Plasmid DNA electrotransfer for intracellular and secreted proteins expression: new methodological developments and applications
Abstract
In vivo electrotransfer is a physical method of gene delivery in various tissues and organs, relying on the injection of a plasmid DNA followed by electric pulse delivery. The importance of the association between cell permeabilization and DNA electrophoresis for electrotransfer efficiency has been highlighted. In vivo electrotransfer is of special interest since it is the most efficient non‐viral strategy of gene delivery and also because of its low cost, easiness of realization and safety. The potentiality of this technique can be further improved by optimizing plasmid biodistribution in the targeted organ, plasmid structure, and the design of the encoded protein. In particular, we found that plasmids of smaller size were electrotransferred more efficiently than large plasmids. It is also of importance to study and understand kinetic expression of the transgene, which can be very variable, depending on many factors including cellular localization of the protein, physiological activity and regulation. The most widely targeted tissue is skeletal muscle, because this strategy is not only promising for the treatment of muscle disorders, but also for the systemic secretion of therapeutic proteins. Vaccination and oncology gene therapy are also major fields of application of electrotransfer, whereas application to other organs such as liver, brain and cornea are expanding. Many published studies have shown that plasmid electrotransfer can lead to long‐lasting therapeutic effects in various pathologies such as cancer, blood disorders, rheumatoid arthritis or muscle ischemia. DNA electrotransfer is also a powerful laboratory tool to study gene function in a given tissue. Copyright © 2004 John Wiley & Sons, Ltd.
Number of times cited: 70
- Shinobu Tsuchiya, Mirei Chiba, Koshi N. Kishimoto, Harukazu Nakamura, Masahiro Tsuchiya and Haruhide Hayashi, Transfer of the bone morphogenetic protein 4 gene into rat periodontal ligament by in vivo electroporation, Archives of Oral Biology, 10.1016/j.archoralbio.2016.11.013, 74, (123-132), (2017).
- Richard Heller, Justin Teissie, Marie-Pierre Rols, Julie Gehl, Gregor Sersa, Lluis M. Mir, Robert E. Neal, Suyashree Bhonsle, Rafael Davalos, Stephen Beebe, Barbara Hargrave, Richard Nuccitelli, Chunqi Jiang, Maja Cemazar, Youssef Tamzali and Natasa Tozon, Medical Applications, Bioelectrics, 10.1007/978-4-431-56095-1_5, (275-388), (2016). 2016 IEEE 7th Latin American Symposium on Circuits & Systems (LASCAS) Florianopolis, Brazil 2016 IEEE 7th Latin American Symposium on Circuits & Systems (LASCAS) IEEE , (2016). 978-1-4673-7835-2 Lucenara dos Santos Pereira and Daniela Ota Hisayasu Suzuki Effects of nanoelectroporation on plasma and nuclear membranes , (2016). 351 354 7451082 , 10.1109/LASCAS.2016.7451082 http://ieeexplore.ieee.org/document/7451082/
- Léa L Lesueur, Lluis M Mir and Franck M André, Overcoming the Specific Toxicity of Large Plasmids Electrotransfer in Primary Cells In Vitro, Molecular Therapy - Nucleic Acids, 5, (e291), (2016).
- Serena Stanga, Nadège Zanou, Emilie Audouard, Bernadette Tasiaux, Sabrina Contino, Gaëlle Vandermeulen, Frédérique René, Jean-Philippe Loeffler, Frédéric Clotman, Philippe Gailly, Ilse Dewachter, Jean-Noël Octave and Pascal Kienlen-Campard, APP-dependent glial cell line-derived neurotrophic factor gene expression drives neuromuscular junction formation, The FASEB Journal, 30, 5, (1696), (2016).
- Daniel Dory, Vincent Le Moigne, Roland Cariolet, Véronique Béven, André Keranflec’h and André Jestin, Targeted Collection of Plasmid DNA in Large and Growing Animal Muscles 6 Weeks after DNA Vaccination with and without Electroporation, Journal of Immunology Research, 2015, (1), (2015).
