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Drug Delivery Letters

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ISSN (Print): 2210-3031
ISSN (Online): 2210-304X

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Review Article

Electroporation: An Effective Method For In Vivo Gene Delivery

Author(s): Arash Nikyar and Azam Bolhassani*

Volume 12, Issue 1, 2022

Published on: 30 March, 2022

Page: [35 - 45] Pages: 11

DOI: 10.2174/2210303112666220127113328

Price: $65

Abstract

Background: Gene therapy is a promising approach for the treatment of various diseases, including cancer, hereditary disorders, and some viral infections.

The development of efficient and safe gene delivery systems is essential for facilitating gene transfer to various organs and tissues in vivo.

Objective: In this review, we briefly describe the principal mechanisms of gene delivery systems, particularly electroporation, and discuss the latest advancements in the application of electroporation for in vivo gene transfer.

Methods: A narrative review of all the relevant publication known to the authors was conducted.

Results: In recent years, electroporation-based strategies have emerged as an auspicious and versatile platform for efficient and controlled delivery of various biomolecules, including nucleic acids. Applying electric pulses of enough magnitude leads to the formation of hydrophilic pores in the cell membrane and allows the entry of otherwise membrane-impermeant molecules, such as DNA. Although electroporation has been initially developed for in vitro transfection of cells, it has recently advanced to preclinical in vivo applications and finally to clinical trials.

Conclusion: Electroporation has already entered the clinical practice for antitumor therapy and may be an essential part of future personalized treatments. Given the ability of electroporation to deliver multiple genes in a single event, it will also certainly be further developed both as a stand-alone delivery approach and when coupled with other technologies.

Keywords: Electroporation, gene transfer techniques, gene therapy, transfection, gene delivery, antitumor therapy.

