Advanced search
Publication Cover
Expert Opinion on Biological Therapy Volume 16, 2016 - Issue 1
Submit an article Journal homepage
247
Views
15
CrossRef citations to date
0
Altmetric
Reviews

Gene transfer by pulsed electric field is highly promising in cutaneous wound healing

Laure GibotInstitute of Pharmacology and Structural Biology (IPBS)- CNRS UMR5089, Toulouse, 31077, France;Université de Toulouse III, Toulouse, 31077, France
&
Marie-Pierre RolsInstitute of Pharmacology and Structural Biology (IPBS)- CNRS UMR5089, Toulouse, 31077, France;Université de Toulouse III, Toulouse, 31077, FranceCorrespondence[email protected]
Pages 67-77 | Published online: 29 Oct 2015

Bibliography

  • Rieger S, Zhao H, Martin P, et al. The role of nuclear hormone receptors in cutaneous wound repair. Cell Biochem Funct. 2015;33:1–13.
  • Gurtner GC, Werner S, Barrandon Y, et al. Wound repair and regeneration. Nature. 2008;453:314–321.
  • Mudge EJ. Recent accomplishments in wound healing. Int Wound J. 2015;12:4–9.
  • Wong SL, Demers M, Martinod K, et al. Diabetes primes neutrophils to undergo NETosis, which impairs wound healing. Nat Med. 2015;21:815–819.
  • Smiell JM, Wieman TJ, Steed DL, et al. Efficacy and safety of becaplermin (recombinant human platelet-derived growth factor-BB) in patients with nonhealing, lower extremity diabetic ulcers: a combined analysis of four randomized studies. Wound Repair Regeneration: Official Publication Wound Healing Society [and] European Tissue Repair Society. 1999;7:335–346.
  • Yao F, Eriksson E. Gene therapy in wound repair and regeneration. Wound Repair Regeneration: Official Publication Wound Healing Society [and] European Tissue Repair Society. 2000;8:443–451.
  • Thomas CE, Ehrhardt A, Kay MA. Progress and problems with the use of viral vectors for gene therapy. Nat Rev Genet. 2003;4:346–358.
  • Hacein-Bey-Abina S, Von Kalle C, Schmidt M, et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science. 2003;302:415–419.
  • Yarmush ML, Golberg A, Sersa G, et al. Electroporation-Based Technologies for Medicine: Principles, Applications, and Challenges. Annu Rev Biomed Eng. 2014;16:295–320.
  • Mir LM, Glass LF, Sersa G, et al. Effective treatment of cutaneous and subcutaneous malignant tumours by electrochemotherapy. Brit J Cancer. 1998;77:2336–2342.
  • Tozon N, Pavlin D, Sersa G, et al. Electrochemotherapy with intravenous bleomycin injection: an observational study in superficial squamous cell carcinoma in cats. J Feline Med Surg. 2013;16:291–299.
  • Tamzali Y, Borde L, Rols MP, et al. Successful treatment of equine sarcoids with cisplatin electrochemotherapy: a retrospective study of 48 cases. Equine Vet J. 2012;44:214–220.
  • Escoffre JM, Rols MP. Electrochemotherapy: Progress and Prospects. Curr Pharm Des. 2012;18:3406–3415.
  • Rols MP, Delteil C, Golzio M, et al. In vivo electrically mediated protein and gene transfer in murine melanoma. Nat Biotechnol. 1998;16:168–171.
  • Gothelf A, Gehl J. Gene electrotransfer to skin; review of existing literature and clinical perspectives. Curr Gene Ther. 2010;10:287–299.
  • Mir LM, Bureau MF, Gehl J, et al. High-efficiency gene transfer into skeletal muscle mediated by electric pulses. Proc Natl Acad Sci USA. 1999;96:4262–4267.
  • Vandermeulen G, Staes E, Vanderhaeghen ML, et al. Optimisation of intradermal DNA electrotransfer for immunisation. J Controlled Release: Official J Controlled Release Society. 2007;124:81–87.
  • Titomirov AV, Sukharev S, Kistanova E. In vivo electroporation and stable transformation of skin cells of newborn mice by plasmid DNA. Biochim Biophys Acta. 1991;1088:131–134.

** The first publication of gene electrotransfer to skin

  • Daud AI, DeConti RC, Andrews S, et al. Phase I trial of interleukin-12 plasmid electroporation in patients with metastatic melanoma. J Clinical Oncology: Official J Am Soc Clin Oncol. 2008;26:5896–5903.

