Dose-dependent thresholds of 10-ns electric pulse induced plasma membrane disruption and cytotoxicity in multiple cell lines

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Ibey, Bennett L ^a   Roth, Caleb C ^c   Pakhomov, Andrei G ^b   Bernhard, Joshua A ^a   Wilmink, Gerald J ^a   Pakhomova, Olga N ^b  

^a AIR FORCE RESEARCH LABORATORY   (United States)

^b OLD DOMINION UNIVERSITY   (United States)

^c GENERAL DYNAMICS INFORMATION TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLSERINE; PROPIDIUM IODIDE; TRYPSIN; CALCIUM; FLUORESCEIN ISOTHIOCYANATE; LIPOCORTIN 5;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL FUNCTION; CELL KILLING; CELL MEMBRANE PERMEABILITY; CELL SIZE; CELL STRAIN GH3; CELL STRAIN U937; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CULTURE MEDIUM; CYTOTOXICITY; DOSIMETRY; EXTRACELLULAR CALCIUM; FEMALE; FLOW CYTOMETRY; HELA CELL; HUMAN; HUMAN CELL; LD 50; LEUKEMIA CELL LINE; MEMBRANE DAMAGE; NONHUMAN; PULSED ELECTRIC FIELD; RADIATION DOSE; RAT; ANIMAL; CELL MEMBRANE; CHO CELL; CONFOCAL MICROSCOPY; CRICETULUS; DRUG EFFECT; ELECTRICITY; ELECTROSTIMULATION; EXTRACELLULAR SPACE; FLUORESCENCE MICROSCOPY; HAMSTER; LIGHT; METABOLISM; RADIATION SCATTERING; TIME;

ANIMALS; ANNEXIN A5; CALCIUM; CELL DEATH; CELL MEMBRANE; CELL SIZE; CELL SURVIVAL; CHO CELLS; CRICETINAE; CRICETULUS; ELECTRIC STIMULATION; ELECTRICITY; EXTRACELLULAR SPACE; FLOW CYTOMETRY; FLUORESCEIN-5-ISOTHIOCYANATE; HELA CELLS; HUMANS; JURKAT CELLS; LIGHT; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; PHOSPHATIDYLSERINES; RATS; SCATTERING, RADIATION; TIME FACTORS; TRYPSIN;

EID: 79251498907     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015642     Document Type: Article

References (55)