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[1]
Duckert, B.; Vinkx, S.; Braeken, D.; Fauvart, M. Single-cell transfection technologies for cell therapies and gene editing. J. Control. Release, 2021, 963-975.
[http://dx.doi.org/10.1016/j.jconrel.2020.10.068]
[2]
Huo, S.; Li, H.; Boersma, A.J.; Herrmann, A. DNA nanotechnology enters cell membranes. In: Advanced Science; John Wiley and Sons Inc., 2019, 6, pp. 1900043.
[3]
Sheikh, S.; Coutts, A.S.; La Thangue, N.B. Transfection. Basic Science Methods for Clinical Researchers; Elsevier Inc., 2017, pp. 191-209.
[http://dx.doi.org/10.1016/B978-0-12-803077-6.00011-4]
[4]
Kim, T.K.; Eberwine, J.H. Mammalian cell transfection: the present and the future. Anal. Bioana.l Chem., 2010, 397(8), 3173.
[http://dx.doi.org/10.1007/s00216-010-3821-6]
[5]
Stepanenko, A.A.; Heng, H.H. Transient and stable vector transfection: Pitfalls, off-target effects, artifacts. Mutat. Res. Rev. Mutat. Res., 2017, 773, 91-103.
[6]
Hasan, M.M.; Ragnarsson, L.; Cardoso, F.C.; Lewis, R.J. Transfection methods for high-throughput cellular assays of voltage-gated calcium and sodium channels involved in pain. PLoS One, 2021, 16, e0243645.
[http://dx.doi.org/10.1371/journal.pone.0243645]
[7]
Nikyar, A.; Bolhassani, A.; Rouhollah, F.; Heshmati, M. Construction of a prokaryotic expression vector harboring two HIV-1 accessory genes. Med. Lab. J., 2021, 15(2), 11-17.
[8]
Rostami, B.; Irani, S.; Bolhassani, A.; Cohan, R.A. Gene and protein delivery using four cell penetrating peptides for HIV-1 vaccine development. IUBMB Life, 2019, 71, 1619-1633.
[9]
Kristensen, M.; Nielsen, H.M. Cell-penetrating peptides as tools to enhance non-injectable delivery of biopharmaceuticals. Tissue Barriers, 2016, 4(2), e1178369.
[10]
Taylor, R.E.; Zahid, M. Cell penetrating peptides, novel vectors for gene therapy. Pharmaceutics, 2020, 12(3), E225.
[http://dx.doi.org/10.3390/pharmaceutics12030225] [PMID: 32138146]
[11]
Pearson, S.; Jia, H.; Kandachi, K. China approves first gene therapy. Nat. Biotechnol., 2004, 22(1), 3-4.
[http://dx.doi.org/10.1038/nbt0104-3]
[12]
Elegheert, J.; Behiels, E.; Scott, S.; Woolley, R.E.; Griffiths, S.C. Lentiviral transduction of mammalian cells for fast, scalable and high-level production of soluble and membrane proteins. Nat. Protoc., 2018, 13, 2991-3017.
[13]
Chong, Z.X.; Yeap, S.K.; Ho, W.Y. Transfection types, methods and strategies: a technical review. PeerJ, 2021, 9, e11165.
[http://dx.doi.org/10.7717/peerj.11165]
[14]
Lee, C.S.; Bishop, E.S.; Zhang, R.; Yu, X.; Farina, E.M.; Yan, S. Adenovirus-mediated gene delivery: Potential applications for gene and cell-based therapies in the new era of personalized medicine. Genes Dis., 2017, 4, 43-63.
[15]
Zabaleta, N.; Salas, D.; Paramo, M.; Hommel, M.; Sier-Ferreira, V.; Hernandez-Alcoceba, R.; Prieto, J.; Bilbao, J.I.; Gonzalez-Aseguinolaza, G. Improvement of adeno-associated virus-mediated liver transduction efficacy by regional administration in Macaca fascicularis. Hum. Gene Ther. Clin. Dev., 2017, 28(2), 68-73.
[http://dx.doi.org/10.1089/humc.2016.183] [PMID: 28285544]
[16]
Lundstrom, K. Viral vectors for COVID-19 vaccine development. Viruses, 2021, 13, 317.
[17]
Jones, I.; Roy, P. Sputnik V. COVID-19 vaccine candidate appears safe and effective. Lancet, 2021, 397(10275), 642-643.
[http://dx.doi.org/10.1016/S0140-6736(21)00191-4] [PMID: 33545098]