* This paper reports the first human clinical trial of gene transfer by electroporation

  • Kee ST, Gehl J, Lee EW. Clinical Aspects of Electroporation. Springer, New York; 2011.
  • Engelke L, Winter G, Hook S, et al. Recent insights into cutaneous immunization: How to vaccinate via the skin. Vaccine. 2015;33:4663–4674.
  • Kotnik T, Frey W, Sack M, et al. Electroporation-based applications in biotechnology. Trends Biotechnol. 2015;33:480–488.
  • Andre FM, Gehl J, Sersa G, et al. Efficiency of high- and low-voltage pulse combinations for gene electrotransfer in muscle, liver, tumor, and skin. Hum Gene Ther. 2008;19:1261–1271.
  • Tonnesen MG, Feng X, Clark RA. Angiogenesis in wound healing. J investigative Dermatology Symposium Proceedings/the Society Investigative Dermatology, Inc [and] European Society Dermatological Research. 2000;5:40–46.
  • Singer AJ, Clark RA. Cutaneous wound healing. N Engl J Med. 1999;341:738–746.

** Essential review on cutaneous wound healing process

  • Nissen NN, Polverini PJ, Koch AE, et al. Vascular endothelial growth factor mediates angiogenic activity during the proliferative phase of wound healing. Am J Pathol. 1998;152:1445–1452.
  • Blakytny R, Jude E. The molecular biology of chronic wounds and delayed healing in diabetes. Diabetic Medicine: J British Diabetic Association. 2006;23:594–608.
  • Tomic-Canic M, Brem H. Gene array technology and pathogenesis of chronic wounds. Am J Surg. 2004;188:67–72.
  • Neumann E, Schaefer-Ridder M, Wang Y, et al. Gene transfer into mouse lyoma cells by electroporation in high electric fields. Embo J. 1982;1:841–845.

* The pioneering study reporting gene transfer in living cells

  • Teissié J, Golzio M, Rols MP. Mechanisms of cell membrane electropermeabilization: a minireview of our present (lack of ?) knowledge. Biochim Biophys Acta. 2005;1724:270–280.
  • Teissie J, Rols MP. An Experimental Evaluation of the Critical Potential Difference Inducing Cell-Membrane Electropermeabilization. Biophys J. 1993;65:409–413.
  • Bernhardt J, Pauly H. On the generation of potential differences across the membranes of ellipsoidal cells in an alternating electrical field. Biophysik. 1973;10:89–98.
  • Rols MP, Teissie J. Electropermeabilization of mammalian cells. Quantitative analysis of the phenomenon. Biophys J. 1990;58:1089–1098.
  • Rols MP, Teissie J. Experimental-Evidence for the Involvement of the Cytoskeleton in Mammalian-Cell Electropermeabilization. Biochim Biophys Acta. 1992;1111:45–50.
  • Escoffre JM, Portet T, Favard C, et al. Electromediated formation of DNA complexes with cell membranes and its consequences for gene delivery. Bba-Biomembranes. 2011;1808:1538–1543.
  • Paganin-Gioanni A, Bellard E, Escoffre JM, et al. Direct visualization at the single-cell level of siRNA electrotransfer into cancer cells. P Natl Acad Sci USA. 2011;108:10443–10447.
  • Escoffre JM, Teissie J, Rols MP. Gene transfer: how can the biological barriers be overcome? The Journal of membrane. Biology. 2010;236:61–74.
  • Golzio M, Teissie J, Rols MP. Direct visualization at the single-cell level of electrically mediated gene delivery. Proc Natl Acad Sci USA. 2002;99:1292–1297.

