Observations of the mechanisms of electromediated DNA uptake - from vesicles to tissues

Current Gene Therapy

Volumn 10, Issue 4, 2010, Pages 256-266

  Golzio, Muriel ^a,b   Escoffre, Jean Michel ^a,b   Portet, Thomas ^a,b   Mauroy, Chloé ^a,b   Teissié, Justin ^a,b   Dean, David S ^a   Rols, Marie Pierre ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

Delivery; Electric field; Electroporation; Gene transfer; Membrane; Microscopy

Indexed keywords

DNA; HYALURONIC ACID; HYALURONIDASE; PLASMID DNA;

ARTICLE; CELL MEMBRANE; CELL VACUOLE; CHO CELL; DNA TRANSFER; ELECTRIC FIELD; ELECTRIC POTENTIAL; ELECTRODE; ELECTROPORATION; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENE TARGETING; LIPID MEMBRANE; MECHANICS; NONHUMAN; NUCLEAR PORE COMPLEX;

ANIMALS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; DNA; ELECTROMAGNETIC FIELDS; ELECTROPORATION; GENE EXPRESSION; GENE TRANSFER TECHNIQUES; MICE; UNILAMELLAR LIPOSOMES;

EID: 77958061119     PISSN: 15665232     EISSN: None     Source Type: Journal    
DOI: 10.2174/156652310791823461     Document Type: Article

References (117)

