The spatially distributed dynamic transmembrane voltage of cells and organelles due to 10 ns pulses: Meshed transport networks

IEEE Transactions on Plasma Science

Volumn 34, Issue 4 II, 2006, Pages 1394-1404

  Smith, Kyle C ^a,b   Gowrishankar, T R ^a   Esser, Axel T ^a   Stewart, Donald A ^a   Weaver, James C ^a  

^a HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

^b USA   (United States)

Author keywords

Asymptotic electroporation model; Meshed transport network; Nanosecond electric field pulses; Supraelectroporation

Indexed keywords

COMPUTATIONAL GEOMETRY; COMPUTER SIMULATION; ELECTRIC CURRENTS; ELECTRIC FIELDS; ELECTRIC POTENTIAL; MATHEMATICAL MODELS; PLASMA DIAGNOSTICS;

ASYMPTOTIC ELECTROPORATION MODEL; MESHED TRANSPORT NETWORK; NANOSECOND ELECTRIC FIELD PULSES; ORGANELLES; PLASMA MEMBRANE; SUPRAELECTROPORATION; TRANSMEMBRANE VOLTAGE;

CELL MEMBRANES;

EID: 33747863576     PISSN: 00933813     EISSN: None     Source Type: Journal    
DOI: 10.1109/TPS.2006.878436     Document Type: Article

References (63)

