Calcium bursts induced by nanosecond electric pulses

Biochemical and Biophysical Research Communications

Volumn 310, Issue 2, 2003, Pages 286-295

  Vernier, P Thomas ^a,b   Sun, Yinghua ^a   Marcu, Laura ^a,c   Salemi, Sarah ^d   Craft, Cheryl M ^d   Gundersen, Martin A ^a  

^a University of Southern California ^*  (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c CEDARS SINAI MEDICAL CENTER   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Calcium burst; Electroperturbation; Electroporation; Phosphatidylserine externalization; Ultra short nanosecond high field electric pulse

Indexed keywords

CALCIUM; CASPASE; PHOSPHATIDYLSERINE;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL MEMBRANE; CELL STRUCTURE; CONTROLLED STUDY; ELECTRIC FIELD; ELECTROPORATION; ENZYME ACTIVATION; EXPOSURE; GENE TRANSLOCATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; LYMPHOBLAST; LYMPHOCYTE; PRIORITY JOURNAL; SYMPTOM;

EID: 0141793941     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2003.08.140     Document Type: Article

References (64)

1. Rols M.-P., Teissie J. Electropermeabilization of mammalian cells: quantitative analysis of the phenomenon. Biophys. J. 58:1990;1089-1098.
2. Mir L.M. Therapeutic perspectives of in vivo cell electropermeabilization. Bioelectrochem. 53:2001;1-10.
3. Zimmermann U. The effect of high intensity electric field pulses on eukaryotic cell membranes: fundamentals and applications. Zimmermann U., Neil G.A. Electromanipulation of Cells. 1996;CRC Press, Boca Raton, FL.
4. Plonsey R., Altman K.W. Electrical stimulation of excitable cells - a model approach. Proc. IEEE. 76:1988;1122-1129.
5. Sher L.D., Kresch E., Schwan H.P. On the possibility of nonthermal biological effects of pulsed electromagnetic radiation. Biophys. J. 10:1970;970-979.
6. Foster K.R. Thermal and nonthermal mechanisms of interaction of radio-frequency energy with biological systems. IEEE Trans. Plasma Sci. 28:2000;15-23.
7. Schoenbach K.H., Beebe S.J., Buescher E.S. Intracellular effect of ultrashort electrical pulses. Bioelectromagnetics. 22:2001;440-448.
8. P.T. Vernier, A. Li, L. Marcu, C.M. Craft, M.A. Gundersen, Ultrashort pulsed electric fields induce membrane phospholipid translocation and caspase activation: differential sensitivities of Jurkat T lymphoblasts and rat glioma C6 cells, IEEE Trans. Dielect. Elect. Insulation (2003), in press.
9. Hofmann F., Ohnimus H., Scheller C., Strupp W., Zimmermann U., Jassoy C. Electric field pulses can induce apoptosis. J. Membr. Biol. 169:1999;103-109.
10. Beebe S.J., Fox P.M., Rec L.J., Somers K., Stark R.H., Schoenbach K.H. Nanosecond pulsed electric field (nsPEF) effects on cells and tissues: apoptosis induction and tumor growth inhibition. IEEE Trans. Plasma Sci. 30:2002;286-292.
11. Deng J., Schoenbach K.H., Buescher E.S., Hair P.S., Fox P.M., Beebe S.J. The effects of intense submicrosecond electrical pulses on cells. Biophys. J. 84:2003;2709-2714.
12. Beebe S.J., Fox P.M., Rec L.J., Willis E.L., Schoenbach K.H. Nanosecond, high-intensity pulsed electric fields induce apoptosis in human cells. FASEB J. 17:2003;1493-1495.
13. Balasubramanian K., Chandra J., Schroit A.J. Immune clearance of phosphatidylserine-expressing cells by phagocytes. J. Biol. Chem. 272:1997;31113-31117.
14. Haest C.W.M., Kamp D., Deuticke B. Transbilayer reorientation of phospholipid probes in the human erythrocyte membrane. Lessons from studies on electroporated and resealed cells. Biochim. Biophys. Acta. 1325:1997;17-33.
15. i signals generated by electroporation functionally mimic those evoked by hormonal stimulation. FASEB J. 13:1999;365-376.
16. 2+ induces transbilayer redistribution of all major phospholipids in human erythrocytes. Biochemistry. 31:1992;6355-6360.
17. McConkey D.J., Orrenius S. The role of calcium in the regulation of apoptosis. Biochem. Biophys. Res. Commun. 239:1997;357-366.