** The first direct visualization at the single-cell level of electrically mediated gene delivery

  • Rosazza C, Buntz A, Riess T, et al. Intracellular tracking of single-plasmid DNA particles after delivery by electroporation. Mol Therapy: J Am Soc Gene Ther. 2013;21:2217–2226.
  • Rosazza C, Escoffre JM, Zumbusch A, et al. The actin cytoskeleton has an active role in the electrotransfer of plasmid DNA in mammalian cells. Mol Therapy: J Am Soc Gene Ther. 2011;19:913–921.
  • Rosazza C, Phez E, Escoffre JM, et al. Cholesterol implications in plasmid DNA electrotransfer: Evidence for the involvement of endocytotic pathways. Int J Pharm. 2012;423:134–143.
  • Satkauskas S, Ruzgys P, Venslauskas MS. Towards the mechanisms for efficient gene transfer into cells and tissues by means of cell electroporation. Expert Opin Biol Ther. 2012;12:275–286.
  • Wu M, Yuan F. Membrane binding of plasmid DNA and endocytic pathways are involved in electrotransfection of mammalian cells. Plos One. 2011;6:e20923.
  • Sukharev SI, Klenchin VA, Serov SM, et al. Electroporation and electrophoretic DNA transfer into cells. The effect of DNA interaction with electropores. Biophys J. 1992;63:1320–1327.
  • Satkauskas S, Bureau MF, Puc M, et al. Mechanisms of in vivo DNA electrotransfer: respective contributions of cell electropermeabilization and DNA electrophoresis. Mol Ther. 2002;5:133–140.
  • Corovic S, Lackovic I, Sustaric P, et al. Modeling of electric field distribution in tissues during electroporation. Biomed Eng Online. 2013;12:16.
  • Lukaski HC, Moore M. Bioelectrical impedance assessment of wound healing. J Diabetes Sci Technol. 2012;6:209–212.
  • Swisher SL, Lin MC, Liao A, et al. Impedance sensing device enables early detection of pressure ulcers in vivo. Nat Commun. 2015;6:6575.
  • Miklavcic D, Beravs K, Semrov D, et al. The importance of electric field distribution for effective in vivo electroporation of tissues. Biophys J. 1998;74:2152–2158.
  • Sersa G, Teissie J, Cemazar M, et al. Electrochemotherapy of tumors as in situ vaccination boosted by immunogene electrotransfer. Cancer Immunology, Immunotherapy: CII. 2015;64:1315–1327.
  • Gilbert RA, Jaroszeski MJ, Heller R. Novel electrode designs for electrochemotherapy. Biochim Biophys Acta. 1997;1334:9–14.
  • Hofmann GA. Instrumentation and electrodes for in vivo electroporation. Methods Mol Med. 2000;37:37–61.
  • Liu F, Huang L. A syringe electrode device for simultaneous injection of DNA and electrotransfer. Mol Ther. 2002;5:323–328.
  • Mazeres S, Sel D, Golzio M, et al. Non invasive contact electrodes for in vivo localized cutaneous electropulsation and associated drug and nucleic acid delivery. J Control Release. 2009;134:125–131.
  • Momose T, Tonegawa A, Takeuchi J, et al. Efficient targeting of gene expression in chick embryos by microelectroporation. Dev Growth Differ. 1999;41:335–344.
  • Olofsson J, Nolkrantz K, Ryttsen F, et al. Single-cell electroporation. Curr Opin Biotech. 2003;14:29–34.
  • Pliquett U, Weaver JC. Feasibility of an electrode-reservoir device for transdermal drug delivery by noninvasive skin electroporation. IEEE Trans Biomed Eng. 2007;54:536–538.
  • Sel D, Mazeres S, Teissie J, et al. Finite-element modeling of needle electrodes in tissue from the perspective of frequent model computation. IEEE Trans Biomed Eng. 2003;50:1221–1232.
  • Daugimont L, Baron N, Vandermeulen G, et al. Hollow microneedle arrays for intradermal drug delivery and DNA electroporation. J Membr Biol. 2010;236:117–125.
  • Dev SB, Dhar D, Krassowska W. Electric field of a six-needle array electrode used in drug and DNA delivery in vivo: analytical versus numerical solution. IEEE Trans Biomed Eng. 2003;50:1296–1300.
  • Mahmood F, Gehl J. Optimizing clinical performance and geometrical robustness of a new electrode device for intracranial tumor electroporation. Bioelectrochemistry. 2011;81:10–16.
  • Vandermeulen G, Vanvarenberg K, De Beuckelaer A, et al. The site of administration influences both the type and the magnitude of the immune response induced by DNA vaccine electroporation. Vaccine. 2015;33:3179–3185.
