Electrotransfer of RNAi-based oligonucleotides for oncology

Anticancer Research

Volumn 31, Issue 12, 2011, Pages 4083-4090

  Chabot, Sophie ^a,b   Pelofy, Sandrine ^a,b   Paganin Gioanni, Aurelie ^a,b   Teissie, Justin ^a,b   Golzio, Muriel ^a,b  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

Electroporation; miRNA; Oligonucleotides; Review; SiRNA

Indexed keywords

BLEOMYCIN; CISPLATIN; MICRORNA; OLIGONUCLEOTIDE; PLASMID DNA; SMALL INTERFERING RNA;

CANCER CELL; CANCER GENE THERAPY; CANCER THERAPY; CANCER TISSUE; CELL PERMEABILIZATION; CLINICAL PRACTICE; CUTANEOUS MELANOMA; ELECTRICAL PARAMETERS; ELECTROCHEMOTHERAPY; ELECTRODE; ELECTROGENOTHERAPY; ELECTROPORATION; FIBROSIS; GENE DELIVERY SYSTEM; GENE SILENCING; HUMAN; LUNG NON SMALL CELL CANCER; MELANOMA; METABOLIC DISORDER; NONHUMAN; ONCOLOGY; PRIORITY JOURNAL; PROSTATE CANCER; PULSE GENERATOR; REVIEW; RNA INTERFERENCE; SARCOIDOSIS; SARCOMA; SOLID TUMOR; SUBCUTANEOUS MELANOMA;

BIOPHYSICS; CLINICAL TRIALS AS TOPIC; CYTOPLASM; ELECTROCHEMISTRY; ELECTRODES; GENE THERAPY; HUMANS; MEDICAL ONCOLOGY; MICRORNAS; NEOPLASMS; OLIGONUCLEOTIDES; RNA INTERFERENCE; SEQUENCE ANALYSIS, DNA;

EID: 84855185769     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (86)

1. Bumcrot D, Manoharan M, Koteliansky V and Sah DW: RNAi therapeutics: a potential new class of pharmaceutical drugs. Nat Chem Biol 2: 711-719, 2006. (Pubitemid 44764213)
2. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE and Mello CC: Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-811, 1998. (Pubitemid 28099681)
3. Lee RC, Feinbaum RL and Ambros V: The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75: 843-854, 1993. (Pubitemid 24014542)
4. Tong AW, Zhang YA and Nemunaitis J: Small interfering RNA for experimental cancer therapy. Curr Opin MoI Ther 7: 114-124, 2005. (Pubitemid 40514680)
5. Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297, 2004.
6. Carthew RW and Sontheimer EJ: Origins and mechanisms of miRNAs and siRNAs. Cell 136: 642-655, 2009.
7. Cemazar M, Golzio M, Escoffre JM, Couderc B, Sersa G and Teissie J: In vivo imaging of tumor growth after electrochemotherapy with cisplatin. Biochem Biophys Res Commun 348: 997-1002, 2006. (Pubitemid 44233513)
8. Cemazar M, Golzio M, Sersa G, Hojman P, Kranjc S, Mesojednik S, Rols MP and Teissie J: Control by pulse parameters of DNA electrotransfer into solid tumors in mice. Gene Ther 16: 635-644, 2009.
9. Golzio M, Mazzolini L, Paganin-Gioanni A and Teissie J: Targeted gene silencing into solid tumors with electrically mediated siRNA delivery. Methods Mol Biol 555: 15-27, 2009.
10. Coster HG: A quantitative analysis of the voltage-current relationships of fixed charge membranes and the associated property of "punch- through". Biophys J 5: 669-686, 1965.
11. Teissie J, Golzio M and Rols MP: Mechanisms of cell membrane electropermeabilization: a minireview of our present (lack of ?) knowledge. Biochim Biophys Acta 1724: 270-280, 2005. (Pubitemid 41080035)
12. Wells DJ: Gene therapy progress and prospects: electroporation and other physical methods. Gene Ther 11: 1363-1369, 2004.
