Low current-driven micro-electroporation allows efficient in vivo delivery of nonviral DNA into the adult mouse brain

Molecular Therapy

Volumn 18, Issue 6, 2010, Pages 1183-1191

  Vry, Jochen De ^a   Martínez Martínez, Pilar ^a   Losen, Mario ^a   Bode, Gerard H ^a   Temel, Yasin ^a,b   Steckler, Thomas ^c   Steinbusch, Harry Wm ^a   Baets, Marc De ^a,d   Prickaerts, Jos ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Johnson and Johnson PRD ^*  (Belgium)

^d HASSELT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; ENHANCED GREEN FLUORESCENT PROTEIN; PLASMID DNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; C57BL 6 MOUSE; CONTROLLED STUDY; ELECTRIC POTENTIAL; ELECTROPORATION; ELECTROSTIMULATION; ENERGY TRANSFER; HUMAN; HUMAN CELL; IN VIVO GENE TRANSFER; INJECTION SITE; MALE; MEMBRANE POTENTIAL; MOUSE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; WAVEFORM; ADMINISTRATION AND DOSAGE; ANIMAL; BRAIN; C57BL MOUSE; GENETIC TRANSFECTION; GENETICS; METABOLISM; PLASMID; PROCEDURES; STEREOTACTIC PROCEDURE; SURGERY;

ANIMALIA; MUS;

ANIMALS; BRAIN; ELECTROPORATION; MALE; MICE; MICE, INBRED C57BL; PLASMIDS; STEREOTAXIC TECHNIQUES; TRANSFECTION;

EID: 77953128360     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2010.62     Document Type: Article

References (50)

