journal article Open Access Mar 06, 2013

Induction of Cell Death Mechanisms and Apoptosis by Nanosecond Pulsed Electric Fields (nsPEFs)

Cells Vol. 2 No. 1 pp. 136-162 · MDPI AG
View at Publisher Save 10.3390/cells2010136
Abstract
Pulse power technology using nanosecond pulsed electric fields (nsPEFs) offers a new stimulus to modulate cell functions or induce cell death for cancer cell ablation. New data and a literature review demonstrate fundamental and basic cellular mechanisms when nsPEFs interact with cellular targets. NsPEFs supra-electroporate cells creating large numbers of nanopores in all cell membranes. While nsPEFs have multiple cellular targets, these studies show that nsPEF-induced dissipation of ΔΨm closely parallels deterioration in cell viability. Increases in intracellular Ca2+ alone were not sufficient for cell death; however, cell death depended of the presence of Ca2+. When both events occur, cell death ensues. Further, direct evidence supports the hypothesis that pulse rise-fall times or high frequency components of nsPEFs are important for decreasing ΔΨm and cell viability. Evidence indicates in Jurkat cells that cytochrome c release from mitochondria is caspase-independent indicating an absence of extrinsic apoptosis and that cell death can be caspase-dependent and –independent. The Ca2+ dependence of nsPEF-induced dissipation of ΔΨm suggests that nanoporation of inner mitochondria membranes is less likely and effects on a Ca2+-dependent protein(s) or the membrane in which it is embedded are more likely a target for nsPEF-induced cell death. The mitochondria permeability transition pore (mPTP) complex is a likely candidate. Data demonstrate that nsPEFs can bypass cancer mutations that evade apoptosis through mechanisms at either the DISC or the apoptosome.
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References
83
[1]
The Hallmarks of Cancer

Douglas Hanahan, Robert A Weinberg

Cell 2000 10.1016/s0092-8674(00)81683-9
[2]
Hallmarks of Cancer: The Next Generation

Douglas Hanahan, Robert A. Weinberg

Cell 2011 10.1016/j.cell.2011.02.013
[3]
Loges "Mechanisms of Resistance to Anti-Angiogenic Therapy and Development of Third-Generation Anti-Angiogenic Drug Candidates" Genes Cancer (2010) 10.1177/1947601909356574
[4]
Mir "Electrochemotherapy potentiation of antitumour effect of bleomycin by local electric pulses" Eur. J. Cancer (1991) 10.1016/0277-5379(91)90064-k
[5]
Sersa "Antitumor effectiveness of electrochemotherapy with cis-diamminedichloroplatinum(II) in mice" Cancer Res. (1995)
[6]
Goto "Highly efficient electro-gene therapy of solid tumor by using an expression plasmid for t herpes simplex virus thymidine kinase gene" Proc. Natl. Acad. Sci. USA (2000) 10.1073/pnas.97.1.354
[7]
Li "Regression of Tumor Growth and Induction of Long-Term Antitumor Memory by Interleukin 12 Electro-Gene Therapy" J. Natl. Cancer Inst. (2002) 10.1093/jnci/94.10.762
[8]
Tissue Ablation with Irreversible Electroporation

