Advertisement

Bioelectrics pp 155-274 | Cite as

Biological Responses

  • Ken-ichi YanoEmail author
  • Lea Rems
  • Tadej Kotnik
  • Damijan Miklavčič
  • James C. Weaver
  • Kyle C. Smith
  • Reuben S. Son
  • Thiruvallur R. Gowrishankar
  • P. Thomas Vernier
  • Zachary A. Levine
  • Marie-Pierre Rols
  • Justin Teissie
  • Lluis M. Mir
  • Andrei G. Pakhomov
  • Peter Nick
  • Wolfgang Frey
  • David A. Dean
  • Keiko Morotomi-Yano
  • Robert E. NealII
  • Suyashree Bhonsle
  • Rafael V. Davalos
  • Stephen J. Beebe
Chapter

Abstract

Cells are the structural and functional unit of all living organisms and exhibit fundamental properties of life. Cells are surrounded by the cell membrane and subdivided into various compartments. Pulsed electric fields (PEFs) exert profound effects on cells by interacting with the cell membrane and other cellular components. This chapter describes the biological effects of PEF at cellular and subcellular levels. First, this chapter begins with the overview of cell exposure to PEF from a biophysical point of view. Second, the interaction of PEF with biological membranes, membrane pore formation, and their physiological significance is described from multifaceted standpoints. Next, this chapter explains subcellular events induced by PEF, including the effect on cytoskeleton and signal transduction. Lastly, detailed description on irreversible electroporation and cell death by PEF is provided. The topics covered in this chapter serve as the basis for the applications of PEF in medicine, environmental science, and food and biomass processing.

Keywords

Electroporation Electropermeabilization Computational model Cell membrane Cellular effect Cell death 

References

  1. 1.
    Cortese, B., Palamà, I.E., D’Amone, S., Gigli, G.: Influence of electrotaxis on cell behaviour. Integr. Biol. 6, 817–830 (2014). doi: 10.1039/C4IB00142G CrossRefGoogle Scholar
  2. 2.
    Levin, M., Stevenson, C.G.: Regulation of cell behavior and tissue patterning by bioelectrical signals: challenges and opportunities for biomedical engineering. Annu. Rev. Biomed. Eng. 14, 295–323 (2012). doi: 10.1146/annurev-bioeng-071811-150114 CrossRefGoogle Scholar
  3. 3.
    Kotnik, T., Kramar, P., Pucihar, G., et al.: Cell membrane electroporation- part 1: the phenomenon. IEEE Electr. Insul. Mag. 28, 14–23 (2012). doi: 10.1109/MEI.2012.6268438 CrossRefGoogle Scholar
  4. 4.
    Klösgen, B., Reichle, C., Kohlsmann, S., Kramer, K.D.: Dielectric spectroscopy as a sensor of membrane headgroup mobility and hydration. Biophys. J. 71, 3251–3260 (1996)CrossRefGoogle Scholar
  5. 5.
    Tielrooij, K.J., Paparo, D., Piatkowski, L., et al.: Dielectric relaxation dynamics of water in model membranes probed by terahertz spectroscopy. Biophys. J. 97, 2484–2492 (2009). doi: 10.1016/j.bpj.2009.08.024 CrossRefGoogle Scholar
  6. 6.
    Feldman, Y., Ermolina, I., Hayashi, Y.: Time domain dielectric spectroscopy study of biological systems. IEEE Trans. Dielectr. Electr. Insul. 10, 728–753 (2003). doi: 10.1109/TDEI.2003.1237324 CrossRefGoogle Scholar
  7. 7.
    Vernier, P.T., Ziegler, M.J.: Nanosecond field alignment of head group and water dipoles in electroporating phospholipid bilayers. J. Phys. Chem. B 111, 12993–12996 (2007). doi: 10.1021/jp077148q CrossRefGoogle Scholar
  8. 8.
    Kotnik, T., Bobanović, F., Miklavčič: Sensitivity of transmembrane voltage induced by applied electric fields—a theoretical analysis. Bioelectrochem. Bioenerg. 43, 285–291 (1997). doi: 10.1016/S0302-4598(97)00023-8 CrossRefGoogle Scholar
  9. 9.
    Kotnik, T., Miklavčič, D., Slivnik, T.: Time course of transmembrane voltage induced by time-varying electric fields—a method for theoretical analysis and its application. Bioelectrochem. Bioenerg. 45, 3–16 (1998). doi: 10.1016/S0302-4598(97)00093-7 CrossRefGoogle Scholar
  10. 10.
    Kotnik, T., Miklavčič, D.: Second-order model of membrane electric field induced by alternating external electric fields. IEEE Trans. Biomed. Eng. 47, 1074–1081 (2000). doi: 10.1109/10.855935 CrossRefGoogle Scholar
  11. 11.
    Hibino, M., Shigemori, M., Itoh, H., et al.: Membrane conductance of an electroporated cell analyzed by submicrosecond imaging of transmembrane potential. Biophys. J. 59, 209–220 (1991)CrossRefGoogle Scholar
  12. 12.
    Hibino, M., Itoh, H., Kinosita, K.: Time courses of cell electroporation as revealed by submicrosecond imaging of transmembrane potential. Biophys. J. 64, 1789–1800 (1993)CrossRefGoogle Scholar
  13. 13.
    Smith, K.C., Weaver, J.C.: Active mechanisms are needed to describe cell responses to submicrosecond, megavolt-per-meter pulses: cell models for ultrashort pulses. Biophys. J. 95, 1547–1563 (2008). doi: 10.1529/biophysj.107.121921 CrossRefGoogle Scholar
  14. 14.
    Kotnik, T., Miklavčič, D.: Theoretical evaluation of voltage inducement on internal membranes of biological cells exposed to electric fields. Biophys. J. 90, 480–491 (2006). doi: 10.1529/biophysj.105.070771 CrossRefGoogle Scholar
  15. 15.
    Kotnik, T., Pucihar, G.: Induced transmembrane voltage—theory, modeling, and experiments. In: Miklavčič, D., Markov, M.S., Pakhomov, A.G. (eds.) Advanced Electroporation Techniques in Biology and Medicine, pp. 51–70. CRC Press, Boca Raton (2010)Google Scholar
  16. 16.
    Asami, K., Takahashi, Y., Takashima, S.: Dielectric properties of mouse lymphocytes and erythrocytes. Biochim. Biophys. Acta. BBA – Mol. Cell Res. 1010, 49–55 (1989). doi: 10.1016/0167-4889(89)90183-3 CrossRefGoogle Scholar
  17. 17.
    Yao, C., Mo, D., Li, C., et al.: Study of transmembrane potentials of inner and outer membranes induced by pulsed-electric-field model and simulation. IEEE Trans. Plasma. Sci. 35, 1541–1549 (2007). doi: 10.1109/TPS.2007.905110 CrossRefGoogle Scholar
  18. 18.
    Retelj, L., Pucihar, G., Miklavčič, D.: Electroporation of intracellular liposomes using nanosecond electric pulses-a theoretical study. IEEE Trans. Biomed. Eng. 60, 2624–2635 (2013). doi: 10.1109/TBME.2013.2262177 CrossRefGoogle Scholar
  19. 19.
    Schoenbach, K.H., Beebe, S.J., Buescher, E.S.: Intracellular effect of ultrashort electrical pulses. Bioelectromagnetics 22, 440–448 (2001). doi: 10.1002/bem.71 CrossRefGoogle Scholar
  20. 20.
    Tekle, E., Oubrahim, H., Dzekunov, S.M., et al.: Selective field effects on intracellular vacuoles and vesicle membranes with nanosecond electric pulses. Biophys. J. 89, 274–284 (2005). doi: 10.1529/biophysj.104.054494 CrossRefGoogle Scholar
  21. 21.
    White, J.A., Blackmore, P.F., Schoenbach, K.H., Beebe, S.J.: Stimulation of capacitative calcium entry in HL-60 cells by nanosecond pulsed electric fields. J. Biol. Chem. 279, 22964–22972 (2004). doi: 10.1074/jbc.M311135200 CrossRefGoogle Scholar
  22. 22.
    Batista Napotnik, T., Reberšek, M., Kotnik, T., et al.: Electropermeabilization of endocytotic vesicles in B16 F1 mouse melanoma cells. Med. Biol. Eng. Comput. 48, 407–413 (2010). doi: 10.1007/s11517-010-0599-9 CrossRefGoogle Scholar
  23. 23.
    Krassowska, W., Filev, P.D.: Modeling electroporation in a single cell. Biophys. J. 92, 404–417 (2007). doi: 10.1529/biophysj.106.094235 CrossRefGoogle Scholar
  24. 24.
    Li, J., Tan, W., Yu, M., Lin, H.: The effect of extracellular conductivity on electroporation-mediated molecular delivery. Biochim. Biophys. Acta 1828, 461–470 (2013). doi: 10.1016/j.bbamem.2012.08.014 CrossRefGoogle Scholar
  25. 25.
    Pucihar, G., Kotnik, T., Valič, B., Miklavčič, D.: Numerical determination of transmembrane voltage induced on irregularly shaped cells. Ann. Biomed. Eng. 34, 642–652 (2006). doi: 10.1007/s10439-005-9076-2 CrossRefGoogle Scholar
  26. 26.
    Hu, Q., Viswanadham, S., Joshi, R.P., et al.: Simulations of transient membrane behavior in cells subjected to a high-intensity ultrashort electric pulse. Phys. Rev. E 71, 031914 (2005). doi: 10.1103/PhysRevE.71.031914 CrossRefGoogle Scholar
  27. 27.
    Gowrishankar, T.R., Smith, K.C., Weaver, J.C.: Transport-based biophysical system models of cells for quantitatively describing responses to electric fields. Proc. IEEE 101, 505–517 (2013). doi: 10.1109/JPROC.2012.2200289 CrossRefGoogle Scholar
  28. 28.
    Pucihar, G., Miklavčič, D., Kotnik, T.: A time-dependent numerical model of transmembrane voltage inducement and electroporation of irregularly shaped cells. IEEE Trans. Biomed. Eng. 56, 1491–1501 (2009). doi: 10.1109/TBME.2009.2014244 CrossRefGoogle Scholar
  29. 29.
    Susil, R., Semrov, D., Miklavčič, D.: Electric field induced transmembrane potential depends on cell density and organization. Electro. Magnetobiol. 17, 391–399 (1998)CrossRefGoogle Scholar
  30. 30.
    Pavlin, M., Pavselj, N., Miklavčič, D.: Dependence of induced transmembrane potential on cell density, arrangement, and cell position inside a cell system. IEEE Trans. Biomed. Eng. 49, 605–612 (2002)CrossRefGoogle Scholar
  31. 31.
    Pucihar, G., Kotnik, T., Teissié, J., Miklavčič, D.: Electropermeabilization of dense cell suspensions. Eur. Biophys. J. 36, 173–185 (2007). doi: 10.1007/s00249-006-0115-1 CrossRefGoogle Scholar
  32. 32.
    Ling, G., Gerard, R.W.: The normal membrane potential of frog sartorius fibers. J. Cell. Comp. Physiol. 34, 383–396 (1949). doi: 10.1002/jcp.1030340304 CrossRefGoogle Scholar
  33. 33.
    Neher, E., Sakmann, B.: Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature 260, 799–802 (1976). doi: 10.1038/260799a0 CrossRefGoogle Scholar
  34. 34.
    Fluhler, E., Burnham, V.G., Loew, L.M.: Spectra, membrane binding, and potentiometric responses of new charge shift probes. Biochemistry (Mosc.) 24, 5749–5755 (1985). doi: 10.1021/bi00342a010 CrossRefGoogle Scholar
  35. 35.
    Gross, D., Loew, L.M., Webb, W.W.: Optical imaging of cell membrane potential changes induced by applied electric fields. Biophys. J. 50, 339–348 (1986)CrossRefGoogle Scholar
  36. 36.
    Pucihar, G., Kotnik, T., Miklavčič, D.: Measuring the induced membrane voltage with Di-8-ANEPPS. J. Vis. Exp. JoVE. (2009). doi: 10.3791/1659 Google Scholar
  37. 37.
    Frey, W., White, J.A., Price, R.O., et al.: Plasma membrane voltage changes during nanosecond pulsed electric field exposure. Biophys. J. 90, 3608–3615 (2006). doi: 10.1529/biophysj.105.072777 CrossRefGoogle Scholar
  38. 38.
    White, J.A., Pliquett, U., Blackmore, P.F., et al.: Plasma membrane charging of Jurkat cells by nanosecond pulsed electric fields. Eur. Biophys. J. 40, 947–957 (2011). doi: 10.1007/s00249-011-0710-7 CrossRefGoogle Scholar
  39. 39.
    Towhidi, L., Kotnik, T., Pucihar, G., et al.: Variability of the minimal transmembrane voltage resulting in detectable membrane electroporation. Electromagn. Biol. Med. 27, 372–385 (2008). doi: 10.1080/15368370802394644 CrossRefGoogle Scholar
  40. 40.
    Gabriel, B., Teissie, J.: Time courses of mammalian cell electropermeabilization observed by millisecond imaging of membrane property changes during the pulse. Biophys. J. 76, 2158–2165 (1999)CrossRefGoogle Scholar
  41. 41.
    Pucihar, G., Kotnik, T., Miklavčič, D., Teissié, J.: Kinetics of transmembrane transport of small molecules into electropermeabilized cells. Biophys. J. 95, 2837–2848 (2008). doi: 10.1529/biophysj.108.135541 CrossRefGoogle Scholar
  42. 42.
    He, H., Chang, D.C., Lee, Y.-K.: Using a micro electroporation chip to determine the optimal physical parameters in the uptake of biomolecules in HeLa cells. Bioelectrochem. Amst. Neth. 70, 363–368 (2007). doi: 10.1016/j.bioelechem.2006.05.008 CrossRefGoogle Scholar
  43. 43.
    Pakhomov, A.G., Gianulis, E., Vernier, P.T., et al.: Multiple nanosecond electric pulses increase the number but not the size of long-lived nanopores in the cell membrane. Biochim. Biophys. Acta. BBA – Biomembr. 1848, 958–966 (2015). doi: 10.1016/j.bbamem.2014.12.026 CrossRefGoogle Scholar
  44. 44.
