Electroporation of intracellular liposomes using nanosecond electric pulses-a theoretical study

IEEE Transactions on Biomedical Engineering

Volumn 60, Issue 9, 2013, Pages 2624-2635

  Retelj, Lea ^a   Pucihar, Gorazd ^a   Miklavcic, Damijan ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

Electroporation; finite element model; liposomes; nanosecond (ns) electric pulses

Indexed keywords

CELL MEMBRANES; CYTOLOGY; FINITE ELEMENT METHOD; ULTRASHORT PULSES;

CYTOPLASMIC CONDUCTIVITY; ELECTRIC PULSE; ELECTROPORATION; FINITE-ELEMENT MODELS; INTRACELLULAR ORGANELLE; NUCLEAR MEMBRANES; PHYSIOLOGICAL CONDITION; THEORETICAL STUDY;

LIPOSOMES;

LIPOSOME;

ARTICLE; CELL MEMBRANE; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL ORGANELLE; CELL VIABILITY; CONTROLLED DRUG RELEASE; CYTOPLASM; DRUG DELIVERY SYSTEM; DRUG RELEASE; ELECTRIC CURRENT; ELECTRIC FIELD; ELECTRIC POTENTIAL; ELECTROCHEMICAL IMPEDANCE SPECTROSCOPY; ELECTROPORATION; FINITE ELEMENT ANALYSIS; HUMAN; HUMAN CELL; IONIC STRENGTH; LIPID VESICLE; MAMMAL CELL; MEMBRANE CONDUCTANCE; MITOCHONDRIAL MEMBRANE POTENTIAL; NANOSECOND ELECTRIC PULSE; NONHUMAN; PROCEDURES CONCERNING CELLS; BIOLOGICAL MODEL; CELL FUNCTION; CHEMISTRY; INTRACELLULAR SPACE; METABOLISM; NANOTECHNOLOGY; PROCEDURES; REPRODUCIBILITY;

CELL PHYSIOLOGICAL PHENOMENA; ELECTROPORATION; FINITE ELEMENT ANALYSIS; INTRACELLULAR SPACE; LIPOSOMES; MODELS, BIOLOGICAL; NANOTECHNOLOGY; REPRODUCIBILITY OF RESULTS;

EID: 84883014925     PISSN: 00189294     EISSN: 15582531     Source Type: Journal    
DOI: 10.1109/TBME.2013.2262177     Document Type: Article

References (72)