- Ursa Lampreht, Urska Kamensek, Monika Stimac, Gregor Sersa, Natasa Tozon, Masa Bosnjak, Andreja Brozic, Geraldo Gileno de Sá Oliveira, Takayuki Nakagawa, Kohei Saeki and Maja Cemazar, Gene Electrotransfer of Canine Interleukin 12 into Canine Melanoma Cell Lines, The Journal of Membrane Biology, 248, 5, (909), (2015).
- Gaëlle Vandermeulen, Catherine Uyttenhove, Etienne De Plaen, Benoît J. Van den Eynde and Véronique Préat, Intramuscular electroporation of a P1A-encoding plasmid vaccine delays P815 mastocytoma growth, Bioelectrochemistry, 10.1016/j.bioelechem.2013.11.002, 100, (112-118), (2014).
- S. Mahindhoratep, H. Ait Bouda, Nelly El Shafey, D. Scherman, A. Kichler, Ch. Pichon, P. Midoux, N. Mignet and M.F. Bureau, NF-kB related transgene expression in mouse tibial cranial muscle after pDNA injection followed or not by electrotransfer, Biochimica et Biophysica Acta (BBA) - General Subjects, 10.1016/j.bbagen.2014.06.013, 1840, 11, (3257-3263), (2014).
- M Quiviger, A Arfi, D Mansard, L Delacotte, M Pastor, D Scherman and C Marie, High and prolonged sulfamidase secretion by the liver of MPS-IIIA mice following hydrodynamic tail vein delivery of antibiotic-free pFAR4 plasmid vector, Gene Therapy, 10.1038/gt.2014.75, 21, 12, (1001-1007), (2014).
- Daekee Kwon, Gwang-Sik Kang, Dong Keun Han, Kwideok Park, Jae-Hwan Kim and Soo-Hong Lee, Establishment and characterization of human engineered cells stably expressing large extracellular matrix proteins, Archives of Pharmacal Research, 37, 1, (149), (2014).
- Yan Luo, Jun Liu, Yongsheng Wang, Jianmin Su, Yongyan Wu, Guangdong Hu, Mingqing Gao, Fusheng Quan and Yong Zhang, PhiC31 integrase‐mediated genomic integration and stable gene expression in the mouse mammary gland after gene electrotransfer, The Journal of Gene Medicine, 15, 10, (356-365), (2013).
- Sophie Chabot, Muriel Golzio and Justin Teissié, Tissue‐Targeted Gene Electrodelivery of Minicircle DNA, Minicircle and Miniplasmid DNA Vectors, (203-213), (2013).
- Shixia Wang and Shan Lu, DNA Immunization, Current Protocols in Molecular Biology, 31, 1, (18.3.1-18.3.24), (2013).
- Vanessa Joubert, Franck M. André, Marco Schmeer, Martin Schleef and Lluis M. Mir, Increased Efficiency of Minicircles Versus Plasmids Under Gene Electrotransfer Suboptimal Conditions: An Influence of the Extracellular Matrix, Minicircle and Miniplasmid DNA Vectors, (215-225), (2013).
- Corinne Marie, Mickaël Quiviger, Helen Foster, George Dickson and Daniel Scherman, Plasmid‐Based Medicinal Products – Focus on pFAR: A Miniplasmid Free of Antibiotic Resistance Markers, Minicircle and Miniplasmid DNA Vectors, (37-58), (2013).
- Felipe Maglietti, Sebastian Michinski, Nahuel Olaiz, Marcelo Castro, Cecilia Suárez, Guillermo Marshall and Maria Rosaria Scarfi, The Role of Ph Fronts in Tissue Electroporation Based Treatments, PLoS ONE, 8, 11, (e80167), (2013).
- S Chabot, J Orio, M Schmeer, M Schleef, M Golzio and J Teissié, Minicircle DNA electrotransfer for efficient tissue-targeted gene delivery, Gene Therapy, 10.1038/gt.2011.215, 20, 1, (62-68), (2012).
