A stochastic model for DNA translocation through an electropore

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 11, 2012, Pages 2494-2501

  Yu, Miao ^a   Tan, Wenchang ^b   Lin, Hao ^a  

^a RUTGERS UNIVERSITY   (United States)

^b PEKING UNIVERSITY   (China)

Author keywords

Diffusion; DNA electrotransfer; Electrophoresis; Electroporation; Fokker Planck equation; Translocation

Indexed keywords

DNA;

DIFFUSION; DNA TRANSFER; ELECTROPHORESIS; ELECTROPORATION; GENE TRANSLOCATION; MATHEMATICAL COMPUTING; MEMBRANE POTENTIAL; PHYSICAL PHENOMENA; PRIORITY JOURNAL; PROBABILITY; QUANTITATIVE ANALYSIS; REACTION TIME; REVIEW; SIMULATION; STOCHASTIC MODEL; VALIDATION PROCESS;

EID: 84864074138     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.05.025     Document Type: Article

References (73)

1. E. Neumann, M. Schaefer-Ridder, Y. Wang, and P. Hofschneider Gene transfer into mouse lyoma cells by electroporation in high electric fields EMBO J. 1 1982 841 845
2. E. Neumann, A.E. Sowers, C. Jordan, Electroporation and Electrofusion in Cell Biology 1989 Plenum Press
3. L. Mir, S. Orlowski, J. B. Jr., J. Teissi, M. Rols, G. Sersa, D. Miklavcic, R. Gilbert, and R. Heller Biomedical applications of electric pulses with special emphasis on antitumor electrochemotherapy Bioelectrochem. Bioenerg. 38 1995 203 207
4. L. Mir Therapeutic perspectives of in vivo cell electropermeabilization Bioelectrochemistry 53 2000 1 10
5. H. Tien, and A. Ottova The bilayer lipid membrane (BLM) under electrical fields IEEE Trans. Dielectr. Electr. Insul. 10 2003 717 727
6. F. Andre, and L. Mir DNA electrotransfer: its principles and an updated review of its therapeutic applications Gene Ther. 11 2004 S33 S42
7. K. Schoenbach, R. Joshi, J. Kolb, N. Chen, M. Stacey, P. Blackmore, E. Buescher, and S. Beebe Ultrashort electrical pulses open a new gateway into biological cells Proc. IEEE 92 2004 1122 1136 (Pubitemid 40890710)
8. A.V. Driessche, P. Ponsaerts, D.V. Bockstaele, V.V. Tendeloo, and Z. Bernema Messenger RNA electroporation: an efficient tool in immunotherapy and stem cell research Folia Histochem. Cytobiol. 43 2005 213 216 (Pubitemid 41582141)
9. C. Chen, S. Smye, M. Robinson, and J. Evans Membrane electroporation theories: a review Med. Biol. Eng. Comput. 44 2006 5 14 (Pubitemid 43949722)
10. B. Rubinsky Irreversible electroporation in medicine Technol. Cancer Res. Treat. 6 2007 255 259 (Pubitemid 47340117)
11. D. Gross, L. Loew, and W. Webb Optical imaging of cell membrane potential changes induced by applied electric fields Biophys. J. 50 1986 339 348
12. J.K. Kinosita, I. Ashikawa, N. Saita, H. Yoshimura, H. Itoh, K. Nagayama, and A. Ikegami Electroporation of cell membrane visualized under a pulsed-laser fluorescence microscope Biophys. J. 53 1988 1015 1019
13. M. Hibino, M. Shigemori, H. Itoh, K. Nagayama, and J.K. Kinosita Membrane conductance of an electroporated cell analyzed by submicrosecond imaging of transmembrane potential Biophys. J. 59 1991 209 220
14. K.R. Foster, and H.P. Schwan Dielectric Properties of Tissues CRC Press 1996 27 106
15. T. Kotnik, G. Pucihar, M. Rebersek, D. Miklavcic, and L. Mir Role of pulse shape in cell membrane electropermeabilization Biochim. Biophys. Acta 1614 2003 193 200 (Pubitemid 36929983)
16. W. Frey, J. White, R. Price, P. Blackmore, R. Joshi, R. Nuccitelli, S. Beebe, K. Schoenbach, and J. Kolby Plasma membrane voltage changes during nanosecond pulsed electric field exposure Biophys. J. 90 2006 3608 3615