13. Heller LC and Heller R: In vivo electroporation for gene therapy. Hum Gene Ther 17: 890-897, 2006. (Pubitemid 46076749)
14. Todorovic V, Sersa G, Mlakar V, Glavac D, Flisar K and Cemazar M: Metastatic potential of melanoma cells is not affected by electrochemotherapy. Melanoma Res 21: 196-205, 2011.
15. Mlakar V, Todorovic V, Cemazar M, Glavac D and Sersa G: Electric pulses used in electrochemotherapy and electrogene therapy do not significantly change the expression profile of genes involved in the development of cancer in malignant melanoma cells. BMC Cancer 9: 299, 2009.
16. Mir LM, Glass LF, Sersa G, Teissie J, Domenge C, Miklavcic D, Jaroszeski MJ, Orlowski S, Reintgen DS, Rudolf Z, Belehradek M, Gilbert R, Rols MP, Belehradek J Jr., Bachaud JM, DeConti R, Stabuc B, Cemazar M, Coninx P and Heller R: Effective treatment of cutaneous and subcutaneous malignant tumours by electrochemotherapy. Br J Cancer 77: 2336-2342, 1998. (Pubitemid 28263963)
17. Sersa G, Stabuc B, Cemazar M, Miklavcic D and Rudolf Z: Electrochemotherapy with cisplatin: the systemic antitumour effectiveness of cisplatin can be potentiated locally by the application of electric pulses in the treatment of malignant melanoma skin metastases. Melanoma Res 10: 381-385, 2000.
18. Gothelf A, Mir LM and Gehl J: Electrochemotherapy: results of cancer treatment using enhanced delivery of bleomycin by electroporation. Cancer Treat Rev 29: 371-387, 2003. (Pubitemid 37185104)
19. Sersa G, Miklavcic D, Cemazar M, Rudolf Z, Pucihar G and Snoj M: Electrochemotherapy in treatment of tumours. Eur J Surg Oncol 34: 232-240, 2008.
20. Daud AI, DeConti RC, Andrews S, Urbas P, Riker AI, Sondak VK, Munster PN, Sullivan DM, Ugen KE, Messina JL and Heller R: Phase I trial of interleukin-12 plasmid electroporation in patients with metastatic melanoma. J Clin Oncol 26: 5896-5903, 2008.
21. Bodles-Brakhop AM, Heller R and Draghia-Akli R: Electroporation for the delivery of DNA-based vaccines and immunotherapeutics: current clinical developments. Mol Ther 17: 585-592, 2009.
22. Castanotto D and Rossi JJ: The promises and pitfalls of RNA-interference-based therapeutics. Nature 457: 426-433, 2009.
