Bioelectric effects of intense ultrashort pulses

Critical Reviews in Biomedical Engineering

Volumn 38, Issue 3, 2010, Pages 255-304

  Joshi, R P ^a   Schoenbach, K H ^a  

^a OLD DOMINION UNIVERSITY   (United States)

Author keywords

Biomedical applications; High voltage cellular effects; Nanosecond pulses; Subcellular responses

Indexed keywords

CALCIUM; CELL DEATH; CELL IMMOBILIZATION; CHARGING TIME; ELECTRIC BREAKDOWN; ELECTROMAGNETIC FIELDS; ELECTROPORATION; GENE TRANSFER; GENES; MEDICAL APPLICATIONS; MOLECULAR DYNAMICS; TARGETED DRUG DELIVERY; TUMORS;

ATOMISTIC MOLECULAR DYNAMICS; BIOMEDICAL APPLICATIONS; CELLULAR EFFECTS; INTRACELLULAR ELECTROEFFECTS; INTRACELLULAR STRUCTURES; NANOSECOND ELECTRICAL PULSE; NANOSECOND PULSE; SUB-CELLULAR;

CONTROLLED DRUG DELIVERY;

CALCIUM; COOLING WATER; DNA; DYE; ETHIDIUM; FLUORESCEIN ISOTHIOCYANATE; ION CHANNEL; LIGAND; LIPOCORTIN 5; PLATELET DERIVED GROWTH FACTOR; PROPIDIUM IODIDE; REACTIVE OXYGEN METABOLITE; RNA; THROMBIN; TRANSFORMING GROWTH FACTOR BETA; TRYPAN BLUE; TUMOR NECROSIS FACTOR;

ACTION POTENTIAL; ANIMAL CELL; APOPTOSIS; BIOFOULING; BIOMEDICAL ENGINEERING; CALCIUM CELL LEVEL; CANCER CELL; CANCER THERAPY; CELL; CELL GRANULE; CELL MEMBRANE; CELL SURVIVAL; DRUG DELIVERY SYSTEM; ELECTRIC FIELD; ELECTRODE; ELECTROPORATION; ELECTROSTIMULATION THERAPY; ENZYME RELEASE; FLUORESCENCE; GENE EXPRESSION; GENE TRANSFER; GEOMETRY; HUMAN; HUMAN CELL; LIPID BILAYER; MATHEMATICAL MODEL; MELANOMA; MEMBRANE POTENTIAL; MOLECULAR DYNAMICS; NANOPORE; NANOSECOND PULSED ELECTRIC FIELD; NANOTECHNOLOGY; NERVE STIMULATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PANCREAS CANCER; PREDICTION; PRIORITY JOURNAL; PULSE GENERATOR; REVIEW; SKIN CANCER; SPINAL CORD INJURY; STROKE; WOUND HEALING;

EID: 78650131676     PISSN: 0278940X     EISSN: None     Source Type: Journal    
DOI: 10.1615/critrevbiomedeng.v38.i3.20     Document Type: Review

References (188)

