Abstract
The skin is a highly complex and immunogenic organ and has important roles in acting as a barrier, temperature regulation, absorption, and sensation. These properties as well as ease of application to the skin also make it an ideal target for gene delivery. Several methods have been developed to penetrate the skin and enhance gene delivery through or within the skin. The physical methods employed include biolistic delivery, which involves the use of heavy metal particles applied at high velocities to penetrate the skin; electroporation has also been developed as a non- or minimally invasive technique for skin penetration, which acts through the application of electric current to permeabilize the cell membranes and allow for uptake of macromolecules; ultrasound, plasma gas, and magnetofection have also been used as alternative methods for gene delivery that are in varying stages of use and development; both thermal and nonthermal ablation will be discussed in this chapter, as well as multiple techniques for tissue abrasion. The preclinical and clinical studies will be discussed for each of these techniques. We will also present conclusions and future directions of this area of research.
References
Abe A, Furumoto H, Yoshida K, Kato T, Saijo Y, Irahara M (2011) Gene gun-mediated skin transfection with FL gene suppresses the growth of murine fibrosarcoma. J Med Invest 58(1–2):39–45
Akowuah EF, Gray C, Lawrie A, Sheridan PJ, Su CH, Bettinger T, Brisken AF, Gunn J, Crossman DC, Francis SE, Baker AH, Newman CM (2005) Ultrasound-mediated delivery of TIMP-3 plasmid DNA into saphenous vein leads to increased lumen size in a porcine interposition graft model. Gene Ther 12(14):1154–1157. doi:10.1038/sj.gt.3302498
Albrecht MT, Eyles JE, Baillie LW, Keane-Myers AM (2012) Immunogenicity and efficacy of an anthrax/plague DNA fusion vaccine in a mouse model. FEMS Immunol Med Microbiol 65(3):505–509. doi:10.1111/j.1574-695X.2012.00974.x
Au JT, Wong J, Mittra A, Carpenter S, Haddad D, Carson J, Jayaraman S, Monette S, Solomon SB, Ezell P, Fong Y (2011) Irreversible electroporation is a surgical ablation technique that enhances gene transfer. Surgery 150(3):474–479. doi:10.1016/j.surg.2011.07.007
Beebe SJ, Fox PM, Rec LJ, Willis EL, Schoenbach KH (2003) Nanosecond, high-intensity pulsed electric fields induce apoptosis in human cells. FASEB J 17(11):1493–1495. doi:10.1096/fj.02-0859fje
Bergman PJ, McKnight J, Novosad A, Charney S, Farrelly J, Craft D, Wulderk M, Jeffers Y, Sadelain M, Hohenhaus AE, Segal N, Gregor P, Engelhorn M, Riviere I, Houghton AN, Wolchok JD (2003) Long-term survival of dogs with advanced malignant melanoma after DNA vaccination with xenogeneic human tyrosinase: a phase I trial. Clin Cancer Res 9(4):1284–1290
Birchall J, Coulman S, Anstey A, Gateley C, Sweetland H, Gershonowitz A, Neville L, Levin G (2006) Cutaneous gene expression of plasmid DNA in excised human skin following delivery via microchannels created by radio frequency ablation. Int J Pharm 312(1–2):15–23. doi:10.1016/j.ijpharm.2005.12.036
Boudreau EF, Josleyn M, Ullman D, Fisher D, Dalrymple L, Sellers-Myers K, Loudon P, Rusnak J, Rivard R, Schmaljohn C, Hooper JW (2012) A Phase 1 clinical trial of Hantaan virus and Puumala virus M-segment DNA vaccines for hemorrhagic fever with renal syndrome. Vaccine 30(11):1951–1958. doi:10.1016/j.vaccine.2012.01.024
Braun RP, Babiuk LA, Loehr BI, van Drunen Littel-van den H (1999) Particle-mediated DNA immunization of cattle confers long-lasting immunity against bovine herpes virus-1. Virology 265(1):46–56. doi:10.1006/viro.1999.0032
Braun RP, Dong L, Jerome S, Herber R, Roberts LK, Payne LG (2008) Multi-antigenic DNA immunization using herpes simplex virus type 2 genomic fragments. Hum Vaccin 4(1):36–43
Brave A, Gudmundsdotter L, Sandstrom E, Haller BK, Hallengard D, Maltais AK, King AD, Stout RR, Blomberg P, Hoglund U, Hejdeman B, Biberfeld G, Wahren B (2010) Biodistribution, persistence and lack of integration of a multigene HIV vaccine delivered by needle-free intradermal injection and electroporation. Vaccine 28(51):8203–8209. doi:10.1016/j.vaccine.2010.08.108
Breton M, Delemotte L, Silve A, Mir LM, Tarek M (2012) Transport of siRNA through lipid membranes driven by nanosecond electric pulses: an experimental and computational study. J Am Chem Soc 134(34):13938–13941. doi:10.1021/ja3052365