  • Vanbever R, Pliquett UF, Preat V, et al. Comparison of the effects of short, high-voltage and long, medium-voltage pulses on skin electrical and transport properties. J Control Release. 1999;60:35–47.
  • Prausnitz MR, Bose VG, Langer R, et al. Electroporation of mammalian skin: a mechanism to enhance transdermal drug delivery. Proc Natl Acad Sci USA. 1993;90:10504–10508.
  • Chen T, Langer R, Weaver JC (1998). Skin electroporation causes molecular transport across the stratum corneum through localized transport regions. J Investigative Dermatology Symposium Proc/Soc Investigative Dermatology, Inc [and] Euro Soc Dermatological Res. 3: 159–165.
  • Gothelf A, Gehl J. Electroporation-Based DNA Delivery Technology: Methods for Gene Electrotransfer to Skin. In: Rinaldi M, Fioretti D, Lurescia S, eds. DNA Vaccines. Vol. 1143. New York: Springer; 2014. p. 115–122.
  • Misra A, Ganga S, Upadhyay P. Needle-free, non-adjuvanted skin immunization by electroporation-enhanced transdermal delivery of diphtheria toxoid and a candidate peptide vaccine against hepatitis B virus. Vaccine. 1999;18:517–523.
  • Gao Z, Wu X, Song N, et al. Electroporation-mediated plasmid gene transfer in rat incisional wound. J Dermatol Sci. 2007;47:161–164.
  • Gothelf A, Eriksen J, Hojman P, et al. Duration and level of transgene expression after gene electrotransfer to skin in mice. Gene Ther. 2010;17:839–845.
  • Heller LC, Jaroszeski MJ, Coppola D, et al. Optimization of cutaneous electrically mediated plasmid DNA delivery using novel electrode. Gene Ther. 2007;14:275–280.
  • Roos AK, Eriksson F, Timmons JA, et al. Skin electroporation: effects on transgene expression, DNA persistence and local tissue environment. Plos One. 2009;4:e7226.
  • Byrnes CK, Malone RW, Akhter N, et al. Electroporation enhances transfection efficiency in murine cutaneous wounds. Wound Repair Regeneration: Official Publication Wound Healing Society [and] European Tissue Repair Society. 2004;12:397–403.
  • Chung AS, Ferrara N. Developmental and pathological angiogenesis. Annu Rev Cell Dev Biol. 2011;27:563–584.
  • Rezende FC, Gomes HC, Lisboa B, et al. Electroporation of vascular endothelial growth factor gene in a unipedicle transverse rectus abdominis myocutaneous flap reduces necrosis. Ann Plast Surg. 2010;64:242–246.
  • Ferraro B, Cruz YL, Coppola D, et al. Intradermal delivery of plasmid VEGF(165) by electroporation promotes wound healing. Mol Therapy: J Am Soc Gene Ther. 2009;17:651–657.
  • Basu G, Downey H, Guo S, et al. Prevention of distal flap necrosis in a rat random skin flap model by gene electro transfer delivering VEGF(165) plasmid. J Gene Med. 2014;16:55–65.
  • Fujihara Y, Koyama H, Nishiyama N, et al. Gene transfer of bFGF to recipient bed improves survival of ischemic skin flap. Br J Plast Surg. 2005;58:511–517.
  • Folkman J. Angiogenesis. Annu Rev Med. 2006;57:1–18.
  • Werner S, Smola H, Liao X, et al. The function of KGF in morphogenesis of epithelium and reepithelialization of wounds. Science. 1994;266:819–822.
  • Werner S, Breeden M, Hubner G, et al. Induction of keratinocyte growth factor expression is reduced and delayed during wound healing in the genetically diabetic mouse. J Invest Dermatol. 1994;103:469–473.
  • Marti G, Ferguson M, Wang J, et al. Electroporative transfection with KGF-1 DNA improves wound healing in a diabetic mouse model. Gene Ther. 2004;11:1780–1785.
  • Lin MP, Marti GP, Dieb R, et al. Delivery of plasmid DNA expression vector for keratinocyte growth factor-1 using electroporation to improve cutaneous wound healing in a septic rat model. Wound Repair Regeneration: Official Publication Wound Healing Society [and] European Tissue Repair Society. 2006;14:618–624.
  • Lee PY, Chesnoy S, Huang L. Electroporatic delivery of TGF-beta1 gene works synergistically with electric therapy to enhance diabetic wound healing in db/db mice. J Invest Dermatol. 2004;123:791–798.