1. M. Hibino, M. Shigemori, H. Itoh, K. Nagayama, and K. Kinosita Jr, "Membrane conductance of an electroporated cell analyzed by submicrosecond imaging of transmembrane potential," Biophys. J., vol. 59, no. 1, pp. 209-220, Jan. 1991.
2. T. Kotnik, G. Pucihar, and D. Miklavcic, "Induced transmembrane voltage and its correlation with electroporation-mediated molecular transport," J. Membr. Biol., vol. 236, no. 1, pp. 3-13, Jul. 2010.
3. T. Y. Tsong, "Electroporation of cell membranes," Biophys. J., vol. 60, no. 2, pp. 297-306, Aug. 1991.
4. J. Teissíe and M. P. Rols, "An experimental evaluation of the critical potential difference inducing cell membrane electropermeabilization, " Biophys. J., vol. 65, no. 1, pp. 409-413, Jul. 1993. (Pubitemid 23206073)
5. E. Neumann, M. Schaefer-Ridder, Y. Wang, and P. H. Hofschneider, "Gene transfer into mouse lyoma cells by electroporation in high electric fields," EMBO J., vol. 1, no. 7, pp. 841-845, 1982.
6. Z. Vasilkoski, A. T. Esser, T. R. Gowrishankar, and J. C. Weaver, "Membrane electroporation: The absolute rate equation and nanosecond time scale pore creation," Phys. Rev. E, vol. 74, no. 2, pp. 021904-1-021904-12, Aug. 2006.
7. A. A. Gurtovenko, J. Anwar, and I. Vattulainen, "Defect-mediated trafficking across cell membranes: Insights from in silico modeling," Chem. Rev., vol. 110, no. 10, pp. 6077-6103, Oct. 2010.
8. L. Delemotte and M. Tarek, "Molecular dynamics simulations of lipid membrane electroporation," J. Membr. Biol., vol. 245, no. 9, pp. 531-543, Sep. 2012.
9. U. Zimmermann, P. Gessner, R. Schnettler, S. Perkins, and S. K. Foung, "Efficient hybridization of mouse-human cell lines by means of hypoosmolar electrofusion," J. Immunol. Methods, vol. 134, no. 1, pp. 43-50, Nov. 1990. (Pubitemid 20350986)
10. M. Ussaj and M. Kanduser, "The systematic study of the electroporation and electrofusion of B16-F1 and CHO cells in isotonic and hypotonic buffer," J. Membr. Biol., vol. 245, no. 9, pp. 583-590, Sep. 2012.
11. R. Heller, M. J. Jaroszeski, D. S. Reintgen, C. A. Puleo, R. C. DeConti, R. A. Gilbert, and L. F. Glass, "Treatment of cutaneous and subcutaneous tumors with electrochemotherapy using intralesional bleomycin," Cancer, vol. 83, no. 1, pp. 148-157, Jul. 1998. (Pubitemid 28299641)
12. L. M. Mir, J. Gehl, G. Sersa, C. G. Collins, J.-R. Garbay, V. Billard, P. F. Geertsen, Z. Rudolf, G. C. O'Sullivan, and M. Marty, "Standard operating procedures of the electrochemotherapy: Instructions for the use of bleomycin or cisplatin administered either systemically or locally and electric pulses delivered by the CliniporatorTM by means of invasive or non-invasive electrodes," Eur. J. Cancer Suppl., vol. 4, no. 11, pp. 14-25, Nov. 2006. (Pubitemid 44755132)
13. G. Sersa, T. Coufer, S. M. Paulin, M. Caemazar, and M. Snoj, "Electrochemotherapy of chest wall breast cancer recurrence," Cancer Treat. Rev., vol. 38, no. 5, pp. 379-386, Aug. 2012.
14. J. Teissíe, J. M. Escoffre, A. Paganin, S. Chabot, E. Bellard, L.Wasungu, M. P. Rols, and M. Golzio, "Drug delivery by electropulsation: Recent developments in oncology," Int. J. Pharm., vol. 423, no. 1, pp. 3-6, Feb. 2012.
15. M. Bettan, M. A. Ivanov, L. M. Mir, F. Boissìere, P. Delaere, and D. Scherman, "Efficient DNA electrotransfer into tumors," Bioelectrochemistry, vol. 52, no. 1, pp. 83-90, Sep. 2000.
16. M. Kanduser, D. Miklavcic, and M. Pavlin, "Mechanisms involved in gene electrotransfer using high-and low-voltage pulses-an in vitro study," Bioelectrochemistry, vol. 74, no. 2, pp. 265-271, Feb. 2009.