1. Neumann E, Schaefer-Ridder M, Wang Y, Hofschneider PH. Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J. 1982;1:841-5.
2. Mir LM, Orlowski S, Belehradek Jr. J, Teissié J, Rols MP, Sersa G, Miklavcic D, Gilbert R, Heller R. Biomedical applications of electric pulses with special emphasis on antitumor electrochemotherapy. Bioelectrochem Bioenerg. 1995;38:203-7.
3. Sersa G, Cemažar M, Miklavcic D. Antitumor effectiveness of electrochemotherapy with cis-diammine-dichloroplatinum(II) in mice. Cancer Res. 1995;55:3450-5.
4. Mouneimne Y, Tosi PF, Barhoumi R, Nicolau C. Electroinsertion of full length recombinant CD4 into red blood cell membrane. Biochim Biophys Acta. 1990;1027:53-8.
5. Raffy S, Teissié J. Insertion of glycophorin A, a transmembraneous protein, in lipid bilayers can be mediated by electropermeabilization. Eur J Biochem. 1995;230:722-32.
6. Zimmermann U. Electric field mediated fusion and related electrical phenomena. Biochim Biophys Acta. 1982;694:227-77.
7. Sowers AE. Cell fusion. New York: Plenum; 1987.
8. Arnold WM. Positioning and levitation media for the separation of biological cells. IEEE Trans Ind Appl. 2001;37:1468-75.
9. Wang RY, Yang YR, Tsai MW, Wang WYJ, Chan RC. Effects of functional electric stimulation on upper limb motor function and shoulder range of motion in hemiplegic patients. Am J Phys Med Rehab. 2002;81:283-90.
10. Foster KR, Schwan HP. Dielectric properties of tissues and biological materials: A critical review. Crit Rev Biomed Eng. 1989;17:25-104.
11. Führ G, Glaser R, Hagedorn R. Rotation of dielectrics in a rotating electric high-frequency field: Model experiments and theoretical explanation of the rotation effect of living cells. Biophys J. 1985;49:395-402.
12. Pohl HA. Dielectrophoresis. London: Cambridge University Press; 1978.
13. Staempfli R. Reversible breakdown of the excitable membrane of a ranvier node. An Acad Brasil Ciens. 1958;30:57-63.
14. Neumann E, Rosenheck K. Permeability changes induced by electrical impulses in vesicular membranes. J Memb Biol. 1972;10:279-90.
15. Schoenbach KH, Xiao S, Joshi RP, Camp JT, Heeren T, Kolb JF, Beebe SJ. The effect of intense subnanosecond electrical pulses on biological cells. IEEE Trans. Plasma Sci. 2008;36:414-24.
16. Kranich A, Ly HK, Hildebrandt P, Murgida DH. Direct observation of the gating step in protein electron transfer: electric-field-controlled protein dynamics. J Am Chem Soc. 2008;130:9844-8.
17. Groves JT, Boxer SG, McConnell, HM. Electric field-induced reorganization of two-component supported bilayer membranes. Proc Natl Acad Sci U S A. 1997;94:13390-5.
18. De Biase PM, Paggi DA, Doctorovich F, Hildebrandt P, Estrin DA, Murgida DH, Marti, MA. Molecular basis for the electric field modulation of cytochrome c structure and function. J Am Chem Soc. 2009;131:16248-56.
19. Schoenbach KH, Beebe SJ, Buescher ES. Intracellular effect of ultrashort electrical pulses. J Bioelectromagn. 2001;22:440-8.
20. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 1997;91:479-89.
21. Vernier, PT, Sun Y, Marcu L, Salemi S, Craft CM, Gundersen MA. Calcium bursts induced by nanosecond electric pulses. Biochem Biophys Res Commun. 2003;310:286-95. (Pubitemid 37163662)
22. Beebe SJ, Blackmore PF, White J, Joshi RP, Schoenbach, KH. Nanosecond pulsed electric fields modulate cell function through intracellular signal transduction mechanisms. Physiol Meas. 2004;25:1077-93.
23. Joshi RP, Nguyen A, Sridhara V, Hu Q, Nuccitelli R, Schoenbach KH. Simulations of intra-cellular calcium release dynamics in response to a high-intensity, ultra-short electric pulse. Phys Rev E. 2007;75:041920.
24. Schoenbach KH, Joshi RP, Kolb J, Chen N, Stacey M, Blackmore P, Buescher ES, Beebe SJ. Ultrashort electrical pulses open a new gateway into biological cells. Proc IEEE. 2004;92:1122-37.
25. Nuccitelli R, Pliquett U, Chen X, Ford, W, Swanson J, Beebe SJ, Kolb JF, Schoenbach KH. Nanosecond pulsed electric fields cause melanomas to self-destruct. Biochem Biophys Res Commun. 2006;343:351-60.
26. Beebe SJ, Fox PM, Rec LJ, Willis EL, Schoenbach KH. Nanosecond, high intensity pulsed electric fields induce apoptosis in human cells. FASEB J. 2003;17:1493-5.
27. Joshi RP, Mishra A, Song J, Pakhomov A, Schoenbach KH. Simulation studies of ultrashort, high-intensity electric pulse induced action potential block in whole-animal nerves. IEEE Trans Biomed Eng. 2008;55:1391-8. (Pubitemid 351440488)
28. Schoenbach KH, Hargrave B, Joshi RP, Kolb JF, Osgood C, Nuccitelli R, Pakhomov A, Swanson RJ, Stacey M, White JA, Xiao S, Zhang J, Beebe SJ, Blackmore PE, Buescher ES. Bioelectric effects of intense nanosecond pulses. IEEE Trans Dielect Elect Insul. 2007;14:1088-119.