23. Sigoillot FD and King RW: Vigilance and validation: Keys to success in RNAi screening. ACS Chem Biol 6: 47-60, 2011.
24. Heidel JD, Hu S, Liu XF, Triche TJ and Davis ME: Lack of interferon response in animals to naked siRNAs. Nat Biotechnol 22: 1579-1582, 2004. (Pubitemid 40039462)
25. Zhang L, Nolan E, Kreitschitz S and Rabussay DP: Enhanced delivery of naked DNA to the skin by non-invasive in vivo electroporation. Biochim Biophys Acta 1572: 1-9, 2002. (Pubitemid 35229983)
26. Kishida T, Asada H, Gojo S, Ohashi S, Shin-Ya M, Yasutomi K, Terauchi R, Takahashi KA, Kubo T, Imanishi J and Mazda O: Sequence-specific gene silencing in murine muscle induced by electroporation-mediated transfer of short interfering RNA. J Gene Med 6: 105-110, 2004. (Pubitemid 40228008)
27. Golzio M, Mazzolini L, Moller P, Rols MP and Teissie J: Inhibition of gene expression in mice muscle by in vivo electrically mediated siRNA delivery. Gene Ther 12: 246-251, 2005. (Pubitemid 40220626)
28. Akaneya Y, Jiang B and Tsumoto T: RNAi-induced gene silencing by local electroporation in targeting brain region. J Neurophysiol 93: 594-602, 2005. (Pubitemid 40626864)
29. Inoue A, Takahashi KA, Mazda O, Terauchi R, Arai Y, Kishida T, Shin-Ya M, Asada H, Morihara T, Tonomura H, Ohashi S, Kajikawa Y, Kawahito Y, Imanishi J, Kawata M and Kubo T: Electro-transfer of small interfering RNA ameliorated arthritis in rats. Biochem Biophys Res Commun 336: 903-908, 2005. (Pubitemid 41338354)
30. Matsuda T and Cepko CL: Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc Natl Acad Sci USA 101: 16-22, 2004. (Pubitemid 38084195)
31. Takabatake Y, Isaka Y, Mizui M, Kawachi H, Shimizu F, Ito T, Hori M and Imai E: Exploring RNA interference as a therapeutic strategy for renal disease. Gene Ther 12: 965-973, 2005. (Pubitemid 40903418)
32. Nakai N, Kishida T, Shin-Ya M, Imanishi J, Ueda Y, Kishimoto S and Mazda O: Therapeutic RNA interference of malignant melanoma by electrotransfer of small interfering RNA targeting Mitf. Gene Ther 14: 357-365, 2007. (Pubitemid 46231929)
33. Golzio M, Mazzolini L, Ledoux A, Paganin A, Izard M, Hellaudais L, Bieth A, Pillaire MJ, Cazaux C, Hoffmann JS, Couderc B and Teissie J: In vivo gene silencing in solid tumors by targeted electrically mediated siRNA delivery. Gene Ther 14: 752-759, 2007. (Pubitemid 46585656)
34. Takei Y, Nemoto T, Mu P, Fujishima T, Ishimoto T, Hayakawa Y, Yuzawa Y, Matsuo S, Muramatsu T and Kadomatsu K: In vivo silencing of a molecular target by short interfering RNA electroporation: tumor vascularization correlates to delivery efficiency. Mol Cancer Ther 7: 211-221, 2008.
35. Lewis DL, Hagstrom JE, Loomis AG, Wolff JA and Herweijer H: Efficient delivery of siRNA for inhibition of gene expression in postnatal mice. Nat Genet 32: 107-108, 2002. (Pubitemid 34977204)
36. McCaffrey AP, Meuse L, Pham TT, Conklin DS, Hannon GJ and Kay MA: RNA interference in adult mice. Nature 418: 38-39, 2002. (Pubitemid 34742563)
37. Jackson AL and Linsley PS: Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application. Nat Rev Drug Discov 9: 57-67, 2010.
38. Stenvang J, Lindow M and Kauppinen S: Targeting of microRNAs for therapeutics. Biochem Soc Trans 36: 1197-1200, 2008.
39. Ambros V: microRNAs: tiny regulators with great potential. Cell 107: 823-826, 2001.
40. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, Downing JR, Jacks T, Horvitz HR and Golub TR: MicroRNA expression profiles classify human cancers. Nature 435: 834-838, 2005. (Pubitemid 40839735)
41. Hernando E: microRNAs and cancer: role in tumorigenesis, patient classification and therapy. Clin Transi Oncol 9: 155-160, 2007.
42. da Costa Martins PA, Salic K, Gladka MM, Armand AS, Leptidis S, El Azzouzi H, Hansen A, Coenen-de Roo CJ, Bierhuizen MF, van der Nagel R, van Kuik J, de Weger R, de Bruin A, Condorelli G, Arbones ML, Eschenhagen T and De Windt LJ: MicroRNA-199b targets the nuclear kinase Dyrk1a in an auto-amplification loop promoting calcineurin/NFAT signalling. Nat Cell Biol 12: 1220-1227, 2010.