17. J. M. Escoffre, T. Portet, C. Favard, J. Teissíe, D. S. Dean, and M. P. Rols, "Electromediated formation of DNA complexes with cell membranes and its consequences for gene delivery," Biochim. Biophys. Acta, vol. 1808, no. 6, pp. 1538-1543, Jun. 2011.
18. N. J. Rowan, S. J. MacGregor, J. G. Anderson, R. A. Fouracre, and O. Farish, "Pulsed electric field inactivation of diarrhoeagenic Bacillus cereus through irreversible electroporation," Lett. Appl. Microbiol., vol. 31, no. 2, pp. 110-114, Aug. 2000. (Pubitemid 30658991)
19. S. Toepfl, V. Heinz, and D. Knorr, "High intensity pulsed electric fields applied for food preservation," Chem. Eng. Process.: Process Intensif., vol. 46, no. 6, pp. 537-546, Jun. 2007. (Pubitemid 46329842)
20. T. R. Gowrishankar, A. T. Esser, Z. Vasilkoski, K. C. Smith, and J. C.Weaver, "Microdosimetry for conventional and supra-electroporation in cells with organelles," Biochem. Biophys. Res. Commun., vol. 341, no. 4, pp. 1266-1276, Mar. 2006. (Pubitemid 43224242)
21. K. H. Schoenbach, S. J. Beebe, and E. S. Buescher, "Intracellular effect of ultrashort electrical pulses," Bioelectromagnetics, vol. 22, no. 6, pp. 440-448, Sep. 2001. (Pubitemid 33617706)
22. E. Tekle, H. Oubrahim, S. M. Dzekunov, J. F. Kolb, K. H. Schoenbach, and P. B. Chock, "Selective field effects on intracellular vacuoles and vesicle membranes with nanosecond electric pulses," Biophys. J., vol. 89, no. 1, pp. 274-284, Jul. 2005. (Pubitemid 41098282)
23. T. Batista Napotnik, M. Rebersek, T.Kotnik, E. Lebrasseur,G.Cabodevila, and D. Miklavcic, "Electropermeabilization of endocytotic vesicles in B16 F1 mouse melanoma cells," Med. Biol. Eng. Comput., vol. 48, no. 5, pp. 407-413, May 2010.
24. N. Chen, K. H. Schoenbach, J. F. Kolb, R. J. Swanson, A. L. Garner, J.Yang, R. P. Joshi, and S. J.Beebe, "Leukemic cell intracellular responses to nanosecond electric fields," Biochem. Biophys. Res. Commun., vol. 317, no. 2, pp. 421-427, Apr. 2004. (Pubitemid 38452500)
25. T. Batista Napotnik, Y. H. Wu, M. A. Gundersen, D. Miklavcic, and P. T. Vernier, "Nanosecond electric pulses cause mitochondrial membrane permeabilization in Jurkat cells," Bioelectromagnetics, vol. 33, no. 3, pp. 257-264, Apr. 2012.
26. P. T. Vernier, Y. Sun, L. Marcu, S. Salemi, C. M. Craft, and M. A. Gundersen, "Calcium bursts induced by nanosecond electric pulses," Biochem. Biophys. Res. Commun., vol. 310, no. 2, pp. 286-295, Oct. 2003. (Pubitemid 37163662)
27. S. S. Scarlett, J. A. White, P. F. Blackmore, K. H. Schoenbach, and J. F. Kolb, "Regulation of intracellular calcium concentration by nanosecond pulsed electric fields," Biochim. Biophys. Acta, vol. 1788, no. 5, pp. 1168-1175, May 2009.
28. S. J. Beebe, J. White, P. F. Blackmore, Y. Deng, K. Somers, and K. H. Schoenbach, "Diverse effects of nanosecond pulsed electric fields on cells and tissues," DNA Cell Biol., vol. 22, no. 12, pp. 785-796, Dec. 2003. (Pubitemid 38033001)
29. A. G. Pakhomov, A. Phinney, J. Ashmore, K.Walker, J. F. Kolb, S. Kono, K. H. Schoenbach, and M. R. Murphy, "Characterization of the cytotoxic effect of high-intensity, 10-ns duration electrical pulses," IEEE Trans. Plasma Sci., vol. 32, no. 4, pp. 1579-1586, Aug. 2004.
30. J. Song, R. P. Joshi, and K. H. Schoenbach, "Synergistic effects of local temperature enhancements on cellular responses in the context of highintensity, ultrashort electric pulses," Med. Biol. Eng. Comput., vol. 49, no. 6, pp. 713-718, Jun. 2011.