    Vasilkoski, Z., Esser, A.T., Gowrishankar, T.R., Weaver, J.C.: Membrane electroporation: the absolute rate equation and nanosecond time scale pore creation. Phys. Rev. E 74, 021904 (2006). doi: 10.1103/PhysRevE.74.021904 CrossRefGoogle Scholar
  45. 45.
    Kotnik, T., Pucihar, G., Miklavčič, D.: Induced transmembrane voltage and its correlation with electroporation-mediated molecular transport. J. Membr. Biol. 236, 3–13 (2010). doi: 10.1007/s00232-010-9279-9 CrossRefGoogle Scholar
  46. 46.
    Smith, K.C.: A unified model of electroporation and molecular transport. Massachusetts Institute of Technology, http://dspace.mit.edu/bitstream/handle/1721.1/63085/725958797.pdf
  47. 47.
    Son, R.S., Smith, K.C., Gowrishankar, T.R., Vernier, P.T., Weaver, J.C.: J. Membr. Biol. 247, 1209 (2014)CrossRefGoogle Scholar
  48. 48.
    Pauly, H., Schwan, H.P.: Z Naturforsch 14B, 125 (1959)Google Scholar
  49. 49.
    Gowrishankar, T.R., Weaver, J.C.: Proc. Natl. Acad. Sci. U. S. A. 100, 3203 (2003)CrossRefGoogle Scholar
  50. 50.
    Smith, K.C., Weaver, J.C.: IEEE Trans. Biomed. Eng. 59, 1514 (2012)CrossRefGoogle Scholar
  51. 51.
    Kinosita, K., Ashikawa, I., Saita, N., Yoshimura, H., Itoh, H., Nagayma, K., Ikegami, A.: Biophys. J. 53, 1015 (1988)CrossRefGoogle Scholar
  52. 52.
    Singer, S.J., Nicolson, G.L.: The fluid mosaic model of the structure of cell membranes. Science 175, 720–731 (1972)CrossRefGoogle Scholar
  53. 53.
    Abidor, I.G., Arakelyan, V.B., Chernomordik, L.V., Chizmadzhev, Y.A., Pastushenko, V.F., Tarasevich, M.R.: Electric breakdown of bilayer lipid membranes I. Main experimental facts and their qualitative discussion. Bioelectrochem. Bioenerg. 6, 37–52 (1979)CrossRefGoogle Scholar
  54. 54.
    Sugar, I.P.: The effects of external fields on the structure of lipid bilayers. J. Physiol. Paris 77, 1035–1042 (1981)Google Scholar
  55. 55.
    Zimmermann, U., Scheurich, P., Pilwat, G., Benz, R.: Cells with manipulated functions: new perspectives for cell biology, medicine, and technology. Angew. Chem. Int. Ed. Engl. 20, 325–344 (1981)CrossRefGoogle Scholar
  56. 56.
    Neumann, E., Schaefer-Ridder, M., Wang, Y., Hofschneider, P.H.: Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J. 1, 841–845 (1982)Google Scholar
  57. 57.
    Sugar, I.P., Neumann, E.: Stochastic model for electric field-induced membrane pores. Electroporation. Biophys. Chem. 19, 211–225 (1984)CrossRefGoogle Scholar
  58. 58.
    Bockmann, R.A., de Groot, B.L., Kakorin, S., Neumann, E., Grubmuller, H.: Kinetics, statistics, and energetics of lipid membrane electroporation studied by molecular dynamics simulations. Biophys. J. 95, 1837–1850 (2008)CrossRefGoogle Scholar
  59. 59.
    Levine, Z.A., Vernier, P.T.: Life cycle of an electropore: field-dependent and field-independent steps in pore creation and annihilation. J. Membr. Biol. 236, 27–36 (2010)CrossRefGoogle Scholar
  60. 60.
    Marracino, P., Amadei, A., Apollonio, F., D’Inzeo, G., Liberti, M., di Crescenzo, A., Fontana, A., Zappacosta, R., Aschi, M.: Modeling of chemical reactions in micelle: water-mediated keto-enol interconversion as a case study. J. Phys. Chem. B 115, 8102–8111 (2011)CrossRefGoogle Scholar
  61. 61.
    van der Ploeg, P., Berendsen, H.J.C.: Molecular dynamics simulation of a bilayer membrane. J. Chem. Phys. 76, 3271–3276 (1982)CrossRefGoogle Scholar
  62. 62.
    Egberts, E., Marrink, S.J., Berendsen, H.J.: Molecular dynamics simulation of a phospholipid membrane. Eur. Biophys. J. 22, 423–436 (1994)CrossRefGoogle Scholar
  63. 63.
    Tieleman, D.P., Leontiadou, H., Mark, A.E., Marrink, S.J.: Simulation of pore formation in lipid bilayers by mechanical stress and electric fields. J. Am. Chem. Soc. 125, 6382–6383 (2003)CrossRefGoogle Scholar
  64. 64.
    Gurtovenko, A.A., Vattulainen, I.: Pore formation coupled to ion transport through lipid membranes as induced by transmembrane ionic charge imbalance: atomistic molecular dynamics study. J. Am. Chem. Soc. 127, 17570–17571 (2005)CrossRefGoogle Scholar
  65. 65.
    Tarek, M.: Membrane electroporation: a molecular dynamics simulation. Biophys. J. 88, 4045–4053 (2005)CrossRefGoogle Scholar
  66. 66.
    Tieleman, D.P.: The molecular basis of electroporation. BMC Biochem. 5, 10 (2004)CrossRefGoogle Scholar
  67. 67.
    Ho, M.C., Levine, Z.A., Vernier, P.T.: Nanoscale, electric field-driven water bridges in vacuum gaps and lipid bilayers. J. Membr. Biol. 246, 793–801 (2013)CrossRefGoogle Scholar
  68. 68.
    Tokman, M., Lee, J.H., Levine, Z.A., Ho, M.C., Colvin, M.E., Vernier, P.T.: Electric field-driven water dipoles: nanoscale architecture of electroporation. PLoS One 8, e61111 (2013)CrossRefGoogle Scholar
  69. 69.
    Neumann, E., Rosenheck, K.: Permeability changes induced by electric impulses in vesicular membranes. J. Membr. Biol. 10, 279–290 (1972)CrossRefGoogle Scholar
  70. 70.
    Weaver, J.C.: Electroporation theory. Concepts and mechanisms. Methods Mol. Biol. 48, 3–28 (1995)Google Scholar
  71. 71.
    Bernhardt, J., Pauly, H.: On the generation of potential differences across the membranes of ellipsoidal cells in an alternating electrical field. Biophysik 10, 89–98 (1973)CrossRefGoogle Scholar
  72. 72.
    Teissie, J., Golzio, M., Rols, M.P.: Mechanisms of cell membrane electropermeabilization: a minireview of our present (lack of ?) knowledge. Biochim. Biophys. Acta 1724, 270–280 (2005)CrossRefGoogle Scholar
  73. 73.
    Robello, M., Gliozzi, A.: Conductance transition induced by an electric field in lipid bilayers. Biochim. Biophys. Acta 982, 173–176 (1989)CrossRefGoogle Scholar
  74. 74.
    Teissie, J., Rols, M.P.: An experimental evaluation of the critical potential difference inducing cell-membrane electropermeabilization. Biophys. J. 65, 409–413 (1993)CrossRefGoogle Scholar
  75. 75.
    Rols, M.P., Teissie, J.: Electropermeabilization of mammalian cells. Quantitative analysis of the phenomenon. Biophys. J. 58, 1089–1098 (1990)CrossRefGoogle Scholar
  76. 76.
    Kotnik, T., Miklavcic, D.: Analytical description of transmembrane voltage induced by electric fields on spheroidal cells. Biophys. J. 79, 670–679 (2000)CrossRefGoogle Scholar
  77. 77.
    Kotnik, T., Pucihar, G., Rebersek, M., Miklavcic, D., Mir, L.M.: Role of pulse shape in cell membrane electropermeabilization. Biochim. Biophys. Acta 1614, 193–200 (2003)CrossRefGoogle Scholar
  78. 78.
    Gehl, J.: Electroporation: theory and methods, perspectives for drug delivery, gene therapy and research. Acta Physiol. Scand. 177, 437–447 (2003)CrossRefGoogle Scholar
  79. 79.
    Staal, L., Gilbert, R.: Generators and applicators: equipment for electroporation. In: Kee, S.T., Gehl, J., Lee, E.W. (eds.) Clinical Aspects of Electroporation. Springer, New York (2011)Google Scholar
  80. 80.
    Gothelf, A., Gehl, J.: Electroporation-based DNA delivery technology: methods for gene electrotransfer to skin. In: Rinaldi, M., Fioretti, D., Iurescia, S. (eds.) DNA Vaccines. Springer, New York (2014)Google Scholar
  81. 81.
    Tamzali, Y., Borde, L., Rols, M.P., Golzio, M., Lyazrhi, F., Teissie, J.: Successful treatment of equine sarcoids with cisplatin electrochemotherapy: a retrospective study of 48 cases. Equine Vet. J. 44, 214–220 (2012)CrossRefGoogle Scholar
  82. 82.
    Rols, M.P., Delteil, C., Serin, G., Teissie, J.: Temperature effects on electrotransfection of mammalian cells. Nucleic Acids Res. 22, 540 (1994)CrossRefGoogle Scholar
  83. 83.
    Rols, M.P., Golzio, M., Gabriel, B., Teissie, J.: Factors controlling electropermeabilisation of cell membranes. Technol. Cancer Res. Treat. 1, 319–328 (2002)CrossRefGoogle Scholar
  84. 84.
    Kinosita Jr., K., Tsong, T.Y.: Formation and resealing of pores of controlled sizes in human erythrocyte membrane. Nature 268, 438–441 (1977)CrossRefGoogle Scholar
  85. 85.
    Kinosita Jr., K., Tsong, T.Y.: Voltage-induced conductance in human erythrocyte membranes. Biochim. Biophys. Acta 554, 479–497 (1979)CrossRefGoogle Scholar
  86. 86.
    Rols, M.P., Teissie, J.: Electropermeabilization of mammalian cells to macromolecules: control by pulse duration. Biophys. J. 75, 1415–1423 (1998)CrossRefGoogle Scholar
  87. 87.
    Pucihar, G., Mir, L.M., Miklavcic, D.: The effect of pulse repetition frequency on the uptake into electropermeabilized cells in vitro with possible applications in electrochemotherapy. Bioelectrochemistry 57, 167–172 (2002)CrossRefGoogle Scholar
  88. 88.
    Rols, M.P., Teissie, J.: Flow cytometry quantification of electropermeabilization. Methods Mol. Biol. 91, 141–147 (1998)Google Scholar
  89. 89.
    Escoffre, J.M., Portet, T., Favard, C., Teissie, J., Dean, D.S., Rols, M.P.: Electromediated formation of DNA complexes with cell membranes and its consequences for gene delivery. Biochim. Biophys. Acta 1808, 1538–1543 (2011)CrossRefGoogle Scholar
  90. 90.
    Orlowski, S., Belehradek Jr., J., Paoletti, C., Mir, L.M.: Transient electropermeabilization of cells in culture. Increase of the cytotoxicity of anticancer drugs. Biochem. Pharmacol. 37, 4727–4733 (1988)CrossRefGoogle Scholar
  91. 91.
    Portet, T., Camps I Febrer, F., Escoffre, J.M., Favard, C., Rols, M.P., Dean, D.S.: Visualization of membrane loss during the shrinkage of giant vesicles under electropulsation. Biophys. J. 96, 4109–4121 (2009)CrossRefGoogle Scholar
  92. 92.
    Chopinet, L., Roduit, C., Rols, M.P., Dague, E.: Destabilization induced by electropermeabilization analyzed by atomic force microscopy. Biochim. Biophys. Acta 1828, 2223–2229 (2013)CrossRefGoogle Scholar
  93. 93.
    Chernysh, A.M., Kozlova, E.K., Moroz, V.V., Borshagovskaya, P.Y., Bliznuk, U.A., Rysaeva, R.M.: Erythrocyte membrane surface after calibrated electroporation: visualization by atomic force microscopy. Bull. Exp. Biol. Med. 148, 455–460 (2009)CrossRefGoogle Scholar
  94. 94.
    Lopez, A., Rols, M.P., Teissie, J.: 31P NMR analysis of membrane phospholipid organization in viable, reversibly electropermeabilized Chinese hamster ovary cells. Biochemistry 27, 1222–1228 (1988)CrossRefGoogle Scholar
  95. 95.
    Stulen, G.: Electric field effects on lipid membrane structure. Biochim. Biophys. Acta 640, 621–627 (1981)CrossRefGoogle Scholar
  96. 96.
    Mauroy, C., Portet, T., Winterhalder, M., Bellard, E., Blache, M.C., Teissie, J., Zumbusch, A., Rols, M.P.: Giant lipid vesicles under electric field pulses assessed by non invasive imaging. Bioelectrochemistry 87, 253–259 (2012)CrossRefGoogle Scholar
  97. 97.
    Silve, A., Leray, I., Mir, L.M.: Demonstration of cell membrane permeabilization to medium-sized molecules caused by a single 10 ns electric pulse. Bioelectrochemistry 87, 260–264 (2012)CrossRefGoogle Scholar
  98. 98.
    Golzio, M., Teissie, J., Rols, M.P.: Direct visualization at the single-cell level of electrically mediated gene delivery. Proc. Natl. Acad. Sci. U. S. A. 99, 1292–1297 (2002)CrossRefGoogle Scholar
  99. 99.
    Rols, M.P., Teissie, J.: Experimental evidence for the involvement of the cytoskeleton in mammalian cell electropermeabilization. Biochim. Biophys. Acta 1111, 45–50 (1992)CrossRefGoogle Scholar
  100. 100.
    Rols, M.P., Delteil, C., Golzio, M., Teissie, J.: Control by ATP and ADP of voltage-induced mammalian-cell-membrane permeabilization, gene transfer and resulting expression. Eur. J. Biochem. 254, 382–388 (1998)CrossRefGoogle Scholar
  101. 101.