[18]
Kaygisiz, K.; Synatschke, C.V. Materials promoting viral gene delivery. Biomater. Sci., 2020, 8(22), 6113-6156.
[http://dx.doi.org/10.1039/D0BM01367F] [PMID: 33025967]
[19]
Kida, H.; Nishimura, K.; Ogawa, K.; Watanabe, A.; Feril, L.B.; Irie, Y.; Endo, H.; Kawakami, S.; Tachibana, K. Nanobubble mediated gene delivery in conjunction with a hand-held ultrasound scanner. Front. Pharmacol., 2020, 11, 363.
[http://dx.doi.org/10.3389/fphar.2020.00363] [PMID: 32300298]
[20]
Shapiro, G.; Wong, A.W.; Bez, M.; Yang, F.; Tam, S.; Even, L.; Sheyn, D.; Ben-David, S.; Tawackoli, W.; Pelled, G.; Ferrara, K.W.; Gazit, D. Multiparameter evaluation of in vivo gene delivery using ultrasound-guided, microbubble-enhanced sonoporation. J. Control. Release, 2016, 223, 157-164.
[http://dx.doi.org/10.1016/j.jconrel.2015.12.001] [PMID: 26682505]
[21]
Chen, Z.; Du, M.; Yan, F. Recent advances about local gene delivery by ultrasound. In: Uchiumi, F. (Eds.). Gene Expression and Control. London: IntechOpen; 2018.
[http://dx.doi.org/10.5772/intechopen.80036]
[22]
Schneckenburger, H. Laser-assisted optoporation of cells and tissues – A mini-review. Biomed. Opt. Express, 2019, 10(6), 2883.
[23]
Pylaev, T.; Vanzha, E.; Avdeeva, E.; Khlebtsov, B.; Khlebtsov, N. A novel cell transfection platform based on laser optoporation mediated by Au nanostar layers. J. Biophotonics, 2019, 12(1), e201800166.
[http://dx.doi.org/10.1002/jbio.201800166] [PMID: 30203552]
[24]
Fajrial, A.K.; He, Q.Q.; Wirusanti, N.I.; Slansky, J.E.; Ding, X. A review of emerging physical transfection methods for CRISPR/Cas9-mediated gene editing. Theranostics, 2020, 10, 5532-5549.
[25]
Chow, Y.T.; Chen, S.; Wang, R.; Liu, C.; Kong, C.W.; Li, R.A.; Cheng, S.H.; Sun, D. Single cell transfection through precise microinjection with quantitatively controlled injection volumes. Sci. Rep., 2016, 6(1), 24127.
[http://dx.doi.org/10.1038/srep24127] [PMID: 27067121]
[26]
Yen, M.C.; Lai, M.D. Biolistic DNA delivery to mice with the low pressure gene gun. Methods Mol. Biol., 2013, 940, 169-174.
[http://dx.doi.org/10.1007/978-1-62703-110-3_14] [PMID: 23104342]
[27]
Miller, K.; Eggenberger, A.L.; Lee, K.; Liu, F.; Kang, M.; Drent, M.; Ruba, A.; Kirscht, T.; Wang, K.; Jiang, S. An improved biolistic delivery and analysis method for evaluation of DNA and CRISPR-Cas delivery efficacy in plant tissue. Sci. Rep., 2021, 11(1), 7695.
[http://dx.doi.org/10.1038/s41598-021-86549-9] [PMID: 33833247]
[28]
Zhao, H.; Avenarius, M.R.; Gillespie, P.G. Improved biolistic transfection of hair cells. PLoS One, 2012, 7(10), e46765.
[http://dx.doi.org/10.1371/journal.pone.0046765] [PMID: 23049715]
[29]
Neumann, E.; Schaefer-Ridder, M.; Wang, Y.; Hofschneider, P.H. Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J., 1982, 1(7), 841-845.
[http://dx.doi.org/10.1002/j.1460-2075.1982.tb01257.x] [PMID: 6329708]
[30]
Cooper, G.M. Structure of the Plasma Membrane, 2000. Available from: https://www.ncbi.nlm.nih.gov/books/NBK9898/
[31]
Shi, J.; Ma, Y.; Zhu, J.; Chen, Y.; Sun, Y.; Yao, Y. A review on electroporation-based intracellular delivery. Molecules, 2018, 23(11), 3044.
[32]
Napotnik, T.B.; Polajžer, T. Miklavčič, D. Cell death due to electroporation - A review. Bioelectrochemistry, 2021, 141, 107871.
[http://dx.doi.org/10.1016/j.bioelechem.2021.107871] [PMID: 34147013]
[33]