Broderick KE, Shen X, Soderholm J, Lin F, McCoy J, Khan AS, Yan J, Morrow MP, Patel A, Kobinger GP, Kemmerrer S, Weiner DB, Sardesai NY (2011) Prototype development and preclinical immunogenicity analysis of a novel minimally invasive electroporation device. Gene Ther 18(3):258–265. doi:10.1038/gt.2010.137
Campochiaro PA, Nguyen QD, Shah SM, Klein ML, Holz E, Frank RN, Saperstein DA, Gupta A, Stout JT, Macko J, DiBartolomeo R, Wei LL (2006) Adenoviral vector-delivered pigment epithelium-derived factor for neovascular age-related macular degeneration: results of a phase I clinical trial. Hum Gene Ther 17(2):167–176. doi:10.1089/hum.2006.17.167
Cassaday RD, Sondel PM, King DM, Macklin MD, Gan J, Warner TF, Zuleger CL, Bridges AJ, Schalch HG, Kim KM, Hank JA, Mahvi DM, Albertini MR (2007) A phase I study of immunization using particle-mediated epidermal delivery of genes for gp100 and GM-CSF into uninvolved skin of melanoma patients. Clin Cancer Res 13(2 Pt 1):540–549. doi:10.1158/1078-0432.CCR-06-2039
Cavazzana-Calvo M, Hacein-Bey S, de Saint Basile G, Gross F, Yvon E, Nusbaum P, Selz F, Hue C, Certain S, Casanova JL, Bousso P, Deist FL, Fischer A (2000) Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 288(5466):669–672
Cesco-Gaspere M, Zentilin L, Giacca M, Burrone OR (2008) Boosting anti-idiotype immune response with recombinant AAV enhances tumour protection induced by gene gun vaccination. Scand J Immunol 68(1):58–66. doi:10.1111/j.1365-3083.2008.02119.x
Chen CH, Ji H, Suh KW, Choti MA, Pardoll DM, Wu TC (1999) Gene gun-mediated DNA vaccination induces antitumor immunity against human papillomavirus type 16 E7-expressing murine tumor metastases in the liver and lungs. Gene Ther 6(12):1972–1981. doi:10.1038/sj.gt.3301067
Chevez-Barrios P, Chintagumpala M, Mieler W, Paysse E, Boniuk M, Kozinetz C, Hurwitz MY, Hurwitz RL (2005) Response of retinoblastoma with vitreous tumor seeding to adenovirus-mediated delivery of thymidine kinase followed by ganciclovir. J Clin Oncol 23(31):7927–7935. doi:10.1200/JCO.2004.00.1883
Choi AH, Basu M, Rae MN, McNeal MM, Ward RL (1998) Particle-bombardment-mediated DNA vaccination with rotavirus VP4 or VP7 induces high levels of serum rotavirus IgG but fails to protect mice against challenge. Virology 250(1):230–240. doi:10.1006/viro.1998.9370
Choi SO, Kim YC, Lee JW, Park JH, Prausnitz MR, Allen MG (2012) Intracellular protein delivery and gene transfection by electroporation using a microneedle electrode array. Small 8(7):1081–1091. doi:10.1002/smll.201101747
Chuang TF, Lee SC, Liao KW, Hsiao YW, Lo CH, Chiang BL, Lin XZ, Tao MH, Chu RM (2009) Electroporation-mediated IL-12 gene therapy in a transplantable canine cancer model. Int J Cancer 125(3):698–707. doi:10.1002/ijc.24418
Connolly RJ, Lopez GA, Hoff AM, Jaroszeski MJ (2009) Plasma facilitated delivery of DNA to skin. Biotechnol Bioeng 104(5):1034–1040. doi:10.1002/bit.22451
Connolly RJ, Lopez GA, Hoff AM, Jaroszeski MJ (2010) Characterization of plasma mediated molecular delivery to cells in vitro. Int J Pharm 389(1–2):53–57. doi:10.1016/j.ijpharm.2010.01.016
Connolly RJ, Rey JI, Lambert VM, Wegerif G, Jaroszeski MJ, Ugen KE (2011) Enhancement of antigen specific humoral immune responses after delivery of a DNA plasmid based vaccine through a contact-independent helium plasma. Vaccine 29(39):6781–6784. doi:10.1016/j.vaccine.2010.12.054
Connolly RJ, Chapman T, Hoff AM, Kutzler MA, Jaroszeski MJ, Ugen KE (2012) Non-contact helium-based plasma for delivery of DNA vaccines: enhancement of humoral and cellular immune responses. Hum Vaccin Immunother 8(11):1729–1733
Daud AI, DeConti RC, Andrews S, Urbas P, Riker AI, Sondak VK, Munster PN, Sullivan DM, Ugen KE, Messina JL, Heller R (2008) Phase I trial of interleukin-12 plasmid electroporation in patients with metastatic melanoma. J Clin Oncol 26(36):5896–5903. doi:10.1200/JCO.2007.15.6794
Dincer Z, Jones S, Haworth R (2006) Preclinical safety assessment of a DNA vaccine using particle-mediated epidermal delivery in domestic pig, minipig and mouse. Exp Toxicol Pathol 57(5–6):351–357. doi:10.1016/j.etp.2006.03.014