    Escoffre, J.M., Bellard, E., Faurie, C., Sebai, S.C., Golzio, M., Teissie, J., Rols, M.P.: Membrane disorder and phospholipid scrambling in electropermeabilized and viable cells. Biochim. Biophys. Acta 1838, 1701–1709 (2014)CrossRefGoogle Scholar
  102. 102.
    Rosazza, C., Buntz, A., Riess, T., Woll, D., Zumbusch, A., Rols, M.P.: Intracellular tracking of single plasmid DNA-particles after delivery by electroporation. Mol. Ther. 21, 2217–2226 (2013)CrossRefGoogle Scholar
  103. 103.
    Mahrour, N., Pologea-Moraru, R., Moisescu, M.G., Orlowski, S., Leveque, P., Mir, L.M.: In vitro increase of the fluid-phase endocytosis induced by pulsed radiofrequency electromagnetic fields: importance of the electric field component. Biochim. Biophys. Acta 1668, 126–137 (2005)CrossRefGoogle Scholar
  104. 104.
    Antov, Y., Barbul, A., Mantsur, H., Korenstein, R.: Electroendocytosis: exposure of cells to pulsed low electric fields enhances adsorption and uptake of macromolecules. Biophys. J. 88, 2206–2223 (2005)CrossRefGoogle Scholar
  105. 105.
    Teissie, J., Knutson, V.P., Tsong, T.Y., Lane, M.D.: Electric pulse-induced fusion of 3T3 cells in monolayer culture. Science 216, 537–538 (1982)CrossRefGoogle Scholar
  106. 106.
    Teissie, J., Rols, M.P.: Fusion of mammalian cells in culture is obtained by creating the contact between cells after their electropermeabilization. Biochem. Biophys. Res. Commun. 140, 258–266 (1986)CrossRefGoogle Scholar
  107. 107.
    Mekid, H., Mir, L.M.: In vivo cell electrofusion. Biochim. Biophys. Acta 1524, 118–130 (2000)CrossRefGoogle Scholar
  108. 108.
    Marrero, B., Heller, R.: The use of an in vitro 3D melanoma model to predict in vivo plasmid transfection using electroporation. Biomaterials 33, 3036–3046 (2012)CrossRefGoogle Scholar
  109. 109.
    Gibot, L., Wasungu, L., Teissie, J., Rols, M.P.: Antitumor drug delivery in multicellular spheroids by electropermeabilization. J. Control. Release 167, 138–147 (2013)CrossRefGoogle Scholar
  110. 110.
    Canatella, P.J., Black, M.M., Bonnichsen, D.M., McKenna, C., Prausnitz, M.R.: Tissue electroporation: quantification and analysis of heterogeneous transport in multicellular environments. Biophys. J. 86, 3260–3268 (2004)CrossRefGoogle Scholar
  111. 111.
    Chopinet, L., Wasungu, L., Rols, M.P.: First explanations for differences in electrotransfection efficiency in vitro and in vivo using spheroid model. Int. J. Pharm. 423, 7–15 (2012)CrossRefGoogle Scholar
  112. 112.
    Rols, M.P., Delteil, C., Golzio, M., Dumond, P., Cros, S., Teissie, J.: In vivo electrically mediated protein and gene transfer in murine melanoma. Nat. Biotechnol. 16, 168–171 (1998)CrossRefGoogle Scholar
  113. 113.
    Gibot, L., Rols, M.P.: Progress and prospects: the use of 3D spheroid model as a relevant way to study and optimize DNA electrotransfer. Curr. Gene Ther. 13, 175–181 (2013)CrossRefGoogle Scholar
  114. 114.
    Madi, M., Rols, M.P., Gibot, L.: Efficient in vitro electropermeabilization of reconstructed human dermal tissue. J. Membr. Biol. 248, 903–908 (2015)CrossRefGoogle Scholar
  115. 115.
    Neumann, E., Sowers, A.E., Jordan, C.A.: Electroporation and Electrofusion in Cell Biology. Plenum, New York (1989)CrossRefGoogle Scholar
  116. 116.
    Saulis, G.: Kinetics of pore disappearance in a cell after electroporation. Biomed. Sci. Instrum. 35, 409–414 (1999)Google Scholar
  117. 117.
    Saulis, G., Venslauskas, M.S., Naktinis, J.: Kinetics of pore resealing in cell membranes after electroporation. Bioelectrochem. Bioenerg. 26, 1–13 (1991)CrossRefGoogle Scholar
  118. 118.
    Smith, K.C., Gowrishankar, T.R., Esser, A.T., Stewart, D.A., Weaver, J.C.: Spatially distributed, dynamic transmembrane voltages of organelle and cell membranes due to 10 ns pulses: predictions of meshed and unmeshed transport network models. IEEE Trans. Plasma Sci. 34, 1394–1404 (2006)CrossRefGoogle Scholar
  119. 119.
    Gowrishankar, T.R., Weaver, J.C.: Electrical behavior and pore accumulation in a multicellular model for conventional and supra-electroporation. Biochem. Biophys. Res. Commun. 349, 643–653 (2006)CrossRefGoogle Scholar
  120. 120.
    Hu, Q., Joshi, R.P., Schoenbach, K.H.: Simulations of nanopore formation and phosphatidylserine externalization in lipid membranes subjected to a high-intensity, ultrashort electric pulse. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 72, 031902 (2005)CrossRefGoogle Scholar
  121. 121.
    Nesin, O.M., Pakhomova, O.N., Xiao, S., Pakhomov, A.G.: Manipulation of cell volume and membrane pore comparison following single cell permeabilization with 60- and 600-ns electric pulses. Biochim. Biophys. Acta 1808, 792–801 (2011)CrossRefGoogle Scholar
  122. 122.
    Pakhomov, A.G., Pakhomova, O.N.: Nanopores: a distinct transmembrane passageway in electroporated cells. In: Pakhomov, A.G., Miklavčič, D., Markov, M.S. (eds.) Advanced Electroporation Techniques in Biology and Medicine, pp. 178–194. CRC Press, Boca Raton (2010)Google Scholar
  123. 123.
    Bowman, A.M., Nesin, O.M., Pakhomova, O.N., Pakhomov, A.G.: Analysis of plasma membrane integrity by fluorescent detection of Tl(+) uptake. J. Membr. Biol. 236, 15–26 (2010)CrossRefGoogle Scholar
  124. 124.
    Glaser, R.W., Leikin, S.L., Chernomordik, L.V., Pastushenko, V.F., Sokirko, A.I.: Reversible electrical breakdown of lipid bilayers: formation and evolution of pores. Biochim. Biophys. Acta 940, 275–287 (1988)CrossRefGoogle Scholar
  125. 125.
    Gabai, V.L., Meriin, A.B., Mosser, D.D., Caron, A.W., Rits, S., Shifrin, V.I., Sherman, M.Y.: Hsp70 prevents activation of stress kinases. A novel pathway of cellular thermotolerance. J. Biol. Chem. 272, 18033–18037 (1997)CrossRefGoogle Scholar
  126. 126.
    Barros, L.F., Hermosilla, T., Castro, J.: Necrotic volume increase and the early physiology of necrosis. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 130, 401–409 (2001)CrossRefGoogle Scholar
  127. 127.
    Barros, L.F., Stutzin, A., Calixto, A., Catalan, M., Castro, J., Hetz, C., Hermosilla, T.: Nonselective cation channels as effectors of free radical-induced rat liver cell necrosis. Hepatology 33, 114–122 (2001)CrossRefGoogle Scholar
  128. 128.
    Dyachok, O., Zhabyeyev, P., McDonald, T.F.: Electroporation-induced inward current in voltage-clamped guinea pig ventricular myocytes. J. Membr. Biol. 238, 69–80 (2010)CrossRefGoogle Scholar
  129. 129.
    Pakhomov, A.G., Bowman, A.M., Ibey, B.L., Andre, F.M., Pakhomova, O.N., Schoenbach, K.H.: Lipid nanopores can form a stable, ion channel-like conduction pathway in cell membrane. Biochem. Biophys. Res. Commun. 385, 181–186 (2009)CrossRefGoogle Scholar
  130. 130.
    Semenov, I., Xiao, S., Pakhomova, O.N., Pakhomov, A.G.: Recruitment of the intracellular Ca by ultrashort electric stimuli: The impact of pulse duration. Cell Calcium 54, 145–150 (2013)CrossRefGoogle Scholar
  131. 131.
    Semenov, I., Xiao, S., Pakhomov, A.G.: Primary pathways of intracellular Ca(2+) mobilization by nanosecond pulsed electric field. Biochim. Biophys. Acta 1828, 981–989 (2013)CrossRefGoogle Scholar
  132. 132.
    Okada, Y.: Ion channels and transporters involved in cell volume regulation and sensor mechanisms. Cell Biochem. Biophys. 41, 233–258 (2004)CrossRefGoogle Scholar
  133. 133.
    Okada, Y., Shimizu, T., Maeno, E., Tanabe, S., Wang, X., Takahashi, N.: Volume-sensitive chloride channels involved in apoptotic volume decrease and cell death. J. Membr. Biol. V209, 21–29 (2006)CrossRefGoogle Scholar
  134. 134.
    Molleman, A.: Patch Clamping: An Introductory Guide to Patch Clamp Electrophysiology. Wiley, Padstow (2002)CrossRefGoogle Scholar
  135. 135.
    Ibey, B.L., Xiao, S., Schoenbach, K.H., Murphy, M.R., Pakhomov, A.G.: Plasma membrane permeabilization by 60- and 600-ns electric pulses is determined by the absorbed dose. Bioelectromagnetics 30, 92–99 (2009)CrossRefGoogle Scholar
  136. 136.
    Varghese, A., Tenbroek, E.M., Coles Jr., J., Sigg, D.C.: Endogenous channels in HEK cells and potential roles in HCN ionic current measurements. Prog. Biophys. Mol. Biol. 90, 26–37 (2006)CrossRefGoogle Scholar
  137. 137.
    Ghamari-Langroudi, M., Bourque, C.W.: Ionic basis of the caesium-induced depolarisation in rat supraoptic nucleus neurones. J. Physiol. 536, 797–808 (2001)CrossRefGoogle Scholar
  138. 138.
    Pakhomov, A.G., Kolb, J.F., White, J.A., Joshi, R.P., Xiao, S., Schoenbach, K.H.: Long-lasting plasma membrane permeabilization in mammalian cells by nanosecond pulsed electric field (nsPEF). Bioelectromagnetics 28, 655–663 (2007)CrossRefGoogle Scholar
  139. 139.
    Andre, F.M., Rassokhin, M.A., Bowman, A.M., Pakhomov, A.G.: Gadolinium blocks membrane permeabilization induced by nanosecond electric pulses and reduces cell death. Bioelectrochemistry 79, 95–100 (2010)CrossRefGoogle Scholar
  140. 140.
    Pakhomov, A.G., Shevin, R., White, J.A., Kolb, J.F., Pakhomova, O.N., Joshi, R.P., Schoenbach, K.H.: Membrane permeabilization and cell damage by ultrashort electric field shocks. Arch. Biochem. Biophys. 465, 109–118 (2007)CrossRefGoogle Scholar
  141. 141.
    Berridge, M.J., Lipp, P., Bootman, M.D.: The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1, 11–21 (2000)CrossRefGoogle Scholar
  142. 142.
    Tolstykh, G.P., Beier, H.T., Roth, C.C., Thompson, G.L., Ibey, B.L.: 600ns pulse electric field-induced phosphatidylinositol-bisphosphate depletion. Bioelectrochemistry 100, 80–87 (2014)CrossRefGoogle Scholar
  143. 143.
    Tolstykh, G.P., Beier, H.T., Roth, C.C., Thompson, G.L., Payne, J.A., Kuipers, M.A., Ibey, B.L.: Activation of intracellular phosphoinositide signaling after a single 600 nanosecond electric pulse. Bioelectrochemistry 94, 23–29 (2013)CrossRefGoogle Scholar
  144. 144.
    Zhivotovsky, B., Orrenius, S.: Calcium and cell death mechanisms: a perspective from the cell death community. Cell Calcium 50, 211–221 (2011)CrossRefGoogle Scholar
  145. 145.
    Nuccitelli, R., Lui, K., Kreis, M., Athos, B., Nuccitelli, P.: Nanosecond pulsed electric field stimulation of reactive oxygen species in human pancreatic cancer cells is Ca(2+)-dependent. Biochem. Biophys. Res. Commun. 435, 580–585 (2013)CrossRefGoogle Scholar
  146. 146.
    Morotomi-Yano, K., Akiyama, H., Yano, K.: Nanosecond pulsed electric fields induce poly(ADP-ribose) formation and non-apoptotic cell death in HeLa S3 cells. Biochem. Biophys. Res. Commun. 438, 557–562 (2013)CrossRefGoogle Scholar
  147. 147.
    Ren, W., Sain, N.M., Beebe, S.J.: Nanosecond pulsed electric fields (nsPEFs) activate intrinsic caspase-dependent and caspase-independent cell death in Jurkat cells. Biochem. Biophys. Res. Commun. 421, 808–812 (2012)CrossRefGoogle Scholar
  148. 148.
    Pakhomova, O.N., Gregory, B., Semenov, I., Pakhomov, A.G.: Calcium-mediated pore expansion and cell death following nanoelectroporation. Biochim. Biophys. Acta 1838, 2547–2554 (2014)CrossRefGoogle Scholar
  149. 149.
    Pakhomova, O.N., Gregory, B.W., Semenov, I., Pakhomov, A.G.: Two modes of cell death caused by exposure to nanosecond pulsed electric field. PLoS One 8, e70278 (2013)CrossRefGoogle Scholar
  150. 150.
    Ibey, B.L., Pakhomov, A.G., Gregory, B.W., Khorokhorina, V.A., Roth, C.C., Rassokhin, M.A., Bernhard, J.A., Wilmink, G.J., Pakhomova, O.N.: Selective cytotoxicity of intense nanosecond-duration electric pulses in mammalian cells. Biochim. Biophys. Acta 1800, 1210–1219 (2010)CrossRefGoogle Scholar
  151. 151.