31. H. Hillaireau and P. Couvreur, "Nanocarriers' entry into the cell: relevance to drug delivery," Cell. Mol. Life Sci., vol. 66, no. 17, pp. 2873-2896, Sep. 2009.
32. L. Huang and Y. Liu, "In vivo delivery of RNAi with lipid-based nanoparticles," Annu. Rev. Biomed. Eng., vol. 13, pp. 507-530, Aug. 2011.
33. T. Benvegnu, L. Lemìegre, and S. Cammas-Marion, "New generation of liposomes called archaeosomes based on natural or synthetic archaeal lipids as innovative formulations for drug delivery," Recent. Pat. Drug Del. Formul., vol. 3, no. 3, pp. 206-220, Nov. 2009.
34. G. B. Patel andW. Chen, "Archaeosomes as drug and vaccine nanodelivery systems," in Nanocarrier Technologies, M. R. Mozafari, Ed. Dordrecht, the Netherlands: Springer-Verlag, 2006, pp. 17-40.
35. G. D. Sprott, S. Sad, L. P. Fleming, C. J. Dicaire, G. B. Patel, and L. Krishnan, "Archaeosomes varying in lipid composition differ in receptor-mediated endocytosis and differentially adjuvant immune responses to entrapped antigen," Archaea, vol. 1, no. 3, pp. 151-164, Oct. 2003. (Pubitemid 38871643)
36. S. J. Beebe, P. M. Fox, L. J. Rec, K. Somers, R. H. Stark, and K. H. Schoenbach, "Nanosecond pulsed electric field (nsPEF) effects on cells and tissues: Apoptosis induction and tumor growth inhibition," IEEE Trans. Plasma Sci., vol. 30, no. 1, pp. 286-292, Feb. 2002. (Pubitemid 34720873)
37. S. Beebe, N. Sain, and W. Ren, "Induction of cell death mechanisms and apoptosis by nanosecond pulsed electric fields (nsPEFs)," Cells, vol. 2, no. 1, pp. 136-162, Mar. 2013.
38. E. H. Hall, K. H. Schoenbach, and S. J. Beebe, "Nanosecond pulsed electric fields induce apoptosis in p53-wildtype and p53-null HCT116 colon carcinoma cells," Apoptosis, vol. 12, no. 9, pp. 1721-1731, Sep. 2007. (Pubitemid 47106883)
39. K. Schoenbach, B. Hargrave, R. Joshi, J. Kolb, R. Nuccitelli, C. Osgood, A. Pakhomov, M. Stacey, R. Swanson, J. White, S. Xiao, J. Zhang, S. Beebe, P. Blackmore, and E. Buescher, "Bioelectric effects of intense nanosecond pulses," IEEE Trans. Dielectr. Electr. Insul., vol. 14, no. 5, pp. 1088-1109, Oct. 2007.
40. R. Nuccitelli, X. Chen, A. G. Pakhomov, W. H. Baldwin, S. Sheikh, J. L. Pomicter,W. Ren, C. Osgood, R. J. Swanson, J. F. Kolb, S. J. Beebe, and K. H. Schoenbach, "A new pulsed electric field therapy for melanoma disrupts the tumor's blood supply and causes complete remission without recurrence," Int. J. Cancer, vol. 125, no. 2, pp. 438-445, Jul. 2009.
41. R. Nuccitelli, K. Tran, S. Sheikh, B. Athos, M. Kreis, and P. Nuccitelli, "Optimized nanosecond pulsed electric field therapy can cause murine malignant melanomas to self-destruct with a single treatment," Int. J. Cancer, vol. 127, no. 7, pp. 1727-1736, Oct. 2010.
42. A. G. Pakhomov, R. Shevin, J. A. White, J. F. Kolb, O. N. Pakhomova, R. P. Joshi, and K. H. Schoenbach, "Membrane permeabilization and cell damage by ultrashort electric field shocks," Arch. Biochem. Biophys., vol. 465, no. 1, pp. 109-118, Sep. 2007. (Pubitemid 47283984)
43. B. L. Ibey, A. G. Pakhomov, B. W. Gregory, V. A. Khorokhorina, C. C. Roth, M. A. Rassokhin, J. A. Bernhard, G. J. Wilmink, and O. N. Pakhomova, "Selective cytotoxicity of intense nanosecond-duration electric pulses in mammalian cells," Biochim. Biophys. Acta, vol. 1800, no. 11, pp. 1210-1219, Nov. 2010.