1. Powell K, Weaver JC. Transient aqueous pores in bilayer membranes: a statistical theory. Bioelectrochem Bioenerg 1986; 15: 211-27.
2. Glaser RW, Leikin SL, Chernomordik LV, Pastushenko VF, Sokirko AI. Reversible electrical breakdown of lipid bilayers: formation and evolution of pores. Biochim Biophys Acta 1988; 940: 275-87.
3. Barnett A, Weaver JC. Electroporation: a unified quantitative theory of reversible electrical breakdown and mechanical rupture in artificial planar lipid membranes. Bioelectrochem Bioenerg 1991; 25: 163-82.
4. Derjaguin B, Gutop Y. Theory of the breakdown (rupture) of free films. Kol loidn Zh 1961; 24: 370-74.
5. Winterhalter M, Helfrich W. Deformation of spherical vesicles by electric fields. J Colloid Interface Sci 1988; 122: 583-6.
6. Kummrow M, Helfrich W. Deformation of giant lipid vesicles by electric fields. Phys Rev 1991; 44: 8356-60.
7. Riske KA, Dimova R. Electro-deformation and poration of giant vesicles viewed with high temporal resolution. Biophys J 2005; 88: 1143-55.
8. Riske KA, Dimova R. Electric pulses induce cylindrical deformations on giant vesicles in salt solutions. Biophys J 2006; 91: 1778-86.
9. Crowley J. Electrical breakdown of bimolecular lipid membranes as an electromechanical instability. Biophys J 1973; 13: 711-24.
10. Tekle E, Astumian RD, Friauf WA, Chock PB. Asymmetric pore distribution and loss of membrane lipid in electroporated DOPC vesicles. Biophys J 2001; 81: 960-8.
11. Needham D, Hochmuth RM. Electro-mechanical permeabilization of lipid vesicles. Role of membrane tension and compressibility. Biophys J 1989; 55: 1001-9.
12. Sandre O, Moreaux L, Brochard-Wyart F. Dynamics of transient pores in stretched vesicles. Proc Natl Acad Sci USA 1999; 96: 10591-6.
13. Brochard-Wyart F, de Gennes PG, Sandre O. Transient pores in streteched vesicles: role of leak-out. Physica 2000; 278: 32-51.
14. Hamada T, Hirabayashi Y, Ohta T, Takagi M. Rythmic pore dunamics in a shrinking lipid vesicle. Phys Rev 2009; 80: 51921.
15. Portet T, Camps i Febrer F, Escoffre JM, Favard C, Rols MP, Dean DS. Visualization of membrane loss during the shrinkage of giant vesicles under electropulsation. Biophys J 2009; 96: 4109-21.
16. Rols MP. Electropermeabilization, a physical method for the delivery of therapeutic molecules into cells. Biochim Biophys Acta 2006; 1758: 423-8.
17. Fournier D, Khalifat N, Puff N, Angelova MI. Chemically triggered ejection of membrane tubules controlled by intermonolayer friction. Phys Rev Lett 2009; 102: 18102.
18. Chernomordik LV, Sokolov AV, Budker VG. Electrostimulated uptake of DNA by liposomes. Biochim Biophys Acta 1990; 1024: 179-83.
19. Lurquin PF, Athanasiou K. Electric field-mediated DNA encapsulation into large liposomes. Biochem Biophys Res Commun 2000; 267: 838-41.
20. Neumann E, Schaefer-Ridder M, Wang Y, Hofschneider PH. Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J 1982; 1: 841-5.
21. + subclone. Biochem Biophys Res Commun 1985; 129: 611-8.
22. Wolf H, Rols MP, Boldt E, Neumann E, Teissie J. Control by pulse parameters of electric field-mediated gene transfer in mammalian cells. Biophys J 1994; 66: 524-31.
23. Eynard N, Rols MP, Ganeva V, Galutzov B, Sabri N, Teissie J. Electrotransformation mechanism of procaryotic and eucaryotic cells: A recent development. Bioelectrochem Bioenerg 1997; 44: 103-10.
24. Rols MP, Dahhou F, Teissie J. Pulse-first heterofusion of cells by electric field pulses and associated loading of macromolecules into mammalian cells. Biotechniques 1994; 17: 762-4.
25. Rols MP, Teissie J. Electropermeabilization of mammalian cells to macromolecules: control by pulse duration. Biophys J 1998; 75: 1415-23.
26. Frantescu A, Tonsing K, Neumann E. Interfacial ternary complex DNA/Ca/lipids at anionic vesicle surfaces. Bioelectrochemistry 2006; 68: 158-70.