    Pickard, B.G.: “second extrinsic organizational mechanism” for orienting cellulose: modelling a role for the plasmalemmal reticulum. Protoplasma 233, 1–29 (2008)CrossRefGoogle Scholar
  152. 152.
    Nick, P.: Microtubules and the tax payer. Protoplasma 249 (Special Issue Applied Plant Cell Biology), 81–94 (2012)Google Scholar
  153. 153.
    Frey, N., Klotz, J., Nick, P.: A kinesin with calponin-homology domain is involved in premitotic nuclear migration. J. Exp. Bot. 61, 3423–3437 (2010)CrossRefGoogle Scholar
  154. 154.
    Murata, T., Wada, M.: Effects of centrifugation on preprophase-band formation in Adiantum (1991)Google Scholar
  155. 155.
    Nick, P.: Signalling to the microtubular cytoskeleton in plants. Int. Rev. Cytol. 184, 33–80 (1998)CrossRefGoogle Scholar
  156. 156.
    Klotz, J., Nick, P.: A novel actin-microtubule cross-linking kinesin, NtKCH, functions in cell expansion and division. New Phytol. 193, 576–589 (2012)CrossRefGoogle Scholar
  157. 157.
    Parthasarathy, M.V.: F-actin architecture in coleoptile epidermal cells. Eur. J. Cell Biol. 39, 1–12 (1985)Google Scholar
  158. 158.
    Grabski, S., Schindler, M.: Auxins and cytokinins as antipodal modulators of elasticity within the actin network of plant cells. Plant Physiol. 110, 965–970 (1996)Google Scholar
  159. 159.
    Grabski, S., Arnoys, E., Busch, B., Schindler, M.: Regulation of actin tension in plant cells by kinases and phosphatases. Plant Physiol. 116, 279–290 (1998)CrossRefGoogle Scholar
  160. 160.
    Waller, F., Nick, P.: Response of actin microfilaments during phytochrome-controlled growth of maize seedlings. Protoplasma 200, 154–162 (1997)CrossRefGoogle Scholar
  161. 161.
    Sonobe, S., Shibaoka, H.: Cortical fine actin filaments in higher plant cells visualized by rhodamine-phalloidin after pretreatment with m-maleimidobenzoyl-N-hydroxysuccinimide ester. Protoplasma 48, 80–86 (1989)CrossRefGoogle Scholar
  162. 162.
    Thimann, K.V., Reese, K., Nachmikas, V.T.: Actin and the elongation of plant cells. Protoplasma 171, 151–166 (1992)CrossRefGoogle Scholar
  163. 163.
    Wang, Q.Y., Nick, P.: The auxin response of actin is altered in the rice mutant Yin-Yang. Protoplasma 204, 22–33 (1998)CrossRefGoogle Scholar
  164. 164.
    Sano, T., Higaki, T., Oda, Y., Hayashi, T., Hasezawa, S.: Appearance of actin microfilament ‘twin peaks’ in mitosis and their function in cell plate formation, as visualized in tobacco BY-2 cells expressing GFP–fimbrin. Plant J. 44, 595–605 (2005)CrossRefGoogle Scholar
  165. 165.
    Maisch, J., Nick, P.: Actin is involved in auxin-dependent patterning. Plant Physiol. 143, 1695–1704 (2007)CrossRefGoogle Scholar
  166. 166.
    Traas, J.A., Doonan, J.H., Rawlins, D.J., Shaw, P.J., Watts, J., Lloyd, C.W.: An actin network is present in the cytoplasm throughout the cell cycle of carrot cells and associates with the dividing (1987)Google Scholar
  167. 167.
    Durst, S., Hedde, P.N., Brochhausen, L., Nick, P., Nienhaus, G.U., Maisch, J.: Organization of perinuclear actin in live tobacco cells observed by PALM with optical sectioning. J. Plant Physiol. 141, 97–108 (2014)CrossRefGoogle Scholar
  168. 168.
    Fosket, D.E., Morejohn, L.C.: Structural and functional organization of tubulin. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 43, 201–240 (1992)CrossRefGoogle Scholar
  169. 169.
    Meagher, R.B., Mckinney, E.C., Vitale, A.V.: The evolution of new structures: clues from plant cytoskeletal genes. Trends Genet. 15, 278–284 (1999)CrossRefGoogle Scholar
  170. 170.
    Meagher, R.B.: Divergence and differential expression of actin gene families in higher plants. Int. Rev. Cytol. 125, 139–163 (1991)CrossRefGoogle Scholar
  171. 171.
    Silflow, C.D., Oppenheimer, D.G., Kopczak, S.D., Ploense, S.E., Ludwig, S.R., Haas, N., Snustad, D.P.: Plant tubulin genes: structure and differential expression during development. Dev. Genet. 8, 435–460 (1987)CrossRefGoogle Scholar
  172. 172.
    Vantard, M., Levilliers, N., Hill, A.M., Adoutte, A., Lambert, A.M.: Incorporation of Paramecium axonemal tubulin into higher plant cells reveals functional sites of microtubule assembly. Proc. Natl. Acad. Sci. U. S. A. 87, 8825–8829 (1990)CrossRefGoogle Scholar
  173. 173.
    Zhang, D., Waldsworth, P., Hepler, P.K.: Microtubule dynamics in living dividing plant cells: confocal imaging of microinjected fluorescent brain tubulin. Proc. Natl. Acad. Sci. U. S. A. 87, 8820–8824 (1990)CrossRefGoogle Scholar
  174. 174.
    Yuan, M., Shaw, P.J., Warn, R.M., Lloyd, C.W.: Dynamic reorientation of cortical microtubules from transverse to longitudinal, in living cells. Proc. Natl. Acad. Sci. U. S. A. 91, 6050–6053 (1994)CrossRefGoogle Scholar
  175. 175.
    Himmelspach, R., Wymer, C.L., Lloyd, C.W., Nick, P.: Gravity-induced reorientation of cortical microtubules observed in vivo. Plant J. 18, 449–453 (1999)CrossRefGoogle Scholar
  176. 176.
    Staiger, C.J., Poulter, N.S., Henty, J.L., Franklin-Tong, V.E., Blanchoin, L.: Regulation of actin dynamics by actin-binding proteins in pollen. J. Exp. Bot. 61, 1969–1986 (2010)CrossRefGoogle Scholar
  177. 177.
    Struk, S., Dhonukshe, P.: MAPs: cellular navigators for microtubule array orientations in Arabidopsis. Plant Cell Rep. 33, 1–21 (2014)CrossRefGoogle Scholar
  178. 178.
    Cai, G., Cresti, M.: Are kinesins required for organelle trafficking in plant cells? Front. Plant Sci. 3, 170 (2012)CrossRefGoogle Scholar
  179. 179.
    Sparkes, I.: Recent advances in understanding plant myosin function: life in the fast lane. Mol. Plant 4, 805–812 (2011)CrossRefGoogle Scholar
  180. 180.
    Geiger, B., Bershadsky, A.: Assembly and mechanosensory function of focal contacts. Curr. Opin. Cell Biol. l3, 584–592 (2001)CrossRefGoogle Scholar
  181. 181.
    Giancotti, G., Ruoslahti, E.: Integrin signalling. Science 285, 1028–1032 (1999)CrossRefGoogle Scholar
  182. 182.
    Canut, H., Carrasco, A., Galaud, J.-P., Cassan, C., Bouyssou, H., Vita, N., Ferrara, P., Pont-Lezica, R.: High affinity RGD-binding sites at the plasma membrane of Arabidopsis thaliana links the cell wall. Plant J. 16, 63–71 (1998)CrossRefGoogle Scholar
  183. 183.
    Wang, X., Zhua, L., Liu, B., Wang, J., Zhao, L., Yuan, M.: Arabidopsis microtubule associated protein 18 functions in directional cell growth by destabilizing cortical microtubules. Plant Cell 19, 877–839 (2007)CrossRefGoogle Scholar
  184. 184.
    Zaban, B., Maisch, J., Nick, P.: Dynamic actin controls polarity induction de novo in protoplasts. J. Int. Plant Biol. 55, 142–159 (2013)CrossRefGoogle Scholar
  185. 185.
    Baluška, F., Šamaj, J., Wojtaszek, P., Volkmann, D., Menzel, D.: Cytoskeleton-plasma membrane-cell wall continuum in plants. Emerging links revisited. Plant Physiol. 133, 482–419 (2003)CrossRefGoogle Scholar
  186. 186.
    Gittes, F., Mickey, B., Nettleton, J., Howard, J.: Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J. Cell Biol. 120, 923–934 (1993)CrossRefGoogle Scholar
  187. 187.
    Ingber, D.E.: Tensegrity l: cell structure and hierarchical systems biology. J. Cell Sci. 116, 1157–1173 (2003)CrossRefGoogle Scholar
  188. 188.
    Ingber, D.E.: Tensegrity II: how structural networks influence cellular information processing networks. J. Cell Sci. 116, 1397–1403 (2003)CrossRefGoogle Scholar
  189. 189.
    Green, P.B.: Organogenesis—a biophysical view. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 3, 51–82 (1980)CrossRefGoogle Scholar
  190. 190.
    Green, P.B.: Mechanism for plant cellular morphogenesis. Science 138, 1401–1405 (1962)Google Scholar
  191. 191.
    Ledbetter, M.C., Porter, K.R.: A microtubule in plant cell fine structure. J. Cell Biol. 12, 239–250 (1963)CrossRefGoogle Scholar
  192. 192.
    Geitmann, A., Ortega, J.K.: Mechanics and modeling of plant cell growth. Trends Plant Sci. 14, 467–478 (2009)CrossRefGoogle Scholar
  193. 193.
    Nick, P.: Control of cell axis. In: Nick, P. (ed.) Plant Microtubules. Plant cell monogr, vol. 143, pp. 3–46. (2008)CrossRefGoogle Scholar
  194. 194.
    Heath, I.B.: A unified hypothesis for the role of membrane bound enzyme complexes and microtubules in plant cell wall synthesis. J. Theor. Biol. 48, 445–449 (1974)MathSciNetCrossRefGoogle Scholar
  195. 195.
    Bichet, A., Desnos, T., Turner, S., Grandjean, O., Höfte, H.: BOTERO1 is required for normal orientation of cortical microtubules and anisotropic cell expansion in Arabidopsis. Plant J. 25, 137–148 (2001)CrossRefGoogle Scholar
  196. 196.
    Zhong, R., Burk, D.H., Morrison, W.H., Ye, Z.H.: A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 14, 3101–3117 (2002)CrossRefGoogle Scholar
  197. 197.
    Paredez, A.R., Somerville, C.R., Ehrhardt, D.W.: Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491–1495 (2006)CrossRefGoogle Scholar
  198. 198.
    Li, S., Lei, L., Somerville, C.R., Gua, Y.: Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes. Proc. Natl. Acad. Sci. U. S. A. 109, 185–190 (2012)CrossRefGoogle Scholar
  199. 199.
    Los, D.A., Murata, N.: Membrane fluidity and its roles in the perception of environmental signals. Biochim. Biophys. Acta 1666, 142–157 (2004)CrossRefGoogle Scholar
  200. 200.
    Fischer, K., Schopfer, P.: Physical strain-mediated microtubule reorientation in the epidermis of gravitropically or phototropically stimulated maize coleoptiles. Plant J. 15, 119–123 (1998)CrossRefGoogle Scholar
  201. 201.
    Turing, A.M.: The chemical basis of morphogenesis. Philos. Trans. R. Soc. Lond. B Biol. 237, 37–72 (1952)MathSciNetCrossRefGoogle Scholar
  202. 202.
    Akhmanova, A., Steinmetz, M.O.: Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat. Rev. Mol. Cell Biol. 9, 309–322 (2008)CrossRefGoogle Scholar
  203. 203.
    Savage, C., Hamelin, M., Culotti, J.G., Coulson, A., Albertson, D.G., Chalfie, M.: mec-7 is a β-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev. 3, 870–881 (1989)CrossRefGoogle Scholar
  204. 204.
    Ding, J.P., Pickard, B.G.: Mechanosensory calcium-selective cation channels in epidermal cells. Plant J. 3, 83–110 (1993)CrossRefGoogle Scholar
  205. 205.
    Mazars, C., Thion, L., Thuleau, P., Graziana, A., Knight, M.R., Moreau, M., Ranjeva, R.: Organization of cytoskeleton controls the changes in cytosolic calcium of cold-shocked Nicotiana plumbaginifolia protoplasts. Cell Calcium 22, 413–420 (1997)CrossRefGoogle Scholar
  206. 206.
    Komis, G., Apostolakos, P., Galatis, B.: Hyperosmotic stress induces formation of tubulin macrotubules in root-tip cells of Triticum turgidum: their probable involvement in protoplast volume control. Plant Cell Physiol. 43, 911–922 (2002)CrossRefGoogle Scholar
  207. 207.
    Wang, S., Kurepa, J., Hashimoto, T., Smalle, J.A.: Salt stress induced disassembly of Arabidopsis cortical microtubule arrays involves 26S proteasome-dependent degradation of SPIRAL1. Plant Cell 23, 3412–3427 (2011)CrossRefGoogle Scholar
  208. 208.
    Guo, L., Devaiah, S.P., Narasimhan, R., Pan, X., Zhang, Y., Zhang, W., Wang, X.: Cytosolic glyceraldehyde-3-phosphate dehydrogenases interact with phospholipase Dδ to transduce hydrogen peroxide signals in the Arabidopsis response to stress. Plant Cell 24, 2200–2212 (2012)CrossRefGoogle Scholar
  209. 209.
    Nick, P.: Microtubules, and signalling in abiotic stress. Plant J. 75, 309–323 (2013)CrossRefGoogle Scholar
  210. 210.
    Mathur, J., Mathur, N., Hülskamp, M.: Simultaneous visualization of peroxisomes and cytoskeletal elements reveals actin and not microtubule-based peroxisome motility in plants. Plant Physiol. 128, 1031–1045 (2002)CrossRefGoogle Scholar
  211. 211.
    Kadota, A., Yamada, N., Suetsugu, N., Hirose, M., Saito, S., Shoda, K.: Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 106, 13106–13111 (2009)CrossRefGoogle Scholar
  212. 212.
