journal article·2022-10-25Open access

Electroporation in Clinical Applications—The Potential of Gene Electrotransfer and Electrochemotherapy

Katarzyna Rakoczy, Monika Kisielewska, Mikołaj Sędzik, Laura Jonderko, Julia Celińska, Natalia Sauer, Wojciech Szlasa, Jolanta Saczko, Vitalij Novickij, Julita Kulbacka

Applied Sciences· Volume 12· Issue 21

Abstract

Electroporation (EP) allows for the transport of molecules into the cytoplasm with significant effectiveness by forming transient pores in the cell membrane using electric pulses. This can be used for cellular transport (RE—reversible electroporation) or ablation (IRE—irreversible electroporation). The first of described options fortifies medicine with novel possibilities: electrochemotherapy (ECT), which creates promising perspectives for cancer treatment, and gene electrotransfer (GET), a powerful method of DNA delivery as well as immunogen electrotransfer. The review constitutes a comprehensive explanation of the mechanism of EP in the case of GET, its present and prospective employment in medicine, including gene delivery, vaccinations, therapy, and transfection, are also presented.
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Research context

OpenAlex topics: Microbial Inactivation Methods · Transgenic Plants and Applications · Microfluidic and Bio-sensing Technologies

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Faculty of Medicine, Wroclaw Medical University, Pasteura 1, 50-367 Wroclaw, Poland

Department of Molecular and Cellular Biology, Faculty of Pharmacy, Wroclaw Medical University, Borowska 211A, 50-556 Wroclaw, Poland

Institute of High Magnetic Fields, Vilnius Gediminas Technical University, Naugarduko 41, 03227 Vilnius, Lithuania

Department of Immunology, State Research Institute Centre for Innovative Medicine, Santariškių 5, 08410 Vilnius, Lithuania

Funding

Statutory Subsidy Funds of the Department of Molecular and Cellular Biology

References (100+)