Yarmush, M.L.; Golberg, A.; Serša, G.; Kotnik, T. Miklavčič, D. Electroporation-based technologies for medicine: Principles, applications, and challenges. Annu. Rev. Biomed. Eng., 2014, 16, 295-320.
[34]
Au, J.T.; Mittra, A.; Song, T.J.; Cavnar, M.; Jun, K.; Carson, J.; Gholami, S.; Haddad, D.; Gaujoux, S.; Monette, S.; Ezell, P.; Wolchok, J.; Fong, Y. Irreversible electroporation facilitates gene transfer of a GM-CSF plasmid with a local and systemic response. Surgery, 2013, 154(3), 496-503.
[http://dx.doi.org/10.1016/j.surg.2013.06.005] [PMID: 23972655]
[35]
Geboers, B.; Scheffer, H.J.; Graybill, P.M.; Ruarus, A.H.; Nieuwenhuizen, S.; Puijk, R.S.; van den Tol, P.M.; Davalos, R.V.; Rubinsky, B.; de Gruij, T.D. Miklavčič, D.; Meijerink, M.R.; High-voltage electrical pulses in oncology: Irreversible electroporation, electrochemotherapy, gene electrotransfer, electrofusion, and electroimmunotherapy. Radiology, 2020, 295(2), 254-272.
[36]
Lambricht, L.; Lopes, A.; Kos, S.; Sersa, G.; Préat, V.; Vandermeulen, G. Clinical potential of electroporation for gene therapy and DNA vaccine delivery. Expert Opin. Drug Deliv., 2016, 13(2), 295-310.
[http://dx.doi.org/10.1517/17425247.2016.1121990] [PMID: 26578324]
[37]
Wells, D.J. Electroporation and ultrasound enhanced non-viral gene delivery in vitro and in vivo. Cell Biol. Toxicol., 2010, 26(1), 21-28.
[38]
Sherba, J.J.; Hogquist, S.; Lin, H.; Shan, J.W.; Shreiber, D.I.; Zahn, J.D. The effects of electroporation buffer composition on cell viability and electro-transfection efficiency. Sci. Rep., 2020, 10(1), 1-9.
[http://dx.doi.org/10.1038/s41598-020-59790-x]
[39]
Potočnik, T.; Miklavčič, D.; Maček Lebar, A. Effect of electroporation and recovery medium pH on cell membrane permeabilization, cell survival and gene transfer efficiency in vitro. Bioelectrochemistry, 2019, 130, 107342.
[http://dx.doi.org/10.1016/j.bioelechem.2019.107342] [PMID: 31404809]
[40]
Forjanič, T.; Miklavčič, D. Numerical study of gene electrotransfer efficiency based on electroporation volume and electrophoretic movement of plasmid DNA. Biomed. Eng. , 2018, 17(1), 1-10.
[http://dx.doi.org/10.1186/s12938-018-0515-3]
[41]
Cao, Y.; Ma, E.; Cestellos-Blanco, S.; Zhang, B.; Qiu, R.; Su, Y.; Doudna, J.A.; Yang, P. Nontoxic nanopore electroporation for effective intracellular delivery of biological macromolecules. Proc. Natl. Acad. Sci. USA, 2019, 116(16), 7899-7904.
[http://dx.doi.org/10.1073/pnas.1818553116] [PMID: 30923112]
[42]
Rosazza, C.; Haberl Meglic, S.; Zumbusch, A.; Rols, M.P.; Miklavcic, D. Gene electrotransfer: a mechanistic perspective. Curr. Gene Ther., 2016, 16(2), 98-129.
[http://dx.doi.org/10.2174/1566523216666160331130040]
[43]
Pavlin, M.; Kandušer, M. New insights into the mechanisms of gene electrotransfer - experimental and theoretical analysis. Sci. Rep., 2015, 5(1), 1-11.
[44]
Shirley, S.A.; Heller, R.; Heller, L.C. Gene ther cancer transl approaches from preclin stud to clin implement. In: Electroporation Gene Therapy, 2013; pp. 93-106.
[45]
Emerson, M.; Renwick, L.; Tate, S.; Rhind, S.; Milne, E. Transfection efficiency and toxicity following delivery of naked plasmid DNA and cationic lipid-DNA complexes to ovine lung segments. Mol. Ther., 2003, 8(4), 646-653.
[46]
Navarro-Quiroga, I.; Chittajallu, R.; Gallo, V.; Haydar, T.F. Long-term, selective gene expression in developing and adult hippocampal pyramidal neurons using focal in utero electroporation. J. Neurosci., 2007, 27(19), 5007-5011.