1. Electroporation and Electrofusion in Cell Biology, E. Neumann, A. E. Sowers, and C. A. Jordan, Eds. New York: Plenum, 1989.
2. J. C. Weaver, "Electroporation: A general phenomenon for manipulating cells and tissue," J. Cell. Biochem., vol. 51, no. 4, pp. 426-435, Apr. 1993.
3. J. A. Nickoloff, Ed., Methods in Molecular Biology, Electroporation Protocols for Microorganisms, vol. 47. Totowa, NJ: Humana Press, 1995.
4. J. A. Nickoloff, Ed., Methods in Molecular Biology, Animal Cell Electroporation & Electrofusion Protocols, vol. 48. Totowa, NJ: Humana Press, 1995.
5. J. A. Nickoloff, Ed., Methods in Molecular Biology, Plant Cell Electroporation & Electrofusion Protocols, vol. 55. Totowa, NJ: Humana Press, 1995.
6. L. M. Mir, S. Orlowski, J. Belehradek, J. Teissie, M. P. Rols, G. Sersa, D. Miklavčič, R. Gilbert, and R. Heller, "Biomedical applications of electric pulses with special emphasis on antitumor electrochemotherapy," Bioelectrochem. Bioenerg., vol. 38, no. 1, pp. 203-207, Aug. 1995.
7. Electrically Mediated Delivery of Molecules to Cells: Electrochemotherapy, Electrogenetherapy and Transdermal Delivery by Electroporation, M. J. Jaroszeski, R. Gilbert, and R. Heller, Eds. Totowa, NJ: Humana Press, 2000.
8. J. C. Weaver, "Electroporation of biological membranes from multicellular to nano scales," IEEE Trans. Dielectr. Electr. Insul., vol. 10, no. 5, pp. 754-768, Oct. 2003.
9. M. Belehradek, C. Domenge, B. Luboinski, S. Orlowski, J. Belehradek, Jr., and L. M. Mir, "Electrochemotherapy, a new antitumor treatment. First clinical phase I-II trial," Cancer, vol. 72, no. 12, pp. 3694-3700, Dec. 1993.
10. A. Gothelf, L. M. Mir, and J. Gehl, "Electrochemotherapy: Results of cancer treatment using enhanced delivery of bleomycin by electroporation," Cancer Treat. Rev., vol. 29, no. 5, pp. 371-387, Oct. 2003.
11. R. Heller, "Delivery of plasmid DNA using in vivo electroporation," Preclinica, vol. 1, pp. 198-208, 2003.
12. D. P. Tieleman, H. Leontiadou, A. E. Mark, and S.-J. Marrink, "Simulation of pore formation in lipid bilayers by mechanical stress and electric fields," J. Amer Chem. Soc., vol. 125, no. 21, pp. 6382-6383, May 2003.
13. D. P. Tieleman, "The molecular basis of electroporation," BMC Biochem., vol. 5, no. 1, p. 10, 2004.
14. Q. Hu, S. Viswandham, R. P. Josh, K. H. Schoenbach, S. J. Beebe, and P. F. Blackmore, "Simulations of transient membrane behavior in cells subject to a high-intensity ultrashort electric pulse," Phys. Rev. E, Stat. Phys. Plasmas Fluids Relat. Interdiscip. Top., vol. 71, no. 3, pp. 03194-1-03194-9, Mar. 2005.
15. A. A. Gurtovenko and I. Vattulainen, "Pore formation coupled to ion transport through lipid membranes as induced by transmembrane ionic charge imbalance: Atomistic molecular dynamics study," J. Amer. Chem. Soc., vol. 127, no. 50, pp. 17570-17571, 2005.
16. K. H. Schoenbach, S. J. Beebe, and E. S. Buescher, "Intracellular effect of ultrashort pulses," Bioelectromagnetics, vol. 22, no. 6, pp. 440-448, Sep. 2001.
17. 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.
18. S. J. Beebe, P. M. Fox, L. J. Rec, L. K. Willis, and K. H. Schoenbach, "Nanosecond, high intensity pulsed electric fields induce apoptosis in human cells," FASEB J., vol. 17, no. 11, pp. 1493-1495, Aug. 2003.
19. 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.
20. J. Deng, K. H. Schoenbach, E. S. Buescher, P. S. Hair, P M. Fox, and S. J. Bebe, "The effects of intense submicrosecond electrical pulses on cells," Biophys. J., vol. 84, no. 4, pp. 2709-2714, 2003.
21. E. S. Buescher and K. H. Schoenbach, "The effects of submicrosecond, high intensity pulsed electric fields on living cells - intracellular electromanipulation," IEEE Trans. Dielectr. Electr. Insul., vol. 10, no. 5, pp. 788-794, Oct. 2003.
22. P. S. Hair, K. H. Schoenbach, and E. S. Buescher, "Submicrosecond, intense pulsed electric field applications to cells show specificity of effects," Bioelectrochemistry, vol. 61, no. 1/2, pp. 65-72, Oct. 2003.