44. B. L. Ibey, C. C. Roth, A. G. Pakhomov, J. A. Bernhard, G. J. Wilmink, and O. N. Pakhomova, "Dose-dependent thresholds of 10-ns electric pulse induced plasma membrane disruption and cytotoxicity in multiple cell lines," PLoS ONE, vol. 6, no. 1, pp. e15642-1-e15642-11, 2011.
45. J. F. Kolb, S. Kono, and K. H. Schoenbach, "Nanosecond pulsed electric field generators for the study of subcellular effects," Bioelectromagnetics, vol. 27, no. 3, pp. 172-187, Apr. 2006.
46. J. Sanders, A. Kuthi, Y. H. Wu, P. Vernier, and M. Gundersen, "A linear, single-stage, nanosecond pulse generator for delivering intense electric fields to biological loads," IEEE Trans. Dielectr. Electr. Insul., vol. 16, no. 4, pp. 1048-1054, Aug. 2009.
47. G. Pucihar, T. Kotnik, B. Valinc, and D. Miklavcic, "Numerical determination of transmembrane voltage induced on irregularly shaped cells," Ann. Biomed. Eng., vol. 34, no. 4, pp. 642-652, Apr. 2006.
48. G. Pucihar, D. Miklavcic, and T. Kotnik, "A time-dependent numerical model of transmembrane voltage inducement and electroporation of irregularly shaped cells," IEEE Trans. Biomed. Eng., vol. 56, no. 5, pp. 1491-1501, May 2009.
49. K. A. DeBruin andW. Krassowska, "Modeling electroporation in a single cell. I. Effects Of field strength and rest potential," Biophys. J., vol. 77, no. 3, pp. 1213-1224, Sep. 1999. (Pubitemid 29407298)
50. R. W. Glaser, S. L. Leikin, L. V. Chernomordik, V. F. Pastushenko, and A. I. Sokirko, "Reversible electrical breakdown of lipid bilayers: Formation and evolution of pores," Biochim. Biophys. Acta, vol. 940, no. 2, pp. 275-287, May 1988.
51. D. Gmajner, P. Ahlin Grabnar, M. Znidaric Tursek, J. Strus, M. Sentjurc, and N. Poklar Ulrih, "Structural characterization of liposomes made of diether archaeal lipids and dipalmitoyl-L-?-phosphatidylcholine," Biophys. Chem., vol. 158, no. 2-3, pp. 150-156, Oct. 2011.
52. A. Di Biasio andC.Cametti, "Dielectric properties of aqueous zwitterionic liposome suspensions," Bioelectrochemistry, vol. 70, no. 2, pp. 328-334, May 2007. (Pubitemid 46509871)
53. M. Pavlin, M. Kanduser, M. Rebersek, G. Pucihar, F. X. Hart, R. Magjarevíc, and D. Miklavcic, "Effect of cell electroporation on the conductivity of a cell suspension," Biophys. J., vol. 88, no. 6, pp. 4378-4390, Jun. 2005. (Pubitemid 40991146)
54. A. L. Garner, G. Chen, N. Chen, V. Sridhara, J. F. Kolb, R. J. Swanson, S. J. Beebe, R. P. Joshi, and K. H. Schoenbach, "Ultrashort electric pulse induced changes in cellular dielectric properties," Biochem. Biophys. Res. Commun., vol. 362, no. 1, pp. 139-144, Oct. 2007. (Pubitemid 47304405)
55. K. C. Smith and J. C. Weaver, "Transmembrane molecular transport during versus after extremely large, nanosecond electric pulses," Biochem. Biophys. Res. Commun., vol. 412, no. 1, pp. 8-12, Aug. 2011.
56. Y. Polevaya, I. Ermolina, M. Schlesinger, B. Z. Ginzburg, and Y. Feldman, "Time domain dielectric spectroscopy study of human cells-Part II: Normal and malignant white blood cells," Biochim. Biophys. Acta, vol. 1419, no. 2, pp. 257-271, Jul. 1999. (Pubitemid 29322715)
57. M. Mazzanti, J. O. Bustamante, and H. Oberleithner, "Electrical dimension of the nuclear envelope," Physiol. Rev., vol. 81, no. 1, pp. 1-19, Jan. 2001. (Pubitemid 32096171)
58. T.Kotnik andD.Miklavcic, "Theoretical evaluation of voltage inducement on internal membranes of biological cells exposed to electric fields," Biophys. J., vol. 90, no. 2, pp. 480-491, Jan. 2006.