    Van Gestel, K., Kohler, R.H., Verbelen, J.P.: Plant mitochondria move on F-actin, but their positioning in the cortical cytoplasm depends on both F-actin and microtubules. J. Exp. Bot. 53, 659–667 (2002)CrossRefGoogle Scholar
  213. 213.
    Boevink, P., Oparka, K., Santa Cruz, S., Martin, B., Betteridge, A., Hawes, C.: Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J. 15, 441–447 (2002)CrossRefGoogle Scholar
  214. 214.
    Rosazza, C., Escoffre, J.M., Zumbusch, A., Rols, M.P.: The actin cytoskeleton has an active role in the electrotransfer of plasmid DNA in mammalian cells. Mol. Ther. 19, 913–921 (2011)CrossRefGoogle Scholar
  215. 215.
    Sheahan, M.B., Rose, R.J., McCurdy, D.W.: Actin-filament-dependent remodeling of the vacuole in cultured mesophyll protoplasts. Protoplasma 230, 141–152 (2007)CrossRefGoogle Scholar
  216. 216.
    Waller, F., Riemann, M., Nick, P.: A role for actin-driven secretion in auxin-induced growth. Protoplasma 219, 72–81 (2002)CrossRefGoogle Scholar
  217. 217.
    Nick, P.: Probing the actin-auxin oscillator. Plant Signal. Behav. 5, 4–9 (2010)CrossRefGoogle Scholar
  218. 218.
    Nick, P., Han, M., An, G.: Auxin stimulates its own transport by actin reorganization. Plant Physiol. 151, 155–167 (2009)CrossRefGoogle Scholar
  219. 219.
    Jones, J.D., Dangl, J.L.: The plant immune system. Nature 444, 323–329 (2006)CrossRefGoogle Scholar
  220. 220.
    Qiao, F., Chang, X.L., Nick, P.: The cytoskeleton enhances gene expression in the response to the Harpin elicitor in grapevine. J. Exp. Bot. 61, 4021–4031 (2010)CrossRefGoogle Scholar
  221. 221.
    Chang, X., Heene, E., Qiao, F., Nick, P.: The phytoalexin resveratrol regulates the initiation of hypersensitive cell death in Vitis cells. PLoS One 6, e26405 (2011)CrossRefGoogle Scholar
  222. 222.
    Guan, X., Buchholz, G., Nick, P.: The cytoskeleton is disrupted by the bacterial effector HrpZ, but not by the bacterial PAMP flg22, in tobacco BY-2 cells. J. Exp. Bot. 64, 1805–1816 (2013)CrossRefGoogle Scholar
  223. 223.
    Gourlay, C.W., Ayscough, K.R.: The actin cytoskeleton: a key regulator of apoptosis and ageing? Nat. Rev. Mol. Cell Biol. 6, 583–589 (2005)CrossRefGoogle Scholar
  224. 224.
    Franklin-Tong, V.E., Gourlay, C.W.: A role for actin in regulating apoptosis/programmed cell death: evidence spanning yeast, plants and animals. Biochem. J. 413, 389–404 (2008)CrossRefGoogle Scholar
  225. 225.
    Smertenko, A., Franklin-Tong, V.E.: Organisation and regulation of the cytoskeleton in plant programmed cell death. Cell Death Diff. 18, 1263–1270 (2011)CrossRefGoogle Scholar
  226. 226.
    Smertenko, A., Bozhkov, P.: The life and death signalling underlying cell fate determination during somatic embryogenesis. Plant Cell Monogr. 22, 131–178 (2014)CrossRefGoogle Scholar
  227. 227.
    Mathur, J., Radhamony, R., Sinclair, A.M., Donoso, A., Dunn, N., Roach, E.: mEosFP-based green-to-red photoconvertible subcellular probes for plants. Plant Physiol. 154, 1573–1587 (2010)CrossRefGoogle Scholar
  228. 228.
    Opatrný, Z., Nick, P., Petrášek, J.: Plant Cell Strains in Fundamental Research and Applications Plant Cell Monographs, vol. 22, pp. 455–481. Springer, Heidelberg (2014)Google Scholar
  229. 229.
    Berghöfer, T., Eing, C., Flickinger, B., Hohenberger, P., Wegner, L., Frey, W., Nick, P.: Nanosecond electric pulses trigger actin responses in plant cells. Biochem. Biophys. Res. Commun. 387, 590–595 (2009)CrossRefGoogle Scholar
  230. 230.
    Hohenberger, P., Eing, C., Straessner, R., Durst, S., Frey, W., Nick, P.: Plant actin controls membrane permeability. BBA Membr. 1808, 2304–2312 (2011)CrossRefGoogle Scholar
  231. 231.
    Kühn, S., Liu, Q., Eing, C., Wüstner, R., Nick, P.: Nanosecond electric pulses target to a plant-specific kinesin at the plasma membrane. J. Membr. Biol. 246, 927–938 (2013)CrossRefGoogle Scholar
  232. 232.
    Campanoni, P., Blasius, B., Nick, P.: Auxin transport synchronizes the pattern of cell division in a tobacco cell line. Plant Physiol. 133, 1251–1260 (2003)CrossRefGoogle Scholar
  233. 233.
    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, 286–292 (2002)CrossRefGoogle Scholar
  234. 234.
    Buescher, E.S., Schoenbach, K.H.: Effects of submicrosecond, high intensity pulsed electric fields on living cells—intracellular electromanipulation. IEEE Trans. Dielectr. Electr. Insul. 10, 5788–5794 (2003)CrossRefGoogle Scholar
  235. 235.
    Chen, C., Smye, S.W., Robinson, M.P., Evans, J.A.: Membrane electroporation theories: a review. Med. Biol. Eng. Comput. 44, 5–14 (2006)CrossRefGoogle Scholar
  236. 236.
    Gowrishankar, T.R., Esser, A.T., Vasilkoski, Z.V., Smith, K.C., Weaver, J.C.: Microdosimetry for conventional and supra-electroporation in cells with organelles. Biochem. Biophys. Res. Commun. 310, 1266–1276 (2006)CrossRefGoogle Scholar
  237. 237.
    Schoenbach, K.H., Joshi, R.P., Chen, C., Kolb, J.F., Chen, N., Stacye, M., Blackmore, P., Buescher, E.S., Beebe, S.J.: Ultrashort electrical pulses open a new gateway into biological cells. Proc. IEEE 92, 1122–1137 (2004)CrossRefGoogle Scholar
  238. 238.
    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, 1493–1495 (2003)Google Scholar
  239. 239.
    Hu, Q., Joshi, P.R., Schoenbach, K.H.: Simulation of nanopore formation and phosphatidylserine externalization in lipid membranes subjected to a high-intensity, ultrashort electric pulses. Phys. Rev. E. 72, 031902 (2005)CrossRefGoogle Scholar
  240. 240.
    Flickinger, B., Berghöfer, T., Hohenberger, P., Eing, C., Frey, W.: Transmembrane potential measurements on plant cells using the voltage-sensitive dye ANNINE-6. Protoplasma 247, 3–12 (2010)CrossRefGoogle Scholar
  241. 241.
    Ibey, B.L., Roth, C.C., Pakhomov, A.G., Bernhard, J.A., Wilmink, G.J., Pakhomova, O.N.: Dose-dependent thresholds of 10-ns electric pulse induced plasma membrane disruption and cytotoxicity in multiple cell lines. PLoS One 6, e15642 (2011)CrossRefGoogle Scholar
  242. 242.
    Breton, M., Delemotte, L., Silve, A., Mir, L.M., Tarek, M.: Transport of siRNA through lipid membranes driven by nanosecond electric pulses: an experimental and computational study. J. Am. Chem. Soc. 134, 13938–13941 (2012)CrossRefGoogle Scholar
  243. 243.
    Preuss, M.L., Kovar, D.R., Lee, Y.R., Staiger, C.J., Delmer, D.P., Liu, B.: A plant-specific kinesin binds to actin microfilaments and interacts with cortical microtubules in cotton fibers. Plant Physiol. 136, 945–3955 (2004)CrossRefGoogle Scholar
  244. 244.
    Huang, B., Babcock, H., Zhuang, X.: Breaking the diffraction barrier: super-resolution imaging of cells. Cell 143, 1047–1058 (2010)CrossRefGoogle Scholar
  245. 245.
    Sparkes, I.A., Graumann, K., Martinière, A., Schoberer, J., Wang, P., Osterrieder, A.: Bleach it, switch it, bounce it, pull it: using lasers to reveal plant cell dynamics. J. Exp. Bot. 62, 1–7 (2011)CrossRefGoogle Scholar
  246. 246.
    Wolfe, J., Dowgert, M.F., Steponkus, P.L.: Dynamics of membrane exchange of the plasma membrane and the lysis of isolated protoplasts during rapid expansions in area. J. Membr. Biol. 86, 127–138 (1985)CrossRefGoogle Scholar
  247. 247.
    Liu, Q., Qiao, F., Ismail, A., Chang, X., Nick, P.: The plant cytoskeleton controls regulatory volume increase. BBA Membr. 1828, 2111–2120 (2013)CrossRefGoogle Scholar
  248. 248.
    Kusaka, N., Maisch, J., Nick, P., Hayashi, K.I., Nozaki, H.: Manipulation of intercellular auxin in a single cell by light with esterase-resistant caged auxins. Chembiochem 10, 2195–2202 (2009)CrossRefGoogle Scholar
  249. 249.
    Durst, S., Nick, P., Maisch, J.: Actin-depolymerizing factor 2 is involved in auxin dependent patterning. J. Plant Physiol. 170, 1057–1066 (2013)CrossRefGoogle Scholar
  250. 250.
    Thompson, G.L., Roth, C., Tolstykh, G., Kuipers, M., Ibey, B.L.: Disruption of the actin cortex contributes to susceptibility of mammalian cells to nanosecond pulsed electric fields. Bioelectromagnetics 35, 262–272 (2014)CrossRefGoogle Scholar
  251. 251.
    Stacey, M., Fox, P., Buescher, S., Kolb, J.: Nanosecond pulsed electric field induced cytoskeleton, nuclear membrane and telomere damage adversely impact cell survival. Bioelectrochemistry 82, 131–134 (2011)CrossRefGoogle Scholar
  252. 252.
    Kanthou, C., Kranjc, S., Sersa, G., Tozer, G., Zupanic, A., Cemazar, M.: The endothelial cytoskeleton as a target of electroporation-based therapies. Mol. Cancer Ther. 5, 3145–3152 (2006)CrossRefGoogle Scholar
  253. 253.
    Teissie, J., Rols, M.P.: Manipulation of cell cytoskeleton affects the lifetime of cell membrane electropermeabilization. Ann. N. Y. Acad. Sci. 720, 98–110 (1994)CrossRefGoogle Scholar
  254. 254.
    Chopinet, L., Batista-Napotnik, T., Montigny, A.: Nanosecond electric pulse effects on gene expression. J. Membr. Biol. 246, 851–859 (2013)CrossRefGoogle Scholar
  255. 255.
    Pakhomov, A.G., Xiao, S., Pakhomova, O.N., Semenov, I., Kuipers, M.A., Ibey, B.L.: Disassembly of actin structures by nanosecond pulsed electric field is a downstream effect of cell swelling. Bioelectrochemistry 100, 88–95 (2014)CrossRefGoogle Scholar
  256. 256.
    Gruenheid, S., Finlay, B.B.: Microbial pathogenesis and cytoskeletal function. Nature 422, 775–781 (2003)CrossRefGoogle Scholar
  257. 257.
    Marsh, M., Bron, R.: SFV infection in CHO cells: cell-type specific restrictions to productive virus entry at the cell surface. J. Cell Sci. 110(Pt 1), 95–103 (1997)Google Scholar
  258. 258.
    Dauty, E., Verkman, A.S.: Actin cytoskeleton as the principal determinant of size-dependent DNA mobility in cytoplasm: a new barrier for non-viral gene delivery. J. Biol. Chem. 280, 7823–7828 (2005)CrossRefGoogle Scholar
  259. 259.
    Badding, M.A., Lapek, J.D., Friedman, A.E., Dean, D.A.: Proteomic and functional analyses of protein-DNA complexes during gene transfer. Mol. Ther. 21, 775–785 (2013)CrossRefGoogle Scholar
  260. 260.
    Chambers, R.: The micromanipulation of living cells. In: Moulton, F.R. (ed.) The Cell and Protoplasm, pp. 20–30. Science press, Washington, DC (1940)Google Scholar
  261. 261.
    Lukacs, G.L., Haggie, P., Seksek, O., Lechardeur, D., Freedman, N., Verkman, A.S.: Size-dependent DNA mobility in cytoplasm and nucleus. J. Biol. Chem. 275, 1625–1629 (2000)CrossRefGoogle Scholar
  262. 262.
    Seksek, O., Biwersi, J., Verkman, A.S.: Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus. J. Cell Biol. 138, 131–142 (1997)CrossRefGoogle Scholar
  263. 263.
    Badding, M.A., Dean, D.A.: Highly acetylated tubulin permits enhanced interactions with and trafficking of plasmids along microtubules. Gene Ther. 20, 616–624 (2013)CrossRefGoogle Scholar
  264. 264.
    Badding, M.A., Vaughan, E.E., Dean, D.A.: Transcription factor plasmid binding modulates microtubule interactions and intracellular trafficking during gene transfer. Gene Ther. 19, 338–346 (2012)CrossRefGoogle Scholar
  265. 265.
    Geiger, R.C., Taylor, W., Glucksberg, M.R., Dean, D.A.: Cyclic stretch-induced reorganization of the cytoskeleton and its role in enhanced gene transfer. Gene Ther. 13, 725–731 (2006)CrossRefGoogle Scholar
  266. 266.
    Vaughan, E.E., Dean, D.A.: Intracellular trafficking of plasmids during transfection is mediated by microtubules. Mol. Ther. 13, 422–428 (2006)CrossRefGoogle Scholar
  267. 267.
    Vaughan, E.E., Geiger, R.C., Miller, A.M., Loh-Marley, P.L., Suzuki, T., Miyata, N., Dean, D.A.: Microtubule acetylation through HDAC6 inhibition results in increased transfection efficiency. Mol. Ther. 16, 1841–1847 (2008)CrossRefGoogle Scholar
  268. 268.