[http://dx.doi.org/10.1523/JNEUROSCI.0867-07.2007] [PMID: 17494686]
[47]
Niwa, M.; Kamiya, A.; Murai, R.; Kubo, K.; Gruber, A.J.; Tomita, K.; Lu, L.; Tomisato, S.; Jaaro-Peled, H.; Seshadri, S.; Hiyama, H.; Huang, B.; Kohda, K.; Noda, Y.; O’Donnell, P.; Nakajima, K.; Sawa, A.; Nabeshima, T. Knockdown of DISC1 by in utero gene transfer disturbs postnatal dopaminergic maturation in the frontal cortex and leads to adult behavioral deficits. Neuron, 2010, 65(4), 480-489.
[http://dx.doi.org/10.1016/j.neuron.2010.01.019] [PMID: 20188653]
[48]
Gubbels, S.P.; Woessner, D.W.; Mitchell, J.C.; Ricci, A.J.; Brigande, J.V. Functional auditory hair cells produced in the mammalian cochlea by in utero gene transfer. Nature, 2008, 455(7212), 537-541.
[http://dx.doi.org/10.1038/nature07265]
[49]
Miwa, T.; Minoda, R.; Ise, M.; Yamada, T.; Yumoto, E. Mouse otocyst transuterine gene transfer restores hearing in mice with connexin 30 deletion-associated hearing loss. Mol. Ther., 2013, 21(6), 1142-1150.
[http://dx.doi.org/10.1038/mt.2013.62] [PMID: 23587925]
[50]
Takeda, H.; Miwa, T.; Kim, M.Y.; Choi, B.Y.; Orita, Y.; Minoda, R. Prenatal electroporation-mediated gene transfer restores Slc26a4 knock-out mouse hearing and vestibular function. Sci. Rep., 2019, 9(1), 1-12.
[http://dx.doi.org/10.1038/s41598-019-54262-3]
[51]
Palanki, R.; Peranteau, W.H.; Mitchell, M.J. Delivery technologies for in utero gene therapy. Adv. Drug Deliv. Rev., 2021, 69, 51-62.
[http://dx.doi.org/10.1016/j.addr.2020.11.002]
[52]
Song, K-M.; Choi, M.J.; Kwon, M-H.; Ghatak, K.; Park, S-H.; Ryu, D-S.; Ryu, J.K.; Suh, J.K. Optimizing in vivo gene transfer into mouse corpus cavernosum by use of surface electroporation. Korean J. Urol., 2015, 56(3), 197-204.
[http://dx.doi.org/10.4111/kju.2015.56.3.197] [PMID: 25763123]
[53]
Pramod, R.K.; Mitra, A. Intratesticular injection followed by electroporation allows gene transfer in caprine spermatogenic cells. Sci. Rep., 2018, 8(1), 1-11.
[http://dx.doi.org/10.1038/s41598-018-21558-9]
[54]
de Miera, C.S.; Parr, E.; Denver, R.J. Bulk electroporationmediated gene transfer into xenopus tadpole brain. Cold Spring Harb. Protoc., 2018. Available from: http://cshprotocols.cshlp.org/content/2018/10/pdb.prot097691.full
[55]
Ohmura, N.; Kawasaki, K.; Satoh, T.; Hata, Y. In vivo electroporation to physiologically identified deep brain regions in postnatal mammals. Brain Struct. Funct., 2014, 220(3), 1307-1316.
[56]
Nomura, T.; Nishimura, Y.; Gotoh, H.; Ono, K. Rapid and efficient gene delivery into the adult mouse brain via focal electroporation. Sci. Rep., 2016, 6(1), 1-9.
[http://dx.doi.org/10.1038/srep29817]
[57]
de Melo, J.; Blackshaw, S. In vivo electroporation of developing mouse retina. J. Vis. Exp., 2011, (52), e2847.
[58]
de Melo, J.; Blackshaw, S. In vivo electroporation of developing mouse retina. Methods Mol. Biol., 2018, 1715, 101-111.
[http://dx.doi.org/10.1007/978-1-4939-7522-8_8]
[59]
Nickerson, J.M.; Goodman, P.; Chrenek, M.A.; Bernal, C.J.; Berglin, L.; Redmond, T.M.; Boatright, J.H. Subretinal delivery and electroporation in pigmented and nonpigmented adult mouse eyes. Methods Mol. Biol., 2012, 884, 53-69.
[http://dx.doi.org/10.1007/978-1-61779-848-1_4] [PMID: 22688698]
[60]
Schwarz, D.; Schaefer, A.T. Targeted in vivo electroporation using nanoengineered microelectrodes. Methods Mol. Biol., 2020, 2050, 113-120.