59. A. Irimajiri, K. Asami, T. Ichinowatari, and Y. Kinoshita, "Passive electrical properties of the membrane and cytoplasm of cultured rat basophil leukemia cells-Part II: Effects of osmotic perturbation," Biochim. Biophys. Acta, vol. 896, no. 2, pp. 214-223, Jan. 1987. (Pubitemid 17002015)
60. V. L. Sukhorukov, R. Reuss, D. Zimmermann, C. Held, K. J. M̈uller, M. Kiesel, P. Gessner, A. Steinbach, W. A. Schenk, E. Bamberg, and U. Zimmermann, "Surviving high-intensity field pulses: Strategies for improving robustness and performance of electrotransfection and electrofusion," J. Membr. Biol., vol. 206, no. 3, pp. 187-201, Aug. 2005. (Pubitemid 43199137)
61. G. Pucihar, T. Kotnik, M. Kanduser, and D. Miklavcic, "The influence of medium conductivity on electropermeabilization and survival of cells in vitro," Bioelectrochemistry, vol. 54, no. 2, pp. 107-115, Nov. 2001. (Pubitemid 32990047)
62. K. C. Smith and J. C.Weaver, "Active mechanisms are needed to describe cell responses to submicrosecond, megavolt-per-meter pulses: cell models for ultrashort pulses," Biophys. J., vol. 95, no. 4, pp. 1547-1563, Aug. 2008.
63. M. Stacey, J. Stickley, P. Fox, V. Statler, K. Schoenbach, S. J. Beebe, and S. Buescher, "Differential effects in cells exposed to ultra-short, high intensity electric fields: Cell survival,DNAdamage, and cell cycle analysis," Mutat. Res., vol. 542, no. 1-2, pp. 65-75, Dec. 2003. (Pubitemid 37486099)
64. M. Stacey, P. Fox, S. Buescher, and J. Kolb, "Nanosecond pulsed electric field induced cytoskeleton, nuclear membrane and telomere damage adversely impact cell survival," Bioelectrochemistry, vol. 82, no. 2, pp. 131-134, Oct. 2011.
65. R. P. Joshi, A. Nguyen, V. Sridhara, Q. Hu, R. Nuccitelli, S. J. Beebe, J. Kolb, and K. H. Schoenbach, "Simulations of intracellular calcium release dynamics in response to a high-intensity, ultrashort electric pulse," Phys. Rev. E, vol. 75, no. 4, pp. 041920-1-041920-10, Apr. 2007.
66. B. L. Ibey, D. G. Mixon, J. A. Payne, A. Bowman, K. Sickendick, G. J. Wilmink, W. P. Roach, and A. G. Pakhomov, "Plasma membrane permeabilization by trains of ultrashort electric pulses," Bioelectrochemistry, vol. 79, no. 1, pp. 114-121, Aug. 2010.
67. P. T. Vernier, Y. Sun, and M. A. Gundersen, "Nanoelectropulse-driven membrane perturbation and small molecule permeabilization," BMC Cell Biol., vol. 7, pp. 37-1-37-16, 2006.
68. A. M. Bowman, O. M. Nesin, O. N. Pakhomova, and A. G. Pakhomov, "Analysis of plasma membrane integrity by fluorescent detection of Tl+ uptake," J. Membr. Biol., vol. 236, no. 1, pp. 15-26, Jul. 2010.
69. O. M. Nesin, O. N. Pakhomova, S. Xiao, and A. G. Pakhomov, "Manipulation of cell volume andmembrane pore comparison following single cell permeabilization with 60-and 600-ns electric pulses," Biochim. Biophys. Acta, vol. 1808, no. 3, pp. 792-801, Mar. 2011.
70. M. Caemazar, T. Jarm, D. Miklavcic, A. Maceek Lebar, A. Ihan, N. A. Kopitar, and G. Sersa, "Effect of electric-field intensity on electropermeabilization and electrosensitivity of various tumor-cell lines in vitro," Electro. Magnetobiol., vol. 17, no. 2, pp. 263-272, Jan. 1998.
71. A. Silve, I. Leray, and L. M. Mir, "Demonstration of cell membrane permeabilization to medium-sized molecules caused by a single 10 ns electric pulse," Bioelectrochemistry, vol. 87, pp. 260-264, Oct. 2012.
72. M. Breton, L. Delemotte, A. Silve, L. M. Mir, and M. Tarek, "Transport of siRNA through lipid membranes driven by nanosecond electric pulses: an experimental and computational study," J. Amer. Chem. Soc., vol. 134, no. 34, pp. 13938-13941, Aug. 2012.