23. P. T. Vernier, L. I. Aimin, L. Marcu, C. M. Craft, and M. A. Gundersen, "Ultrashort pulsed electric fields induce membrane phospholipid translocation and capase activation: Differential sensitivities of Jurkat T lymphoblasts and rat glioma C6 cells," IEEE Trans. Dielectr. Electr. Insul., vol. 10, no. 5, pp. 795-809, Oct. 2003.
24. S. J. Beebe, J. White, P. F. Blackmore, Y. Deng, K. Sommers, 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.
25. 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, DNA damage, and cell cycle analysis," Mutat. Res., vol. 542, no. 1/2, pp. 65-75, Dec. 2003.
26. J. A. White, P. F. Blackmore, K. H. Schoenbach, and S. J. Beebe, "Stimulation of capacitive calcium entry in HL-60 cells by nanosecond pulsed electric fields (nsPEF)," J. Biol. Chem., vol. 279, no. 22, pp. 22964-22972, May 2004.
27. 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.
28. P. T. Vernier, Y. Sun, L. Marcu, C. M. Craft, and M. A. Gundersen, "Nanoelectropulse-induced phosphatidylserine translocation," Biophys. J., vol. 86, no. 6, pp. 4040-4048, Jun. 2004.
29. K. H. Schoenbach, R. P. Joshi, J. R. Kolb, N. Chen, M. Stacey, P. F. Blackmore, E. S. Buescher, and S. J. Beebe, "Ultrashort electrical pulses open a new gateway into biological cells," Proc. Inst. Electr. Eng., vol. 92, no. 7, pp. 1122-1137, Jul. 2004.
30. D. A. Stewart, T. R. Gowrishankar, and J. C. Weaver, "Transport lattice approach to describing cell electroporation: Use of a local asymptotic model," IEEE Trans. Plasma Sci., vol. 32, no. 4, pp. 1696-1708, Aug. 2004.
31. T. R. Gowrishankar, A. T. Esser, Z. Vasilkoski, K. C. Smith, and J. C. Weaver, "Microdosimetry for conventional and supraelectroporation in cells with organelles," Biochem. Biophys. Res. Commun., vol. 341, no. 4, pp. 1266-1276, Mar. 2006.
32. A. Barnett and J. C. Weaver, "Electroporation: A unified, quantitative theory of reversible electrical breakdown and rupture," Bioelectrochem. Bioenerg., vol. 25, pp. 163-182, 1991.
33. S. A. Freeman, M. A. Wang, and J. C. Weaver, "Theory of electroporation for a planar bilayer membrane: Predictions of the fractional aqueous area, change in capacitance and pore-pore separation," Biophys. J., vol. 67, pp. 42-56, 1994.
34. K. A. DeBruin and W. Krassowska, "Electroporation and shock-induced transmembrane potential in a cardiac fiber during defibrillation strength shocks," Ann. Biomed. Eng., vol. 26, no. 4, pp. 584-596, Jul./Aug. 1998.
35. R. P. Joshi and K. H. Schoenbach, "Electroporation dynamics in biological cells subjected to ultrafast electrical pulses: A numerical simulation study," Phys. Rev. E, Stat. Phys. Plasmas Fluids Relat. Interdiscip. Top., vol. 62, no. 1, pp. 1025-1033, Jul. 2000.
36. R. P. Joshi, Q. Hu, R. Aly, K. H. Schoenbach, and H. P. Hjalmarson, "Self-consistent simulations of electroporation dynamics in biological cells subjected to ultrashort pulses," Phys. Rev. E, Stat. Phys. Plasmas Fluids Relat. Interdiscip. Top., vol. 64, no. 1, pp. 011913-1-011913-10, Jul. 2001.
37. R. P. Joshi, Q. Hu, K. H. Schoenbach, and H. P. Hjalmarson, "Improved energy model for membrane electroporation in biological cells subjected to electrical pulses," Phys. Rev. E, Stat. Phys. Plasmas Fluids Relat. Interdiscip. Top., vol. 65, no. 4, pp. 041920-1-041920-8, Apr. 2002.
38. R. P. Joshi and K. H. Schoenbach, "Mechanism for membrane electroporation irreversibility under high-intensiy, ultrashort pulse conditions," Phys. Rev. E, Stat. Phys. Plasmas Fluids Relat. Interdiscip. Top., vol. 66, no. 5, pp. 052901-1-052901-4, Nov. 2002.
39. K. C. Smith, J. C. Neu, and W. Krassowska, "Model of creation and evolution of stable electropores for DNA delivery," Biophys. J., vol. 86, no. 5, pp. 2813-2826, May 2004.
40. R. P. Joshi, Q. Hu, K. H. Schoenbach, and S. J. Beebe, "Energy landscape-model analysis for irreversibility and its pulse-width dependence in cells subjected to a high-intensity ultrashort electric pulse," Phys. Rev. E, Stat. Phys. Plasmas Fluids Relat. Interdiscip. Top., vol. 69, no. 5, pp. 051901-1-051901-10, May 2004.
41. T. R. Gowrishankar and J. C. Weaver, "An approach to electrical modeling of single and multiple cells," Proc. Nat. Acad. Sci., vol. 100, no. 6, pp. 3203-3208, Mar. 2003.