- Eva Brand, Kathrin Ralla and Peter Neubauer, Strategies for Plasmid DNA Production in Escherichia coli , Biopharmaceutical Production Technology, (1-41), (2012).
- Celine Baligand, Gregory Jouvion, Olivier Schakman, Helene Gilson, Claire Wary, Jean‐Paul Thissen and Pierre G. Carlier, Multiparametric functional nuclear magnetic resonance imaging shows alterations associated with plasmid electrotransfer in mouse skeletal muscle, The Journal of Gene Medicine, 14, 9-10, (598-608), (2012).
- Michel F. Bureau, Luc Wasungu, Lauriane Jugé, Daniel Scherman, Marie‐Pierre Rols and Nathalie Mignet, Investigating relationship between transfection and permeabilization by the electric field and/or the Pluronic® L64 in vitro and in vivo, The Journal of Gene Medicine, 14, 3, (204-215), (2012).
- Sascha Kopic, Maximilian E. H. Wagner, Christoph Griessenauer, Thenral Socrates, Markus Ritter and John P. Geibel, Vacuolar-type H+-ATPase-mediated proton transport in the rat parietal cell, Pflügers Archiv - European Journal of Physiology, 463, 3, (419), (2012).
- Gaëlle Vandermeulen, Takis Athanasopoulos, Anita Trundley, Keith Foster, Véronique Préat, Rafael J. Yáñez-Muñoz and George Dickson, Highly potent delivery method of gp160 envelope vaccine combining lentivirus-like particles and DNA electrotransfer, Journal of Controlled Release, 159, 3, (376), (2012).
- A D Kandasamy, M M Sung, J J Boisvenue, A J Barr and J R B Dyck, Adiponectin gene therapy ameliorates high-fat, high-sucrose diet-induced metabolic perturbations in mice, Nutrition & Diabetes, 2, 9, (e45), (2012).
- Natalie A. Hutnick, Devin J.F. Myles, Bernadette Ferraro, Colleen Lucke, Feng Lin, Jian Yan, Kate E. Broderick, Amir S. Khan, Niranjian Y. Sardesai and David B. Weiner, Intradermal DNA Vaccination Enhanced by Low-Current Electroporation Improves Antigen Expression and Induces Robust Cellular and Humoral Immune Responses, Human Gene Therapy, 23, 9, (943), (2012).
- Gao Sun and Guy A Rutter, Targeting the AMP-regulated kinase family to treat diabetes: a research update, Diabetes Management, 1, 3, (333), (2011).
- Gaëlle Vandermeulen, Corinne Marie, Daniel Scherman and Véronique Préat, New Generation of Plasmid Backbones Devoid of Antibiotic Resistance Marker for Gene Therapy Trials, Molecular Therapy, 10.1038/mt.2011.182, 19, 11, (1942-1949), (2011).
- Julien Verrax, Florence Defresne, Florence Lair, Gaëlle Vandermeulen, Géraldine Rath, Chantal Dessy, Véronique Préat and Olivier Feron, Delivery of Soluble VEGF Receptor 1 (sFlt1) by Gene Electrotransfer as a New Antiangiogenic Cancer Therapy, Molecular Pharmaceutics, 8, 3, (701), (2011).
- Lior Dassau, Lisa R. Conti, Carolyn M. Radeke, Louis J. Ptáček and Carol A. Vandenberg, Kir2.6 Regulates the Surface Expression of Kir2.x Inward Rectifier Potassium Channels, Journal of Biological Chemistry, 286, 11, (9526), (2011).
- Kaustubh A. Jinturkar, Mohan N. Rathi and Ambikanandan Misra, Gene Delivery Using Physical Methods, Challenges in Delivery of Therapeutic Genomics and Proteomics, 10.1016/B978-0-12-384964-9.00003-7, (83-126), (2011).