18. 2+ entry - role of actin cytoskeleton. J. Biol. Chem. 276:2001;5134-5139.
19. M. Behrend, A. Kuthi, X. Gu, P.T. Vernier, L. Marcu, C.M. Craft, and M.A. Gundersen, Pulse generators for pulsed electric field exposure of biological cells and tissues, IEEE Trans. Dielect. Elect. Insulation (2003), in press.
20. Martin S.J., Reutelingsperger C.P., McGahon A.J., Rader J.A., van Schie R.C., LaFace D.M., Green D.R. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182:1995;1545-1556.
21. Ferraro-Peyret C., Quemeneur L., Flacher M., Revillard J.P., Genestier L. Caspase-independent phosphatidylserine exposure during apoptosis of primary T lymphocytes. J. Immunol. 169:2002;4805-4810.
22. 3+ concentrations block the calcium release-activated channel, and impair CD69 and CD25 expression in CD3- or thapsigargin-activated Jurkat cells. Biochem. J. 313(Pt 3):1996;909-913.
23. 2+-conducting ion channels in mechanically induced signal transduction of airway epithelial cells. J. Cell Sci. 107(Pt 11):1994;3037-3044.
24. Yang X.C., Sachs F. Block of stretch-activated ion channels in Xenopus oocytes by gadolinium and calcium ions. Science. 243:1989;1068-1071.
25. McDonald T.F., Pelzer S., Trautwein W., Pelzer D.J. Regulation and modulation of calcium channels in cardiac, skeletal, and smooth muscle cells. Physiol. Rev. 74:1994;365-507.
26. Bernardi P. Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by the proton electrochemical gradient. Evidence that the pore can be opened by membrane depolarization. J. Biol. Chem. 267:1992;8834-8839.
27. Zamzami N., Marchetti P., Castedo M., Decaudin D., Macho A., Hirsch T., Susin S.A., Petit P.X., Mignotte B., Kroemer G. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182:1995;367-377.
28. 2+ uniporter. Mol. Biol. Cell. 12:2001;63-71.
29. 2+-ATPase. Proc. Natl. Acad. Sci. USA. 87:1990;2466-2470.
30. Verhoven B., Schlegel R.A., Williamson P. Mechanisms of phosphatidylserine exposure, a phagocyte recognition signal, on apoptotic T lymphocytes. J. Exp. Med. 182:1995;1597-1601.
31. Zwaal R.F.A., Schroit A.J. Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood. 89:1997;1121-1132.
32. Fadok V.A., de Cathelineau A., Daleke D.L., Henson P.M., Bratton D.L. Loss of phospholipid asymmetry and surface exposure of phosphatidylserine is required for phagocytosis of apoptotic cells by macrophages and fibroblasts. J. Biol. Chem. 276:2001;1071-1077.
33. Polevaya Y., Ermolina I., Schlesinger M., Ginzburg B.-Z., Feldman Y. Time domain dielectric spectroscopy study of human cells. II. Normal and malignant white blood cells. Biochim. Biophys. Acta. 1419:1999;257-271.
34. Moll G.N., Konings W.N., Driessen A.J.M. The lantibiotic nisin induces transmembrane movement of a fluorescent phospholipid. J. Bacteriol. 180:1998;6565-6570.
35. Zhang P.C., Keleshian A.M., Sachs F. Voltage-induced membrane movement. Nature. 413:2001;428-432.
36. Sugar I.P. A theory of the electric field-induced phase transition of phospholipid bilayers. Biochim. Biophys. Acta. 556:1979;72-85.
37. Groves J.T., Boxer S.G., McConnell H.M. Electric field-induced critical demixing in lipid bilayer membranes. Proc. Natl. Acad. Sci. USA. 95:1998;935-938.
38. Gabriel B., Teissie J. Direct observation in the millisecond time range of fluorescent molecule symmetrical interaction with the electropermeabilized cell membrane. Biophys. J. 73:1997;2630-2637.
39. Buton X., Morrot G., Fellmann P., Seigneuret M. Ultrafast glycerophospholipid-selective transbilayer motion mediated by a protein in the endoplasmic reticulum membrane. J. Biol. Chem. 271:1996;6651-6657.
40. 2+-dependent transbilayer movement of phospholipid. J. Biol. Chem. 271:1996;17205-17210.
41. Gleiss B., Gogvadze V., Orrenius S., Fadeel B. Fas-triggered phosphatidylserine exposure is modulated by intracellular ATP. FEBS Lett. 519:2002;153-158.