Donate A, Coppola D, Cruz Y, Heller R (2011) Evaluation of a novel non-penetrating electrode for use in DNA vaccination. PLoS One 6(4):e19181. doi:10.1371/journal.pone.0019181
Duvshani-Eshet M, Adam D, Machluf M (2006) The effects of albumin-coated microbubbles in DNA delivery mediated by therapeutic ultrasound. J Control Release 112(2):156–166. doi:10.1016/j.jconrel.2006.02.013
Eberling JL, Jagust WJ, Christine CW, Starr P, Larson P, Bankiewicz KS, Aminoff MJ (2008) Results from a phase I safety trial of hAADC gene therapy for Parkinson disease. Neurology 70(21):1980–1983. doi:10.1212/01.wnl.0000312381.29287.ff
Escoffre JM, Rols MP (2012) Electrochemotherapy: progress and prospects. Curr Pharm Des 18(23):3406–3415
Ferraro B, Cruz YL, Coppola D, Heller R (2009) Intradermal delivery of plasmid VEGF(165) by electroporation promotes wound healing. Mol Ther 17(4):651–657. doi:10.1038/mt.2009.12
Ferraro B, Heller LC, Cruz YL, Guo S, Donate A, Heller R (2011) Evaluation of delivery conditions for cutaneous plasmid electrotransfer using a multielectrode array. Gene Ther 18(5):496–500. doi:10.1038/gt.2010.171
Fischer AJ, Stanke JJ, Omar G, Askwith CC, Burry RW (2006) Ultrasound-mediated gene transfer into neuronal cells. J Biotechnol 122(4):393–411. doi:10.1016/j.jbiotec.2005.10.006
Furlani EP, Ng KC (2008) Nanoscale magnetic biotransport with application to magnetofection. Phys Rev E Stat Nonlin Soft Matter Phys 77(6 Pt 1):061914
Gilbert RA, Jaroszeski MJ, Heller R (1997) Novel electrode designs for electrochemotherapy. Biochim Biophys Acta 1334(1):9–14
Gill HS, Andrews SN, Sakthivel SK, Fedanov A, Williams IR, Garber DA, Priddy FH, Yellin S, Feinberg MB, Staprans SI, Prausnitz MR (2009) Selective removal of stratum corneum by microdermabrasion to increase skin permeability. Eur J Pharm Sci 38(2):95–103. doi:10.1016/j.ejps.2009.06.004
Ginsberg BA, Gallardo HF, Rasalan TS, Adamow M, Mu Z, Tandon S, Bewkes BB, Roman RA, Chapman PB, Schwartz GK, Carvajal RD, Panageas KS, Terzulli SL, Houghton AN, Yuan JD, Wolchok JD (2010) Immunologic response to xenogeneic gp100 DNA in melanoma patients: comparison of particle-mediated epidermal delivery with intramuscular injection. Clin Cancer Res 16(15):4057–4065. doi:10.1158/1078-0432.CCR-10-1093
Glenn GM, Thomas DN, Poffenberger KL, Flyer DC, Ellingsworth LR, Andersen BH, Frech SA (2009) Safety and immunogenicity of an influenza vaccine A/H5N1 (A/Vietnam/1194/2004) when coadministered with a heat-labile enterotoxin (LT) adjuvant patch. Vaccine 27(Suppl 6):G60–G66. doi:10.1016/j.vaccine.2009.10.031
Gnjatic S, Nishikawa H, Jungbluth AA, Gure AO, Ritter G, Jager E, Knuth A, Chen YT, Old LJ (2006) NY-ESO-1: review of an immunogenic tumor antigen. Adv Cancer Res 95:1–30. doi:10.1016/S0065-230X(06)95001-5
Gnjatic S, Altorki NK, Tang DN, Tu SM, Kundra V, Ritter G, Old LJ, Logothetis CJ, Sharma P (2009) NY-ESO-1 DNA vaccine induces T-cell responses that are suppressed by regulatory T cells. Clin Cancer Res 15(6):2130–2139. doi:10.1158/1078-0432.CCR-08-2632
Gothelf A, Gehl J (2010) Gene electrotransfer to skin; review of existing literature and clinical perspectives. Curr Gene Ther 10(4):287–299
Gothelf A, Eriksen J, Hojman P, Gehl J (2010a) Duration and level of transgene expression after gene electrotransfer to skin in mice. Gene Ther 17(7):839–845. doi:10.1038/gt.2010.35
Gothelf A, Hojman P, Gehl J (2010b) Therapeutic levels of erythropoietin (EPO) achieved after gene electrotransfer to skin in mice. Gene Ther 17(9):1077–1084. doi:10.1038/gt.2010.46
Gothelf A, Mahmood F, Dagnaes-Hansen F, Gehl J (2011) Efficacy of transgene expression in porcine skin as a function of electrode choice. Bioelectrochemistry 82(2):95–102. doi:10.1016/j.bioelechem.2011.06.001
Guo DP, Li XY, Sun P, Wang ZG, Chen XY, Chen Q, Fan LM, Zhang B, Shao LZ, Li XR (2004) Ultrasound/microbubble enhances foreign gene expression in ECV304 cells and murine myocardium. Acta Biochim Biophys Sin 36(12):824–831
Guo DP, Li XY, Sun P, Tang YB, Chen XY, Chen Q, Fan LM, Zang B, Shao LZ, Li XR (2006) Ultrasound-targeted microbubble destruction improves the low density lipoprotein receptor gene expression in HepG2 cells. Biochem Biophys Res Commun 343(2):470–474. doi:10.1016/j.bbrc.2006.02.179