- Kazuki Yamaguchi, Loreto B. Feril, Katsuro Tachibana, Akira Takahashi, Miki Matsuo, Hitomi Endo, Yoshimi Harada and Juichiro Nakayama, Ultrasound-mediated interferon β gene transfection inhibits growth of malignant melanoma, Biochemical and Biophysical Research Communications, 411, 1, (137), (2011).
- Corinne Marie, Gaëlle Vandermeulen, Mickaël Quiviger, Magali Richard, Véronique Préat and Daniel Scherman, pFARs, Plasmids free of antibiotic resistance markers, display high‐level transgene expression in muscle, skin and tumour cells, The Journal of Gene Medicine, 12, 4, (323-332), (2010).
- Anne Denys, Allan Thiolat, Delphyne Descamps, Delphine Lemeiter, Karim Benihoud, Nakacha Bessis and Marie‐Christophe Boissier, Intra‐articular electrotransfer of mouse soluble tumour necrosis factor receptor in a murine model of rheumatoid arthritis, The Journal of Gene Medicine, 12, 8, (659-668), (2010).
- Jochen De Vry, Pilar Martínez-Martínez, Mario Losen, Gerard H Bode, Yasin Temel, Thomas Steckler, Harry WM Steinbusch, Marc De Baets and Jos Prickaerts, Low Current-driven Micro-electroporation Allows Efficient In Vivo Delivery of Nonviral DNA into the Adult Mouse Brain, Molecular Therapy, 18, 6, (1183), (2010).
- Jochen De Vry, Pilar Martínez-Martínez, Mario Losen, Yasin Temel, Thomas Steckler, Harry W.M. Steinbusch, Marc H. De Baets and Jos Prickaerts, In vivo electroporation of the central nervous system: A non-viral approach for targeted gene delivery, Progress in Neurobiology, 10.1016/j.pneurobio.2010.10.001, 92, 3, (227-244), (2010).
- Yun-Zhou Yu, Na Li, Shuang Wang, Wei-Yuan Yu and Zhi-Wei Sun, Improved immunogenicity and protective efficacy of a replicon DNA vaccine encoding the Hc domain of botulinum neurotoxin serotype A by electric pulses and protein boosting, Immunopharmacology and Immunotoxicology, 31, 3, (397), (2009).
- James A. Williams, Aaron E. Carnes and Clague P. Hodgson, Plasmid DNA vaccine vector design: Impact on efficacy, safety and upstream production, Biotechnology Advances, 10.1016/j.biotechadv.2009.02.003, 27, 4, (353-370), (2009).
- Kazuki Yamaguchi, Loreto B. Feril, Yoshimi Harada, Hitomi Endo, Yutaka Irie, Juichiro Nakayama and Katsuro Tachibana, Growth inhibition of neurofibroma by ultrasound-mediated interferon γ transfection, Journal of Medical Ultrasonics, 36, 1, (3), (2009).
- Jean-Michel Escoffre, Thomas Portet, Luc Wasungu, Justin Teissié, David Dean and Marie-Pierre Rols, What is (Still not) Known of the Mechanism by Which Electroporation Mediates Gene Transfer and Expression in Cells and Tissues, Molecular Biotechnology, 41, 3, (286), (2009).
- Hélène Gilson, Olivier Schakman, Stéphanie Kalista, Pascale Lause, Kunihiro Tsuchida and Jean-Paul Thissen, Follistatin induces muscle hypertrophy through satellite cell proliferation and inhibition of both myostatin and activin, American Journal of Physiology-Endocrinology and Metabolism, 297, 1, (E157), (2009).
- Joshua W. Henshaw and Fan Yuan, Field distribution and DNA transport in solid tumors during electric field‐mediated gene delivery, Journal of Pharmaceutical Sciences, 97, 2, (691-711), (2007).
- Jun-ichiro Jo and Yasuhiko Tabata, Non-viral gene transfection technologies for genetic engineering of stem cells, European Journal of Pharmaceutics and Biopharmaceutics, 10.1016/j.ejpb.2007.04.021, 68, 1, (90-104), (2008).