17. T. Kotnik, and D. Miklavcic Theoretical evaluation of voltage inducement on internal membranes of biological cells exposed to electric fields Biophys. J. 90 2006 480 491
18. B. Flickinger, T. Berghöfer, P. Hohenberger, C. Eing, and W. Frey Transmembrane potential measurements on plant cells using the voltage-sensitive dye annine-6 Protoplasma 247 2010 3 12
19. D.C. Chang, and T.S. Reese Changes in membrane structure induced by electroporation as revealed by rapid-freezing electron microscopy Biophys. J. 58 1990 1 12 (Pubitemid 20237931)
20. A. Barnett The current-voltage relation of an aqueous pore in a lipid bilayer membrane Biochim. Biophys. Acta 1025 1990 10 14 (Pubitemid 20183614)
21. A. Barnett, and J.C. Weaver Electroporation: a unified, quantitative theory of reversible electrical breakdown and mechanical rupture in artificial planar bilayer membranes Bioelectrochem. Bioenerg. 25 1991 163 182
22. J. Neu, and W. Krassowska Asymptotic model of electroporation Phys. Rev. E 59 1999 3471 3482 (Pubitemid 129306005)
23. H. Leontiadou, A. Mark, and S. Marrink Molecular dynamics simulations of hydrophilic pores in lipid bilayers Biophys. J. 86 2004 2156 2164 (Pubitemid 38524406)
24. Z. Vasilkoski, A. Esser, T. Gowrishankar, and J. Weaver Membrane electroporation: the absolute rate equation and nanosecond time scale pore creation Phys. Rev. E 74 2006 021904
25. Z. Levine, and P. Vernier Life cycle of an electropore: field-dependent and field-independent steps in pore creation and annihilation J. Membr. Biol. 236 2010 27 36
26. J. Li, and H. Lin The current-voltage relation for electropores with conductivity gradients Biomicrofluidics 4 2010 013206
27. C. Wilhelm, M. Winterhalter, U. Zimmermann, and R. Benz Kinetics of pore size during irreversible electrical breakdown of lipid bilayer membranes Biophys. J. 64 1993 121 128 (Pubitemid 23063933)
28. M. Spassova, I. Tsoneva, A. Petrov, J. Petkova, and E. Neumann Dip patch clamp currents suggest electrodiffusive transport of the polyelectrolyte DNA through lipid bilayers Biophys. Chem. 52 1994 267 274 (Pubitemid 24333511)
29. C. Djuzenova, U. Zimmermann, H. Frank, V. Sukhorukov, E. Richter, and G. Fuhr Effect of medium conductivity and composition on the uptake of propidium iodide into electropermeabilized myeloma cells Biochim. Biophys. Acta 1284 1996 143 152 (Pubitemid 26356148)
30. L. Wegner, B. Flickinger, C. Eing, T. Berghöfer, P. Hohenberger, W. Frey, and P. Nick A patch clamp study on the electro-permeabilization of higher plant cells: supra-physiological voltages induce a high-conductance, K + selective state of the plasma membrane Biochim. Biophys. Acta 1808 2011 1728 1736
31. M. Puc, T. Kotnik, L. Mir, and D. Miklavcic Quantitative model of small molecules uptake after in vitro cell electropermeabilization Bioelectrochemistry 60 2003 1 10 (Pubitemid 36945000)
32. J. Li, and H. Lin Numerical simulation of molecular uptake via electroporation Bioelectrochemistry 82 2011 10 21
33. J. Li, W. Tan, H. Lin, The effect of extracellular conductivity on electroporation mediated molecular delivery, in press.
34. S. Movahed, and D. Li Electrokinetic transport through the nanopores in cell membrane during electroporation J. Colloid Interface Sci. 369 2012 442 452
35. B. Gabriel, and J. Teissie Time courses of mammalian cell electropermeabilization observed by millisecond imaging of membrane property changes during the pulse Biophys. J. 76 1999 2158 2165 (Pubitemid 29266368)