1. Teissie J, Eynard N, Gabriel B, Rols MP, 1999, Electropermeabilization of cell membranes. Adv Drug Deliv Rev 35: 3-19.
2. Neumann E, Sowers AE, Jordan CA, eds. 1989, Electroporation and Electrofusion in Cell Biology. New York Plenum.
3. Weaver JC, 2003, Electroporation of Biological Membranes from Multicellular to Nano Scales. IEEE Transactions on Dielectrics and Electrical Insulation 10: 754-768.
4. Mir LM, Orlowski S, Belehradek J Jr, Paoletti C, 1991, Electrochemotherapy potentiation of antitumour effect of bleomycin by local electric pulses. European Journal of Cancer and Clinical Oncology 27: 68-72.
5. Heller R, Jaroszeski MJ, Reintgen DS, Puleo CA, DeConti RC, 1998, Treatment of cutaneous and subcutaneous tumors with electrochemotherapy using intralesional bleomycin. Cancer 83: 148-157.
6. Mir LM, Glass LF, Sersa G, Teissie J, Domenge C, 1998, Effective treatment of cutaneous and subcutaneous malignant tumours by electrochemotherapy. Br J Cancer 77: 2336-2342.
7. Cemazar M, Grosel A, Glavac D, Kotnik V, Skobrne M, 2003, Effects of electrogenetherapy with p53wt combined with cisplatin on curvival of human tumor cell lines with different p53 status. DNA Cell Biol 22: 765-775.
8. Davalos R, Mir L, Rubinsky B, 2005, Tissue Ablation with Irreversible Electroporation. Annals of Biomedical Engineering 33: 223-231.
9. Neal R, Davalos R, 2009, The feasibility of irreversible electroporation for the treatment of breast cancer and other heterogeneous systems. Ann Biomed Eng 37: 2615-2625.
10. Rubinsky J, Onik G, Mikus P, Rubinsky B, 2008, Optimal parameters for the destruction of prostate cancer using irreversible electroporation. J Urol 180: 2668-2674.
11. Al-Sakere B, Andre F, Bernat C, Connault E, Opolon P, 2007, Tumor ablation with irreversible electroporation. PLoS One 2: e1135.
12. Miller L, Leor J, Rubinsky B, 2005, Cancer cells ablation with irreversible electroporation. Technol Cancer Res Treat 4: 699-705.
13. Rubinsky B, eds. 2010, Irreversible Electroporation. Berlin Heidelberg Springer-Verlag.
14. LandstrÖM FJ, Nilsson CO, Crafoord S, Reizenstein JA, Adamsson GBM, 2010, Electroporation Therapy of Skin Cancer in the Head and Neck Area. Dermatologic Surgery 36: 1245-1250.
15. Hall E, Schoenbach K, Beebe S, 2007, Nanosecond pulsed electric fields induce apoptosis in p53-wildtype and p53-null HCT116 colon carcinoma cells. Apoptosis 12: 1721-1731.
16. Beebe SJ, Fox PM, Rec LJ, Somers K, Stark RH, 2002, Nanosecond Pulsed Electric Field (nsPEF) Effects on Cells and Tissues: Apoptosis Induction and Tumor Growth Inhibition. IEEE Transactions on Plasma Science 30: 286-292.
17. Beebe SJ, Fox PM, Rec LJ, Willis EL, Schoenbach KH, 2003, Nanosecond, high-intensity pulsed electric fields induce apoptosis in human cells. Faseb J 17: 1493-1495.
18. Deng J, Schoenbach KH, Buescher ES, Hair PS, Fox PM, 2003, The effects of intense submicrosecond electrical pulses on cells. Biophys J 84: 2709-2714.
19. Schoenbach KS, Hargrave B, Joshi RP, Kolb J, Osgood C, 2007, Bioelectric Effects of Nanosecond Pulses. IEEE Transactions on Dielectrics and Electrical Insulation 14: 1088-1109.
20. Hall E, Schoenbach K, Beebe S, 2005, Nanosecond pulsed electric fields (nsPEF) induce direct electric field effects and biological effects on human colon carcinoma cells. DNA and cell biology 24: 283-291.
21. Garon EB, Sawcer D, Vernier PT, Tang T, Sun Y, 2007, 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 121: 675-682.
22. Nuccitelli R, Chen X, Pakhomov AG, Baldwin WH, Sheikh S, 2009, A new pulsed electric field therapy for melanoma disrupts the tumor's blood supply and causes complete remission without recurrence. Int J Cancer 125: 438-445.
23. Nuccitelli R, Pliquett U, Chen X, Ford W, James Swanson R, 2006, Nanosecond pulsed electric fields cause melanomas to self-destruct. Biochem Biophys Res Commun 343: 351-360.
24. Xiao S, Altunc S, Kumar P, Baum CE, Schoenbach KH, 2010, A Reflector Antenna for Focusing Subnanosecond Pulses in the Near Field. IEEE Antennas and Propogation Society 9: 12-15.
25. Chen X, Liang J, Wang S, Wang Z, Parini C, 2008, Small ultra wideband antennas for medical imaging. Antennas and Propagation Conference, 2008 LAPC 2008 Loughborough pp. 28-31.
26. Schoenbach KH, Shu X, Camp JT, 2008, Subnanosecond Electrical Pulses for Medical Therapies and Medical Imaging. IEEE International Power Modulators and High Voltage Conference, Proceedings of the 2008 pp. 60-60.
27. Xiao S, Migliaccio MA, Camp JC, Kolb JF, Schoenbach KH, 2007, A wide-band focusing system for bioelectric applications. Pulsed Power Conference, 2007 16th IEEE International 1: 744-747.
28. Stacey M, Stickley J, Fox P, Statler V, Schoenbach K, 2003, Differential effects in cells exposed to ultra-short, high intensity electric fields: cell survival, DNA damage, and cell cycle analysis. Mutat Res 542: 65-75.
29. Ibey BL, Pakhomov AG, Gregory BW, Khorokhorina VA, Roth CC, 2010, Selective cytotoxicity of intense nanosecond-duration electric pulses in mammalian cells. Biochimica et Biophysica Acta (BBA)- General Subjects 1800: 1210-1219.