- Shixia Wang, Chunghua Zhang, Lu Zhang, Jun Li, Zuhu Huang and Shan Lu, The relative immunogenicity of DNA vaccines delivered by the intramuscular needle injection, electroporation and gene gun methods, Vaccine, 26, 17, (2100), (2008).
- C. Bloquel, A. Denys, M. C. Boissier, F. Apparailly, P. Bigey, D. Scherman and N. Bessis, Intra‐articular electrotransfer of plasmid encoding soluble TNF receptor variants in normal and arthritic mice, The Journal of Gene Medicine, 9, 11, (986-993), (2007).
- Gra??yna Klupi??ska, Tomasz Poplawski, J??zef Drzewoski, Agnieszka Harasiuk, Russel J. Reiter, Janusz Blasiak and Jan Chojnacki, Therapeutic Effect of Melatonin in Patients With Functional Dyspepsia, Journal of Clinical Gastroenterology, 41, 3, (270), (2007).
- Feng Liu, Demet Sag, Jue Wang, Lisa M Shollenberger, Feilong Niu, Xing Yuan, Shyh-Dar Li, Mike Thompson and Paul Monahan, Sine-wave Current for Efficient and Safe In Vivo Gene Transfer, Molecular Therapy, 10.1038/sj.mt.6300261, 15, 10, (1842-1847), (2007).
- Gaëlle Vandermeulen, Edith Staes, Marie Lise Vanderhaeghen, Michel Francis Bureau, Daniel Scherman and Véronique Préat, Optimisation of intradermal DNA electrotransfer for immunisation, Journal of Controlled Release, 124, 1-2, (81), (2007).
- Yoka H. Kusumanto, Nanno H. Mulder, Wendy A. Dam, Mario H. Losen, Coby Meijer and Geke A. P. Hospers, Improvement of In Vivo Transfer of Plasmid DNA in Muscle: Comparison of Electroporation versus Ultrasound , Drug Delivery, 10.1080/10717540601098807, 14, 5, (273-277), (2008).
- H Guo, J C K Leung, L Y Y Chan, A W L Tsang, M F Lam, H Y Lan and K N Lai, Ultrasound-contrast agent mediated naked gene delivery in the peritoneal cavity of adult rat, Gene Therapy, 14, 24, (1712), (2007).
- Riad Antoine Bejjani, Charlotte Andrieu, Carole Bloquel, Marianne Berdugo, David BenEzra and Francine Behar-Cohen, Electrically Assisted Ocular Gene Therapy, Survey of Ophthalmology, 52, 2, (196), (2007).
- David Cukjati, Danute Batiuskaite, Franck André, Damijan Miklavčič and Lluis M. Mir, Real time electroporation control for accurate and safe in vivo non-viral gene therapy, Bioelectrochemistry, 70, 2, (501), (2007).
- Loreto B. Feril, Ryohei Ogawa, Katsuro Tachibana and Takashi Kondo, Optimized ultrasound‐mediated gene transfection in cancer cells, Cancer Science, 97, 10, (1111-1114), (2006).
- Masa‐Aki Shibata, Yuko Ito, Junji Morimoto, Ken Kusakabe, Ryoji Yoshinaka and Yoshinori Otsuki, In vivo electrogene transfer of interleukin‐12 inhibits tumor growth and lymph node and lung metastases in mouse mammary carcinomas, The Journal of Gene Medicine, 8, 3, (335-352), (2005).
- Emmanuelle E. Fabre, Pascal Bigey, Cécile Orsini and Daniel Scherman, Comparison of promoter region constructs for in vivo intramuscular expression, The Journal of Gene Medicine, 8, 5, (636-645), (2006).
- Marie-Pierre Rols, Electropermeabilization, a physical method for the delivery of therapeutic molecules into cells, Biochimica et Biophysica Acta (BBA) - Biomembranes, 1758, 3, (423), (2006).