Show source-provided references
1. What do drug transporters really do?10.1038/nrd4461 ↗
2. Secondary Active Transporters10.1007/978-3-030-18768-2_9 ↗
3. Electroporation-Mediated Gene Delivery10.1016/bs.adgen.2014.10.003 ↗
4. Intracellular delivery by membrane disruption: Mechanisms, strategies, and concepts10.1021/acs.chemrev.7b00678 ↗
5. Electroporation theory. Concepts and mechanisms
6. Electroporation for the efficient transfection of mammalian cells with DNA10.1093/nar/15.3.1311 ↗
7. DNA transfection by electroporation10.1101/pdb.prot095471 ↗
8. Chemically induced mutagenesis in a shuttle vector with a low-background mutant frequency10.1073/pnas.83.10.3402 ↗
9. The effect of electroporation type pulsed electric fields on DNA in aqueous solution10.1177/153303461000900412 ↗
10. Electroporation10.1101/pdb.top096271 ↗
11. High electrical field effects on cell membranes10.1016/j.bioelechem.2006.10.004 ↗
12. Membrane Electroporation and Electropermeabilization: Mechanisms and Models10.1146/annurev-biophys-052118-115451 ↗
13. Theory of electroporation of planar bilayer membranes: Predictions of the aqueous area, change in capacitance, and pore-pore separation10.1016/S0006-3495(94)80453-9 ↗
14. Membrane Electroporation: A Molecular Dynamics Simulation10.1529/biophysj.104.050617 ↗
15. Electroporation and shock-induced transmembrane potential in a cardiac fiber during defibrillation strength shocks10.1114/1.101 ↗
16. “Classical” Electropermeabilization Modeling at the Cell Scale10.1007/s00285-012-0629-3 ↗
17. Effect of electric fields on light-scattering and fluorescence of chromaffin granules10.1007/BF01870624 ↗
18. Conducting and permeable states of cell membrane submitted to high voltage pulses: Mathematical and numerical studies validated by the experiments10.1016/j.jtbi.2014.06.027 ↗
19. Kinetics of permeability changes induced by electric impulses in chromaffin granules10.1007/BF01905221 ↗
20. Electric field-mediated fusion and related electrical phenomena10.1016/0304-4157(82)90007-7 ↗
21. Microtubule Cytoskeleton Remodeling by Nanosecond Pulsed Electric Fields10.1002/adbi.202000070 ↗
22. Phosphorus-31 NMR analysis of membrane phospholipid organization in viable, reversibly electropermeabilized Chinese hamster ovary cells10.1021/bi00404a023 ↗
23. Varnai, R., Koskinen, L., Mäntylä, L., Szabo, I., FitzGerald, L., and Sipeky, C. (2019). Pharmacogenomic Biomarkers in Docetaxel Treatment of Prostate Cancer: From Discovery to Implementation. Genes, 10.10.3390/genes10080599 ↗
24. Nanosecond field alignment of head group and water dipoles in electroporating phospholipid bilayers10.1021/jp077148q ↗
25. Mechanisms of cell membrane electropermeabilization: A minireview of our present (lack of?) knowledge10.1016/j.bbagen.2005.05.006 ↗
26. Cell death due to electroporation—A review10.1016/j.bioelechem.2021.107871 ↗
27. Irreversible electroporation: Evolution of a laboratory technique in interventional oncology
28. Irreversible electroporation in medicine10.1177/153303460700600401 ↗
29. A study of the immunological response to tumor ablation with irreversible electroporation10.1177/153303460700600406 ↗
30. Electrochemotherapy as a new modality in interventional oncology: A review10.1177/1533033818785329 ↗
31. Electrochemotherapy with bleomycin for basal cell carcinomas: A systematic review10.1111/jdv.17492 ↗
32. Electrochemotherapy and Ablative Therapies in Non-melanoma Skin Cancer10.1016/j.clon.2019.08.010 ↗
33. Electrochemotherapy: From the drawing board into medical practice10.1186/1475-925X-13-29 ↗
34. Electro-gene-transfer: A new approach for muscle gene delivery10.1023/A:1022927822244 ↗
35. Shi, J., Ma, Y., Zhu, J., Chen, Y., Sun, Y., Yao, Y., Yang, Z., and Xie, J. (2018). A Review on Electroporation-Based Intracellular Delivery. Molecules, 23.10.3390/molecules23113044 ↗
36. Clinical potential of electroporation for gene therapy and DNA vaccine delivery10.1517/17425247.2016.1121990 ↗
37. Chemically modified oligonucleotide-increased stability negatively correlates with its efficacy despite efficient electrotransfer10.1007/s00232-012-9468-9 ↗
38. Electric field orientation for gene delivery using high-voltage and low-voltage pulses10.1007/s00232-012-9475-x ↗
39. Pulmonary gene delivery—Realities and possibilities10.1177/1535370220965985 ↗