R. V. Davalos, L. M. Mir, B. Rubinsky

Annals of Biomedical Engineering 2005 10.1007/s10439-005-8981-8
[9]
Beebe "Nanosecond pulsed electric field (nsPEF) effects on cells and tissues: apoptosis induction and tumor growth inhibition" IEEE Trans. Plasma Sci. (2002) 10.1109/tps.2002.1003872
[10]
Nuccitelli "Nanosecond pulsed electric fields cause melanomas to self-destruct" Biochem. Biophys. Res. Commun. (2006) 10.1016/j.bbrc.2006.02.181
[11]
Garon "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) 10.1002/ijc.22723
[12]
Chen "Apoptosis initiation and angiogenesis inhibition: Melanoma targets for nanosecond pulsed electric fields" Pigment. Cell Melanoma Res. (2010) 10.1111/j.1755-148x.2010.00704.x
[13]
Chen "Long term survival of mice with hepatocellular carcinoma after pulse power ablation with nanosecond pulsed electric fields" Technol. Cancer Res. Treat. (2012) 10.7785/tcrt.2012.500237
[14]
Tiong "Systematic review and meta-analysis of survival and disease recurrence after radiofrequency ablation for hepatocellular carcinoma" Br. J. Surg. (2011) 10.1002/bjs.7669
[15]
Sersa "Electrochemotherapy of solid tumors—Preclinical and clinical experience" Conf. Proc. IEEE Eng. Med. Biol. Soc. (2011)
[16]
Daud "Phase I trial of interleukin-12 plasmid electroporation in patients with metastatic melanoma" J. Clin. Oncol. (2008) 10.1200/jco.2007.15.6794
[17]
Heller "Electroporation based gene therapy—From the bench to the bedside" Conf. Proc. IEEE Eng. Med. Biol. Soc. (2011)
[18]
Neal "Successful treatment of a large soft tissue sarcoma with irreversible electroporation" J. Clin. Oncol. (2011) 10.1200/jco.2010.33.0902
[19]
Kingham "Ablation of Perivascular Hepatic Malignant Tumors with Irreversible Electroporation" J. Am. Coll. Surg. (2012) 10.1016/j.jamcollsurg.2012.04.029
[20]
Stewart "Transport lattice approach to describing electroporation: use of local asymptotic model" IEEE Transact. Plasma Sci. (2004) 10.1109/tps.2004.832639
[21]
Gowrishankar "Microdosimetry for conventional and supra-electroporation in cells with organelles" Biochem. Biophys. Res. Commun. (2006) 10.1016/j.bbrc.2006.01.094
[22]
Beebe "Nanosecond, high-intensity pulsed electric fields induce apoptosis in human cells" FASEB J. (2003) 10.1096/fj.02-0859fje
[23]
Vernier "Ultrashort pulsed electric fields induce membrane phospholipid translocation and caspase activation: Differential sensitivities of Jurkat T lymphoblasts and rat glioma C6 cells" IEEE Trans. Dielectr. Electr. Insul. (2003) 10.1109/tdei.2003.1237329
[24]
Beebe "Nanosecond pulsed electric fields modulate cell function through intracellular signal transduction mechanisms" Physiol. Meas. (2004) 10.1088/0967-3334/25/4/023
[25]
Hall "Nanosecond pulsed electric fields induce apoptosis in p53-wildtype and p53-null HCT116 colon carcinoma cells" Apoptosis (2007) 10.1007/s10495-007-0083-7
[26]
Ford "Nanosecond pulsed electric fields stimulate apoptosis without release of pro-apoptotic factors from mitochondria in B16f10 melanoma" Arch. Biochem. Biophys (2010) 10.1016/j.abb.2010.03.008
[27]
Ren "An apoptosis targeted stimulus with nanosecond pulsed electric fields (nsPEFs) in E4 squamous cell carcinoma" Apoptosis (2011) 10.1007/s10495-010-0572-y
[28]
Ren "Nanosecond pulsed electric fields (nsPEFs) activate intrinsic caspase-dependent and caspase-independent cell death in Jurkat cells" Biochem Biophys. Res. Commun. (2012) 10.1016/j.bbrc.2012.04.094
[29]
Schoenbach "Intracellular effect of ultrashort electrical pulses" Bioelectromagnetics (2001) 10.1002/bem.71
[30]