29. Mir LM, Orlowski S, Belehradek Jr. J, Teissie J, Rols MP, Sersa G, Miklavcic D, Gilbert R, Heller R. Biomedical applications of electric pulses with special emphasis on antitumor electrochemotherapy. Bioelectrochem Bioenerg. 1995;38:203-7.
30. Teissie J, Eynard N, Gabriel B, Rols MP. Electropermeabilization of cell membranes. Adv Drug Deliv Rev. 1999;35:3-19.
31. Neumann E, Kakorin S, Toensig K. Fundamentals of electroporative delivery of drugs and genes. Bioelectrochem Bioenerg. 1999;48:3-16.
32. Schwan HP. Biophysics of the interaction of electromagnetic energy with cells and membranes. In: Grandolfo M, Michaelson SM, Rindl A, editors. Biological effects and dosimetry of nonionizing radiation. New York; Plenum Press; 1983, p. 213-31.
33. Foster KR. Thermal and nonthermal mechanisms of interaction of radio-frequency energy with biological systems. IEEE Trans Plasma Sci. 2000;28:15-23.
34. Foster KR, Schwan HP. Dielectric properties of tissues - A review. In Polk C, Postow E, editors. Handbook of biological effects of electromagnetic radiation. Boca Raton: CRC Press; 1995. p. 26-102.
35. Kotnik T, Miklavcic D. Second-order model of membrane electric field induced by alternating external electric fields. IEEE Trans Biomed Eng. 2000;47:1074-81. (Pubitemid 30614841)
36. Kotnik T, Miclavcic D. Theoretical evaluation of voltage inducement on internal membranes of biological cells exposed to electric fields. Biophys J. 2006;90:480-91.
37. Vasilkoski Z, Esser AT, Gowrishankar TR, Weaver JC. Membrane electroporation: the absolute rate equation and nanosecond time scale pore creation. Phys Rev E. 2006;74:021904.
38. Abidor IG, Arakelyan VB, Chernomordik LV, Chizmadzhev YA, Pastushenko VF, Tarasevich MR. Electric breakdown of bilayer lipid membrane. The main experimental facts and their qualitative discussions. Bioelectrochem Bioenerg. 1979;6:37-52.
39. Joshi RP, Hu Q, Schoenbach KH, Beebe SJ. Energy-landscape- model analysis for irreversibility and its pulse-width dependence in cells subjected to a high-intensity ultrashort electric pulse. Phys Rev E. 2004;69:051901.
40. Joshi RP, Hu Q, Aly R, Schoenbach KH, Hjalmarson HP. Self-consistent simulations of electroporation dynamics in biological cells subjected to ultrafast electrical pulses. Phys Rev E. 2001;64:011913.
41. Ermolina I, Polevaya Y, Feldman Y, Ginzburg B, Schlesinger M. Study of normal and malignant white blood cells by time domain dielectric spectroscopy. IEEE Trans Dielect Elect Insul. 2001;8:253-61. (Pubitemid 32444407)
42. Feldman Y, Ermolina I, Hayashi Y. Time domain dielectric spectroscopy study of biological systems. IEEE Trans Dielect Elect Insul. 2003;10:728-53.
43. Joshi RP, Hu Q, Schoenbach KH. Modeling studies of cell response to ultrashort, high-intensity electric fields - implications for intracellular manipulation. IEEE Trans Plasma Sci. 2004;32:1677-86.
44. Joshi RP, Hu Q, Schoenbach KH, Hjalmarson HP. Improved energy model for membrane electroporation in biological cells subjected to electrical pulses. Phys Rev E. 2002;65:041920.
45. Weaver JC, Mintzer RA. Decreased bilayer stability due to transmembrane potentials. Phys Lett A. 1981;86:57-9.
46. Weaver JC, Chizmadzhev Y. Theory of electroporation: a review. Bioelectrochem Bioenerg. 1996;41:135-60.
47. Glaser RW, Leikin SL, Chernomordik LV, Pastushenko VF, Sokirko AI. Reversible electrical breakdown of lipid bilayers: formation and evolution of pores. Biochim Biophys Acta. 1988;940:275-87.
48. Pastushenko VF, Chhizmadzhev YA. Electrical breakdown of lipid vesicles. Biofizika. 1983;28:1036-9.
49. Winterhalter M, Helfrich W. Effect of voltage on pores in membranes. Phys Rev A. 1987;36:5874-6.
50. Neu JC, Krassowska W. Singular perturbation analysis of the pore creation transient. Phys Rev E. 2006;74:031917.
51. Smoluchowski M. Drei vortrage uber diffusion, Brownsche bewegung und koagulation von kolloidteilchen. Phys Zeits. 1916;17:557-85.
52. Chandrasekhar S. Stochastic problems in physics and astronomy. Rev Mod Phys. 1943;15:1-89.
53. Kramers HA. Brownian motion in a field of force and the diffusion model of chemical reactions. Physica. 1940;7:284-304.
54. Joshi RP, Schoenbach KH. Electroporation dynamics in biological cells subjected to ultrafast electrical pulses: a numerical simulation study. Phys Rev E. 2000;62:1025-33.
55. Freeman SA, Wang MA, Weaver JC. Theory of electroporation of planar bilayer membranes: Predictions of the aqueous area, change in capacitance, and pore-pore separation. Biophys J. 1994;67:42-56.
56. Barnett A, Weaver JC. A unified, quantitative theory of reversible electrical breakdown and rupture. Bioelectrochem Bioenerg. 1991;25:163-82.