Guo S, Donate A, Basu G, Lundberg C, Heller L, Heller R (2011) Electro-gene transfer to skin using a noninvasive multielectrode array. J Control Release 151(3):256–262. doi:10.1016/j.jconrel.2011.01.014
Ha RY, Nojima K, Adams WP Jr, Brown SA (2005) Analysis of facial skin thickness: defining the relative thickness index. Plast Reconstr Surg 115(6):1769–1773
Han R, Peng X, Reed CA, Cladel NM, Budgeon LR, Pickel MD, Christensen ND (2002) Gene gun-mediated intracutaneous vaccination with papillomavirus E7 gene delays cancer development of papillomavirus-induced skin papillomas on rabbits. Cancer Detect Prev 26(6):458–467
Harvey BG, Leopold PL, Hackett NR, Grasso TM, Williams PM, Tucker AL, Kaner RJ, Ferris B, Gonda I, Sweeney TD, Ramalingam R, Kovesdi I, Shak S, Crystal RG (1999) Airway epithelial CFTR mRNA expression in cystic fibrosis patients after repetitive administration of a recombinant adenovirus. J Clin Invest 104(9):1245–1255. doi:10.1172/JCI7935
Heller L, Pottinger C, Jaroszeski MJ, Gilbert R, Heller R (2000) In vivo electroporation of plasmids encoding GM-CSF or interleukin-2 into existing B16 melanomas combined with electrochemotherapy induces long-term antitumour immunity. Melanoma Res 10(6):577–583
Heller R, Schultz J, Lucas ML, Jaroszeski MJ, Heller LC, Gilbert RA, Moelling K, Nicolau C (2001) Intradermal delivery of interleukin-12 plasmid DNA by in vivo electroporation. DNA Cell Biol 20(1):21–26. doi:10.1089/10445490150504666
Heller L, Merkler K, Westover J, Cruz Y, Coppola D, Benson K, Daud A, Heller R (2006) Evaluation of toxicity following electrically mediated interleukin-12 gene delivery in a B16 mouse melanoma model. Clin Cancer Res 12(10):3177–3183. doi:10.1158/1078-0432.CCR-05-2727
Heller LC, Jaroszeski MJ, Coppola D, McCray AN, Hickey J, Heller R (2007) Optimization of cutaneous electrically mediated plasmid DNA delivery using novel electrode. Gene Ther 14(3):275–280. doi:10.1038/sj.gt.3302867
Heller R, Cruz Y, Heller LC, Gilbert RA, Jaroszeski MJ (2010) Electrically mediated delivery of plasmid DNA to the skin, using a multielectrode array. Hum Gene Ther 21(3):357–362. doi:10.1089/hum.2009.065
Hirao LA, Draghia-Akli R, Prigge JT, Yang M, Satishchandran A, Wu L, Hammarlund E, Khan AS, Babas T, Rhodes L, Silvera P, Slifka M, Sardesai NY, Weiner DB (2011) Multivalent smallpox DNA vaccine delivered by intradermal electroporation drives protective immunity in nonhuman primates against lethal monkeypox challenge. J Infect Dis 203(1):95–102. doi:10.1093/infdis/jiq017
Holzbach T, Vlaskou D, Neshkova I, Konerding MA, Wortler K, Mykhaylyk O, Gansbacher B, Machens HG, Plank C, Giunta RE (2010) Non-viral VEGF(165) gene therapy--magnetofection of acoustically active magnetic lipospheres (‘magnetobubbles’) increases tissue survival in an oversized skin flap model. J Cell Mol Med 14(3):587–599. doi:10.1111/j.1582-4934.2008.00592.x
Hooper JW, Thompson E, Wilhelmsen C, Zimmerman M, Ichou MA, Steffen SE, Schmaljohn CS, Schmaljohn AL, Jahrling PB (2004) Smallpox DNA vaccine protects nonhuman primates against lethal monkeypox. J Virol 78(9):4433–4443
Horton HM, Lalor PA, Rolland AP (2008) IL-2 plasmid electroporation: from preclinical studies to phase I clinical trial. Methods Mol Biol 423:361–372. doi:10.1007/978-1-59745-194-9_28
Hyde SC, Southern KW, Gileadi U, Fitzjohn EM, Mofford KA, Waddell BE, Gooi HC, Goddard CA, Hannavy K, Smyth SE, Egan JJ, Sorgi FL, Huang L, Cuthbert AW, Evans MJ, Colledge WH, Higgins CF, Webb AK, Gill DR (2000) Repeat administration of DNA/liposomes to the nasal epithelium of patients with cystic fibrosis. Gene Ther 7(13):1156–1165. doi:10.1038/sj.gt.3301212
Iizuka H (1994) Epidermal turnover time. J Dermatol Sci 8(3):215–217
Irvine KR, Rao JB, Rosenberg SA, Restifo NP (1996) Cytokine enhancement of DNA immunization leads to effective treatment of established pulmonary metastases. J Immunol 156(1):238–245
Jones S, Evans K, McElwaine-Johnn H, Sharpe M, Oxford J, Lambkin-Williams R, Mant T, Nolan A, Zambon M, Ellis J, Beadle J, Loudon PT (2009) DNA vaccination protects against an influenza challenge in a double-blind randomised placebo-controlled phase 1b clinical trial. Vaccine 27(18):2506–2512. doi:10.1016/j.vaccine.2009.02.061
Joseph SK, Sambanthamoorthy S, Dakshinamoorthy G, Munirathinam G, Ramaswamy K (2012) Protective immune responses to biolistic DNA vaccination of Brugia malayi abundant larval transcript-2. Vaccine 30(45):6477–6482. doi:10.1016/j.vaccine.2012.07.084