42. D. C. Mikulecky, "Network thermodynamic simulation of biological systems: An overview," Math. Comput. Simul., vol. 24, no. 6, pp. 437-441, Dec. 1982.
43. T. R. Gowrishankar, D. A. Stewart, G. T. Martin, and J. C. Weaver, "Transport lattice models of heat transport in skin with spatially heterogeneous, temperature-dependent perfusion," Biomed. Eng. Online, vol. 3, no. 1, p. 42, Nov. 2004.
44. T. R. Gowrishankar, D. Stewart, and J. C. Weaver, "Model of a confined spherical cell in uniform and heterogeneous applied electric fields "Bioelectrochemistry, vol. 68, no. 2, pp. 181-190, May 2006.
45. D. A. Stewart, T. R. Gowrishankar, and J. C. Weaver, "Three dimensional transport lattice model for describing action potentials in axons stimulated by external electrodes," Bioelectrochemistry, vol. 69, pp. 88-93, 2006.
46. D. A. Stewart, T. R. Gowrishankar, and J. C. Weaver, "Skin heating and injury by prolonged millimeter wave exposure: Theory based on a skin model coupled to a whole body model and local biochemical release from cells at supraphysiologic temperatures," IEEE Trans. Plasma Sci., vol. 34, no. 4, Pt. 2, pp. 1480-1493, Aug. 2006.
47. D. A. Stewart, T. R. Gowrishankar, K. C. Smith, and J. C. Weaver, "Cylindrical cell membranes in uniform applied electric fields: Validation of a transport lattice method," IEEE Trans. Biomed. Eng., vol. 52, no. 10, pp. 1643-1653, Oct. 2005.
48. K. C. Smith, "Modeling cell and tissue electroporation," M.S. thesis, 2006.
49. P. Persson and G. Strang, "A simple mesh generator in matlab," SIAM Rev., vol. 46, no. 2, pp. 329-345, 2004.
50. K. A. DeBruin and W. Krassowska, "Modeling electroporation in a single cell: I. Effects of field strength and rest potential," Biophys. J., vol. 77, no. 3, pp. 1213-1224, 1999.
51. J. C. Neu and W. Krassowska, "Asymptotic model of electroporation," Phys. Rev. E, Stat. Phys. Plasmas Fluids Relat. Interdiscip. Top., vol. 59, no. 3, pp. 3471-3482, Mar. 1999.
52. Z. Vasilkoski, A. T. Esser, T. R. Gowrishankar, and J. C. Weaver, "Membrane electroporation: The absolute rate equation and nanosecond timescale pore creation," Phys. Rev. E, Stat. Phys. Plasmas Fluids Relat. Interdiscip. Top., submitted for publication.
53. V. F. Pastushenko, Y. A. Chizmadzhev, and V. B. Arakelyan, "Electric breakdown of bilayer membranes: II. Calculation of the membrane lifetime in the steady-state diffusion approximation," Bioelectrochem. Bioenerg., vol. 6, pp. 53-62, 1979.
54. V. B. Arakelyan, Y. A. Chizmadzhev, and V. F. Pastushenko, "Electric breakdown of bilayer membranes: V. consideration of the kinetic stage in the case of the membrane containing an arbitrary number of defects," Bioelectrochem. Bioenerg., vol. 6, pp. 81-87, 1979.
55. V. F. Pastushenko, V. B. Arakelyan, and Y. A. Chizmadzhev, "Electric breakdown of bilayer membranes: VI. A stochastic theory taking into account the processes of defect formation and death: Membrane lifetime distribution function," Bioelectrochem. Bioenerg., vol. 6, pp. 89-95, 1979.
56. V. F. Pastushenko, V. B. Arakelyan, and Y. A. Chizmadzhev, "Electric breakdown of bilayer membranes: VII. A stochastic theory taking into account the processes of defect formation and death: Statistical properties," Bioelectrochem. Bioenerg., vol. 6, pp. 97-104, 1979.
57. K. T. Powell and J. C. Weaver, "Transient aqueous pores in bilayer membranes: A statistical theory," Bioelectrochem. Bioelectroenerg., vol. 15, pp. 211-227, 1986.
58. 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.
59. G. Kron, "Electric circuits models of the Schroedinger equation," Phys. Rev., vol. 67, no. 1/2, pp. 39-43, Jan. 1945.
60. A. T. Esser,. Unpublished.
61. A. Vladimirescu, The SPICE Book. New York: Wiley, 1994.
62. M. Hibino, H. Itoh, and K. Kinosita, "Time courses of cell electroporation as revealed by submicrosecond imaging of transmembrane potential," Biophys. J., vol. 64, no. 6, pp. 1789-1800, Jun. 1993.
63. W. Frey, J. A. White, R. O. Price, P. F. Blackmore, R. P. Joshi, R. Nuccitelli, S. J. Beebe, K. H. Schoenbach, and J. F. Kolb, "Plasma membrane voltage changes during nanosecond pulsed electric field exposures," Biophys. J., vol. 90, no. 10, pp. 3608-3615, May 2006.