30. Vernier PT, Yinghua S, Jingjing W, Mya Mya T, Garon E, 2005, Nanoelectropulse Intracellular Perturbation and Electropermeabilization Technology: Phospholipid Translocation, Calcium Bursts, Chromatin Rearrangement, Cardiomyocyte Activation, and Tumor Cell Sensitivity. Engineering in Medicine and Biology Society, 2005 IEEE-EMBS 2005 27th Annual International Conference of the pp. 5850-5853.
31. Pakhomov AG, Phinney A, Ashmore J, Walker K, Kolb JF, 2004, Characterization of the cytotoxic effect of high-intensity, 10-ns duration electrical pulses. IEEE Transactions on Plasma Science 32: 1579-1585.
32. Ibey BL, Mixon DG, Payne JA, Bowman A, Sickendick K, 2010, Plasma membrane permeabilization by trains of ultrashort electric pulses. Bioelectrochemistry 79: 114-121.
33. Vernier PT, Sun Y, Gundersen MA, 2006, Nanoelectropulse-driven membrane perturbation and small molecule permeabilization. BMC Cell Biol 7: 37.
34. Vernier PT, Sun Y, Marcu L, Craft CM, Gundersen MA, 2004, Nanoelectropulse-induced phosphatidylserine translocation. Biophys J 86: 4040-4048.
35. Pakhomov AG, Bowman AM, Ibey BL, Andre FM, Pakhomova ON, 2009, Lipid nanopores can form a stable, ion channel-like conduction pathway in cell membrane. Biochem Biophys Res Commun 385: 181-186.
36. Ibey BL, Xiao S, Schoenbach KH, Murphy MR, Pakhomov AG, 2009, Plasma membrane permeabilization by 60- and 600-ns electric pulses is determined by the absorbed dose. Bioelectromagnetics 30: 92-99.
37. Pakhomov AG, Kolb JF, White JA, Joshi RP, Xiao S, 2007, Long-lasting plasma membrane permeabilization in mammalian cells by nanosecond pulsed electric field (nsPEF). Bioelectromagnetics 28: 655-663.
38. Vernier PT, Ziegler MJ, Sun Y, Chang WV, Gundersen MA, 2006, Nanopore Formation and Phosphatidylserine Externalization in a Phospholipid Bilayer at High Transmembrane Potential. Journal of the American Chemical Society 128: 6288-6289.
39. Vernier PT, Aimin L, Marcu L, Craft CM, Gundersen MA, 2003, Ultrashort pulsed electric fields induce membrane phospholipid translocation and caspase activation: differential sensitivities of Jurkat T lymphoblasts and rat glioma C6 cells. Dielectrics and Electrical Insulation, IEEE Transactions on 10: 795-809.
40. Kolb JF, Kono S, Schoenbach KH, 2006, Nanosecond pulsed electric field generators for the study of subcellular effects. Bioelectromagnetics 27: 172-187.
41. Kennedy SM, Ji Z, Hedstrom JC, Booske JH, Hagness SC, 2008, Quantification of Electroporative Uptake Kinetics and Electric Field Heterogeneity Effects in Cells. Biophysical journal 94: 5018-5027.
42. Chen G, Daly K, 2007, Delayed poration after ultrashort electric pulses on Jurkat cell. Ljubljana, Slovenia 15th International Symposium on High Voltage Engineering.
43. Hampton MB, Vanags DM, Isabella Pörn-Ares M, Orrenius S, 1996, Involvement of extracellular calcium in phosphatidylserine exposure during apoptosis. FEBS Letters 399: 277-282.
44. Pakhomov AG, Shevin R, White JA, Kolb JF, Pakhomova ON, 2007, Membrane permeabilization and cell damage by ultrashort electric field shocks. Arch Biochem Biophys 465: 109-118.
45. Grosse C, Schwan HP, 1992, Cellular membrane potentials induced by alternating fields. Biophysical journal 63: 1632-1642.
46. Chang DC, eds. 1992, Guide to Electroporation and Electrofusion. San Diego Academic Press, Inc.
47. Kotnik T, Miklavcic D, 2006, Theoretical Evaluation of Voltage Inducement on Internal Membranes of Biological Cells Exposed to Electric Fields. Biophysical journal 90: 480-491.
48. Agarwal A, Zudans I, Weber EA, Olofsson J, Orwar O, 2007, Effect of Cell Size and Shape on Single-Cell Electroporation. Analytical Chemistry 79: 3589-3596.
49. Vasilkoski Z, Esser AT, Gowrishankar TR, Weaver JC, 2006, Membrane electroporation: The absolute rate equation and nanosecond time scale pore creation. Physical Review E 74.
50. Smith KC, Weaver JC, 2008, Active Mechanisms Are Needed to Describe Cell Responses to Submicrosecond, Megavolt-per-Meter Pulses: Cell Models for Ultrashort Pulses. Biophysical Journal 95: 1547-1563.
51. Cemazar M, Jarm T, Miklavcic D, Lebar A, Ihan A, 1998, Effect of Electric-Field Intensity on Electropermeabilization and Electrosensitmty of Various Tumor-Cell Lines In Vitro. Electromagnetic Biology and Medicine 17: 263-272.
52. Winterbourne DJ, Thomas S, Hermon-Taylor J, Hussain I, Johnstone AP, 1998, Electric shock-mediated transfection of cells. Characterization and optimization of electrical parameters. Biochemical Journal 251: 427-434.
53. Lorenz A, Just W, da Silva Cardoso M, Klotz G, 1988, Electroporation-mediated transfection of Acholeplasma laidlawii with mycoplasma virus L1 and L3 DNA. J Virol 62: 3050-3052.
54. Saulis G, 1997, Pore disappearance in a cell after electroporation: theoretical simulation and comparison with experiments. Biophysical journal 73: 1299-1309.
55. Saulis G, 1999, Kinetics of pore disappearance in a cell after electroporation. Biomed Sci Instrum 35: 409-414.