Kalat M, Kupcu Z, Schuller S, Zalusky D, Zehetner M, Paster W, Schweighoffer T (2002) In vivo plasmid electroporation induces tumor antigen-specific CD8+ T-cell responses and delays tumor growth in a syngeneic mouse melanoma model. Cancer Res 62(19):5489–5494
Kami D, Takeda S, Itakura Y, Gojo S, Watanabe M, Toyoda M (2011) Application of magnetic nanoparticles to gene delivery. Int J Mol Sci 12(6):3705–3722. doi:10.3390/ijms12063705
Kaplitt MG, Feigin A, Tang C, Fitzsimons HL, Mattis P, Lawlor PA, Bland RJ, Young D, Strybing K, Eidelberg D, During MJ (2007) Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson’s disease: an open label, phase I trial. Lancet 369(9579):2097–2105. doi:10.1016/S0140-6736(07)60982-9
Kastrup J, Jorgensen E, Ruck A, Tagil K, Glogar D, Ruzyllo W, Botker HE, Dudek D, Drvota V, Hesse B, Thuesen L, Blomberg P, Gyongyosi M, Sylven C (2005) Direct intramyocardial plasmid vascular endothelial growth factor-A165 gene therapy in patients with stable severe angina pectoris A randomized double-blind placebo-controlled study: the Euroinject One trial. J Am Coll Cardiol 45(7):982–988. doi:10.1016/j.jacc.2004.12.068
Kim D, Hoory T, Monie A, Ting JP, Hung CF, Wu TC (2008) Enhancement of DNA vaccine potency through coadministration of CIITA DNA with DNA vaccines via gene gun. J Immunol 180(10):7019–7027
Kim HS, Lim SH, Song JY, Kim MY, Lee JH, Park JG, Kim HO, Park YM (2009) Skin barrier function recovery after diamond microdermabrasion. J Dermatol 36(10):529–533. doi:10.1111/j.1346-8138.2009.00695.x
Kim EK, Hovsepian RV, Mathew P, Paul MD (2011) Dermabrasion. Clin Plast Surg 38(3):391–395. doi:10.1016/j.cps.2011.05.001, v–vi
Klein RM, Wolf ED, Wu R, Sanford JC (1992) High-velocity microprojectiles for delivering nucleic acids into living cells. 1987. Biotechnology 24:384–386
Kodama T, Tomita Y, Koshiyama K, Blomley MJ (2006) Transfection effect of microbubbles on cells in superposed ultrasound waves and behavior of cavitation bubble. Ultrasound Med Biol 32(6):905–914. doi:10.1016/j.ultrasmedbio.2006.03.004
Krotz F, de Wit C, Sohn HY, Zahler S, Gloe T, Pohl U, Plank C (2003a) Magnetofection – a highly efficient tool for antisense oligonucleotide delivery in vitro and in vivo. Mol Ther 7(5 Pt 1):700–710
Krotz F, Sohn HY, Gloe T, Plank C, Pohl U (2003b) Magnetofection potentiates gene delivery to cultured endothelial cells. J Vasc Res 40(5):425–434. doi:10.1159/000073901
Kuo SP (2008) Plasma assisted decontamination of bacterial spores. Open Biomed Eng J 2:36–42. doi:10.2174/1874120700802010036
Larregina AT, Watkins SC, Erdos G, Spencer LA, Storkus WJ, Beer Stolz D, Falo LD Jr (2001) Direct transfection and activation of human cutaneous dendritic cells. Gene Ther 8(8):608–617. doi:10.1038/sj.gt.3301404
Levine BL, Humeau LM, Boyer J, MacGregor RR, Rebello T, Lu X, Binder GK, Slepushkin V, Lemiale F, Mascola JR, Bushman FD, Dropulic B, June CH (2006) Gene transfer in humans using a conditionally replicating lentiviral vector. Proc Natl Acad Sci U S A 103(46):17372–17377. doi:10.1073/pnas.0608138103
Liang HD, Lu QL, Xue SA, Halliwell M, Kodama T, Cosgrove DO, Stauss HJ, Partridge TA, Blomley MJ (2004) Optimisation of ultrasound-mediated gene transfer (sonoporation) in skeletal muscle cells. Ultrasound Med Biol 30(11):1523–1529. doi:10.1016/j.ultrasmedbio.2004.08.021
Liao JC, Gregor P, Wolchok JD, Orlandi F, Craft D, Leung C, Houghton AN, Bergman PJ (2006) Vaccination with human tyrosinase DNA induces antibody responses in dogs with advanced melanoma. Cancer Immun 6:8
Lin F, Shen X, Kichaev G, Mendoza JM, Yang M, Armendi P, Yan J, Kobinger GP, Bello A, Khan AS, Broderick KE, Sardesai NY (2012) Optimization of electroporation-enhanced intradermal delivery of DNA vaccine using a minimally invasive surface device. Hum Gene Ther Methods 23(3):157–168. doi:10.1089/hgtb.2011.209
Liu Y, Yang H, Sakanishi A (2006) Ultrasound: mechanical gene transfer into plant cells by sonoporation. Biotechnol Adv 24(1):1–16. doi:10.1016/j.biotechadv.2005.04.002
Lohr F, Lo DY, Zaharoff DA, Hu K, Zhang X, Li Y, Zhao Y, Dewhirst MW, Yuan F, Li CY (2001) Effective tumor therapy with plasmid-encoded cytokines combined with in vivo electroporation. Cancer Res 61(8):3281–3284