43. Long J, Wang Y, Wang W, Chang BH and Danesh FR: Identification of microRNA-93 as a novel regulator of vascular endothelial growth factor in hyperglycemic conditions. J Biol Chem 285: 23457-23465, 2010.
44. Ji Q, Hao X, Meng Y, Zhang M, Desano J, Fan D and Xu L: Restoration of tumor suppressor miR-34 inhibits human p53-mutant gastric cancer tumorspheres. BMC Cancer 8: 266, 2008.
45. Matsubara H, Takeuchi T, Nishikawa E, Yanagisawa K, Hayashita Y, Ebi H, Yamada H, Suzuki M, Nagino M, Nimura Y, Osada H and Takahashi T: Apoptosis induction by antisense oligonucleotides against miR-17-5p and miR-20a in lung cancers overexpressing miR-17-92. Oncogene 26: 6099-6105, 2007. (Pubitemid 47373805)
46. Dalmay T: MicroRNAs and cancer. J Intern Med 263: 366-375, 2008.
47. Care A, Catalucci D, Felicetti F, Bonci D, Addario A, Gallo P, Bang ML, Segnalini, Gu Y, Dalton ND, Elia L, Latronico MV, Hoydal M, Autore C, Russo MA, Dorn GW 2nd, Ellingsen O, Ruiz-Lozano P, Peterson KL, Croce CM, Peschle C and Condorelli G: MicroRNA-133 controls cardiac hypertrophy. Nat Med 13: 613-618, 2007.
48. Mercatelli N, Coppola V, Bonci D, Miele F, Costantini A, Guadagnoli M, Bonanno E, Muto G, Frajese GV, De Maria R, Spagnoli LG, Farace MG and Ciafre SA: The inhibition of the highly expressed miR-221 and miR-222 impairs the growth of prostate carcinoma xenografts in mice. PLoS One 3: e4029, 2008.
49. Clape C, Fritz V, Henriquet C, Apparailly F, Fernandez PL, Iborra F, Avances C, Villalba M, Culine S and Fajas L: miR-143 interferes with ERK5 signaling, and abrogates prostate cancer progression in mice. PLoS One 4: e7542, 2009.
50. Corey DR: Chemical modification: the key to clinical application of RNA interference? J Clin Invest 117: 3615-3622, 2007.
51. Braasch DA, Jensen S, Liu Y, Kaur K, Arar K, White MA and Corey DR: RNA interference in mammalian cells by chemically-modified RNA. Biochemistry 42: 7967-7975, 2003. (Pubitemid 36807714)
52. Kumar R, Singh SK, Koshkin AA, Rajwanshi VK, Meldgaard M and Wengel J: The first analogues of LNA (locked nucleic acids): phosphorothioate-LNA and 2′-thio-LNA. Bioorg Med Chem Lett 8: 2219-2222, 1998. (Pubitemid 28561609)
53. Kaur H, Babu BR and Maiti S: Perspectives on chemistry and therapeutic applications of Locked Nucleic Acid (LNA). Chem Rev 107: 4672-4697, 2007. (Pubitemid 350225863)
54. Crinelli R, Bianchi M, Gentilini L and Magnani M: Design and characterization of decoy oligonucleotides containing locked nucleic acids. Nucleic Acids Res 30: 2435-2443, 2002. (Pubitemid 34618995)
55. Wahlestedt C, Salmi P, Good L, Kela J, Johnsson T, Hokfelt T, Broberger C, Porreca F, Lai J, Ren K, Ossipov M, Koshkin A, Jakobsen N, Skouv J, Oerum H, Jacobsen MH and Wengel J: Potent and nontoxic antisense oligonucleotides containing locked nucleic acids. Proc Natl Acad Sci USA 97: 5633-5638, 2000. (Pubitemid 30313770)
56. Lanford RE, Hildebrandt-Eriksen ES, Petri A, Persson R, Lindow M, Munk ME, Kauppinen S and Orum H: Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327: 198-201, 2010.