27. Xie TD, Tsong TY. Study of mechanisms of electric field-induced DNA transfection. V. Effects of DNA topology on surface binding, cell uptake, expression, and integration into host chromosomes of DNA in the mammalian cell. Biophys J 1993; 65: 1684-9.
28. Golzio M, Teissie J, Rols MP. Direct visualization at the single-cell level of electrically mediated gene delivery. Proc Natl Acad Sci USA 2002; 99: 1292-7.
29. Tsong TY. Electroporation of cell membranes. Biophys J 1991; 60: 297-306.
30. Klenchin VA, Sukharev SI, Serov SM, Chernomordik LV, Chizmadzhev Y. Electrically induced DNA uptake by cells is a fast process involving DNA electrophoresis. Biophys J 1991; 60: 804-11.
31. Chang DC, Saunders JA, Sowers AE. Guide To Electroporation and Electrofusion. Academic Press 1991.
32. Bloomfield V, Crothers D, Tinico I. Nucleic acids structures, properties and functions. In: University Science Books 1999.
33. Rols MP, Coulet D, Teissie J. Highly efficient transfection of mammalian cells by electric field pulses. Application to large volumes of cell culture by using a flow system. Eur J Biochem 1992; 206: 115-21.
34. Li LH, Sen A, Murphy SP, Jahreis GP, Fuji H, Hui SW. Apoptosis induced by DNA uptake limits transfection efficiency. Exp Cell Res 1999; 253: 541-50.
35. Shimokawa T, Okumura K, Ra C. DNA induces apoptosis in electroporated human promonocytic cell line U937. Biochem Biophys Res Commun 2000; 270: 94-9.
36. Kubiniec RT, Liang H, Hui SW. Effects of pulse length and pulse strength on transfection by electroporation. Biotechniques 1990, 8: 16-20.
37. Heller R, Jaroszeski M, Atkin A, et al. In vivo gene electroinjection and expression in rat liver. FEBS Lett 1996; 389: 225-8.
38. Kanduser M, Miklavcic D, Pavlin M. Mechanisms involved in gene electrotransfer using high-and low-voltage pulses--an in vitro study. Bioelectrochemistry 2009; 74: 265-71.
39. Ferreira E, Potier E, Logeart-Avramoglou D, Salomskaite-Davalgiene S, Mir LM, Petite H. Optimization of a gene electrotransfer method for mesenchymal stem cell transfection. Gene Ther 2008; 15: 537-44.
40. Phez E, Faurie C, Golzio M, Teissie J, Rols MP. New insights in the visualization of membrane permeabilization and DNA/membrane interaction of cells submitted to electric pulses. Biochim Biophys Acta 2005; 1724: 248-54.
41. Faurie C, Rebersek M, Golzio M, et al. Electrically mediated gene transfer and expression are controlled by the life-time of DNA/Membrane complex formation. J Gene Med 2010; 12: 117-25.
42. Rols MP, Delteil C, Serin G, Teissie J. Temperature effects on electrotransfection of mammalian cells. Nucleic Acids Res 1994; 22: 540.
43. Golzio M, Mora MP, Raynaud C, Delteil C, Teissie J, Rols MP. Control by osmotic pressure of voltage-induced permeabilization and gene transfer in mammalian cells. Biophys J 1998; 74: 3015-22.
44. Rols MP, 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 1998; 254: 382-8.
45. Golzio M, Teissie J, Rols MP. Cell synchronization effect on mammalian cell permeabilization and gene delivery by electric field. Biochim Biophys Acta 2002; 1563: 23-8.
46. Pouton CW, Wagstaff KM, Roth DM, Moseley GW, Jans DA. Targeted delivery to the nucleus. Adv Drug Deliv Rev 2007; 59: 698-717.
47. Munkonge FM, Amin V, Hyde SC. et al. Identification and functional characterization of cytoplasmic determinants of plasmid DNA nuclear import. J Biol Chem 2009; 284: 26978-87.
48. Munkonge FM, Dean DA, Hillery E, Griesenbach U, Alton EW. Emerging significance of plasmid DNA nuclear import in gene therapy. Adv Drug Deliv Rev 2003; 55: 749-60.
49. van der Aa MA, Mastrobattista E, Oosting RS, Hennink WE, Koning GA, Crommelin DJ. The nuclear pore complex: the gateway to successful nonviral gene delivery. Pharm Res 2006; 23: 447-459.