- Laurent Grossin, Christel Cournil-Henrionnet, Astrid Pinzano, Nadège Gaborit, Dominique Dumas, Stéphanie Etienne, Jean François Stoltz, Bernard Terlain, Patrick Netter, Lluis M. Mir and Pierre Gillet, Gene transfer with HSP 70 in rat chondrocytes confers cytoprotection in vitro and during experimental osteoarthritis, The FASEB Journal, 20, 1, (65), (2006).
- Anna-Karin Roos, Sonia Moreno, Christoph Leder, Maxim Pavlenko, Alan King and Pavel Pisa, Enhancement of cellular immune response to a prostate cancer DNA vaccine by intradermal electroporation, Molecular Therapy, 13, 2, (320), (2006).
- Wolfgang Jechlinger, Optimization and delivery of plasmid DNA for vaccination, Expert Review of Vaccines, 5, 6, (803), (2006).
- K Foster, H Foster and J G Dickson, Gene therapy progress and prospects: Duchenne muscular dystrophy, Gene Therapy, 10.1038/sj.gt.3302877, 13, 24, (1677-1685), (2006).
- Gérald J. Prud'homme, DNA vaccination against tumors, The Journal of Gene Medicine, 7, 1, (3-17), (2004).
- Anne-Cécile Durieux, Régis Bonnefoy and Damien Freyssenet, Kinetic of transgene expression after electrotransfer into skeletal muscle: Importance of promoter origin/strength, Biochimica et Biophysica Acta (BBA) - General Subjects, 1725, 3, (403), (2005).
- A Leroy-Willig, M F Bureau, D Scherman and P G Carlier, In vivo NMR imaging evaluation of efficiency and toxicity of gene electrotransfer in rat muscle, Gene Therapy, 12, 19, (1434), (2005).
- Xue-Dong Wang, Jian-Guo Tang, Xiao-lei Xie, Ji-Chun Yang, Shuai Li, Jian-Guo Ji and Jun Gu, A comprehensive study of optimal conditions for naked plasmid DNA transfer into skeletal muscle by electroporation, The Journal of Gene Medicine, 7, 9, (1235), (2005).
- D. Castell, R. Bagin, B. Goldlust, J. Major and B. Hepburn, Comparison of the effects of immediate-release omeprazole powder for oral suspension and pantoprazole delayed-release tablets on nocturnal acid breakthrough in patients with symptomatic gastro-oesophageal reflux disease, Alimentary Pharmacology and Therapeutics, 21, 12, (1467), (2005).
- Emilie Phez, Cécile Faurie, Muriel Golzio, Justin Teissié and Marie-Pierre Rols, New insights in the visualization of membrane permeabilization and DNA/membrane interaction of cells submitted to electric pulses, Biochimica et Biophysica Acta (BBA) - General Subjects, 10.1016/j.bbagen.2005.04.005, 1724, 3, (248-254), (2005).
- E P Papapetrou, N C Zoumbos and A Athanassiadou, Genetic modification of hematopoietic stem cells with nonviral systems: past progress and future prospects, Gene Therapy, 10.1038/sj.gt.3302626, 12, (S118-S130), (2005).
- C. Faurie, M. Golzio, E. Phez, J. Teissié and M.-P. Rols, Electric Field-Induced Cell Membrane Permeabilization and Gene Transfer: Theory and Experiments, Engineering in Life Sciences, 5, 2, (179), (2005).
- F André and L M Mir, DNA electrotransfer: its principles and an updated review of its therapeutic applications, Gene Therapy, 10.1038/sj.gt.3302367, 11, S1, (S33-S42), (2004).
- D J Wells, Gene Therapy Progress and Prospects: Electroporation and other physical methods, Gene Therapy, 11, 18, (1363), (2004).
- Eric M. Jacobson, Erlinda Concepcion, Kenneth Ho, Peter Kopp, Jussara Vono Toniolo, Yaron Tomer and Marian Ludgate, cDNA Immunization of Mice with Human Thyroglobulin Generates Both Humoral and T Cell Responses: A Novel Model of Thyroid Autoimmunity, PLoS ONE, 10.1371/journal.pone.0019200, 6, 4, (e19200), (2011).