* This paper underlines the role of the electric field applied in gene electrotherapy in wound healing

  • Liu L, Marti GP, Wei X, et al. Age-dependent impairment of HIF-1alpha expression in diabetic mice: Correction with electroporation-facilitated gene therapy increases wound healing, angiogenesis, and circulating angiogenic cells. J Cell Physiol. 2008;217:319–327.
  • Chereddy KK, Her CH, Comune M, et al. PLGA nanoparticles loaded with host defense peptide LL37 promote wound healing. J Control Release. 2014;194:138–147.
  • Steinstraesser L, Koehler T, Jacobsen F, et al. Host defense peptides in wound healing. Mol Med. 2008;14:528–537.
  • Heilborn JD, Nilsson MF, Kratz G, et al. The cathelicidin anti-microbial peptide LL-37 is involved in re-epithelialization of human skin wounds and is lacking in chronic ulcer epithelium. J Invest Dermatol. 2003;120:379–389.
  • Steinstraesser L, Lam MC, Jacobsen F, et al. Skin electroporation of a plasmid encoding hCAP-18/LL-37 host defense peptide promotes wound healing. Mol Therapy: J Am Soc Gene Ther. 2014;22:734–742.
  • Ferraro B, Cruz YL, Baldwin M, et al. Increased perfusion and angiogenesis in a hindlimb ischemia model with plasmid FGF-2 delivered by noninvasive electroporation. Gene Ther. 2010;17:763–769.
  • Golberg A, Fischer J, Rubinsky B. The Use of Irreversible Electroporation in Food Preservation. In: Rubinsky B, ed. Irreversible Electroporation. Berlin Heidelberg: Springer; 2010. p. 273–312.
  • Golberg A, Broelsch GF, Vecchio D, et al. Pulsed electric fields for burn wound disinfection in a murine model. J Burn Care Research: Official Publication American Burn Association. 2015;36:7–13.
  • Arena CB, Sano MB, Rossmeisl JH Jr., et al. High-frequency irreversible electroporation (H-FIRE) for non-thermal ablation without muscle contraction. Biomed Eng Online. 2011;10:102.
  • Golberg A, Rubinsky B. Towards electroporation based treatment planning considering electric field induced muscle contractions. Technol Cancer Res Treat. 2012;11:189–201.
  • Young JL, Dean DA. Electroporation-mediated gene delivery. Adv Genet. 2015;89:49–88.
  • Marty M, Sersa G, Garbay JR, et al. Electrochemotherapy - An easy, highly effective and safe treatment of cutaneous and subcutaneous metastases: Results of ESOPE (European Standard Operating Procedures of Electrochemotherapy). Eur J Cancer Supplements. 2006;4:3–13.
  • Tsujie M, Isaka Y, Nakamura H, et al. Electroporation-mediated gene transfer that targets glomeruli. J Am Soc Nephrology: JASN. 2001;12:949–954.
  • Kloth LC. Electrical stimulation for wound healing: a review of evidence from in vitro studies, animal experiments, and clinical trials. Int J Low Extrem Wounds. 2005;4:23–44.

* This review focuses on electric stimulation in wound healing

  • Reid B, Zhao M. The Electrical Response to Injury: Molecular Mechanisms and Wound Healing. Adv Wound Care. 2014;3:184–201.
  • Polak A, Franek A, Taradaj J. High-Voltage Pulsed Current Electrical Stimulation in Wound Treatment. Adv Wound Care. 2014;3:104–117.
  • Park HJ, Rouabhia M, Lavertu D, et al. Electrical Stimulation Modulates the Expression of Multiple Wound Healing Genes in Primary Human Dermal Fibroblasts. Tissue Eng Part. 2015;21:1982–1990.
  • Stimac M, Dolinsek T, Lampreht U, et al. Gene Electrotransfer of Plasmid with Tissue Specific Promoter Encoding shRNA against Endoglin Exerts Antitumor Efficacy against Murine TS/A Tumors by Vascular Targeted Effects. PLoS One. 2015;10:e0124913.
  • Shirley SA, Lundberg CG, Li F, et al. Controlled gene delivery can enhance therapeutic outcome for cancer immune therapy for melanoma. Curr Gene Ther. 2015;15:32–43.
  • Hojman P, Spanggaard I, Olsen CH, et al. Calcium electrotransfer for termination of transgene expression in muscle. Hum Gene Ther. 2011;22:753–760.
  • Calvet CY, Thalmensi J, Liard C, et al. Optimization of a gene electrotransfer procedure for efficient intradermal immunization with an hTERT-based DNA vaccine in mice. Mol Ther Methods Clin Dev. 2014;1:14045.
  • Athanasiou KA, Eswaramoorthy R, Hadidi P, et al. Self-organization and the self-assembling process in tissue engineering. Annu Rev Biomed Eng. 2013;15:115–136.
  • Gibot L, Galbraith T, Huot J, et al. A preexisting microvascular network benefits in vivo revascularization of a microvascularized tissue-engineered skin substitute. Tissue Eng Part. 2010;16:3199–3206.
  • Gibot L, Auger FA, Lacroix D. The pivotal role of vascularization in tissue engineering. Annu Rev Biomed Eng. 2013;15:177–200.
  • Madi M, Rols MP, Gibot L. Efficient In Vitro Electropermeabilization of Reconstructed Human Dermal Tissue. J Membr Biol. 2015;248:903–908.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.