Stacey "Differential effects in cells exposed to ultra-short, high intensity electric fields: Cell survival, DNA damage, and cell cycle analysis" Mutat. Res. (2003) 10.1016/j.mrgentox.2003.08.006
[31]
Stacey "Nanosecond pulsed electric field induced cytoskeleton, nuclear membrane and telomere damage adversely impact cell survival" Bioelectrochemistry (2011) 10.1016/j.bioelechem.2011.06.002
[32]
Beebe "Diverse effects of nanosecond pulsed electric fields on cells and tissues" DNA Cell Biol. (2003) 10.1089/104454903322624993
[33]
Vernier "Calcium bursts induced by nanosecond electric pulses" Biochem. Biophys. Res. Commun. (2003) 10.1016/j.bbrc.2003.08.140
[34]
White "Stimulation of capacitative Ca2+ entry in HL-60 cells by nanosecond pulsed electric fields" J. Biol. Chem. (2004) 10.1074/jbc.m311135200
[35]
Buescher "Submicrosecond intense pulsed electric field effects on intracellular free Ca2+: mechanisms and effects" IEEE Trans. Plasma Sci. (2004) 10.1109/tps.2004.832643
[36]
Zhang "Nanosecond pulse electric field (nanopulse): A novel non-ligand agonist for platelet activation" Arch. Biochem. Biophys. (2008) 10.1016/j.abb.2007.12.009
[37]
Vernier "Mitochondrial membrane permeabilization with nanosecond electric pulses" Conf. Proc. IEEE Eng. Med. Biol. Soc. (2011)
[38]
Wu "Nanosecond electric pulses cause mitochondrial membrane permeabilization in Jurkat cells" Bioelectromagnetics (2012) 10.1002/bem.20707
[39]
Shawgo "Caspase-mediated Bak activation and cytochrome c release during intrinsic apoptotic cell death in Jurkat cells" J. Biol. Chem. (2008) 10.1074/jbc.m807656200
[40]
Shelton "Cleavage of Bid by executioner caspases mediates feed forward amplification of mitochondrial outer membrane permeabilization during genotoxic stress-induced apoptosis in Jurkat cells" J. Biol. Chem. (2009) 10.1074/jbc.m809392200
[41]
Shelton "Activation of caspase-9, but not caspase-2 or caspase-8, is essential for heat-induced apoptosis in Jurkat cells" J. Biol. Chem. (2010) 10.1074/jbc.m110.167635
[42]
Deng "The effects of intense submicrosecond electrical pulses on cells" Biophys. J. (2003) 10.1016/s0006-3495(03)75076-0
[43]
Tekle "Selective field effects on intracellular vacuoles and vesicle membranes with nanosecond electric pulses" Biophys. J. (2005) 10.1529/biophysj.104.054494
[44]
Pakhomov "Lipid nanopores can form a stable, ion channel-like conduction pathway in cell membrane" Biochem Biophys. Res. Commun. (2009) 10.1016/j.bbrc.2009.05.035
[45]
Bowman "Analysis of plasma membrane integrity by fluorescent detection of Tl(+) uptake" J. Membr. Biol. (2010) 10.1007/s00232-010-9269-y
[46]
Creighton, T.E. (1993). Proteins: Structures and Molecular Properties, WH Freeman.
[47]
Tieleman "The molecular basis of electroporation" BMC Biochem. (2004) 10.1186/1471-2091-5-10
[48]
Tarek "Membrane electroporation: a molecular dynamics simulation" Biophys. J. (2005) 10.1529/biophysj.104.050617
[49]
Vernier "Nanopore formation and phosphatidylserine externalization in a phospholipid bilayer at high transmembrane potential" J. Am. Chem. Soc. (2006) 10.1021/ja0588306
[50]
Levine "Life cycle of an electropore: field-dependent and field-independent steps in pore creation and annihilation" J. Membr. Biol. (2010) 10.1007/s00232-010-9277-y

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Published
Mar 06, 2013
Vol/Issue
2(1)
Pages
136-162
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Stephen Beebe, Nova Sain, Wei Ren (2013). Induction of Cell Death Mechanisms and Apoptosis by Nanosecond Pulsed Electric Fields (nsPEFs). Cells, 2(1), 136-162. https://doi.org/10.3390/cells2010136