42. Freeman S.A., Wang M.A., Weaver J.C. Theory of electroporation of planar bilayer membranes: predictions of the aqueous area, change in capacitance, and pore-pore separation. Biophys. J. 67:1994;42-56.
43. Zimmermann U., Pilwat G., Riemann F. Dielectric breakdown of cell membranes. Biophys. J. 14:1974;881-899.
44. Hibino M., Itoh H., Kinosita K. Time courses of cell electroporation as revealed by submicrosecond imaging of transmembrane potential. Biophys. J. 64:1993;1789-1800.
45. Gabriel B., Teissie J. Time courses of electropermeabilization observed by millisecond imaging of membrane property changes during the pulse. Biophys. J. 76:1999;2158-2165.
46. DeBruin K.A., Krassowska W. Modeling electroporation in a single cell. I. Effects of field strength and rest potential. Biophys. J. 77:1999;1213-1224.
47. Joshi R.P., Hu Q., Aly R., Schoenbach K.H., Hjalmarson H.P. Self-consistent simulations of electroporation dynamics in biological cells subjected to ultrashort electrical pulses. Phys. Rev. E. 64:2001;011913.
48. Melikov K.C., Frolov V.A., Shcherbakov A., Samsonov A.V., Chizmadzhev Y.A. Voltage-induced nonconductive pre-pores and metastable single pores in unmodified planar lipid bilayer. Biophys. J. 80:2001;1829-1836.
49. 2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science. 262:1993;744-747.
50. 2+ release from the endoplasmic reticulum. J. Biol. Chem. 278:2003;15153-15161.
51. 2+ mobilization promotes cytochrome c release during apoptosis. J. Biol. Chem. 277:2002;20301-20308.
52. Blom W.M., De Bont H.J., Nagelkerke J.F. Regional loss of the mitochondrial membrane potential in the hepatocyte is rapidly followed by externalization of phosphatidylserines at that specific site during apoptosis. J. Biol. Chem. 278:2003;12467-12474.
53. Hoth M., Fanger C.M., Lewis R.S. Mitochondrial regulation of store-operated calcium signaling in T lymphocytes. J. Cell Biol. 137:1997;633-648.
54. Fernandez-Diaz M.D., Barsotti L., Dumay E., Cheftel J.C. Effects of pulsed electric fields on ovalbumin solutions and dialyzed egg white. J. Agric. Food Chem. 48:2000;2332-2339.
55. + channels mainly resulted from supramembrane potential-mediated electroconformational changes. Biophys. J. 75:1998;196-206.
56. Niggel J., Sigurdson W., Sachs F. Mechanically induced calcium movements in astrocytes, bovine aortic endothelial cells and C6 glioma cells. J. Membr. Biol. 174:2000;121-134.
57. Manno S., Takakuwa Y., Mohandas N. Identification of a functional role for lipid asymmetry in biological membranes: phosphatidylserine-skeletal protein interactions modulate membrane stability. Proc. Natl. Acad. Sci. USA. 99:2002;1943-1948.
58. Oettgen H.C., Terhorst C., Cantley L.C., Rosoff P.M. Stimulation of the T3-T cell receptor complex induces a membrane-potential-sensitive calcium influx. Cell. 40:1985;583-590.
59. Imboden J.B., Stobo J.D. Transmembrane signalling by the T cell antigen receptor. Perturbation of the T3-antigen receptor complex generates inositol phosphates and releases calcium ions from intracellular stores. J. Exp. Med. 161:1985;446-456.
60. Parekh A.B., Fleig A., Penner R. The store-operated calcium current I(CRAC): nonlinear activation by InsP3 and dissociation from calcium release. Cell. 89:1997;973-980.
61. Liu K.Q., Bunnell S.C., Gurniak C.B., Berg L.J. T cell receptor-initiated calcium release is uncoupled from capacitative calcium entry in Itk-deficient T cells. J. Exp. Med. 187:1998;1721-1727.
62. Wurth G.A., Zweifach A. Evidence that cytosolic calcium increases are not sufficient to stimulate phospholipid scrambling in human T-lymphocytes. Biochem. J. 362:2002;701-708.
63. Orrenius S., Zhivotovsky B., Nicotera P. Calcium: regulation of cell death: the calcium-apoptosis link. Nat. Rev. Mol. Cell. Biol. 4:2003;552-565.
64. Hajnoczky G., Davies E., Madesh M. Calcium signaling and apoptosis. Biochem. Biophys. Res. Commun. 304:2003;445-454.