57. Adair RK. Constraints on biological effects of weak extremely- low-frequency electromagnetic fields. Phys Rev A. 1991;43:1039-48.
58. Foster KR, Schwan HP. Handbook of biological effects of electromagnetic fields. Polk C, Postow E, editors. Boca Raton: CRC Press; 1986.
59. Krassowska W, Neu JC. Response of a single cell to an external electric field. Biophys J. 1994;66:1768-76. (Pubitemid 24167930)
60. Beeler GW, Reuter H. Reconstruction of the action potential of ventricular myocardial fibres. J Physiol. 1977;268:177-210.
61. Smith KC, Gowrishankar TR, Esser AT, Stewart DA, Weaver JC. The spatially distributed dynamic transmembrane voltage of cells and organelles due to 10 ns pulses: meshed transport networks. IEEE Trans Plasma Sci. 2006;34:1394-404.
62. Stewart DA, Gowrishankar TR, Weaver JC. Three dimensional transport lattice model for describing action potentials in axons stimulated by external electrodes. Bioelectrochemistry. 2006;69:88-93.
63. Weaver JC. Electroporation of biological membranes from multicellular to nanoscales. IEEE Trans Dielect Elect Insul. 2003;10:754-68.
64. Gowrishankar TR, Esser AT, Vasilkoski Z, Smith KC, Weaver JC. Microdosimetry for conventional and supra-electroporation in cells with organelles. Biochem Biophys Res Commun. 2006;341:1266-76.
65. Joshi RP, Song J, Sridhara V. Aspects of lipid membrane bio-responses to subnanosecond, ultrahigh voltage pulsing. IEEE Trans Dielect Elect Insul. 2009;16:1243-50.
66. Marrink SJ, Berger O, Tieleman P, Jahnig F. Adhesion forces of lipids in a phospholipid membrane studied by molecular dynamics simulations. Biophys J. 1998;74:931-43. (Pubitemid 28345286)
67. White SH. Comments on electrical breakdown of bimolecular lipid membranes as an electromechanical instability. Biophys J. 1974;14:155-8.
68. Sukharev SI, Blount P, Martinac B, Blattner FR, Kung C. A large conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature. 1994;368:265-8. (Pubitemid 24108847)
69. Benachir T, Lafleur M. Osmotic and pH transmembrane gradients control the lytic power of melittin. Biophys J. 1996;70:831-40.
70. James SR, Demel RA, Downes CP. Interfacial hydrolysis of phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-biphosphate by turkey erythrocyte phopholipase C. Biochem J. 1994;298:499-506.
71. Isambert H. Understanding the electroporation of cells and artificial bilayer membranes. Phys Rev. Lett 1998;80:3404-7.
72. Farago O, Santangelo CD. Pore formation in fluctuating membranes. J Chem Phys. 2005;122:044901.
73. Tolpekina TV, den Otter WK, Briels WJ. Nucleation free energy of pore formation in an amphiphilic bilayer studied by molecular dynamics simulations. J Chem Phys. 2004;121:12060-6.
74. Chen N, Schoenbach KH, Kolb JF, Swanson RJ, Garner AL, Yang J, Joshi RP, Beebe SJ. Leukemic cell intracellular responses to nanosecond electric fields. Biochem Biophys Res Comm. 2004;317:421-7.
75. Pakhomov AG, Shevin R, White JA, Kolb JF, Pakhomova ON, Joshi RP, Schoenbach KH. Membrane permeabilization and cell damage by ultrashort electric field shocks. Arch Biochem Biophys. 2007;465:109-18. (Pubitemid 47283984)
76. Kennedy SM, Ji Z, Hedstrom JC, Booske JH, Hagness SC. Quantification of electroporative uptake kinetics and electric field heterogeneity effects in cells. Biophys J. 2008;94:5018-27.
77. Gimsa J, Wachner D. A polarization model overcoming the geometric restrictions of the Laplace solution for spheroidal cells: obtaining new equations for field-induced forces and transmembrane potential. Biophys J. 1999;77:1316-26.
78. Batzing BL. Microbiology: an introduction. Pacific Grove: Thompson Learning; 2002.
79. Radu M, Ionescu M, Irimescu N, Iliescu K, Pologea-Moraru R, Kovacs E. Orientation behavior of retinal photoreceptors in alternating electric fields. Biophys J. 2005;89:3548-54. (Pubitemid 41636107)
80. Asencor FJ, Santamaria C, Iglesias FJ, Dominguez A. Dielectric energy of orientation in dead and living cells of Schizosaccharomyces pombe: fitting of experimental results to a theoretical model. Biophys J. 1993;64:1626-31.
81. Pucihar G, Kotnik T, Valic B, Miklavcic D. Numerical determination of transmembrane voltage induced on irregularly shaped cell. Ann Biomed Eng. 2006;34:642-52.
82. Kotnik T, Miklavcic D. Analytical description of transmembrane voltage induced by electric fields on spheroidal cells. Biophys J. 2000;79:670-9.
83. Maswiwat K, Wachner D, Warnke R, Gima J. Simplified equations for the transmembrane potential induced in ellipsoidal cells of rotational symmetry. J Phys D. 2007;40:914-23. (Pubitemid 46485798)