50. Miller AM, Dean DA. Tissue-specific and transcription factormediated nuclear entry of DNA. Adv Drug Deliv Rev 2009; 61: 603-13.
51. Wasungu L, Escoffre JM, Valette A, Teissie J, Rols MP. A 3D in vitro spheroid model as a way to study the mechanisms of electroporation. Int J Pharm 2009; 379: 278-84.
52. Titomirov AV, Sukharev S, Kistanova E. In vivo electroporation and stable transformation of skin cells of newborn mice by plasmid DNA. Biochim Biophys Acta 1991; 1088: 131-4.
53. Vandermeulen G, Staes E, Vanderhaeghen ML, Bureau MF, Scherman D, Preat V. Optimisation of intradermal DNA electrotransfer for immunisation. J Control Release 2007; 124: 81-7.
54. Rols MP, Delteil C, Golzio M, Dumond P, Cros S, Teissie J. In vivo electrically mediated protein and gene transfer in murine melanoma. Nat Biotechnol 1998; 16: 168-71.
55. Nishi T, Yoshizato K, Yamashiro S, et al. High-efficiency in vivo gene transfer using intraarterial plasmid DNA injection following in vivo electroporation. Cancer Res 1996; 56: 1050-5.
56. Liu F, Huang L. Electric gene transfer to the liver following systemic administration of plasmid DNA. Gene Ther 2002; 9: 1116-9.
57. Aihara H, Miyazaki J. Gene transfer into muscle by electroporation in vivo. Nat Biotechnol 1998; 16: 867-70.
58. Mir LM, Bureau MF, Gehl J, et al. High-efficiency gene transfer into skeletal muscle mediated by electric pulses. Proc Natl Acad Sci USA 1999; 96: 4262-7.
59. Dean DA. Nonviral gene transfer to skeletal, smooth, and cardiac muscle in living animals. Am J Physiol Cell Physiol 2005; 289: C233-245.
60. Harrison RL, Byrne BJ, Tung L. Electroporation-mediated gene transfer in cardiac tissue. FEBS Lett 1998; 435: 1-5.
61. Dean DA, Machado-Aranda D, Blair-Parks K, Yeldandi AV, Young JL. Electroporation as a method for high-level nonviral gene transfer to the lung. Gene Ther 2003; 10: 1608-15.
62. Zhou R, Norton JE, Zhang N, Dean DA. Electroporation-mediated transfer of plasmids to the lung results in reduced TLR9 signaling and inflammation. Gene Ther 2007; 14: 775-80.
63. Dezawa M, Takano M, Negishi H, Mo X, Oshitari T, Sawada H. Gene transfer into retinal ganglion cells by in vivo electroporation: a new approach. Micron 2002; 33: 1-6.
64. Lin CR, Tai MH, Cheng JT, et al. Electroporation for direct spinal gene transfer in rats. Neurosci Lett 2002; 317: 1-4.
65. Blair-Parks K, Weston BC, Dean DA. High-level gene transfer to the cornea using electroporation. J Gene Med 2002; 4: 92-100.
66. Tsujie M, Isaka Y, Nakamura H, Imai E, Hori M. Electroporationmediated gene transfer that targets glomeruli. J Am Soc Nephrol 2001; 12: 949-54.
67. Isaka Y, Yamada K, Takabatake Y, et al. Electroporation-mediated HGF gene transfection protected the kidney against graft injury. Gene Ther 2005; 12: 815-20.
68. Inoue T, Krumlauf R. An impulse to the brain--using in vivo electroporation. Nat Neurosci Suppl 2001; 4: 1156-8.
69. Grossin L, Gaborit N, Mir L, Netter P, Gillet P. Gene therapy in cartilage using electroporation. Joint Bone Spine 2003; 70: 480-2.
70. Harimoto K, Sugimura K, Lee CR, Kuratsukuri K, Kishimoto T. In vivo gene transfer methods in the bladder without viral vectors. Br J Urol 1998; 81: 870-4.
71. Tupin E, Poirier B, Bureau MF, et al. Non-viral gene transfer of murine spleen cells achieved by in vivo electroporation. Gene Ther 2003; 10: 569-79.
72. Matsumoto T, Komori K, Shoji T, et al. Successful and optimized in vivo gene transfer to rabbit carotid artery mediated by electronic pulse. Gene Ther 2001; 8: 1174-9.
73. Jayankura M, Boggione C, Frisen C, et al. In situ gene transfer into animal tendons by injection of naked DNA and electrotransfer. J Gene Med 2003; 5: 618-24.
74. Mir LM, Moller PH, Andre F, Gehl J. Electric pulse-mediated gene delivery to various animal tissues. Adv Genet 2005; 54: 83-114.