[http://dx.doi.org/10.1007/978-1-4939-9740-4_12] [PMID: 31468485]
[61]
Toualbi, L.; Toms, M.; Moosajee, M. The landscape of non-viral gene augmentation strategies for inherited retinal diseases. Int. J. Mol. Sci., 2021, 22(5), 2318.
[http://dx.doi.org/10.3390/ijms22052318]
[62]
Machado-Aranda, D.; Raghavendran, K. Electroporation-mediated delivery of genes in rodent models of lung contusion. Methods Mol. Biol., 2014, 1121, 205-221.
[http://dx.doi.org/10.1007/978-1-4614-9632-8_18] [PMID: 24510825]
[63]
Dean, D.A.; Barravecchia, M.; Danziger, B.; Lin, X. Use of electroporation for efficacious gene delivery to the lungs. ECS Trans., 2011, 35(7), 167.
[http://dx.doi.org/10.1149/1.3571989]
[64]
Dolgachev, V.A.; Goldberg, R.; Suresh, M.V.; Thomas, B.; Talarico, N.; Hemmila, M.R. Electroporation-mediated delivery of the FER gene in the resolution of trauma-related fatal pneumonia. Gene Ther., 2016, 23(11), 785.
[http://dx.doi.org/10.1038/gt.2016.58]
[65]
Dolgachev, V.; Panicker, S.; Balijepalli, S.; McCandless, L.K.; Yin, Y.; Swamy, S. Electroporation-mediated delivery of FER gene enhances innate immune response and improves survival in a murine model of pneumonia. Gene Ther., 2018, 25(5), 359-375.
[http://dx.doi.org/10.1038/s41434-018-0022-y]
[66]
Lin, X. Barravecchia, M.; Kothari, P.; Young, J.L.; Dean, D.A. β1-Na+,K+-ATPase gene therapy upregulates tight junctions to rescue lipopolysaccharide-induced acute lung injury. Gene Ther., 2016, 23(6), 489-499.
[67]
Barnett, R.C.; Lin, X.; Barravecchia, M.; Norman, R.A.; Bentley, K.L. de M.; Fazal, F. Featured article: electroporation-mediated gene delivery of surfactant protein B (SP-B) restores expression and improves survival in mouse model of SP-B deficiency. 2017, 242(13), 1345-1354.
[68]
Katayama, R.; Kimura, T.; Tomita, T.; Matsuno, H.; Morita, Y.; Matsushita, I.; Gejo, R. Efficient gene delivery to articular cartilage using electroporation. Mod. Rheumatol., 2003, 13(3), 243-249.
[69]
Grossin, L.; Cournil-Henrionnet, C.; Mir, L.M.; Liagre, B.; Dumas, D.; Etienne, S.; Guingamp, C.; Netter, P.; Gillet, P. Direct gene transfer into rat articular cartilage by in vivo electroporation. FASEB J., 2003, 17(8), 829-835.
[http://dx.doi.org/10.1096/fj.02-0518com] [PMID: 12724342]
[70]
Haag, J.; Voigt, R.; Soeder, S.; Aigner, T. Efficient non-viral transfection of primary human adult chondrocytes in a high-throughput format. Osteoarthritis Cartilage, 2009, 17(6), 813-817.
[http://dx.doi.org/10.1016/j.joca.2008.11.004] [PMID: 19056302]
[71]
Mir, L.M.; Moller, P.H.; André, F.; Gehl, J. Electric pulse-mediated gene delivery to various animal tissues. Adv. Genet., 2005, 54, 83-114.
[http://dx.doi.org/10.1016/S0065-2660(05)54005-7] [PMID: 16096009]
[72]
He, Z.; Leong, D.J.; Zhuo, Z.; Majeska, R.J.; Cardoso, L.; Spray, D.C.; Goldring, M.B.; Cobelli, N.J.; Sun, H.B. Strain-induced mechanotransduction through primary cilia, extracellular ATP, purinergic calcium signaling, and ERK1/2 transactivates CITED2 and downregulates MMP-1 and MMP-13 gene expression in chondrocytes. Osteoarthritis Cartilage, 2016, 24(5), 892-901.
[73]
Khoury, M.; Bigey, P.; Louis-Plence, P.; Noel, D.; Rhinn, H.; Scherman, D.; Jorgensen, C.; Apparailly, F. A comparative study on intra-articularversus systemic gene electrotransfer in experimental arthritis. J. Gene Med., 2006, 8(8), 1027-1036.
