asymmetric pore distribution and loss of membrane lipid in electroporated DOPC vesicles. Biophys. J. 81:960-968.
19. - → AgBr. J. Phys. Chem. B. 102:9319-9322.
20. Correa, N. M., H. G. Zhang, and Z. A. Schelly. 2000. Preparation of AgBr quantum dots via electroporation of vesicles. J. Am. Chem. Soc. 122:6432-6434.
21. Chiu, D. T., C. F. Wilson, F. Ryttsen, A. Stromberg, C. Farre, A. Karlsson, S. Nordohm, A. Gaggar, B. P. Modi, A. Moscho, R. A. Garza-Lopez, O. Arwar, and R. N. Zaré. 1999. Chemical transformations in individual ultrasmall biomimetic containers. Science. 283:1892-1895.
22. Schwan, H. P. 1983. Biophysics of the interaction of electromagnetic energy with cells and membranes. In Biological Effects and Dosimetry of Non-Ionizing Radiation. M. Grandolfo, S.M. Michaelson, and A. Rindi, editors. Plenum Press, New York. 213-231.
23. Neumann, E., and K. Rosenheck. 1973. Potential difference across vesicular membranes. J. Membr. Biol. 14:194-196.
24. Kotnik, T., and D. Miklavicic. 2000. Analytical description of transmembrane voltage induced by electric field on spheroidal cells. Biophys. J. 79:670-679.
25. Lojewska, Z., D. L. Farkas, B. Ehrenberg, and L. M. Loew. 1989. Analysis of the effect of medium conductance on the amplitude and kinetics of the membrane potentials induced by externally applied electric fields. Biophys. J. 56:121-128.
26. Tekle, E., R. D. Astumian, and P. B. Chock. 1990. Electropermeabilization of cell membranes: effect of the resting membrane potential. Biochem. Biophys. Res. Commun. 172:282-287.
27. Hibino, M., H. Itoh, and K. Kinosita, Jr. 1993. Time course of cell electroporation as revealed by submicrosecond imaging of transmembrane potential. Biophys. J. 64:1789-1800.
28. Schoenbach, K. H., S. Katsuki, R. H. Stark, E. S. Buescher, and S. J. Beebe. 2002. Bioelectrics-new applications for pulsed power technology. IEEE Trans. Plasma Sci. 30:293-300.
29. Sixou, S., and J. Teissie. 1990. Specific electropermeabilization of leukocytes in a blood sample and application to large volume cells. Biochim. Biophys. Acta. 1028:154-160.
30. Gowrishankar, T. R., and J. C. Weaver. 2003. An approach to electrical modeling of single and multiple cells. Proc. Natl. Acad. Sci. USA. 100:3203-3208.
31. Schoenbach, K. H., S. J. Beebe, and E. S. Buescher. 2001. Intracellular effect of ultrashort electrical pulses. J. Bioelectromagnet. 22:440-448.
32. Schoenbach, K. H., R. P. Joshi, J. F. Kolb, N. Chen, M. Stacey, P. F. Blackmore, E. S. Buescher, and S. J. Beebe. 2004. Ultrashort electrical pulses open a new gateway into biological cells. Proc. IEEE. 92:1122-1137.
33. Moscho, A., O. Orwar, D. T. Chiu, B. P. Modi, and R. N. Zare. 1996. Rapid preparation of giant unilamellar vesicles. Proc. Natl. Acad. Sci. USA. 93:11443-11447.
34. Hope, M. J., M. B. Bally, G. Webb, and P. R. Cullis. 1985. Production of large unilamellar vesicles by a rapid extrusion procedure-characterization of size distribution, trapped volume and ability to maintain a membrane-potential. Biochim. Biophys. Acta. 812:55-65.
35. Tekle, E., and Z. A. Schelly. 1994. Modeling the electric birefringence relaxations of AOT/Isooctane/H2O water-in-oil microemulsions. J. Phys. Chem. 98:7657-7664.
36. Kakorin, S., E. Redeker, and E. Neumann. 1998. Electroporative deformation of salt-filled lipid vesicles. Eur. Biophys. J. 27:43-53.
37. Vernier, T. P., A. Li, L. Marcu, C. M. Craft, and M. A. Gundersen. 2003. Ultrashort pulsed electric fields induce membrane phospholipids translocation and caspase activation: differential sensitivities of Jurkat T lymphoblasts and Rat Glioma C6 cells. IEEE Trans Dielectr. Electr., Insul. 10:795-809.
38. Beebe, S. J., P. M. Fox, L. J. Rec, L. K. Willis, and K. H. Schoenbach. 2003. Nanosecond high intensity pulsed electric fields induce apoptosis in human cells. FASEB J. 30:286-292.
39. Vernier, T. P., Y. H. Sun, L. Marcu, C. M. Craft, and M. A. Gundersen. 2004. Nanoelectropore-induced phosphatidylserine translocation. Biophys. J. 86:4040-4048.
40. Brown, F. D., A. L. Rozelle, H. L. Yin, T. Balla, and J. G. Donaldson. 2001. Phosphatidylinositol 4,5-bisphosphate and Arf-regulated membrane traffic. J. Biol. Chem. 154:1007-1017.
41. White, J. A., P. F. Blackmore, K. H. Schoenbach, and S. J. Beebe. 2004. Stimulation of capacitative calcium entry in HL-60 cells by nanosecond pulsed electric fields. J. Biol. Chem. 279:22964-22972.
42. Hibino, M., M. Shigemori, H. Itoh, K. Nagayama, and K. Kinosita, Jr. 1991. Membrane conductance of electroporated cell analyzed by submicrosecond imaging of transmembrane potential. Biophys. J. 59:209-220.
43. Okada, C. Y., and M. Rechsteiner. 1982. Introduction of macromolecules into cultured mammalian cells by osmotic lysis of pinocytic vesicles. Cell. 29:33-41.
44. Wang, J., E. Tekle, H. Oubrahim, J. J. Mieyal, E. R. Stadtman, and P. B. Chock. 2003. Stable and controllable RNA interference: investigating the physiological function of glutathionylated actin. Proc. Natl. Acad. Sci. USA. 100:5103-5106.
45. Benz, R., F. Beckers, and U. Zimmermann. 1979. Reversible electrical breakdown of lipid bilayer membranes: a charge-pulse study. J. Membr. Biol. 48:181-204.
46. Muller, K. J., V. L. Sukhorukov, and U. Zimmermann. 2001. Reversible electropermeabilization of mammalian cells by high-intensity, ultra-short pulses of submicrosecond duration. J. Membr. Biol. 184:161-170.