Loudon PT, Yager EJ, Lynch DT, Narendran A, Stagnar C, Franchini AM, Fuller JT, White PA, Nyuandi J, Wiley CA, Murphey-Corb M, Fuller DH (2010) GM-CSF increases mucosal and systemic immunogenicity of an H1N1 influenza DNA vaccine administered into the epidermis of non-human primates. PLoS One 5(6):e11021. doi:10.1371/journal.pone.0011021
Lucas ML, Heller L, Coppola D, Heller R (2002) IL-12 plasmid delivery by in vivo electroporation for the successful treatment of established subcutaneous B16.F10 melanoma. Mol Ther 5(6):668–675. doi:10.1006/mthe.2002.0601
Lunn DP, Soboll G, Schram BR, Quass J, McGregor MW, Drape RJ, Macklin MD, McCabe DE, Swain WF, Olsen CW (1999) Antibody responses to DNA vaccination of horses using the influenza virus hemagglutinin gene. Vaccine 17(18):2245–2258
Macpherson JL, Boyd MP, Arndt AJ, Todd AV, Fanning GC, Ely JA, Elliott F, Knop A, Raponi M, Murray J, Gerlach W, Sun LQ, Penny R, Symonds GP, Carr A, Cooper DA (2005) Long-term survival and concomitant gene expression of ribozyme-transduced CD4+ T-lymphocytes in HIV-infected patients. J Gene Med 7(5):552–564. doi:10.1002/jgm.705
Makinen K, Manninen H, Hedman M, Matsi P, Mussalo H, Alhava E, Yla-Herttuala S (2002) Increased vascularity detected by digital subtraction angiography after VEGF gene transfer to human lower limb artery: a randomized, placebo-controlled, double-blinded phase II study. Mol Ther 6(1):127–133. doi:10.1006/mthe.2002.0638
Marrero B, Shirley S, Heller R (2014). Delivery of interleukin-15 to B16 melanoma by electroproation leads to tumor regression and long term survival. TCRT 13(6):551–560. doi:10.7785/tcrt.2013.600252
Matyas GR, Friedlander AM, Glenn GM, Little S, Yu J, Alving CR (2004) Needle-free skin patch vaccination method for anthrax. Infect Immun 72(2):1181–1183
Mavilio F, Pellegrini G, Ferrari S, Di Nunzio F, Di Iorio E, Recchia A, Maruggi G, Ferrari G, Provasi E, Bonini C, Capurro S, Conti A, Magnoni C, Giannetti A, De Luca M (2006) Correction of junctional epidermolysis bullosa by transplantation of genetically modified epidermal stem cells. Nat Med 12(12):1397–1402. doi:10.1038/nm1504
Mehier-Humbert S, Bettinger T, Yan F, Guy RH (2005) Ultrasound-mediated gene delivery: kinetics of plasmid internalization and gene expression. J Control Rel 104(1):203–211. doi:10.1016/j.jconrel.2005.01.011
Michel MS, Erben P, Trojan L, Schaaf A, Kiknavelidze K, Knoll T, Alken P (2004) Acoustic energy: a new transfection method for cancer of the prostate, cancer of the bladder and benign kidney cells. Anticancer Res 24(4):2303–2308
Miller DL, Dou C (2004a) Membrane damage thresholds for 1- to 10-MHz pulsed ultrasound exposure of phagocytic cells loaded with contrast agent gas bodies in vitro. Ultrasound Med Biol 30(7):973–977. doi:10.1016/j.ultrasmedbio.2004.05.010
Miller DL, Dou C (2004b) Membrane damage thresholds for pulsed or continuous ultrasound in phagocytic cells loaded with contrast agent gas bodies. Ultrasound Med Biol 30(3):405–411. doi:10.1016/j.ultrasmedbio.2003.11.013
Miller DL, Dou C (2004c) Theoretical gas body pulsation in relation to empirical gas-body destabilization and to cell membrane damage thresholds. J Acoust Soc Am 116(6):3742–3749
Morris AD, McCombs GB, Akan T, Hynes W, Laroussi M, Tolle SL (2009) Cold plasma technology: bactericidal effects on Geobacillus stearothermophilus and Bacillus cereus microorganisms. J Dent Hyg 83(2):55–61
Moss RB, Rodman D, Spencer LT, Aitken ML, Zeitlin PL, Waltz D, Milla C, Brody AS, Clancy JP, Ramsey B, Hamblett N, Heald AE (2004) Repeated adeno-associated virus serotype 2 aerosol-mediated cystic fibrosis transmembrane regulator gene transfer to the lungs of patients with cystic fibrosis: a multicenter, double-blind, placebo-controlled trial. Chest 125(2):509–521
Neumann E, Schaefer-Ridder M, Wang Y, Hofschneider PH (1982) Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J 1(7):841–845
Newman CM, Bettinger T (2007) Gene therapy progress and prospects: ultrasound for gene transfer. Gene Ther 14(6):465–475. doi:10.1038/sj.gt.3302925