84. Hu Q, Joshi RP. Analysis of intense, subnanosecond electrical pulse-induced transmembrane voltage in spheroidal cells with arbitrary orientation. IEEE Trans Biomed Eng. 2009;56:1617-26.
85. Schoenbach KH, Baum CE, Joshi RP, Beebe SJ. A scaling law for membrane permeabilization with nanopulses. IEEE Trans Dielect Elect Insul. 2009;16:1224-35.
86. Nuccitelli R, Chen X, Pakhomov AG, Baldwin WH, Sheikh S, Pomicter JL, Ren W, Osgood C, Swanson RJ, Kolb JF, Beebe SJ, Schoenbach KH. A new pulsed electric field therapy for melanoma disrupts the tumor's blood supply and causes complete remission without recurrence. Int J Cancer. 2009;125:438-45.
87. Cole KS. Electric impedance of marine egg membranes. Trans Faraday Soc. 1937;33:966-72.
88. Tieleman DP, Marrink SJ, Berendsen HJC. A computer perspective of membranes: molecular dynamics studies of lipid bilayer systems. Biochim Biophys Acta. 1997;1331:235-70.
89. Ash WL, Zlomislic MR, Oloo EO, Tieleman DP. Computer simulations of membrane proteins. Biochim Biophys Acta. 2004;1666:158-89.
90. Siu SWI, Vácha R, Jungwirth P, Böckmann RA. Biomolecular simulations of membranes: Physical properties from different force fields. J Chem Phys. 2008;128:125103.
91. Bockmann RA, de Groot BL, Kakorin S, Neumann E, Grubmuller H. Kinetics, statistics, and energetics of lipid membrane electroporation studied by molecular dynamics simulations. Biophys J. 2008;95:1837-50.
92. Wohlert J, den Otter WK, Edholm WO, Briels WJ. Free energy of a trans-membrane pore calculated from atomistic molecular dynamics simulations. J Chem Phys. 2006;124:154905.
93. Vernier PT, Ziegler MJ, Sun Y, Chang WV, Gundersen MA, Tieleman DP. Nanopore formation and phosphatidylserine externalization in a phospholipid bilayer at high transmembrane potential. J Am Chem Soc. 2006;128:6288-9.
94. Hu Q, Joshi RP, Schoenbach KH. Simulations of nanopore formation and phosphatidylserine externalization in lipid membranes subjected to a high-intensity, ultrashort electric pulse. Phys Rev E. 2005;72:031902.
95. Hu Q, Viswanadham S, Joshi RP, Schoenbach KH, Beebe SJ, Blackmore PF. Simulations of transient membrane behavior in cells subjected to a high-intensity ultrashort electrical pulse. Phys Rev E. 2005;71:031914.
96. Tieleman D, Leontiadou H, Mark AE, Marrink SJ. Simulation of pore formation in lipid bilayers by mechanical stress and electric fields. J Am Chem Soc. 2003;125:6382-3. (Pubitemid 36605403)
97. Heng JB, Aksimentiev A, Ho C, Marks P, Grinkova YV, Sligar S, Schulten K, Timp G. Stretching DNA using the electric field in a synthetic nanopore. Nano Lett. 2005;5:1883-8.
98. Hu Q, Sridhara V, Joshi RP, Kolb JF, Schoenbach KH. Molecular dynamics analysis of high electric pulse effects on bilayer membranes containing DPPC and DPPS. IEEE Trans Plasma Sci. 2006;34:1405-11.
99. Verhoven B, Schlegel RA, Williamson P. Mechanisms of phosphatidylserine exposure, a phagocyte recognition signal, on apoptotic T lymphocytes. J Exp Med. 1995;182:1597-601.
100. Seigneuret M, Devaux PF. ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes. Proc Natl Acad Sci U S A. 1984;81:3751-5. (Pubitemid 14087796)
101. Basse F, Stout JG, Sims PJ, Wiedmer TJ. Isolation of an erythrocyte membrane protein that mediates Ca2+-dependent transbilayer movement of phospholipid. Biol Chem. 1996;271:17205-10.
102. Comfurius P, Williamson P, Smeets EF, Schlegel RA, Bevers EM, Zwaal RF. Reconstitution of phospholipid scramblase activity from human blood platelets. Biochemistry. 1996;35:7631-4.
103. Balasubramanian K, Schroit AJ. Aminophospholipid asymmetry: a matter of life and death. Annu Rev Physiol. 2003;65:701-34. (Pubitemid 38249174)
104. Vernier PT, Sun Y, Marcu L, Craft CM, Gundersen MA. Nanosecond pulsed electric fields perturb membrane phospholipids in T lymphoblasts. FEBS Lett. 2004;572:103-8.
105. Sachs RK, Hahnfeld P, Brenner DJ. The link between low-LET dose-response relations and the underlying kinetics of damage production/repair/misrepair. Int J Radiat Biol. 1997;72:351-74.
106. Wang CKC, Zhang X. A nanodosimetry-based linear-quadratic model of cell survival for mixed-LET radiations. Phys Med Biol. 2006;51:6087-98. (Pubitemid 46217651)
107. Pakhomov AG, Phinney A, Ashmore J, Walker III K, Kolb JF, Kono S, Schoenbach KH, Murphy MR. Characterization of the cytotoxic effect of high-intensity, 10-ns duration electrical pulses. IEEE Trans Plasma Sci. 2004;32:1579-86.
108. Pakhomov AG, Walker K, Kolb JF, Schoenbach KH, Stuck B, Murphy MR. The rules of cell survival after exposure to high-intensity, ultrashort electrical pulses. In: Proceedings of the 26th Annual Meeting of the Bioelectromagnetics Society, Washington, DC; 2004 June 21-24. p. 7-8. Published by the Bioelectromagnetics Society, Washington DC.