1. Chen, C, Smye, SW, Robinson, MP and Evans, JA (2006). Membrane electroporation theories: a review. Med Biol Eng Comput 44: 5-14.
2. Bloquel, C, Fabre, E, Bureau, MF and Scherman, D (2004). Plasmid DNA electrotransfer for intracellular and secreted proteins expression: new methodological developments and applications. J Gene Med 6 Suppl 1: S11-S23.
3. Satkauskas, S, André, F, Bureau, MF, Scherman, D, Miklavcic, D and Mir, LM (2005). Electrophoretic component of electric pulses determines the effcacy of in vivo DNA electrotransfer. Hum Gene Ther 16: 1194-1201.
4. Satkauskas, S, Bureau, MF, Puc, M, Mahfoudi, A, Scherman, D, Miklavcic, D et al. (2002). Mechanisms of in vivo DNA electrotransfer: respective contributions of cell electropermeabilization and DNA electrophoresis. Mol Ther 5: 133-140.
5. Liu, F, Heston, S, Shollenberger, LM, Sun, B, Mickle, M, Lovell, M et al. (2006). Mechanism of in vivo DNA transport into cells by electroporation: electrophoresis across the plasma membrane may not be involved. J Gene Med 8: 353-361.
6. Zhang, X and Godbey, WT (2006). Viral vectors for gene delivery in tissue engineering. Adv Drug Deliv Rev 58: 515-534. (Pubitemid 43928170)
7. Thomas, CE, Ehrhardt, A and Kay, MA (2003). Progress and problems with the use of viral vectors for gene therapy. Nat Rev Genet 4: 346-358.
8. Titomirov, AV, Sukharev, S and Kistanova, E (1991). In vivo electroporation and stable transformation of skin cells of newborn mice by plasmid DNA. Biochim Biophys Acta 1088: 131-134.
9. Heller, R, Jaroszeski, M, Atkin, A, Moradpour, D, Gilbert, R, Wands, J et al. (1996). In vivo gene electroinjection and expression in rat liver. FEBS Lett 389: 225-228.
10. Nishi, T, Yoshizato, K, Yamashiro, S, Takeshima, H, Sato, K, Hamada, K et al. (1996). High-effciency in vivo gene transfer using intraarterial plasmid DNA injection following in vivo electroporation. Cancer Res 56: 1050-1055.
11. Medi, BM, Hoselton, S, Marepalli, RB and Singh, J (2005). Skin targeted DNA vaccine delivery using electroporation in rabbits. I: effcacy. Int J Pharm 294: 53-63.
12. Ferraro, B, Cruz, YL, Coppola, D and Heller, R (2009). Intradermal delivery of plasmid VEGF(165) by electroporation promotes wound healing. Mol Ther 17: 651-657.
13. Suzuki, T, Shin, BC, Fujikura, K, Matsuzaki, T and Takata, K (1998). Direct gene transfer into rat liver cells by in vivo electroporation. FEBS Lett 425: 436-440.
14. Mir, LM, Bureau, MF, Gehl, J, Rangara, R, Rouy, D, Caillaud, JM et al. (1999). High-effciency gene transfer into skeletal muscle mediated by electric pulses. Proc Natl Acad Sci USA 96: 4262-4267.
15. Losen, M, Stassen, MH, Martínez-Martínez, P, Machiels, BM, Duimel, H, Frederik, P et al. (2005). Increased expression of rapsyn in muscles prevents acetylcholine receptor loss in experimental autoimmune myasthenia gravis. Brain 128(Pt 10): 2327-2337.
16. Martínez-Martínez, P, Losen, M, Duimel, H, Frederik, P, Spaans, F, Molenaar, P et al. (2007). Overexpression of rapsyn in rat muscle increases acetylcholine receptor levels in chronic experimental autoimmune myasthenia gravis. Am J Pathol 170: 644-657.
17. Martínez-Martínez, P, Phernambucq, M, Steinbusch, L, Schaeffer, L, Berrih-Aknin, S, Duimel, H et al. (2009). Silencing rapsyn in vivo decreases acetylcholine receptors and augments sodium channels and secondary postsynaptic membrane folding. Neurobiol Dis 35: 14-23.
18. Aihara, H and Miyazaki, J (1998). Gene transfer into muscle by electroporation in vivo. Nat Biotechnol 16: 867-870.
19. Kachi, S, Oshima, Y, Esumi, N, Kachi, M, Rogers, B, Zack, DJ et al. (2005). Nonviral ocular gene transfer. Gene Ther 12: 843-851.
20. Hibbitt, O, Coward, K, Kubota, H, Prathalingham, N, Holt, W, Kohri, K et al. (2006). In vivo gene transfer by electroporation allows expression of a fuorescent transgene in hamster testis and epididymal sperm and has no adverse effects upon testicular integrity or sperm quality. Biol Reprod 74: 95-101.
21. Rols, MP, Delteil, C, Golzio, M, Dumond, P, Cros, S and Teissie, J (1998). In vivo electrically mediated protein and gene transfer in murine melanoma. Nat Biotechnol 16: 168-171.
22. Luo, J, Ju, MJ and Redies, C (2006). Regionalized cadherin-7 expression by radial glia is regulated by Shh and Pax7 during chicken spinal cord development. Neuroscience 142: 1133-1143.
23. Barnabé-Heider, F, Meletis, K, Eriksson, M, Bergmann, O, Sabelström, H, Harvey, MA et al. (2008). Genetic manipulation of adult mouse neurogenic niches by in vivo electroporation. Nat Methods 5: 189-196.
24. Wang, H, Ko, CH, Koletar, MM, Ralph, MR and Yeomans, J (2007). Casein kinase I epsilon gene transfer into the suprachiasmatic nucleus via electroporation lengthens circadian periods of tau mutant hamsters. Eur J Neurosci 25: 3359-3366.
25. Yamaguchi, S, Katagiri, S, Hirose, N, Fujimoto, Y, Mori, M, Fujii-Taira, I et al. (2007). In-vivo gene transfer into newly hatched chick brain by electroporation. Neuroreport 18: 735-739.