Niesalla H, de Andres X, Barbezange C, Fraisier C, Reina R, Arnarson H, Biescas E, Mazzei M, McNeilly TN, Liu C, Watkins C, Perez M, Carrozza ML, Bandecchi P, Solano C, Crespo H, Glaria I, Huard C, Shaw DJ, de Blas I, de Andres D, Tolari F, Rosati S, Suzan-Monti M, Andresdottir V, Torsteinsdottir S, Petursson G, Badiola J, Lujan L, Pepin M, Amorena B, Blacklaws B, Harkiss GD (2009) Systemic DNA immunization against ovine lentivirus using particle-mediated epidermal delivery and modified vaccinia Ankara encoding the gag and/or env genes. Vaccine 27(2):260–269. doi:10.1016/j.vaccine.2008.10.042
Nuccitelli R, Pliquett U, Chen X, Ford W, James Swanson R, Beebe SJ, Kolb JF, Schoenbach KH (2006) Nanosecond pulsed electric fields cause melanomas to self-destruct. Biochem Biophys Res Commun 343(2):351–360. doi:10.1016/j.bbrc.2006.02.181
Nuccitelli R, Tran K, Sheikh S, Athos B, Kreis M, Nuccitelli P (2010) Optimized nanosecond pulsed electric field therapy can cause murine malignant melanomas to self-destruct with a single treatment. Int J Cancer 127(7):1727–1736. doi:10.1002/ijc.25364
O’Brien WD Jr (2007) Ultrasound-biophysics mechanisms. Prog Biophys Mol Biol 93(1–3):212–255. doi:10.1016/j.pbiomolbio.2006.07.010
Ogawa Y, Morikawa N, Ohkubo-Suzuki A, Miyoshi S, Arakawa H, Kita Y, Nishimura S (2005) An epoch-making application of discharge plasma phenomenon to gene-transfer. Biotechnol Bioeng 92(7):865–870. doi:10.1002/bit.20659
Pislaru SV, Pislaru C, Kinnick RR, Singh R, Gulati R, Greenleaf JF, Simari RD (2003) Optimization of ultrasound-mediated gene transfer: comparison of contrast agents and ultrasound modalities. Eur Heart J 24(18):1690–1698
Plank C, Rosenecker J (2009) Magnetofection: the use of magnetic nanoparticles for nucleic acid delivery. Cold Spring Harb Protoc 2009(6):pdb prot5230. doi:10.1101/pdb.prot5230
Plank C, Scherer F, Schillinger U, Bergemann C, Anton M (2003a) Magnetofection: enhancing and targeting gene delivery with superparamagnetic nanoparticles and magnetic fields. J Liposome Res 13(1):29–32. doi:10.1081/LPR-120017486
Plank C, Schillinger U, Scherer F, Bergemann C, Remy JS, Krotz F, Anton M, Lausier J, Rosenecker J (2003b) The magnetofection method: using magnetic force to enhance gene delivery. Biol Chem 384(5):737–747. doi:10.1515/BC.2003.082
Plank C, Zelphati O, Mykhaylyk O (2011) Magnetically enhanced nucleic acid delivery. Ten years of magnetofection-progress and prospects. Adv Drug Deliv Rev 63(14–15):1300–1331. doi:10.1016/j.addr.2011.08.002
Powell JS, Ragni MV, White GC 2nd, Lusher JM, Hillman-Wiseman C, Moon TE, Cole V, Ramanathan-Girish S, Roehl H, Sajjadi N, Jolly DJ, Hurst D (2003) Phase 1 trial of FVIII gene transfer for severe hemophilia A using a retroviral construct administered by peripheral intravenous infusion. Blood 102(6):2038–2045. doi:10.1182/blood-2003-01-0167
Rahim A, Taylor SL, Bush NL, ter Haar GR, Bamber JC, Porter CD (2006a) Physical parameters affecting ultrasound/microbubble-mediated gene delivery efficiency in vitro. Ultrasound Med Biol 32(8):1269–1279. doi:10.1016/j.ultrasmedbio.2006.04.014
Rahim AA, Taylor SL, Bush NL, ter Haar GR, Bamber JC, Porter CD (2006b) Spatial and acoustic pressure dependence of microbubble-mediated gene delivery targeted using focused ultrasound. J Gene Med 8(11):1347–1357. doi:10.1002/jgm.962
Rajagopalan S, Mohler ER 3rd, Lederman RJ, Mendelsohn FO, Saucedo JF, Goldman CK, Blebea J, Macko J, Kessler PD, Rasmussen HS, Annex BH (2003) Regional angiogenesis with vascular endothelial growth factor in peripheral arterial disease: a phase II randomized, double-blind, controlled study of adenoviral delivery of vascular endothelial growth factor 121 in patients with disabling intermittent claudication. Circulation 108(16):1933–1938. doi:10.1161/01.CIR.0000093398.16124.29
Rajendran S, O’Hanlon D, Morrissey D, O’Donovan T, O’Sullivan GC, Tangney M (2011) Preclinical evaluation of gene delivery methods for the treatment of loco-regional disease in breast cancer. Exp Biol Med (Maywood) 236(4):423–434. doi:10.1258/ebm.2011.010234
Rakhmilevich AL, Turner J, Ford MJ, McCabe D, Sun WH, Sondel PM, Grota K, Yang NS (1996) Gene gun-mediated skin transfection with interleukin 12 gene results in regression of established primary and metastatic murine tumors. Proc Natl Acad Sci U S A 93(13):6291–6296