    Mesika, A., Kiss, V., Brumfeld, V., Ghosh, G., Reich, Z.: Enhanced intracellular mobility and nuclear accumulation of DNA plasmids associated with a karyophilic protein. Hum. Gene Ther. 16, 200–208 (2005)CrossRefGoogle Scholar
  269. 269.
    Leopold, P.L., Kreitzer, G., Miyazawa, N., Rempel, S., Pfister, K.K., Rodriguez-Boulan, E., Crystal, R.G.: Dynein- and microtubule-mediated translocation of adenovirus serotype 5 occurs after endosomal lysis. Hum. Gene Ther. 11, 151–165 (2000)CrossRefGoogle Scholar
  270. 270.
    Miller, A.M., Munkonge, F.M., Alton, E.W., Dean, D.A.: Identification of protein cofactors necessary for sequence-specific plasmid DNA nuclear import. Mol. Ther. 17, 1897–1903 (2009)CrossRefGoogle Scholar
  271. 271.
    Munkonge, F.M., Amin, V., Hyde, S.C., Green, A.M., Pringle, I.A., Gill, D.R., Smith, J.W., Hooley, R.P., Xenariou, S., Ward, M.A., Leeds, N., Leung, K.Y., Chan, M., Hillery, E., Geddes, D.M., Griesenbach, U., Postel, E.H., Dean, D.A., Dunn, M.J., Alton, E.W.: Identification and functional characterization of cytoplasmic determinants of plasmid DNA nuclear import. J. Biol. Chem. 284, 26978–26987 (2009)CrossRefGoogle Scholar
  272. 272.
    Dean, D.A.: Import of plasmid DNA into the nucleus is sequence specific. Exp. Cell Res. 230, 293–302 (1997)CrossRefGoogle Scholar
  273. 273.
    Dean, D.A., Dean, B.S., Muller, S., Smith, L.C.: Sequence requirements for plasmid nuclear entry. Exp. Cell Res. 253, 713–722 (1999)CrossRefGoogle Scholar
  274. 274.
    Vacik, J., Dean, B.S., Zimmer, W.E., Dean, D.A.: Cell-specific nuclear import of plasmid DNA. Gene Ther. 6, 1006–1014 (1999)CrossRefGoogle Scholar
  275. 275.
    Langle-Rouault, F., Patzel, V., Benavente, A., Taillez, M., Silvestre, N., Bompard, A., Sczakiel, G., Jacobs, E., Rittner, K.: Up to 100-fold increase of apparent gene expression in the presence of Epstein-Barr virus oriP sequences and EBNA1: implications of the nuclear import of plasmids. J. Virol. 72, 6181–6185 (1998)Google Scholar
  276. 276.
    Mesika, A., Grigoreva, I., Zohar, M., Reich, Z.: A regulated, NFkappaB-assisted import of plasmid DNA into mammalian cell nuclei. Mol. Ther. 3, 653–657 (2001)CrossRefGoogle Scholar
  277. 277.
    Degiulio, J.V., Kaufman, C.D., Dean, D.A.: The SP-C promoter facilitates alveolar type II epithelial cell-specific plasmid nuclear import and gene expression. Gene Ther. 17, 541–549 (2010)CrossRefGoogle Scholar
  278. 278.
    Sacramento, C.B., Moraes, J.Z., Denapolis, P.M., Han, S.W.: Gene expression promoted by the SV40 DNA targeting sequence and the hypoxia-responsive element under normoxia and hypoxia. Braz. J. Med. Biol. Res. 43, 722–727 (2010)CrossRefGoogle Scholar
  279. 279.
    Cramer, F., Christensen, C.L., Poulsen, T.T., Badding, M.A., Dean, D.A., Poulsen, H.S.: Insertion of a nuclear factor kappa B DNA nuclear-targeting sequence potentiates suicide gene therapy efficacy in lung cancer cell lines. Cancer Gene Ther. 19, 675–683 (2012)CrossRefGoogle Scholar
  280. 280.
    Wente, S.R., Rout, M.P.: The nuclear pore complex and nuclear transport. Cold Spring Harb. Perspect. Biol. 2, a000562 (2010)CrossRefGoogle Scholar
  281. 281.
    Wilson, G.L., Dean, B.S., Wang, G., Dean, D.A.: Nuclear import of plasmid DNA in digitonin-permeabilized cells requires both cytoplasmic factors and specific DNA sequences. J. Biol. Chem. 274, 22025–22032 (1999)CrossRefGoogle Scholar
  282. 282.
    Colin, M., Moritz, S., Fontanges, P., Kornprobst, M., Delouis, C., Keller, M., Miller, A.D., Capeau, J., Coutelle, C., Brahimi-Horn, M.C.: The nuclear pore complex is involved in nuclear transfer of plasmid DNA condensed with an oligolysine-RGD peptide containing nuclear localisation properties. Gene Ther. 8, 1643–1653 (2001)CrossRefGoogle Scholar
  283. 283.
    Sebestyén, M.G., Ludtke, J.L., Bassik, M.C., Zhang, G., Budker, V., Lukhtanov, E.A., Hagstrom, J.E., Wolff, J.A.: DNA vector chemistry: the covalent attachment of signal peptides to plasmid DNA. Nat. Biotechnol. 16, 80–85 (1998)CrossRefGoogle Scholar
  284. 284.
    Swindle, C.S., Zou, N., Van Tine, B.A., Shaw, G.M., Engler, J.A., Chow, L.T.: Human papillomavirus DNA replication compartments in a transient DNA replication system. J. Virol. 73, 1001–1009 (1999)Google Scholar
  285. 285.
    Tang, Q., Bell, P., Tegtmeyer, P., Maul, G.G.: Replication but not transcription of simian virus 40 DNA is dependent on nuclear domain 10. J. Virol. 74, 9694–9700 (2000)CrossRefGoogle Scholar
  286. 286.
    Ondrej, V., Kozubek, S., Lukasova, E., Falk, M., Matula, P., Matula, P., Kozubek, M.: Directional motion of foreign plasmid DNA to nuclear HP1 foci. Chromosome Res. 14, 505–514 (2006)CrossRefGoogle Scholar
  287. 287.
    Gasiorowski, J.Z., Dean, D.A.: Intranuclear trafficking of episomal DNA is transcription-dependent. Mol. Ther. 15, 2132–2139 (2007)CrossRefGoogle Scholar
  288. 288.
    Kopp, K., Gasiorowski, J.Z., Chen, D., Gilmore, R., Norton, J.T., Wang, C., Leary, D.J., Chan, E.K., Dean, D.A., Huang, S.: Pol I transcription and pre-rRNA processing are coordinated in a transcription-dependent manner in mammalian cells. Mol. Biol. Cell 18, 394–403 (2007)CrossRefGoogle Scholar
  289. 289.
    Xu, M., Cook, P.R.: Similar active genes cluster in specialized transcription factories. J. Cell Biol. 181, 615–623 (2008)CrossRefGoogle Scholar
  290. 290.
    Larkin, J.D., Papantonis, A., Cook, P.R.: Promoter type influences transcriptional topography by targeting genes to distinct nucleoplasmic sites. J. Cell Sci. 126, 2052–2059 (2013)CrossRefGoogle Scholar
  291. 291.
    Alberts, B., Johnson, A., Lewis, J., Morgan, D., Raff, M., Roberts, K., Walter, P.: Molecular Biology of the Cell, 6th edn. Garland Publishing, New York (2014)Google Scholar
  292. 292.
    Kyriakis, J.M., Avruch, J.: Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81, 807–869 (2001)Google Scholar
  293. 293.
    Morotomi-Yano, K., Akiyama, H., Yano, K.: Nanosecond pulsed electric fields activate MAPK pathways in human cells. Arch. Biochem. Biophys. 515, 99–106 (2011)CrossRefGoogle Scholar
  294. 294.
    Hardie, D.G.: AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev. 25, 1895–1908 (2011)CrossRefGoogle Scholar
  295. 295.
    Morotomi-Yano, K., Akiyama, H., Yano, K.: Nanosecond pulsed electric fields activate AMP-activated protein kinase: implications for calcium-mediated activation of cellular signaling. Biochem. Biophys. Res. Commun. 428, 371–375 (2012)CrossRefGoogle Scholar
  296. 296.
    Morotomi-Yano, K., Oyadomari, S., Akiyama, H., Yano, K.: Nanosecond pulsed electric fields act as a novel cellular stress that induces translational suppression accompanied by eIF2alpha phosphorylation and 4E-BP1 dephosphorylation. Exp. Cell Res. 318, 1733–1744 (2012)CrossRefGoogle Scholar
  297. 297.
    Wek, R.C., Jiang, H.Y., Anthony, T.G.: Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 34, 7–11 (2006)CrossRefGoogle Scholar
  298. 298.
    Mir, L.M., Glass, L.F., Sersa, G., Teissie, J., Domenge, C., Miklavčič, D., Jaroszeski, M.J., Orlowski, S., Reintgen, D.S., Rudolf, Z., et al.: Effective treatment of cutaneous and subcutaneous malignant tumours by electrochemotherapy. Br. J. Cancer 77(12), 2336–2342 (1998)CrossRefGoogle Scholar
  299. 299.
    Mir, L.M., Bureau, M.F., Gehl, J., Rangara, R., Rouy, D., Caillaud, J.-M., Delaere, P., Branellec, D., Schwartz, B., Scherman, D.: High-efficiency gene transfer into skeletal muscle mediated by electric pulses. Proc. Natl. Acad. Sci. 96(8), 4262–4267 (1999)CrossRefGoogle Scholar
  300. 300.
    Larkin, J.O., Collins, C.G., Aarons, S., Tangney, M., Whelan, M., O’Reily, S., Breathnach, O., Soden, D.M., O’Sullivan, G.C.: Electrochemotherapy: aspects of preclinical development and early clinical experience. Ann. Surg. 245(3), 469 (2007)CrossRefGoogle Scholar
  301. 301.
    Davalos, R.V., Mir, L.M., Rubinsky, B.: Tissue ablation with irreversible electroporation. Ann. Biomed. Eng. 33(2), 223–231 (2005)CrossRefGoogle Scholar
  302. 302.
    Edd, J.F., Horowitz, L., Davalos, R.V., Mir, L.M., Rubinsky, B.: In vivo results of a new focal tissue ablation technique: irreversible electroporation. IEEE Trans. Biomed. Eng. 53(7), 1409–1415 (2006)CrossRefGoogle Scholar
  303. 303.
    Al-Sakere, B., Andre, F., Bernat, C., Connault, E., Opolon, P., Davalos, R.V., Rubinsky, B., Mir, L.M.: Tumor ablation with irreversible electroporation. PLoS One 2(11), e1135 (2007)CrossRefGoogle Scholar
  304. 304.
    Pucihar, G., Krmelj, J., Rebersek, M., Napotnik, T.B., Miklavčič, D.: Equivalent pulse parameters for electroporation. IEEE Trans. Biomed. Eng. 58(11), 3279–3288 (2011). doi: 3210.1109/TBME.2011.2167232. Epub 2162011 Sep 2167236CrossRefGoogle Scholar
  305. 305.
    Rubinsky, J., Onik, G., Mikus, P., Rubinsky, B.: Optimal parameters for the destruction of prostate cancer using irreversible electroporation. J. Urol. 180(6), 2668–2674 (2008). Epub 2008 Oct 2631CrossRefGoogle Scholar
  306. 306.
    Jiang, C., Shao, Q., Bischof, J.: Pulse timing during irreversible electroporation achieves enhanced destruction in a hindlimb model of cancer. Ann. Biomed. Eng. 1, 1 (2014)Google Scholar
  307. 307.
    Appelbaum, L., Ben-David, E., Faroja, M., Nissenbaum, Y., Sosna, J., Goldberg, S.N.: Irreversible electroporation ablation: creation of large-volume ablation zones in in vivo porcine liver with four-electrode arrays. Radiology 270(2), 416–424 (2014)CrossRefGoogle Scholar
  308. 308.
    Diller, K.R.: Modeling of bioheat transfer processes at high and low temperatures. Adv. Heat Transf. 22, 157–357 (1992)CrossRefGoogle Scholar
  309. 309.
    Davalos, R.V., Rubinsky, B.: Temperature considerations during irreversible electroporation. Int. J. Heat Mass Transf. 51(23), 5617–5622 (2008)zbMATHCrossRefGoogle Scholar
  310. 310.
    Thomsen, S., Pearce. J.A.: Thermal damage and rate processes in biologic tissues. In: Optical-Thermal Response of Laser-Irradiated Tissue, pp. 487–549. Springer, Dordrecht (2011)Google Scholar
  311. 311.
    Davalos, R.V., Rubinsky, B., Mir, L.M.: Theoretical analysis of the thermal effects during in vivo tissue electroporation. Bioelectrochemistry 61(1–2), 99–107 (2003)CrossRefGoogle Scholar
  312. 312.
    Neal II, R.E., Davalos, R.V.: The feasibility of irreversible electroporation for the treatment of breast cancer and other heterogeneous systems. Ann. Biomed. Eng. 37(12), 2615–2625 (2009)CrossRefGoogle Scholar
  313. 313.
    Županič, A., Miklavčič, D.: Tissue heating during tumor ablation with irreversible electroporation. Electrotechnol. Rev. 78, 42–47 (2011)Google Scholar
  314. 314.
    Garcia, P.A., Rossmeisl, J.H., Neal, R.E., Ellis, T.L., Davalos, R.V.: A parametric study delineating irreversible electroporation from thermal damage based on a minimally invasive intracranial procedure. Biomed. Eng. Online 10(1), 34 (2011)CrossRefGoogle Scholar
  315. 315.
    Shafiee, H., Garcia, P.A., Davalos, R.V.: A preliminary study to delineate irreversible electroporation from thermal damage using the arrhenius equation. J. Biomech. Eng. 131(7), 074509 (2009)CrossRefGoogle Scholar
  316. 316.
    Garcia, P.A., Davalos, R.V., Miklavčič, D.: A numerical investigation of the electric and thermal cell kill distributions in electroporation-based therapies in tissue. PLoS One 9(8), e103083 (2014)CrossRefGoogle Scholar
  317. 317.