36. K. Muller, V. Sukhorukov, and U. Zimmermann Reversible electropermeabilization of mammalian cells by high-intensity, ultra-short pulses of submicrosecond duration J. Membr. Biol. 184 2001 161 170 (Pubitemid 33064357)
37. L. Mir, M. Bureau, J. Gehl, R. Rangara, D. Rouyi, J. Caillaud, P. Delaere, D. Branelleci, B. Schwartz, and D. Scherman High-efficiency gene transfer into skeletal muscle mediated by electric pulses Proc. Natl. Acad. Sci. 96 1999 4262 4267 (Pubitemid 29190324)
38. M. Rols, and J. Teissie Electropermeabilization of mammalian cells to macromolecules: control by pulse duration Biophys. J. 75 1998 1415 1423 (Pubitemid 28397611)
39. C. Faurie, E. Phez, M. Golzio, C. Vossen, J. Lesbordes, C. Delteil, J. Teissié, and M. Rols Effect of electric field vectoriality on electrically mediated gene delivery in mammalian cells Biochim. Biophys. Acta 1665 2004 92 100 (Pubitemid 39303574)
40. S. Satkauskas, F. Andre, M. Bureau, D. Scherman, D. Miklavcic, and L. Mir Electrophoretic component of electric pulses determines the efficacy of in vivo DNA electrotransfer Hum. Gene Ther. 16 2005 1194 1201 (Pubitemid 41443711)
41. V. Preat, and N. Pavselj DNA electrotransfer into the skin using a combination of one high- and one low-voltage pulse J. Control. Release 106 2005 407 415 (Pubitemid 41187449)
42. F. Liu, S. Heston, L. Shollenberger, B. Sun, M. Mickle, M. Lovell, and L. Huang Mechanism of in vivo DNA transport into cells by electroporation: electrophoresis across the plasma membrane may not be involved J. Gene Med. 8 2006 353 361
43. M. Kanduser, D. Miklavcic, and M. Pavlin Mechanisms involved in gene electrotransfer using high- and low-voltage pulses-an in vitro study Bioelectrochemistry 74 2009 265 271
44. D. Miklavcic, and L. Towhidi Numerical study of the electroporation pulse shape effect on molecular uptake of biological cells Radiol. Oncol. 44 2010 34 41
45. M. Pavlin, K. Flisar, and M. Kanduser The role of electrophoresis in gene electrotransfer J. Membr. Biol. 236 2010 75 79
46. J. Escoffre, T. Portet, L. Wasungu, J. Teissie, D. Dean, and M. Rols What is (still not) known of the mechanism by which electroporation mediates gene transfer and expression in cells and tissues Mol. Biotechnol. 41 2009 286 295
47. M. Golzio, J. Teissie, and M. Rols Direct visualization at the single-cell level of electrically mediated gene delivery Proc. Natl. Acad. Sci. 99 2001 1292 1297 (Pubitemid 34136486)
48. E. Phez, C. Faurie, M. Golzio, J. Teissie, and M. Rols New insights in the visualization of membrane permeabilization and DNA/membrane interaction of cells submitted to electric pulses Biochim. Biophys. Acta 1724 2005 248 254 (Pubitemid 41080034)
49. M. Rols Electropermeabilization, a physical method for the delivery of therapeutic molecules into cells Biochim. Biophys. Acta 1758 2006 423 428
50. C. Faurie, M. Rebersek, M. Golzio, M. Kanduser, J. Escoffre, M. Pavlin, J. Teissie, D. Miklavcic, and M. Rols Electro-mediated gene transfer and expression are controlled by the life-time of DNA/membrane complex formation J. Gene Med. 12 2010 117 125
51. J. Escoffre, T. Portet, C. Favard, J. Teissié, D. Dean, and M. Rols Electromediated formation of DNA complexes with cell membranes and its consequences for gene delivery Biochim. Biophys. Acta 1808 2011 1538 1543
52. U. Zimmermann, R. Schnettler, G. Klock, and H. Watzka Mechanisms of electrostimulated uptake of macromolecules into living cells Naturwissenschaften 77 1990 543 545
53. M. Wu, and F. Yuan Membrane binding of plasmid DNA and endocytic pathways are involved in electrotransfection of mammalian cells PLoS One 6 2011 e20923