75. Golzio M, Rols MP, Gabriel B, Teissie J. Optical imaging of in vivo gene expression: a critical assessment of the methodology and associated technologies. Gene Ther 2004; 11(Suppl 1): S85-91.
76. Andre F, Mir LM. DNA electrotransfer: its principles and an updated review of its therapeutic applications. Gene Ther 2004; (Suppl 11): S33-42.
77. Rizzuto G, Cappelletti M, Maione D, et al. Efficient and regulated erythropoietin production by naked DNA injection and muscle electroporation. Proc Natl Acad Sci USA 1999; 96: 6417-22.
78. Widera G, Austin M, Rabussay D, C, et al. Increased DNA vaccine delivery and immunogenicity by electroporation in vivo. J Immunol 2000; 164: 4635-40.
79. Dupuis M, Denis-Mize K, Woo C, et al. Distribution of DNA vaccines determines their immunogenicity after intramuscular injection in mice. J Immunol 2000; 165: 2850-8.
80. Lucas ML, Heller L, Coppola D, Heller R. IL-12 plasmid delivery by in vivo electroporation for the successful treatment of established subcutaneous B16.F10 melanoma. Mol Ther 2002; 5: 668-75.
81. Andre FM, Cournil-Henrionnet C, Vernerey D, Opolon P, Mir LM. Variability of naked DNA expression after direct local injection: the influence of the injection speed. Gene Ther 2006; 13: 1619-27.
82. Golzio M, Rols MP, Teissie J. In vitro and in vivo electric fieldmediated permeabilization, gene transfer, and expression. Methods 2004; 33: 126-35.
83. Satkauskas S, Bureau MF, Mahfoudi A, Mir LM. Slow accumulation of plasmid in muscle cells: supporting evidence for a mechanism of DNA uptake by receptor-mediated endocytosis. Mol Ther 2001; 4: 317-23.
84. Cemazar M, Golzio M, Sersa G, et al. Control by pulse parameters of DNA electrotransfer into solid tumors in mice. Gene Ther 2009; 16: 635-44.
85. Niu G, Heller R, Catlett-Falcone R, et al. Gene therapy with dominant-negative Stat3 suppresses growth of the murine melanoma B16 tumor in vivo. Cancer Res 1999; 59: 5059-63.
86. Lucas ML, Jaroszeski MJ, Gilbert R, Heller R. In vivo electroporation using an exponentially enhanced pulse: a new waveform. DNA Cell Biol 2001; 20: 183-8.
87. Satkauskas S, Bureau MF, Puc M, et al. Mechanisms of in vivo DNA electrotransfer: respective contributions of cell electropermeabilization and DNA electrophoresis. Mol Ther 2002; 5: 133-40.
88. Gehl J, Sorensen TH, Nielsen K, et al. In vivo electroporation of skeletal muscle: threshold, efficacy and relation to electric field distribution. Biochim Biophys Acta 1999, 1428: 233-40.
89. Jaroszeski MJ, Gilbert RA, Heller R. In vivo antitumor effects of electrochemotherapy in a hepatoma model. Biochim Biophys Acta 1997; 1334: 15-8.
90. Gilbert RA, Jaroszeski MJ, Heller R. Novel electrode designs for electrochemotherapy. Biochim Biophys Acta 1997; 1334: 9-14.
91. Miklavcic D, Beravs K, Semrov D, Cemazar M, Demsar F, Sersa G. The importance of electric field distribution for effective in vivo electroporation of tissues. Biophys J 1998; 74: 2152-8.
92. Dev SB, Dhar D, Krassowska W. Electric field of a six-needle array electrode used in drug and DNA delivery in vivo: analytical versus numerical solution. IEEE Trans Biomed Eng 2003; 50: 1296-300.
93. Semrov D, Miklavcic D. Calculation of the electrical parameters in electrochemotherapy of solid tumours in mice. Comput Biol Med 1998; 28: 439-48.
94. Gowrishankar TR, Weaver JC. An approach to electrical modeling of single and multiple cells. Proc Natl Acad Sci USA 2003; 100: 3203-8.
95. Kinosita K Jr, Tsong TY. Voltage-induced conductance in human erythrocyte membranes. Biochim Biophys Acta 1979; 554: 479-97.
96. Abidor IG, Li LH, Hui SW. Studies of cell pellets: II. Osmotic properties, electroporation, and related phenomena: membrane interactions. Biophys J 1994; 67: 427-35.