57. Paganin-Gioanni A, Bellard E, Escoffre JM, Rols MP, Teissie J and Golzio M: Direct visualization at the single-cell level of siRNA electrotransfer into cancer cells. Proc Natl Acad Sci USA 108: 10443-10447, 2011.
58. Paganin-Gioanni A, Bellard E, Couderc B, Teissie J and Golzio M: Tracking in vitro and in vivo siRNA electrotransfer in tumor cells. J RNAi Gene Silencing 4: 281-288, 2008.
59. Golzio M, Teissie J and Rols MP: Direct visualization at the single-cell level of electrically mediated gene delivery. Proc Natl Acad Sci USA 99: 1292-1297, 2002. (Pubitemid 34136486)
60. Escoffre JM, Portet T, Wasungu L, Teissie J, Dean D and Rols MP: What is (still not) known of the mechanism by which electroporation mediates gene transfer and expression in cells and tissues. Mol Biotechnol 41: 286-295, 2009.
61. Puc M, Kotnik T, Mir LM and Miklavcic D: Quantitative model of small molecules uptake after in vitro cell electropermeabilization. Bioelectrochemistry 60: 1-10, 2003. (Pubitemid 36945000)
62. Braasch DA, Liu Y and Corey DR: Antisense inhibition of gene expression in cells by oligonucleotides incorporating locked nucleic acids: effect of mRNA target sequence and chimera design. Nucleic Acids Res 30: 5160-5167, 2002. (Pubitemid 36033034)
63. Corsten MF, Miranda R, Kasmieh R, Krichevsky AM, Weissleder R and Shah K: MicroRNA-21 knockdown disrupts glioma growth in vivo and displays synergistic cytotoxicity with neural precursor cell delivered S-TRAIL in human gliomas. Cancer Res 67: 8994-9000, 2007. (Pubitemid 47535880)
64. Kis E, Olah J, Ocsai H, Baltas E, Gyulai R, Kemeny L and Horvath AR: Electrochemotherapy of cutaneous metastases of melanoma a case series study and systematic review of the evidence. Dermatol Surg 37: 816-824, 2011.
65. Mir LM, Devauchelle P, Quintin-Colonna F, Delisle F, Doliger S, Fradelizi D, Belehradek JJr and Orlowski S: First clinical trial of cat soft-tissue sarcomas treatment by electrochemotherapy. Br J Cancer 76: 1617-1622, 1997. (Pubitemid 27520591)
66. Rols MP, Tamzali Y and Teissie J: Electrochemotherapy of horses. A preliminary clinical report. Bioelectrochemistry 55: 101-105, 2002. (Pubitemid 34084760)
67. Aihara H and Miyazaki J: Gene transfer into muscle by electroporation in vivo. Nat Biotechnol 16: 867-870, 1998. (Pubitemid 28405859)
68. Mir LM, Bureau MF, Gehl J, Rangara R, Rouy D, Caillaud JM, Delaere P, Branellec D, Schwartz, B and Scherman D: High-efficiency gene transfer into skeletal muscle mediated by electric pulses. Proc Natl Acad Sci USA 96: 4262-4267, 1999. (Pubitemid 29190324)
69. Dean DA: Nonviral gene transfer to skeletal, smooth, and cardiac muscle in living animals. Am J Physiol Cell Physiol 289: C233-245, 2005.
70. Heller R, Jaroszeski M, Atkin A, Moradpour D, Gilbert R, Wands J and Nicolau C: In vivo gene electroinjection and expression in rat liver. FEBS Lett 389: 225-228, 1996. (Pubitemid 26251823)
71. Liu F and Huang L: Electric gene transfer to the liver following systemic administration of plasmid DNA. Gene Ther 9: 1116-1119, 2002.
72. Titomirov AV, Sukharev S and Kistanova E: In vivo electroporation and stable transformation of skin cells of newborn mice by plasmid DNA. Biochim Biophys Acta 1088: 131-134, 1991.