[http://dx.doi.org/10.1002/jgm.922] [PMID: 16733831]
[74]
Hsieh, M.K.; Wu, C.J.; Chen, C.C.; Tsai, T.T.; Niu, C.C.; Wu, S.C.; Lai, P.L. BMP-2 gene transfection of bone marrow stromal cells to induce osteoblastic differentiation in a rat calvarial defect model. Mater. Sci. Eng. C, 2018, 91, 806-816.
[http://dx.doi.org/10.1016/j.msec.2018.06.004] [PMID: 30033316]
[75]
Lee, E.; Ko, J-Y.; Kim, J.; Park, J-W.; Lee, S. Im, G-I. Osteogenesis and angiogenesis are simultaneously enhanced in BMP2-/VEGF-transfected adipose stem cells through activation of the YAP/TAZ signaling pathway. Biomater. Sci., 2019, 7(11), 4588-4602.
[http://dx.doi.org/10.1039/C9BM01037H] [PMID: 31435635]
[76]
Gantenbein, B.; Tang, S.; Guerrero, J.; Higuita-Castro, N.; Salazar-Puerta, A.I.; Croft, A.S.; Gazdhar, A.; Purmessur, D. Non-viral Gene delivery methods for bone and joints. Front. Bioeng. Biotechnol., 2020, 8, 598466.
[http://dx.doi.org/10.3389/fbioe.2020.598466] [PMID: 33330428]
[77]
Taylor, J.; Babbs, C.F.; Alzghoul, M.B.; Olsen, A.; Latour, M.; Pond, A.L. Optimization of ectopic gene expression in skeletal muscle through DNA transfer by electroporation. BMC Biotechnol., 2004, 4(1), 1-8.
[78]
Relaix, F.; Zammit, P.S. Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development, 2012, 139(16), 2845-2856.
[http://dx.doi.org/10.1242/dev.069088] [PMID: 22833472]
[79]
Mennuni, C.; Calvaruso, F.; Zampaglione, I.; Rizzuto, G.; Rinaudo, D.; Dammassa, E. Hyaluronidase increases electrogene transfer efficiency in skeletal muscle. Hum. Gene Ther., 2004, 13(3), 355-365.
[80]
Peri, D.; Deville, M.; Poignard, C.; Signori, E.; Natalini, R. Numerical optimization of plasmid DNA delivery combined with hyaluronidase injection for electroporation protocol. Comput. Methods Programs Biomed., 2020, 186, 105204.
[http://dx.doi.org/10.1016/j.cmpb.2019.105204] [PMID: 31760303]
[81]
Sokołowska, E.; Błachnio-Zabielska, A.U. A critical review of electroporation as a plasmid delivery system in mouse skeletal muscle. Int. J. Mol. Sci., 2019, 20(11), E2776.
[http://dx.doi.org/10.3390/ijms20112776] [PMID: 31174257]
[82]
Williams, P.D.; Kingston, P.A. Plasmid-mediated gene therapy for cardiovascular disease. Cardiovasc. Res., 2011, 91(4), 565-576.
[http://dx.doi.org/10.1093/cvr/cvr197] [PMID: 21742674]
[83]
Spugnini, E.P.; Scimeca, M.; Amadio, B.; Cortese, G.; Fanciulli, M.; Vincenzi, B. Definition of a novel plasmid-based gene transfection protocol of mammalian skeletal muscles by means of in vivo electroporation. Int. J. Mol. Sci., 2020, 21(18), 6494.
[http://dx.doi.org/10.3390/ijms21186494]
[84]
Martins, L.; Gallo, C.C.; Honda, T.S.B.; Alves, P.T.; Stilhano, R.S.; Rosa, D.S. Skeletal muscle healing by M1-like macrophages produced by transient expression of exogenous GM-CSF. Stem Cell Res. Ther., 2020, 11(1), 1-12.
[http://dx.doi.org/10.1186/s13287-020-01992-1]
[85]
Derenne, A.; Tassin, A.; Nguyen, T.H.; De Roeck, E.; Jenart, V.; Ansseau, E. Induction of a local muscular dystrophy using electroporation in vivo: an easy tool for screening therapeutics. Sci. Rep., 2020, 10, 11301.
[http://dx.doi.org/10.1038/s41598-020-68135-7]
[86]
Sutter, M.A.; Cremona, T.P.; Nita, I.; Cavarra, E.; Lungarella, G.; Lewis, E.C. In vivo electroporation-mediated, intrahepatic alpha1 antitrypsin gene transfer reduces pulmonary emphysema in pallid mice. Pharm., 2020, 12(9), 793.
[87]