    Qin, Z., Jiang, J., Long, G., Lindgren, B., Bischof, J.C.: Irreversible electroporation: an in vivo study with dorsal skin fold chamber. Ann. Biomed. Eng. 41(3), 619–629 (2013)CrossRefGoogle Scholar
  318. 318.
    Garcia, P., Rossmeisl, J., Neal, R., Ellis, T., Olson, J., Henao-Guerrero, N., Robertson, J., Davalos, R.: Intracranial nonthermal irreversible electroporation: in vivo analysis. J. Membr. Biol. 236(1), 127–136 (2010)CrossRefGoogle Scholar
  319. 319.
    Long, G., Bakos, G., Shires, P.K., Gritter, L., Crissman, J.W., Harris, J.L., Clymer, J.W.: Histological and finite element analysis of cell death due to irreversible electroporation. Technol. Cancer Res. Treat. 13(6), 561–569 (2014)Google Scholar
  320. 320.
    Neal 2nd, R.E., Rossmeisl Jr., J.H., Garcia, P.A., Lanz, O.I., Henao-Guerrero, N., Davalos, R.V.: Successful treatment of a large soft tissue sarcoma with irreversible electroporation. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 29(13), e372–e377 (2011)CrossRefGoogle Scholar
  321. 321.
    Bower, M., Sherwood, L., Li, Y., Martin, R.: Irreversible electroporation of the pancreas: definitive local therapy without systemic effects. J. Surg. Oncol. 104(1), 22–28 (2011)CrossRefGoogle Scholar
  322. 322.
    Neal 2nd, R.E., Millar, J.L., Kavnoudias, H., Royce, P., Rosenfeldt, F., Pham, A., Smith, R., Davalos, R.V., Thomson, K.R.: In vivo characterization and numerical simulation of prostate properties for non-thermal irreversible electroporation ablation. Prostate 74(5), 458–468 (2014)CrossRefGoogle Scholar
  323. 323.
    Edd, J.F., Davalos, R.V.: Mathematical modeling of irreversible electroporation for treatment planning. Technol. Cancer Res. Treat. 6(4), 275–286 (2007)CrossRefGoogle Scholar
  324. 324.
    Ben-David, E., Ahmed, M., Faroja, M., Moussa, M., Wandel, A., Sosna, J., Appelbaum, L., Nissenbaum, I., Goldberg, S.N.: Irreversible electroporation: treatment effect is susceptible to local environment and tissue properties. Radiology 11, 11 (2013)Google Scholar
  325. 325.
    Neal II, R.E., Singh, R., Hatcher, H.C., Kock, N.D., Torti, S.V., Davalos, R.V.: Treatment of breast cancer through the application of irreversible electroporation using a novel minimally invasive single needle electrode. Breast Cancer Res. Treat. 123(1), 295–301 (2010)CrossRefGoogle Scholar
  326. 326.
    Corovic, S., Zupanic, A., Kranjc, S., Al Sakere, B., Leroy-Willig, A., Mir, L.M., Miklavčič, D.: The influence of skeletal muscle anisotropy on electroporation: in vivo study and numerical modeling. Med. Biol. Eng. Comput. 48(7), 637–648 (2010)CrossRefGoogle Scholar
  327. 327.
    Neal II, R., Smith, R., Kavnoudias, H., Rosenfeldt, F., Ou, R., Mclean, C., Davalos, R., Thomson, K.: The effects of metallic implants on electroporation therapies: feasibility of irreversible electroporation for brachytherapy salvage. Cardiovasc. Interv. Radiol. 36(6), 1638–1645 (2013)CrossRefGoogle Scholar
  328. 328.
    Duck, F.A.: Physical Properties of Tissue: A Comprehensive Reference Book. Academic, New York (1990)Google Scholar
  329. 329.
    Neal II, R.E., Garcia, P.A., Robertson, J.L., Davalos, R.V.: Experimental characterization and numerical modeling of tissue electrical conductivity during pulsed electric fields for irreversible electroporation treatment planning. IEEE Trans. Biomed. Eng. 59(4), 1076–1085 (2012). Epub 2012 Jan 1076CrossRefGoogle Scholar
  330. 330.
    Osswald, K.: Messung der Leitfähigkeit und Dielektrizitätskonstante biologischer Gewebe und Flüssigkeiten bei kurzen Wellen. Akad. Verlagsges. (1937)Google Scholar
  331. 331.
    Mcrae, D.A., Esrick, M.A.: The dielectric parameters of excised EMT-6 tumours and their change during hyperthermia. Phys. Med. Biol. 37(11), 2045 (1992)CrossRefGoogle Scholar
  332. 332.
    Sel, D., Cukjati, D., Batiuskaite, D., Slivnik, T., Mir, L.M., Miklavčič, D.: Sequential finite element model of tissue electropermeabilization. IEEE Trans. Biomed. Eng. 52(5), 816–827 (2005)CrossRefGoogle Scholar
  333. 333.
    Ivorra, A., Rubinsky, B.: In vivo electrical impedance measurements during and after electroporation of rat liver. Bioelectrochemistry 70(2), 287–295 (2007)CrossRefGoogle Scholar
  334. 334.
    Pavšelj, N., Miklavčič, D.: Numerical modeling in electroporation-based biomedical applications. Radiol. Oncol. 42(3), 159–168 (2008)CrossRefGoogle Scholar
  335. 335.
    Ivorra, A., Mir, L.M., Rubinsky, B.: Electric field redistribution due to conductivity Changes during tissue electroporation: experiments with a simple vegetal model. In: IFMBE Proceedings, vol. 25/13, edn, pp. 59–62. Springer, Berlin/Heidelberg (2009)Google Scholar
  336. 336.
    Corovic, S., Lackovic, I., Sustaric, P., Sustar, T., Rodic, T., Miklavčič, D.: Modeling of electric field distribution in tissues during electroporation. Biomed. Eng. Online 12(1), 16 (2013)CrossRefGoogle Scholar
  337. 337.
    Neal, R.E., Garcia, P.A., Kavnoudias, H., Rosenfeldt, F., Mclean, C.A., Earl, V., Bergman, J., Davalos, R.V., Thomson, K.R.: In vivo irreversible electroporation kidney ablation: experimentally correlated numerical models. IEEE Trans. Biomed. Eng. 62(2), 561–569 (2015). doi: 510.1109/TBME.2014.2360374. Epub 2362014 Sep 2360325CrossRefGoogle Scholar
  338. 338.
    Gaylor, D.C., Prakah-Asante, K., Lee, R.C.: Significance of cell size and tissue structure in electrical trauma. J. Theor. Biol. 133(2), 223–237 (1988)CrossRefGoogle Scholar
  339. 339.
    Neal II, R.E., Rossmeisl Jr., J.H., Garcia, P.A., Lanz, O.I., Henao-Guerrero, N., Davalos, R.V.: Successful treatment of a large soft tissue sarcoma with irreversible electroporation. J. Clin. Oncol. 29(13), e372–e377 (2011)CrossRefGoogle Scholar
  340. 340.
    Wimmer, T., Srimathveeravalli, G., Gutta, N., Ezell, P.C., Monette, S., Maybody, M., Erinjery, J.P., Durack, J.C., Coleman, J.A., Solomon, S.B.: Planning irreversible electroporation in the porcine kidney: are numerical simulations reliable for predicting empiric ablation outcomes? Cardiovasc. Intervent. Radiol. 38(1), 182–190 (2015)CrossRefGoogle Scholar
  341. 341.
    Miklavčič, D., Semrov, D., Mekid, H., Mir, L.M.: A validated model of in vivo electric field distribution in tissues for electrochemotherapy and for DNA electrotransfer for gene therapy. Biochim. Biophys. Acta 1523(1), 73–83 (2000)CrossRefGoogle Scholar
  342. 342.
    Wimmer, T., Srimathveeravalli, G., Gutta, N., Ezell, P.C., Monette, S., Kingham, T.P., Maybody, M., Durack, J.C., Fong, Y., Solomon, S.B.: Comparison of simulation-based treatment planning with imaging and pathology outcomes for percutaneous CT-guided irreversible electroporation of the porcine pancreas: a pilot study. J. Vasc. Interv. Radiol. 24(11), 1709–1718 (2013)CrossRefGoogle Scholar
  343. 343.
    Majno, G., Joris, I.: Apoptosis, oncosis, and necrosis: an overview of cell death. Am. J. Pathol. 146, 3–15 (1995)Google Scholar
  344. 344.
    Galluzzi, L., Bravo-San Pedro, J.M., Vitale, I., Aaronson, S.A., Abrams, J.M., Adam, D., et al. (2014a) Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ. 2014 Sept 19. doi:  10.1038/cdd.2014.137
  345. 345.
    Galluzzi, L., Kepp, O., Krautwald, S., Kroemer, G., Linkermann, A.: Molecular mechanisms of regulated necrosis. Semin. Cell Dev. Biol. 35, 24–32 (2014)CrossRefGoogle Scholar
  346. 346.
    Kerr, J.F., Wyllie, A.H., Currie, A.R.: Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239–257 (1972)CrossRefGoogle Scholar
  347. 347.
    Degterev, A., Yuan, J.: Expansion and evolution of cell death programmes. Nat. Rev. Mol. Cell Biol. 9, 378–390 (2008)CrossRefGoogle Scholar
  348. 348.
    Arvanitis, M., Li, D.D., Lee, K., Mylonakis, E.: Apoptosis in C. elegans: lessons for cancer and immunity. Front Cell Infect. Microbiol. 3, 67 (2013)CrossRefGoogle Scholar
  349. 349.
    Galluzzi, L., Vitale, I., Abrams, J.M., Alnemri, E.S., Baehrecke, E.H., Blagosklonny, M.V., et al.: Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 19, 107–120 (2012)CrossRefGoogle Scholar
  350. 350.
    Yan, Q., Liu, J.P., Li, D.W.: Apoptosis in lens development and pathology. Differentiation 74, 195–211 (2006)CrossRefGoogle Scholar
  351. 351.
    Taylor, E.L., Rossi, A.G., Dransfield, I., Hart, S.P.: Analysis of neutrophil apoptosis. Methods Mol. Biol. 412, 177–200 (2007)CrossRefGoogle Scholar
  352. 352.
    Kroemer, G., El-Deiry, W.S., Golstein, P., Peter, M.E., Vaux, D., Vandenabeele, P., et al.: Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ. 2, 1463–1467 (2005)CrossRefGoogle Scholar
  353. 353.
    Kroemer, G., Galluzzi, L., Vandenabeele, P., Abrams, J., Alnemri, E.S., Baehrecke, E.H., et al.: Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 16, 3–11 (2009)CrossRefGoogle Scholar
  354. 354.
    Galluzzi, L., Maiuri, M.C., Vitale, I., Zischka, H., Castedo, M., Zitvogel, L., Kroemer, G.: Cell death modalities: classification and pathophysiological implications. Cell Death Differ. 14, 1237–1243 (2007)CrossRefGoogle Scholar
  355. 355.
    Fulda, S., Gorman, A.M., Hori, O., Samali, A.: Cellular stress responses: cell survival and cell death. Int. J. Cell Biol. 2010, 214074 (2010)Google Scholar
  356. 356.
    Clarke, P.G.: Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. (Berl.) 181, 195–213 (1990)CrossRefGoogle Scholar
  357. 357.
    Kroemer, G., Mariño, G., Levine, B.: Autophagy and the integrated stress response. Mol. Cell 40, 280–293 (2010)CrossRefGoogle Scholar
  358. 358.
    Eisenberg-Lerner, A., Bialik, S., Simon, H.U., Kimchi, A.: Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ. 16, 966–975 (2009)CrossRefGoogle Scholar
  359. 359.
    Ellis, H.M., Horvitz, H.R.: Genetic control of programmed cell death in the nematode C. elegans. Cell 44, 817–829 (1986)CrossRefGoogle Scholar
  360. 360.
    Scaffidi, C., Fulda, S., Srinivasan, A., Friesen, C., Li, F., Tomaselli, K.J., Debatin, K.M., Krammer, P.H., Peter, M.E.: Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17, 1675–1687 (1998)CrossRefGoogle Scholar
  361. 361.
    Muppidi, J.R., Siegel, R.M.: Ligand-independent redistribution of Fas (CD95) into lipid rafts mediates clonotypic T cell death. Nat. Immunol. 5, 182–189 (2004)CrossRefGoogle Scholar
  362. 362.
    Hengartner, M.O.: The biochemistry of apoptosis. Nature 407, 770–776 (2000)CrossRefGoogle Scholar
  363. 363.
    Jost, P.J., Grabow, S., Gray, D., McKenzie, M.D., Nachbur, U., Huang, D.C., Bouillet, P., Thomas, H.E., Borner, C., Silke, J., Strasser, A., Kaufmann, T.: XIAP discriminates between type I and type II FAS-induced apoptosis. Nature 460, 1035–1039 (2009)CrossRefGoogle Scholar
  364. 364.
    Willis, S.N., Adams, J.M.: Life in the balance: how BH3-only proteins induce apoptosis. Curr. Opin. Cell Biol. 17, 617–625 (2005)CrossRefGoogle Scholar
  365. 365.
    Shamas-Din, A., Brahmbhatt, H., Leber, B., Andrews, D.W.: BH3-only proteins: orchestrators of apoptosis. Biochim. Biophys. Acta 1813, 508–520 (2011)CrossRefGoogle Scholar
  366. 366.
    Tourneur, L., Chiocchia, G.: FADD: a regulator of life and death. Trends Immunol. 31, 260–269 (2010)CrossRefGoogle Scholar
  367. 367.
    Festjens, N., Vanden Berghe, T., Vandenabeele, P.: Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim. Biophys. Acta 1757, 1371–1387 (2006)CrossRefGoogle Scholar
  368. 368.
    Sosna, J., Voigt, S., Mathieu, S., Lange, A., Thon, L., Davarnia, P., Herdegen, T., Linkermann, A., Rittger, A., Chan, F.K., Kabelitz, D., Schütze, S., Adam, D.: TNF-induced necroptosis and PARP-1-mediated necrosis represent distinct routes to programmed necrotic cell death. Cell. Mol. Life Sci. 71, 331–348 (2014)CrossRefGoogle Scholar
  369. 369.