40. Venkatesh, A., Ma, S., Langellotto, F., Gao, G., and Punzo, C. (2013). Retinal gene delivery by rAAV and DNA electroporation. Curr. Protoc. Microbiol.10.1002/9780471729259.mc14d04s28 ↗
41. Answered and Unanswered Questions in Early-Stage Viral Vector Transduction Biology and Innate Primary Cell Toxicity for Ex-Vivo Gene Editing10.3389/fimmu.2021.660302 ↗
42. Immune responses to AAV vectors: Overcoming barriers to successful gene therapy10.1182/blood-2013-01-306647 ↗
43. Immunogenicity and toxicity of AAV gene therapy10.3389/fimmu.2022.975803 ↗
44. Cell-selective viral gene delivery vectors for the vasculature10.1113/expphysiol.2004.028126 ↗
45. Gene transfer to skeletal muscle by site-specific delivery of electroporation and ultrasound10.1016/j.bbrc.2012.06.090 ↗
46. Gene Electrotransfer: A Mechanistic Perspective10.2174/1566523216666160331130040 ↗
47. Gene electrotransfer: From biophysical mechanisms to in vivo applications: Part 1- Biophysical mechanisms10.1007/s12551-009-0022-7 ↗
48. Towards the mechanisms for efficient gene transfer into cells and tissues by means of cell electroporation10.1517/14712598.2012.654775 ↗
49. Mechanisms involved in gene electrotransfer using high- and low-voltage pulses—An in vitro study10.1016/j.bioelechem.2008.09.002 ↗
50. Efficiency of high- and low-voltage pulse combinations for gene electrotransfer in muscle, liver, tumor, and skin10.1089/hum.2008.060 ↗
51. Control by pulse parameters of DNA electrotransfer into solid tumors in mice10.1038/gt.2009.10 ↗
52. Endocytosis and Endosomal Trafficking of DNA After Gene Electrotransfer In Vitro10.1038/mtna.2015.59 ↗
53. The role of electrically stimulated endocytosis in gene electrotransfer10.1016/j.bioelechem.2011.08.005 ↗
54. New era of electrochemotherapy in treatment of liver tumors in conjunction with immunotherapies10.3748/wjg.v27.i48.8216 ↗
55. Remic, T., Sersa, G., Ursic, K., Cemazar, M., and Kamensek, U. (2020). Development of Tumor Cell-Based Vaccine with IL-12 Gene Electrotransfer as Adjuvant. Vaccines, 8.10.3390/vaccines8010111 ↗
56. Mutational burden, MHC-I expression and immune infiltration as limiting factors for in situ vaccination by TNFα and IL-12 gene electrotransfer10.1016/j.bioelechem.2021.107831 ↗
57. DNA vaccine for cancer immunotherapy10.4161/21645515.2014.980686 ↗
58. Electrochemotherapy of tumors as in situ vaccination boosted by immunogene electrotransfer10.1007/s00262-015-1724-2 ↗
59. Plasmid IL-12 electroporation in melanoma10.4161/hv.22573 ↗
60. IL-12 plasmid delivery by in vivo electroporation for the successful treatment of established subcutaneous B16.F10 melanoma10.1006/mthe.2002.0601 ↗
61. Potentiation of electrochemotherapy effectiveness by immunostimulation with IL-12 gene electrotransfer in mice is dependent on tumor immune status10.1016/j.jconrel.2021.03.009 ↗
62. Gene Electrotransfer of Plasmid-Encoding IL-12 Recruits the M1 Macrophages and Antigen-Presenting Cells Inducing the Eradication of Aggressive B16F10 Murine Melanoma
63. Electrochemotherapy (ECT) and irreversible electroporation (IRE)-advanced techniques for treating deep-seated tumors based on electroporation10.1186/1475-925X-14-S3-I1 ↗
64. Toxicity of anticancer agents mediated by electroporation in vitro10.1097/00001813-200003000-00008 ↗
65. Electrochemotherapy with bleomycin and cisplatin enhances cytotoxicity in primary and metastatic uveal melanoma cell lines in vitro10.4149/neo_2018_170329N227 ↗
66. Feasibility and safety of electrochemotherapy (ECT) in the pancreas: A pre-clinical investigation10.1515/raon-2015-0013 ↗
67. The use of high-frequency short bipolar pulses in cisplatin electrochemotherapy in vitro10.2478/raon-2019-0025 ↗
68. Gene electrotransfer of IL-2 and IL-12 plasmids effectively eradicated murine B16.F10 melanoma10.1016/j.bioelechem.2021.107843 ↗
69. New generation of plasmid backbones devoid of antibiotic resistance marker for gene therapy trials10.1038/mt.2011.182 ↗
70. Kos, S., Bosnjak, M., Jesenko, T., Markelc, B., Kamensek, U., Znidar, K., Matkovic, U., Rencelj, A., Sersa, G., and Hudej, R. (2021). Non-Clinical In Vitro Evaluation of Antibiotic Resistance Gene-Free Plasmids Encoding Human or Murine IL-12 Intended for First-in-Human Clinical Study. Pharmaceutics, 13.10.3390/pharmaceutics13101739 ↗
71. Maintenance and gene electrotransfer efficiency of antibiotic resistance gene-free plasmids encoding mouse, canine and human interleukin-12 orthologues10.1016/j.heliyon.2022.e08879 ↗