109. Song J, Joshi RP, Beebe SJ. Cellular apoptosis by nanosecond, high-intensity electric pulses: model evaluation of the pulsing threshold and extrinsic pathway. Bioelectrochemistry. 2010;79:179-86
110. Bagci EZ, Vodovotz Y, Billiar TR, Ermentrout GB, Bahar I. Bistability in apoptosis: Roles of Bax, Bcl-2, and mitochondrial permeability transition pores. Biophys J. 2006;90:1546-59.
111. Simons K, Toomre D. Lipid rafts and signal transduction. Nature Rev. 2000;1:31-9.
112. Holthius JCM, Levine TP. Lipid traffic: floppy drives and a super-highway. Nature Rev. 2005;6:209-20.
113. Mollinedo F, Gajate C. Fas/CD95 death receptor and lipid rafts: new targets for apoptosis-directed cancer therapy. Drug Resist Updat. 2006;9:51-73.
114. Kolb JF, Kono S, Schoenbach KH. Nanosecond pulsed electric field generators for the study of subcellular effects. Bioelectromagn J. 2006;27:172-87.
115. Mankowski J, Kristiansen M. A review of short pulse generator technology. IEEE Trans Plasma Sci. 2000;28:102-8.
116. Sun Y, Xiao S, White JA, Kolb JF, Stacey M, Schoenbach KH. Compact, nanosecond, high repetition rate, pulse generator for bioelectric studies. IEEE Trans Dielect Elect Insul. 2007;14:863-70.
117. Heeren T, Camp JT, Kolb JF, Schoenbach KH, Katsuki S, Akiyama H. 250 kV Sub-nanosecond pulse generator with adjustable pulse-width. IEEE Trans Dielect Elect Insul. 2007;14:884-8. (Pubitemid 47237045)
118. Benz R, Zimmermann U. The resealing process of lipid bilayers after reversible electrical breakdown. Biochim Biophys Acta. 1981;640:169-78.
119. Neumann E. The relaxation hysteresis of membrane electroporation. In: Neumann E, Sowers AE, Jordan CA, editors. Electroporation and electrofusion in cell biology. New York: Plenum Press; 1989. p. 61-147.
120. Shirakashi R, Sukhorukov VL, Tanasawa I, Zimmermann U. Measurement of the permeability and resealing time constant of the electroporated mammalian cell membranes. Int J Heat Mass Transfer. 2004;47:4517-24.
121. Frey W, White JA, Price RO, Blackmore PF, Joshi RP, Nuccitelli R, Beebe SJ, Schoenbach KH, Kolb JF. Plasma membrane voltage changes during nanosecond pulsed electric field exposure, Biophys J. 2006;90:3608-15.
122. Kuhn B, Fromherz P, Denk W. High sensitivity of Starkshift voltage-sensing dyes by one- or two-photon excitation near the red spectral edge. Biophys J. 2004;87:631-9.
123. Pakhomov AG, Bowman AM, Ibey BL, Andre FM, Pakhomova ON, Schoenbach KH. Lipid nanopores can form a stable, ion channel-like conduction pathway in cell membrane. Biochem Biophys Res Comm. 2009;385:181-6.
124. Joshi RP, Hu Q. Analysis of cell membrane permeabilization mechanics and pore shape due to ultrashort electrical pulsing. Med Biol Eng Comput. 2010;48:837-44.
125. Resat H, Mezei M. Grand canonical Monte Carlo simulation of water positions in crystal hydrates. J Am Chem Soc. 1994;116:7451-2. (Pubitemid 24981460)
126. Truskett TM, Debenedetti PG, Torquato SJ. Thermodynamic implications of confinement for a waterlike fluid. Chem Phys. 2001;114:2401-18.
127. Giaya A, Thompson RW. Observations on an equation of state for water confined in narrow slit-pores. J Chem Phys. 2002;116:2565-71.
128. Hall E, Schoenbach KH, Beebe SJ. Nanosecond pulsed electric fields have differential effects on cells in S-phase. DNA Cell Biol. 2007;26:160-71.
129. Beebe SJ, White JA, Blackmore PF, Deng Y, Somers K, Schoenbach KH. Diverse effects of nanosecond pulsed electric fields on cells and tissues. DNA Cell Biol. 2003;22:785-96. (Pubitemid 38033001)
130. Buescher ES, Schoenbach KH. Effects of submicrosecond, high intensity pulsed electric fields on living cells - intracellular electromanipulation. IEEE Trans Dielect Elect Ins. 2003;10:788-94.
131. Tekle E, Oubrahim H, Dzekunov SM, Kolb JF, Schoenbach KH, Chock BP. Selective field effects on intracellular vacuoles and vesicle membranes with nano-second electric pulses. Biophys J. 2005;89:274-84.
132. Deng J, Schoenbach KH, Buescher ES, Hair PS, Fox PM, Beebe SJ. The effects of intense submicrosecond electrical pulses on cells. Biophys J. 2003;84:2709-14.
133. White JA, Blackmore PF, Schoenbach KH, Beebe SJ. Stimulation of capacitative calcium entry in HL-60 cells by nanosecond pulsed electric fields (nsPEF). J Biol Chem. 2004;279:22964-74.
134. Vernier PT, Li A, Marcu L, Craft CM, Gundersen MA. Ultrashort pulsed electric fields induce membrane phospholipid translocation and caspase activation: differential sensititivities of jurkat T lymphoblasts and rat glioma C6 cells. IEEE Trans Dielect Elect Insul. 2003;10:795-809.