    Vandenabeele, P., Galluzzi, L., Vanden Berghe, T., Kroemer, G.: Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 11, 700–714 (2010)CrossRefGoogle Scholar
  370. 370.
    Schoenbach, K.H., Joshi, R.P., Stark, R.H., Dobbs, F., Beebe, S.J.: Bacterial decontamination of liquids with pulsed electric fields. IEEE Trans. Dielectr. Electr. Insul. 7, 637–645 (2000)CrossRefGoogle Scholar
  371. 371.
    Beebe, S.J., White, J.A., Blackmore, P.F., Deng, Y., Somers, K., Schoenbach, K.H.: Diverse effects of nanosecond pulsed electric fields on cells and tissues. DNA Cell Biol. 22, 785–796 (2003)CrossRefGoogle Scholar
  372. 372.
    Vernier, P.T., Aimin, L., Marcu, L., Craft, C.M., Gundersen, M.A.: 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. 10, 795–809 (2003)CrossRefGoogle Scholar
  373. 373.
    Hall, E.H., Schoenbach, K.H., Beebe, S.J.: Nanosecond pulsed electric fields induce apoptosis in p53-wildtype and p53-null HCT116 colon carcinoma cells. Apoptosis 12, 1721–1731 (2007)CrossRefGoogle Scholar
  374. 374.
    Ford, W.E., Ren, W., Blackmore, P.F., Schoenbach, K.H., Beebe, S.J.: Nanosecond pulsed electric fields stimulate apoptosis without release of pro-apoptotic factors from mitochondria in B16f10 melanoma. Arch. Biochem. Biophys. 497, 82–89 (2010)CrossRefGoogle Scholar
  375. 375.
    Ren, W., Beebe, S.J.: An apoptosis targeted stimulus with nanosecond pulsed electric fields (nsPEFs) in E4 squamous cell carcinoma. Apoptosis 16, 382–393 (2011)CrossRefGoogle Scholar
  376. 376.
    Chen, X., Yin, S., Hu, C., Chen, X., Jiang, K., Ye, S., Feng, X., Fan, S., Xie, H., Zhou, L., Zheng, S.: Comparative study of nanosecond electric fields in vitro and in vivo on hepatocellular carcinoma indicate macrophage infiltration contribute to tumor ablation in vivo. PLoS One 9, e86421 (2014)CrossRefGoogle Scholar
  377. 377.
    Fadeel, B., Xue, D.: The ins and outs of phospholipid asymmetry in the plasma membrane: roles in health and disease. Crit. Rev. Biochem. Mol. Biol. 44, 264–277 (2009)CrossRefGoogle Scholar
  378. 378.
    Segawa, K., Kurata, S., Yanagihashi, Y., Brummelkamp, T.R., Matsuda, F., Nagata, S.: Caspase-mediated cleavage of phospholipid flippase for apoptotic phosphatidylserine exposure. Science 344, 1164–1168 (2014)CrossRefGoogle Scholar
  379. 379.
    Suzuki, J., Denning, D.P., Imanishi, E., Horvitz, H.R., Nagata, S.: Xk-related protein 8 and CED-8 promote phosphatidylserine exposure in apoptotic cells. Science 341, 403–406 (2013)CrossRefGoogle Scholar
  380. 380.
    Vernier, P.T., Ziegler, M.J., Sun, Y., Gundersen, M.A., Tieleman, D.P.: Nanopore-facilitated, voltage-driven phosphatidylserine translocation in lipid bilayers—in cells and in silico. Phys. Biol. 3, 233–2147 (2006)CrossRefGoogle Scholar
  381. 381.
    Tekle, E., Wolfe, M.D., Oubrahim, H., Chock, P.B.: Phagocytic clearance of electric field induced ‘apoptosis-mimetic’ cells. Biochem. Biophys. Res. Commun. 376, 256–260 (2008)CrossRefGoogle Scholar
  382. 382.
    Wang, Y., Dawson, V.L., Dawson, T.M.: Poly(ADP-ribose) signals to mitochondrial AIF: a key event in parthanatos. Exp. Neurol. 218, 193–202 (2009)CrossRefGoogle Scholar
  383. 383.
    Charriaut-Marlangue, C., Ben-Ari, Y.: A cautionary note on the use of the TUNEL stain to determine apoptosis. Neuroreport 7, 61–64 (1995)CrossRefGoogle Scholar
  384. 384.
    de Torres, C., Munell, F., Ferrer, I., Reventós, J., Macaya, A.: Identification of necrotic cell death by the TUNEL assay in the hypoxic-ischemic neonatal rat brain. Neurosci. Lett. 230, 1–4 (1997)CrossRefGoogle Scholar
  385. 385.
    Kanoh, M., Takemura, G., Misao, J., Hayakawa, Y., Aoyama, T., Nishigaki, K., Noda, T., Fujiwara, T., Fukuda, K., Minatoguchi, S., Fujiwara, H.: Significance of myocytes with positive DNA in situ nick end-labeling (TUNEL) in hearts with dilated cardiomyopathy: not apoptosis but DNA repair. Circulation 99, 2757–2764 (1999)CrossRefGoogle Scholar
  386. 386.
    Grasl-Kraupp, B., Ruttkay-Nedecky, B., Koudelka, H., Bukowska, K., Bursch, W., Schulte-Hermann, R.: In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatology 21, 1465–1468 (1995)Google Scholar
  387. 387.
    Smith, M.A., Schnellmann, R.G.: Calpains, mitochondria, and apoptosis. Cardiovasc. Res. 96, 32–37 (2012)CrossRefGoogle Scholar
  388. 388.
    Song, J., Joshi, R.P., Beebe, S.J.: Cellular apoptosis by nanosecond, high-intensity electric pulses: model evaluation of the pulsing threshold and extrinsic pathway. Bioelectrochemistry 79, 179–186 (2010)CrossRefGoogle Scholar
  389. 389.
    Estlack, L.E., Roth, C.C., Thompson 3rd, G.L., Lambert 3rd, W.A., Ibey, B.L.: Nanosecond pulsed electric fields modulate the expression of Fas/CD95 death receptor pathway regulators in U937 and Jurkat Cells. Apoptosis 19, 1755–1768 (2014)CrossRefGoogle Scholar
  390. 390.
    Beebe, S.J., Sain, N.M., Ren, W.: Induction of cell death mechanisms and apoptosis by nanosecond pulsed electric fields (nsPEFs). Cells 2, 136–162 (2013)CrossRefGoogle Scholar
  391. 391.
    Morotomi-Yano, K., Akiyama, H., Yano, K.: Different involvement of extracellular calcium in two modes of cell death induced by nanosecond pulsed electric fields. Arch. Biochem. Biophys. 555–556, 47–54 (2014)CrossRefGoogle Scholar
  392. 392.
    Ibey, B.L., Ullery, J.C., Pakhomova, O.N., Roth, C.C., Semenov, I., Beier, H.T., Tarango, M., Xiao, S., Schoenbach, K.H., Pakhomov, A.G.: Bipolar nanosecond electric pulses are less efficient at electropermeabilization and killing cells than monopolar pulses. Biochem. Biophys. Res. Commun. 443, 568–573 (2014)CrossRefGoogle Scholar
  393. 393.
    Kotnik, T., Mir, L.M., Flisar, K., Puc, M., Miklavčič, D.: Cell membrane electropermeabilization by symmetrical bipolar rectangular pulses. Part I. Increased efficiency of permeabilization. Bioelectrochemistry 54, 83–90 (2001)CrossRefGoogle Scholar
  394. 394.
    Tekle, E., Astumian, R.D., Chock, P.B.: Electroporation by using bipolar oscillating electric field: an improved method for DNA transfection of NIH 3T3 cells. Proc. Natl. Acad. Sci. U. S. A. 88, 4230–4234 (1991)CrossRefGoogle Scholar
  395. 395.
    Jacobson, J., Duchen, M.R.: Mitochondrial oxidative stress and cell death in astrocytes—requirement for stored Ca2+ and sustained opening of the permeability transition pore. J. Cell Sci. 115, 1175–1188 (2002)Google Scholar
  396. 396.
    Brookes, P.S., Yoon, Y., Robotham, J.L., Anders, M.W., Sheu, S.S.: Ca2+, ATP, and ROS: a mitochondrial love-hate triangle. Am. J. Physiol. Cell Physiol. 287, C817–C833 (2004)CrossRefGoogle Scholar
  397. 397.
    Pakhomova, O.N., Khorokhorina, V.A., Bowman, A.M., Rodaitė-Riševičienė, R., Saulis, G., Xiao, S., Pakhomov, A.G.: Oxidative effects of nanosecond pulsed electric field exposure in cells and cell-free media. Arch. Biochem. Biophys. 527, 55–64 (2012)CrossRefGoogle Scholar
  398. 398.
    Sato, T., Machida, T., Takahashi, S., Iyama, S., Sato, Y., Kuribayashi, K., Takada, K., Oku, T., Kawano, Y., Okamoto, T., Takimoto, R., Matsunaga, T., Takayama, T., Takahashi, M., Kato, J., Niitsu, Y.: Fas-mediated apoptosome formation is dependent on reactive oxygen species derived from mitochondrial permeability transition in Jurkat cells. J. Immunol. 173, 285–296 (2004)CrossRefGoogle Scholar
  399. 399.
    Stacey, M., Stickley, J., Fox, P., Statler, V., Schoenbach, K., Beebe, S.J., Buescher, S.: 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 (2003)CrossRefGoogle Scholar
  400. 400.
    Romeo, S., Zeni, L., Sarti, M., Sannino, A., Scarfı’, M.R., et al.: DNA electrophoretic migration patterns change after exposure of jurkat cells to a single intense nanosecond electric pulse. PLoS One 6, e28419 (2011)CrossRefGoogle Scholar
  401. 401.
    Nuccitelli, R., Pliquett, U., Chen, X., Ford, W., James Swanson, R., Beebe, S.J., Kolb, J.F., Schoenbach, K.H.: Nanosecond pulsed electric fields cause melanomas to self-destruct. Biochem. Biophys. Res. Commun. 343, 351–360 (2006)CrossRefGoogle Scholar
  402. 402.
    Nuccitelli, R., Chen, X., Pakhomov, A.G., Baldwin, W.H., Sheikh, S., Pomicter, J.L., Ren, W., Osgood, C., Swanson, R.J., Kolb, J.F., Beebe, S.J., Schoenbach, K.H.: 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 (2009)CrossRefGoogle Scholar
  403. 403.
    Chen, X., Zhuang, J., Kolb, J.F., Schoenbach, K.H., Beebe, S.J.: Long term survival of mice with hepatocellular carcinoma after pulse power ablation with nanosecond pulsed electric fields. Technol. Cancer Res. Treat. 11, 83–93 (2012)Google Scholar
  404. 404.
    Chen, R., Sain, N.M., Harlow, K.T., Chen, Y.J., Shires, P.K., Heller, R., Beebe, S.J.: A protective effect after clearance of orthotopic rat hepatocellular carcinoma by nanosecond pulsed electric fields. Eur. J. Cancer 50, 2705–2713 (2014)CrossRefGoogle Scholar
  405. 405.
    Nuccitelli, R., Tran, K., Lui, K., Huynh, J., Athos, B., Kreis, M., Nuccitelli, P., De Fabo, E.C.: Pigment Cell Melanoma Res. 25, 618–629 (2012)CrossRefGoogle Scholar
  406. 406.
    Nuccitelli, R., Wood, R., Kreis, M., Athos, B., Huynh, J., Lui, K., Nuccitelli, P., Epstein Jr., E.H.: First-in-human trial of nanoelectroablation therapy for basal cell carcinoma: proof of method. Exp. Dermatol. 23, 135–137 (2014)CrossRefGoogle Scholar

Copyright information

© Springer Japan 2017

Authors and Affiliations

  • Ken-ichi Yano
    • 1
    Email author
  • Lea Rems
    • 2
  • Tadej Kotnik
    • 2
  • Damijan Miklavčič
    • 2
  • James C. Weaver
    • 3
  • Kyle C. Smith
    • 3
  • Reuben S. Son
    • 3
  • Thiruvallur R. Gowrishankar
    • 3
  • P. Thomas Vernier
    • 4
  • Zachary A. Levine
    • 5
  • Marie-Pierre Rols
    • 6
  • Justin Teissie
    • 6
  • Lluis M. Mir
    • 7
  • Andrei G. Pakhomov
    • 4
  • Peter Nick
    • 8
  • Wolfgang Frey
    • 9
  • David A. Dean
    • 10
  • Keiko Morotomi-Yano
    • 11
  • Robert E. NealII
    • 12
  • Suyashree Bhonsle
    • 13
  • Rafael V. Davalos
    • 13
  • Stephen J. Beebe
    • 4
  1. 1.Kumamoto UniversityKumamotoJapan
  2. 2.Faculty of Electrical EngineeringUniversity of LjubljanaLjubljanaSlovenia
  3. 3.Harvard-MIT Division of Health Sciences and TechnologyMassachusetts Institute of TechnologyCambridgeUSA
  4. 4.Frank Reidy Research Center for BioelectricsOld Dominion UniversityNorfolkUSA
  5. 5.Department of PhysicsUniversity of California Santa BarbaraSanta BarbaraUSA
  6. 6.Institute of Pharmacology and Structural BiologyCNRS and University of ToulouseToulouseFrance
  7. 7.Vectorology and Antitumor TherapiesUMR 8203, CNRS, Univ. Paris-Sud, Université Paris-Saclay, Gustave RoussyVillejuifFrance
  8. 8.Botanical InstituteKarlsruhe Institute of TechnologyKarlsruheGermany
  9. 9.Institute for Pulsed Power and Microwave TechnologyKarlsruhe Institute of TechnologyEggenstein-LeopoldshafenGermany
  10. 10.Department of PediatricsUniversity of RochesterRochesterUSA
  11. 11.Institute of Pulsed Power ScienceKumamoto UniversityKumamotoJapan
  12. 12.AngioDynamics Inc.QueensburyUSA
  13. 13.Biomedical EngineeringVirginia TechBlacksburgUSA

Personalised recommendations