Sharma, D.; Arora, S.; Singh, J.; Layek, B. A review of the tortuous path of nonviral gene delivery and recent progress. Int. J. Biol. Macromol., 2021, 183, 2055-2073.
[http://dx.doi.org/10.1016/j.ijbiomac.2021.05.192] [PMID: 34087309]
[88]
Babiuk, S.; Baca-Estrada, M.E.; Foldvari, M.; Middleton, D.M.; Rabussay, D.; Widera, G.; Babiuk, L.A. Increased gene expression and inflammatory cell infiltration caused by electroporation are both important for improving the efficacy of DNA vaccines. J. Biotechnol., 2004, 110(1), 1-10.
[http://dx.doi.org/10.1016/j.jbiotec.2004.01.015] [PMID: 15099900]
[89]
Calvet, C.Y.; André, F.M.; Mir, L.M. Dual therapeutic benefit of electroporation-mediated DNA vaccination in vivo: Enhanced gene transfer and adjuvant activity. OncoImmunology, 2014, 3(4), e28540.
[90]
Andrews, C.D.; Luo, Y.; Sun, M.; Yu, J.; Goff, A.J.; Glass, P.J.; Padte, N.N.; Huang, Y.; Ho, D.D. In vivo production of monoclonal antibodies by gene transfer via electroporation protects against lethal influenza and ebola infections. Mol. Ther. Methods Clin. Dev., 2017, 7, 74-82.
[http://dx.doi.org/10.1016/j.omtm.2017.09.003] [PMID: 29034261]
[91]
Cervia, L.D.; Yuan, F. Current progress in electrotransfection as a nonviral method for gene delivery. Mol. Pharm., 2018, 15(9), 3617-3624.
[http://dx.doi.org/10.1021/acs.molpharmaceut.8b00207] [PMID: 29889538]
[92]
Nagarsheth, N.; Wicha, M.S.; Zou, W. Chemokines in the cancer microenvironment and their relevance in cancer immunotherapy. Nat. Rev. Immunol., 2017, 17(9), 559-572.
[http://dx.doi.org/10.1038/nri.2017.49]
[93]
Burkart, C.; Mukhopadhyay, A.; Shirley, S.A.; Connolly, R.J.; Wright, J.H.; Bahrami, A. Improving therapeutic efficacy of IL-12 intratumoral gene electrotransfer through novel plasmid design and modified parameters. Gene Ther., 2018, 25(2), 93-103.
[94]
Cemazar, M.; Jarm, T.; Sersa, G. Cancer electrogene therapy with interleukin-12. Curr. Gene Ther., 2010, 10(4), 300-311.
[http://dx.doi.org/10.2174/156652310791823425] [PMID: 20560875]
[95]
Greaney, S.K.; Algazi, A.P.; Tsai, K.K.; Takamura, K.T.; Chen, L.; Twitty, C.G.; Zhang, L.; Paciorek, A.; Pierce, R.H.; Le, M.H.; Daud, A.I.; Fong, L. Intratumoral plasmid IL12 electroporation therapy in patients with advanced melanoma induces systemic and intratumoral T-cell responses. Cancer Immunol. Res., 2020, 8(2), 246-254.
[http://dx.doi.org/10.1158/2326-6066.CIR-19-0359] [PMID: 31852717]
[96]
Komel, T.; Bosnjak, M.; Kranjc Brezar, S.; De Robertis, M.; Mastrodonato, M.; Scillitani, G.; Pesole, G.; Signori, E.; Sersa, G.; Cemazar, M. Gene electrotransfer of IL-2 and IL-12 plasmids effectively eradicated murine B16.F10 melanoma. Bioelectrochemistry, 2021, 141, 107843.
[http://dx.doi.org/10.1016/j.bioelechem.2021.107843] [PMID: 34139572]
[97]
Mukhopadhyay, A.; Wright, J.; Shirley, S.; Canton, D.A.; Burkart, C.; Connolly, R.J.; Campbell, J.S.; Pierce, R.H. Characterization of abscopal effects of intratumoral electroporation-mediated IL-12 gene therapy. Gene Ther., 2019, 26(1-2), 1-15.
[http://dx.doi.org/10.1038/s41434-018-0044-5] [PMID: 30323352]
[98]
Kranjc, M.; Kranjc Brezar, S.; Serša, G. Miklavčič, D. Contactless delivery of plasmid encoding EGFP in vivo by high-intensity pulsed electromagnetic field. Bioelectrochemistry, 2021, 141, 107847.
[http://dx.doi.org/10.1016/j.bioelechem.2021.107847] [PMID: 34058542]

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