135. Beebe SJ, Fox PM, Rec LC, Somers K, Stark RH, Schoenbach KH. Nanosecond pulsed electric field (nsPEF) effects on cells and tissues: apoptosis induction and tumor growth inhibition. IEEE Trans Plasma Sci. 2002;30:286-92. (Pubitemid 34720873)
136. Berridge MJ, Bootman MD, Lipp P. Calcium - a life and death signal. Nature. 1998;395:645-8.
137. Susin SA, Zamzami N, Kroemer G. Mitochondria as regulators of apoptosis: doubt no more. Biochim Biophys Acta. 1998;1366:151-65.
138. Scarlett SS, White JA, Blackmore PF, Schoenbach KH, Kolb JF. Regulation of intracellular calcium concentration by nanosecond pulsed electric fields. Biochim Biophys Acta . 2009;1788:1168-75.
139. Craviso GL, Chatterjee P, Maalouf G, Cerjanic A, Yoon J, Chatterjee I, Vernier PT. Nanosecond electric pulse-induced increase in intracellular calcium in adrenal chromaffin cells triggers calcium-dependent catecholamine release. IEEE Trans Dielect Elect Insul. 2009;16:1294-301.
140. Vernier PT, Sun Y, Chen MT, Gundersen MA, Craviso GL. Nanosecond electric pulse-induced calcium entry into chromaffin cells. Bioelectrochemistry. 2008;73:1-4.
141. Zhang J, Blackmore PF, Hargrave BY, Xiao S, Beebe SJ, Schoenbach KH. The characteristics of nanosecond pulsed electrical field stimulation on platelet aggregation in vitro. Arch Biochem Biophys. 2008;471:240-8.
142. Afford S, Randhawa S. Apoptosis. J. Clin Pathol: Mol Path. 2000;53:55-63.
143. Krammer PH. CD95's deadly mission in the immune system. Nature. 2000;407:789-95.
144. Horvitz HR. Genetic control of programmed cell death in the nematode Caenorhabditis elegans. Cancer Res. (Suppl.) 1999;59:1701-6.
145. Jacobson MD, Weil M, Raff MC. Programmed cell death in animal development. Cell. 1997;88:347-54.
146. Green DR. Apoptotic pathways: Paper wraps stone blunts scissors. Cell. 2000;102:1-4.
147. Peter ME, Krammer PH. The CD95 death-inducing signaling complex and beyond. Cell Death Differ. 2003;10:26-35.
148. Budihardjo I, Oliver H, Lutter M, Luo X, Wang X. Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol. 1999;15:269-90. (Pubitemid 32250377)
149. Zoratti M, Szabo I. The mitochondrial permeability transition. Biochim Biophys Acta. 1995;1241:139-76.
150. Marzo I, Brenner C, Zamzami N, Jürgensmeier JM, Susin SA, Vieira HLA, Prévost MC, Xie Z, Matsuyama S, Reed JC, Kroemer G. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science. 1998;281:2027-31.
151. Henshall DC, Bonislawski DP, Skradski SL, Lan JQ, Meller R, Simon RP, Cleavage of bid may amplify caspase-8-induced neuronal death following focally evoked limbic seizures. Neurobiol Dis. 2001;8:568-80.
152. Stacey M, Stickley J, Fox P, Statler V, Schoenbach KH, Beebe SJ, Buescher S. Differential effects in Cells exposed to ultra-short, high intensity electric fields: cell survival, DNA damage, and cell cycle analysis. Mutat Res. 2003;542:65-75. (Pubitemid 37486099)
153. Halestrap AP, McStay GP, Clarce SJ. The permeability transition pore complex: another view. Biochimie. 2002;84:153-66.
154. Savill J, Haslett C. Granulocyte clearance by apoptosis in the resolution of inflammation. Semin Cell Biol. 1995;6:385-93.
155. Tsujimot Y, Shimizu S. The voltage-dependent anion channel: an essential player in apoptosis. Biochimie. 2002;84:187-93.
156. Walker K III, Pakhomova ON, Kolb JF, Schoenbach KH, Stuck BE, Murphy MR, Pakhomov AG. Oxygen enhances lethal effect of high-intensity, ultrashort electrical pulses. Bioelectromagn J. 2006;27:221-5.
157. Wartenberg M, Wirtz N, Grob A, Niedermeier W, Hescheler J, Peters C, Sauer H. Direct current electrical fields induce apoptosis in oral mucosa cancer cells by NADPH oxidase-derived reactive oxygen species. Bioelectromagnetics. 2008;29:47-54.
158. Kannan K, Jain SK. Oxidative stress and apoptosis. Pathophysiology. 2000;7:153-63.
159. Zamzami N, Hirsch T, Dallaporta B, Petit PX, Kroemer G. Mitochondrial implication in accidental and programmed cell death: apoptosis and necrosis. J Bioenerg Biomembr. 1997;29;185-93.
160. Nawarathna D, Miller Jr. JH, Claycomb JR, Cardenas G, Warmflash D. Harmonic response of cellular membrane pumps to low frequency electric fields. Phys Rev Lett. 2005;95:158103.
161. Schoenbach KH, Peterkin FE, Alden RW, Beebe SJ. The effect of pulsed electric fields on biological cells: experiments and applications. IEEE Trans Plasma Sci. 1997;25:284-92.
162. Gothelf A, Mir LM, Gehl J. Electrochemotherapy: results of cancer treatment using enhanced delivery of bleomycin by electroporation. Cancer Treat Rev. 2003;29:371-87. (Pubitemid 37185104)
163. Larkin JO, Collins CG, Aarons S, Tangney M, Whelan M, O'Reily S, Breatnach O, Soden DM, O'Sullivan GC. Electrochemotherapy: aspects of preclinical development and early clinical experience. Ann Surg. 2007;245:469-79.