72. Evaluation of p21 promoter for interleukin 12 radiation induced transcriptional targeting in a mouse tumor model10.1186/1476-4598-12-136 ↗
73. Intradermal delivery of plasmid VEGF(165) by electroporation promotes wound healing10.1038/mt.2009.12 ↗
74. Skin electroporation of a plasmid encoding hCAP-18/LL-37 host defense peptide promotes wound healing10.1038/mt.2013.258 ↗
75. Electroporation-mediated delivery of a naked DNA plasmid expressing VEGF to the porcine heart enhances protein expression10.1038/gt.2009.153 ↗
76. Ayuni, E.L., Gazdhar, A., Giraud, M.N., Kadner, A., Gugger, M., Cecchini, M., Caus, T., Carrel, T.P., Schmid, R.A., and Tevaearai, H.T. (2011). In Vivo Electroporation Mediated Gene Delivery to the Beating Heart. PLoS ONE, 5.10.1371/journal.pone.0014467 ↗
77. Electroporation-mediated gene transfer directly to the swine heart10.1038/gt.2012.15 ↗
78. Electroporation as a method for high-level nonviral gene transfer to the lung10.1038/sj.gt.3302053 ↗
79. Targeted gene transfer of hepatocyte growth factor to alveolar type II epithelial cells reduces lung fibrosis in rats10.1089/hum.2012.098 ↗
80. da Luz, J.C.D.S., Antunes, F., Clavijo-Salomon, M.A., Signori, E., Tessarollo, N.G., and Strauss, B.E. (2021). Clinical Applications and Immunological Aspects of Electroporation-Based Therapies. Vaccines, 9.10.3390/vaccines9070727 ↗
81. Intratumoral plasmid IL-12 electroporation therapy in advanced melanoma patients induces systemic and intratumoral T cell responses: T cell responses induced by plasmid IL-12 electroporation10.1158/2326-6066.CIR-19-0359 ↗
82. Shi, G., Edelblute, C., Arpag, S., Lundberg, C., and Heller, R. (2018). IL-12 Gene Electrotransfer Triggers a Change in Immune Response within Mouse Tumors. Cancers, 10.10.3390/cancers10120498 ↗
83. Pre-clinical investigation of the synergy effect of interleukin-12 gene-electro-transfer during partially irreversible electropermeabilization against melanoma10.1186/s40425-019-0638-5 ↗
84. IL-12 gene therapy using an electrically mediated nonviral approach reduces metastatic growth of melanoma10.1089/104454903322624966 ↗
85. Local and systemic antitumor effect of intratumoral and peritumoral IL-12 electrogene therapy on murine sarcoma10.4161/cbt.8.22.9734 ↗
86. Potentiation of electrochemotherapy by intramuscular IL-12 gene electrotransfer in murine sarcoma and carcinoma with different immunogenicity10.2478/v10019-012-0044-9 ↗
87. Antitumor in situ vaccination effect of TNFα and IL-12 plasmid DNA electrotransfer in a murine melanoma model10.1007/s00262-018-2133-0 ↗
88. Electroporation-mediated IL-12 gene therapy in a transplantable canine cancer model10.1002/ijc.24418 ↗
89. Efficacy and safety of electrochemotherapy combined with peritumoral IL-12 gene electrotransfer of canine mast cell tumours10.1111/vco.12208 ↗
90. Phase I Trial of Interleukin-12 Plasmid Electroporation in Patients With Metastatic Melanoma10.1200/JCO.2007.15.6794 ↗
91. Regression of subcutaneous B16 melanoma tumors after intratumoral delivery of an IL-15-expressing plasmid followed by in vivo electroporation10.1038/sj.cgt.7700973 ↗
92. Shirley, S.A., Lundberg, C.G., and Heller, R. (2020). Electrotransfer of IL-15/IL-15Rα Complex for the Treatment of Established Melanoma. Cancers, 12.10.3390/cancers12103072 ↗
93. Gene electrotransfer of proinflammatory chemokines CCL5 and CCL17 as a novel approach of modifying cytokine expression profile in the tumor microenvironment10.1016/j.bioelechem.2021.107795 ↗
94. Electrogenetherapy of B16.F10 murine melanoma tumors with an interleukin-28 expressing DNA plasmid10.4161/hv.22560 ↗
95. Electrochemotherapy of skin metastases from malignant melanoma: A PRISMA-compliant systematic review10.1007/s10585-022-10180-9 ↗
96. Electrochemotherapy in the treatment of melanoma skin metastases: A report on 31 cases
97. The use of electrochemotherapy in combination with immunotherapy in the treatment of metastatic melanoma: A focused review10.1111/ijd.14314 ↗
98. Electroporation-enhanced delivery of nucleic acid vaccines10.1586/14760584.2015.990890 ↗
99. Electroporation delivery of DNA vaccines: Prospects for success10.1016/j.coi.2011.03.008 ↗
100. Calcium Electrotransfer for Termination of Transgene Expression in Muscle10.1089/hum.2010.209 ↗