54. R. Lin, D. Chang, and Y. Lee Single-cell electroendocytosis on a micro chip using in situ fluorescence microscopy Biomed. Microdevices 13 2011 1063 1073
55. C. Rosazza, E. Phez, J. Escoffre, L. Cezanne, A. Zumbusch, and M. Rols Cholesterol implications in plasmid DNA electrotransfer: evidence for the involvement of endocytotic pathways Int. J. Pharm. 423 2012 134 143
56. M. Pavlin, M. Kanduser, G. Pucihar, and D. Miklavcic The role of electrically stimulated endocytosis in gene electrotransfer IFMBE Proc. 29 2010 679 682
57. S. Sukharev, V. Klenchin, S. Serov, L. Chernomordik, and Y. Chizmadzhev Electroporation and electrophoretic DNA transfer into cells: the effect of DNA interaction with electropores Biophys. J. 63 1992 1320 1327 (Pubitemid 23004481)
58. M. Bureau, J. Gehl, V. Deleuze, L. Mir, and D. Scherman Importance of association between permeabilization and electrophoretic forces for intramuscular DNA electrotransfer Biochim. Biophys. Acta 1474 2000 353 359 (Pubitemid 30209876)
59. S. Satkauskas, M. Bureau, M. Puc, A. Mahfoudi, D. Scherman, D. Miklavcic, and L. Mir Mechanisms of in vivo DNA electrotransfer: respective contributions of cell electropermeabilization and DNA electrophoresis Mol. Ther. 5 2002 133 140 (Pubitemid 34144829)
60. F. André, J. Gehl, G. Sersa, V. Préat, P. Hojman, J. Eriksen, M. Golzio, M. Cemazar, N. Pavselj, M.P. Rols, D. Miklavcic, E. Neumann, J. Teissié, and L. Mir Efficiency of high- and low-voltage pulse combinations for gene electrotransfer in muscle, liver, tumor, and skin Hum. Gene Ther. 19 2008 1261 1271
61. W. Sung, and P. Park Polymer translocation through a pore in a membrane Phys. Rev. Lett. 77 1996 783 786
62. M. Muthukumar Polymer translocation through a hole J. Chem. Phys. 111 1999 10371 10374 (Pubitemid 129590277)
63. E. Slonkina, and A. Kolomeisky Polymer translocation through a long nanopore J. Chem. Phys. 118 2003 7112 7118
64. J. Viovy Electrophoresis of DNA and other polyelectrolytes: physical mechanisms Rev. Mod. Phys. 72 2000 813 871
65. J. Li, M. Gershow, D. Stein, E. Brandin, and J. Golovchenko DNA molecules and configurations in a solid-state nanopore microscope Nat. Mater. 2 2003 611 615
66. E. Eisenriegler, K. Kremer, and K. Binder Adsorption of polymer chains at surfaces: scaling and Monte Carlo analyses J. Chem. Phys. 77 1982 6296 6319
67. M. Muthukumar Theory of capture rate in polymer translocation J. Chem. Phys. 132 2010 195101
68. K. Smith, J. Neu, and W. Krassowska Model of creation and evolution of stable electropores for DNA delivery Biophys. J. 86 2004 2813 2826 (Pubitemid 38552687)
69. E. Dauty, and A. Verkman Actin cytoskeleton as the principal determinant of size-dependent DNA mobility in cytoplasm J. Biol. Chem. 280 2005 7823 7828 (Pubitemid 40349677)
70. K.D. Kihm, A. Banerjee, C.K. Choi, and T. Takagi Near-wall hindered Brownian diffusion of nanoparticles examined by three-dimensional ratiometric total internal reflection fluorescence microscopy (3-D R-TIRFM) Exp. Fluids 37 2004 811 824 (Pubitemid 40003009)
71. A. Storm, C. Storm, J. Chen, H. Zandbergen, J. Joanny, and C. Dekker Fast DNA translocation through a solid-state nanopore Nano Lett. 5 2005 1193 1197 (Pubitemid 41084390)
72. U. Keyser, B. Koeleman, S. Dorp, D. Krapf, R. Smeets, S. Lemay, N. Dekker, and C. Dekker Direct force measurements on DNA in a solid-state nanopore Nat. Phys. 2 2006 473 477 (Pubitemid 44022563)
73. S. Ghosal Electrokinetic-flow-induced viscous drag on a tethered DNA inside a nanopore Phys. Rev. E 76 2007 061916