73. Vandermeulen G, Staes E, Vanderhaeghen ML, Bureau MF, Scherman D and Preat V: Optimisation of intradermal DNA electrotransfer for immunisation. J Control Release 124: 81-87, 2007. (Pubitemid 350088207)
74. Tupin E, Poirier B, Bureau MF, Khallou-Laschet J, Vranckx R, Caligiuri G, Gaston AT, Duong Van Huyen JP, Scherman D, Bariety J, Michel JB and Nicoletti A: Non-viral gene transfer of murine spleen cells achieved by in vivo electroporation. Gene Ther 10: 569-579, 2003. (Pubitemid 36432608)
75. Isaka Y, Yamada K, Takabatake Y, Mizui M, Miura-Tsujie M, Ichimaru N, Yazawa K, Utsugi R, Okuyama A, Hori M, Imai E and Takahara S: Electroporation-mediated HGF gene transfection protected the kidney against graft injury. Gene Ther 12: 815-820, 2005. (Pubitemid 40753973)
76. Saito T and Nakatsuji N: Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev Biol 240: 237-246, 2001. (Pubitemid 33141120)
77. Khoury M, Bigey P, Louis-Plence P, Noel D, Rhinn H, Scherman D, Jorgensen C and Apparailly F: A comparative study on intra-articular versus systemic gene electrotransfer in experimental arthritis. J Gene Med 8: 1027-1036, 2006. (Pubitemid 44282999)
78. Bureau MF, Gehl J, Deleuze V, Mir LM and Scherman D: Importance of association between permeabilization and electrophoretic forces for intramuscular DNA electrotransfer. Biochim Biophys Acta 1474: 353-359, 2000. (Pubitemid 30209876)
79. Satkauskas S, Bureau MF, Puc M, Mahfoudi A, Scherman D, Miklavcic D and Mir LM: Mechanisms of in vivo DNA electrotransfer: respective contributions of cell electropermeabilization and DNA electrophoresis. Mol Ther 5: 133-140, 2002. (Pubitemid 34144829)
80. Mazeres S, Sel D, Golzio M, Pucihar G, Tamzali Y, Miklavcic D and Teissie J: Non invasive contact electrodes for in vivo localized cutaneous electropulsation and associated drug and nucleic acid delivery. J Control Release 134: 125-131, 2009.
81. Gehl J, Sorensen TH, Nielsen K, Raskmark P, Nielsen SL, Skovsgaard T and Mir LM: In vivo electroporation of skeletal muscle: threshold, efficacy and relation to electric field distribution. Biochim Biophys Acta 1428: 233-240, 1999. (Pubitemid 29352271)
82. Gilbert RA, Jaroszeski MJ and Heller R: Novel electrode designs for electrochemotherapy. Biochim Biophys Acta 1334: 9-14, 1997. (Pubitemid 27063940)
83. Spugnini EP, Citro G and Porrello A: Rational design of new electrodes for electrochemotherapy. J Exp Clin Cancer Res 24: 245-254, 2005. (Pubitemid 41039609)
84. Pavselj N and Miklavcic D: A numerical model of permeabilized skin with local transport regions. IEEE Trans Biomed Eng 55: 1927-1930, 2008. (Pubitemid 351871646)
85. Davis ME, Zuckerman JE, Choi CH, Seligson D, Tolcher A, Alabi CA, Yen Y, Heidel JD and Ribas A: Evidence of RNAi in humans from systemically administered siRNA via targeted nanoparticles. Nature 464: 1067-1070, 2010.
86. Aleku M, Schulz P, Keil O, Santel A, Schaeper U, Dieckhoff B, Janke O, Endruschat J, Durieux B, Roder N, Loffler K, Lange C, Fechtner M, Mopert K, Fisch G, Dames S, Arnold W, Jochims K, Giese K, Wiedenmann B, Scholz A and Kaufmann J: Atu027, a liposomal small interfering RNA formulation targeting protein kinase N3, inhibits cancer progression. Cancer Res 68: 9788-9798, 2008.