26. Boutin, C, Diestel, S, Desoeuvre, A, Tiveron, MC and Cremer, H (2008). Effcient in vivo electroporation of the postnatal rodent forebrain. PLoS ONE 3: e1883.
27. Akaneya, Y, Jiang, B and Tsumoto, T (2005). RNAi-induced gene silencing by local electroporation in targeting brain region. J Neurophysiol 93: 594-602.
28. Wei, F, Xia, XM, Tang, J, Ao, H, Ko, S, Liauw, J et al. (2003). Calmodulin regulates synaptic plasticity in the anterior cingulate cortex and behavioral responses: a microelectroporation study in adult rodents. J Neurosci 23: 8402-8409.
29. Prud'homme, GJ, Glinka, Y, Khan, AS and Draghia-Akli, R (2006). Electroporation-enhanced nonviral gene transfer for the prevention or treatment of immunological, endocrine and neoplastic diseases. Curr Gene Ther 6: 243-273.
30. Temel, Y, Visser-Vandewalle, V, van der Wolf, M, Spincemaille, GH, Desbonnet, L, Hoogland, G et al. (2004). Monopolar versus bipolar high frequency stimulation in the rat subthalamic nucleus: differences in histological damage. Neurosci Lett 367: 92-96.
31. Zampaglione, I, Arcuri, M, Cappelletti, M, Ciliberto, G, Perretta, G, Nicosia, A et al. (2005). In vivo DNA gene electro-transfer: a systematic analysis of different electrical parameters. J Gene Med 7: 1475-1481.
32. Brown, PA, Davis, WC and Draghia-Akli, R (2004). Immune-enhancing effects of growth hormone-releasing hormone delivered by plasmid injection and electroporation. Mol Ther 10: 644-651.
33. Khan, AS, Pope, MA and Draghia-Akli, R (2005). Highly effcient constant-current electroporation increases in vivo plasmid expression. DNA Cell Biol 24: 810-818.
34. Haas, K, Sin, WC, Javaherian, A, Li, Z and Cline, HT (2001). Single-cell electroporation for gene transfer in vivo. Neuron 29: 583-591.
35. Nagayama, S, Zeng, S, Xiong, W, Fletcher, ML, Masurkar, AV, Davis, DJ et al. (2007). In vivo simultaneous tracing and Ca(2+) imaging of local neuronal circuits. Neuron 53: 789-803.
36. Glogauer, M, Lee, W and McCulloch, CA (1993). Induced endocytosis in human fbroblasts by electrical felds. Exp Cell Res 208: 232-240.
37. Satkauskas, S, Bureau, MF, Mahfoudi, A and Mir, LM (2001). Slow accumulation of plasmid in muscle cells: supporting evidence for a mechanism of DNA uptake by receptor-mediated endocytosis. Mol Ther 4: 317-323.
38. Antov, Y, Barbul, A, Mantsur, H and Korenstein, R (2005). Electroendocytosis: exposure of cells to pulsed low electric felds enhances adsorption and uptake of macromolecules. Biophys J 88: 2206-2223.
39. Deng, PY and Lei, S (2007). Long-term depression in identifed stellate neurons of juvenile rat entorhinal cortex. J Neurophysiol 97: 727-737.
40. von Gersdorff, K, Sanders, NN, Vandenbroucke, R, De Smedt, SC, Wagner, E and Ogris, M (2006). The internalization route resulting in successful gene expression depends on both cell line and polyethylenimine polyplex type. Mol Ther 14: 745-753.
41. Rejman, J, Bragonzi, A and Conese, M (2005). Role of clathrin-and caveolae-mediated endocytosis in gene transfer mediated by lipo-and polyplexes. Mol Ther 12: 468-474.
42. Rejman, J, Conese, M and Hoekstra, D (2006). Gene transfer by means of lipo-and polyplexes: role of clathrin and caveolae-mediated endocytosis. J Liposome Res 16: 237-247.
43. van der Aa, MA, Huth, US, Häfele, SY, Schubert, R, Oosting, RS, Mastrobattista, E et al. (2007). Cellular uptake of cationic polymer-DNA complexes via caveolae plays a pivotal role in gene transfection in COS-7 cells. Pharm Res 24: 1590-1598.
44. Van Harreveld, A and Khattab, FI (1969). Changes in extracellular space of the mouse cerebral cortex during hydroxyadipaldehyde fxation and osmium tetroxide post-fxation. J Cell Sci 4: 437-453.
45. Chesler, AT, Le Pichon, CE, Brann, JH, Araneda, RC, Zou, DJ and Firestein, S (2008). Selective gene expression by postnatal electroporation during olfactory interneuron nurogenesis. PLoS ONE 3: e1517.
46. Miyasaka, N, Arimatsu, Y and Takiguchihayashi, K (1999). Foreign gene expression in an organotypic culture of cortical anlage after in vivo electroporation. Neuroreport 10: 2319-2323.
47. Johanson, CE, Duncan, JA 3rd, Klinge, PM, Brinker, T, Stopa, EG and Silverberg, GD (2008). Multiplicity of cerebrospinal fuid functions: New challenges in health and disease. Cerebrospinal Fluid Res 5: 10.
48. Stelten, BM, Noblesse, LH, Ackermans, L, Temel, Y and Visser-Vandewalle, V (2008). The neurosurgical treatment of addiction. Neurosurg Focus 25: E5.
49. Temel, Y, Boothman, LJ, Blokland, A, Magill, PJ, Steinbusch, HW, Visser-Vandewalle, V et al. (2007). Inhibition of 5-HT neuron activity and induction of depressive-like behavior by high-frequency stimulation of the subthalamic nucleus. Proc Natl Acad Sci USA 104: 17087-17092.
50. Strackx, E, Van den Hove, DL, Steinbusch, HP, Steinbusch, HW, Vles, JS, Blanco, CE et al. (2008). A combined behavioral and morphological study on the effects of fetal asphyxia on the nigrostriatal dopaminergic system in adult rats. Exp Neurol 211: 413-422