164. Miklavcic D, Snoj M, Zupanic A, Kos B, Cemazar M, Kropivnik M, Brack M, Pecnik T, Gadzijev E, Sersa G. Towards treatment planning and treatment of deep-seated solid tumors by electrochemotherapy. BioMed Eng On- Line. 2010;9:10(1-8).
165. Mir LM. Therapeutic perspectives of in vivo cell electropermeabilization. Bioelectrochemistry. 2001;53: -10.
166. Waters RL, McNeal DR, Faloon W, Clifford B. Functional electrical stimulation of the peroneal nerve for hemiplegia. J Bone Joint Surg Am. 1985;67:792-3.
167. Tanagho EA, Schmidt RA, Orvis BR. Neural stimulation for control of voiding dysfunction: a preliminary report in 22 patients with serious neuropathic voiding disorders. J Urol. 1989;142:340-5.
168. Stein RB, Chong SL, James KB, Kido A, Bell GJ, Tubman LA, Belanger M. Electrical stimulation for therapy and mobility after spinal cord injury. Prog Brain Res. 2002;137:27-34.
169. Baker LL, McNeal DR, Benton LA, Bowman BR, Waters RL. Neuromuscular electrical stimulation: a practical guide. 3rd ed. Downey, CA: Rancho Rehabilitation Engineering Program (Rancho Los Amigo Medical Centre); 1993.
170. Taylor CW. Store-operated Ca2+ entry: a STIMulating stOrai. Trends Biochem Sci. 2006;31:597-601.
171. Chen X, Swanson RJ, Kolb JF, Nuccitelli R, Schoenbach KH. Histopathology of normal skin and melanomas after nanosecond pulsed electric field (nsPEF) treatment. Melanoma Res. 2009;19:361-71.
172. Esser AT, Smith KC, Gowrishankar TR, Weaver JC. Towards solid tumor treatment by nanosecond pulsed electric fields. Technol Cancer Res Treat. 2009;8:289-306.
173. Folpe AL, Cooper K. Best practices in diagnostic immunohistochemistry: pleomorphic cutaneous spindle cell tumors. Arch Pathol Lab Med. 2007;131:1517-24. (Pubitemid 47606717)
174. Garon EB, Sawcer D, Vernier PT, Tang T, Sun Y, Marcu L, Gundersen MA, Koeffler HP. In vitro and in vivo evaluation and a case report of intense nanosecond pulsed electric field as a local therapy for human malignancies. Int J Cancer. 2007;121:675-82.
175. Popovic MR, Thrasher TA. Neuroprostheses. In: Wnek GE, Bowlin GL, editors. Encyclopedia of biomaterials and biomedical engineering. vol. 2. New York: Marcel Dekker; 2004. p. 1056-7.
176. Marsolais EB, Kobetic R. Functional walking in paralyzed patients by means of electrical stimulation. Clin Orthopaed Rel Res. 1983;175:30-6.
177. Tsai SJ, Lew HL, Date E, Bih LI. Treatment of detrusorsphincter dyssynergia by pudendal nerve block in patients with spinal cord injury. Arch Phys Med Rehabil. 2002;83:714-7.
178. Fang ZP, Mortimer JT. A method to effect physiological recruitment order in electrically activated muscle. IEEE Trans Biomed Eng. 1991;38:175-9.
179. Bhadra N, Kilgore K. Direct current electrical conduction block of peripheral nerve. IEEE Trans. Neural Systems and Rehab. Engr. 2004;12:313-24.
180. Tai C, de Groat WC, Roppolo JR. Simulation analysis of conduction block in unmyelinated axons induced by high-frequency biphasic electrical currents. IEEE Trans Biomed Eng. 2005;52:1323-32. (Pubitemid 40961382)
181. Whitwam JG, Kidd C. The use of direct current to cause selective block of large fibers in peripheral nerves. Br. J. Anaesth. 1975;47:1123-33.
182. Pakhomov A, Kolb JF, Joshi RP, Schoenbach KH, Dayton T, Comeaux J, Ashmore J, Beason C. Neuromuscular disruption with ultrashort electrical pulses. Proc SPIE. 2006;6219:621903. (Pubitemid 44243335)
183. Despa F, Basati S, Zhang ZD, D'Andrea J, Reilly JP, Bodnar EN, Lee RC. Electromuscular incapacitation results from stimulation of spinal reflexes. Bioelectromagnetics. 2009;30:411-21.
184. Joshi RP, Mishra A, Xiao S, Pakhomov A. Model study of time-dependent muscle response to pulsed electrical stimulation. Bioelectromagnetics. 2010;31:361-70.
185. Wexler AS, Ding J, Binder-Macleod SA. A mathematical model that predicts skeletal muscle force. IEEE Trans Biomed Eng. 1997;44:337-48. (Pubitemid 27183855)
186. Hofmann GA. Instrumentation and electrodes for in vivo electroporation, In: Jaroszewski MJ, Heller R, Gilbert R, editors. Electrochemotherapy, electrogenetherapy, and transdermal drug delivery. Totowa, NJ: Humana Press; 2000. p. 37-61.
187. Xiao S, Altunc S, Kumar P, Baum CE, Schoenbach KH. A reflector antenna for focusing subnanosecond pulses in the near field. IEEE Antennas Wireless Lett. 2010;9:12-5.
188. Lazebnik M, McCartney L, Popovic D, Watkins CB, Lindstrom MJ, Harter J, Sewall S, Magliocco A, Booske JH, Okoniewski M, Hagness SC. A large-scale study of the ultrawideband microwave dielectric properties of normal breast tissue obtained from reduction surgeries. Phys Med Biol. 2007;52:6093-115. (Pubitemid 350093183)