97. Pavlin M, Pavselj N, Miklavcic D. Dependence of induced transmembrane potential on cell density, arrangement, and cell position inside a cell system. IEEE Trans Biomed Eng 2002; 49: 605-12.
98. Heller LC, Ingram SF, Lucas ML, Gilbert RA, Heller R. Effect of electrically mediated intratumor and intramuscular delivery of a plasmid encoding IFN alpha on visible B16 mouse melanomas. Technol Cancer Res Treat 2002; 1: 205-9.
99. Miklavcic D, Semrov D, Mekid H, Mir LM. A validated model of in vivo electric field distribution in tissues for electrochemotherapy and for DNA electrotransfer for gene therapy. Biochim Biophys Acta 2000; 1523: 73-83.
100. Dona M, Sandri M, Rossini K, Dell'Aica I, Podhorska-Okolow M, Carraro U. Functional in vivo gene transfer into the myofibers of adult skeletal muscle. Biochem Biophys Res Commun 2003; 312: 1132-8.
101. Babiuk S, van Drunen Littel-van den Hurk S, Babiuk LA. Delivery of DNA vaccines using electroporation. Methods Mol Med 2006; 127: 73-82.
102. Zhang L, Nolan E, Kreitschitz S, Rabussay DP. Enhanced delivery of naked DNA to the skin by non-invasive in vivo electroporation. Biochim Biophys Acta 2002; 1572: 1-9.
103. Liu F, Huang L. A syringe electrode device for simultaneous injection of DNA and electrotransfer. Mol Ther 2002; 5: 323-8.
104. Hartikka J, Sukhu L, Buchner C, et al. Electroporation-facilitated delivery of plasmid DNA in skeletal muscle: plasmid dependence of muscle damage and effect of poloxamer 188. Mol Ther 2001; 4: 407-15.
105. Lee WR, Shen SC, Fang CL, Zhuo RZ, Fang JY. Topical delivery of methotrexate via skin pretreated with physical enhancement techniques: low-fluence erbium:YAG laser and electroporation. Lasers Surg Med 2008; 40: 468-76.
106. Gehl J, Skovsgaard T, Mir LM. Vascular reactions to in vivo electroporation: characterization and consequences for drug and gene delivery. Biochim Biophys Acta 2002; 1569: 51-8.
107. Molnar MJ, Gilbert R, Lu Y, et al. Factors influencing the efficacy, longevity, and safety of electroporation-assisted plasmid-based gene transfer into mouse muscles. Mol Ther 2004; 10: 447-55.
108. Roos AK, Eriksson F, Timmons JA, et al. Skin electroporation: effects on transgene expression, DNA persistence and local tissue environment. PLoS One 2009; 4: e7226.
109. Wolff JA, Ludtke JJ, Acsadi G, Williams P, Jani A. Long-term persistence of plasmid DNA and foreign gene expression in mouse muscle, Hum Mol Genet 1992; 1: 363-9.
110. Orsag P, Kvardova V, Raska M, Miller AD, Ledvina M, Turanek J. Quantitative real-time PCR study on persistence of pDNA vaccine pVax-Hsp60 TM814 in beef muscles. Genet Vaccines Ther 2008; 6: 11.
111. Pluen A, Boucher Y, Ramanujan S, et al. Role of tumor-host interactions in interstitial diffusion of macromolecules: cranial vs. subcutaneous tumors. Proc Natl Acad Sci USA 2001, 98: 4628-33.
112. Mennuni C, Calvaruso F, Zampaglione I, et al. Hyaluronidase increases electrogene transfer efficiency in skeletal muscle. Hum Gene Ther 2002; 13: 355-65.
113. McMahon JM, Signori E, Wells KE, Fazio VM, Wells DJ. Optimisation of electrotransfer of plasmid into skeletal muscle by pretreatment with hyaluronidase increased expression with reduced muscle damage. Gene Ther 2001; 8: 1264-70.
114. Alexandrakis G, Brown EB, Tong RT, et al. Two-photon fluorescence correlation microscopy reveals the two-phase nature of transport in tumors. Nat Med 2004; 10: 203-7.
115. Yamashita Y, Shimada M, Tachibana K, et al. In vivo gene transfer into muscle via electro-sonoporation. Hum Gene Ther 2002; 13: 2079-84.
116. Favard C, Dean DS, Rols MP. Electrotransfer as a non viral method of gene delivery. Curr Gene Ther 2007; 7: 67-77.
117. Reed SD, Li S. Electroporation advances in large animals. Curr Gene Ther 2009; [Epub ahead of Print].