Rakhmilevich AL, Imboden M, Hao Z, Macklin MD, Roberts T, Wright KM, Albertini MR, Yang NS, Sondel PM (2001) Effective particle-mediated vaccination against mouse melanoma by coadministration of plasmid DNA encoding Gp100 and granulocyte-macrophage colony-stimulating factor. Clin Cancer Res 7(4):952–961
Roberts LK, Barr LJ, Fuller DH, McMahon CW, Leese PT, Jones S (2005) Clinical safety and efficacy of a powdered Hepatitis B nucleic acid vaccine delivered to the epidermis by a commercial prototype device. Vaccine 23(40):4867–4878. doi:10.1016/j.vaccine.2005.05.026
Romero NB, Braun S, Benveniste O, Leturcq F, Hogrel JY, Morris GE, Barois A, Eymard B, Payan C, Ortega V, Boch AL, Lejean L, Thioudellet C, Mourot B, Escot C, Choquel A, Recan D, Kaplan JC, Dickson G, Klatzmann D, Molinier-Frenckel V, Guillet JG, Squiban P, Herson S, Fardeau M (2004) Phase I study of dystrophin plasmid-based gene therapy in Duchenne/Becker muscular dystrophy. Hum Gene Ther 15(11):1065–1076. doi:10.1089/hum.2004.15.1065
Roos AK, Eriksson F, Timmons JA, Gerhardt J, Nyman U, Gudmundsdotter L, Brave A, Wahren B, Pisa P (2009a) Skin electroporation: effects on transgene expression, DNA persistence and local tissue environment. PLoS One 4(9):e7226. doi:10.1371/journal.pone.0007226
Roos AK, Eriksson F, Walters DC, Pisa P, King AD (2009b) Optimization of skin electroporation in mice to increase tolerability of DNA vaccine delivery to patients. Mol Ther 17(9):1637–1642. doi:10.1038/mt.2009.120
Roth DA, Tawa NE Jr, O’Brien JM, Treco DA, Selden RF (2001) Nonviral transfer of the gene encoding coagulation factor VIII in patients with severe hemophilia A. N Engl J Med 344(23):1735–1742. doi:10.1056/NEJM200106073442301
Rottinghaus ST, Poland GA, Jacobson RM, Barr LJ, Roy MJ (2003) Hepatitis B DNA vaccine induces protective antibody responses in human non-responders to conventional vaccination. Vaccine 21(31):4604–4608
Roy MJ, Wu MS, Barr LJ, Fuller JT, Tussey LG, Speller S, Culp J, Burkholder JK, Swain WF, Dixon RM, Widera G, Vessey R, King A, Ogg G, Gallimore A, Haynes JR, Heydenburg Fuller D (2000) Induction of antigen-specific CD8+ T cells, T helper cells, and protective levels of antibody in humans by particle-mediated administration of a hepatitis B virus DNA vaccine. Vaccine 19(7–8):764–778
Russell JA, Roy MK, Sanford JC (1992) Physical trauma and tungsten toxicity reduce the efficiency of biolistic transformation. Plant Physiol 98(3):1050–1056
Sakai Y, Khajoee V, Ogawa Y, Kusuhara K, Katayama Y, Hara T (2006) A novel transfection method for mammalian cells using gas plasma. J Biotechnol 121(3):299–308. doi:10.1016/j.jbiotec.2005.08.020
Sakakima Y, Hayashi S, Yagi Y, Hayakawa A, Tachibana K, Nakao A (2005) Gene therapy for hepatocellular carcinoma using sonoporation enhanced by contrast agents. Cancer Gene Ther 12(11):884–889. doi:10.1038/sj.cgt.7700850
Sanford JC, Smith FD, Russell JA (1993) Optimizing the biolistic process for different biological applications. Methods Enzymol 217:483–509
Scherer F, Anton M, Schillinger U, Henke J, Bergemann C, Kruger A, Gansbacher B, Plank C (2002) Magnetofection: enhancing and targeting gene delivery by magnetic force in vitro and in vivo. Gene Ther 9(2):102–109. doi:10.1038/sj.gt.3301624
Scholtz V, Julak J, Kriha V, Mosinger J (2007a) Decontamination effects of low-temperature plasma generated by corona discharge. Part I: an overview. Prague Med Rep 108(2):115–127
Scholtz V, Julak J, Kriha V, Mosinger J, Kopecka S (2007b) Decontamination effects of low-temperature plasma generated by corona discharge. Part II: new insights. Prague Med Rep 108(2):128–146
Seid RC Jr, Look JL, Ruiz C, Frolov V, Flyer D, Schafer J, Ellingsworth L (2012) Transcutaneous immunization with Intercell’s vaccine delivery system. Vaccine 30(29):4349–4354. doi:10.1016/j.vaccine.2011.09.113
Sharpe M, Lynch D, Topham S, Major D, Wood J, Loudon P (2007) Protection of mice from H5N1 influenza challenge by prophylactic DNA vaccination using particle mediated epidermal delivery. Vaccine 25(34):6392–6398. doi:10.1016/j.vaccine.2007.06.009
Shen X, Soderholm J, Lin F, Kobinger G, Bello A, Gregg DA, Broderick KE, Sardesai NY (2012) Influenza A vaccines using linear expression cassettes delivered via electroporation afford full protection against challenge in a mouse model. Vaccine 30(48):6946–6954. doi:10.1016/j.vaccine.2012.02.071
Singh R, Kostarelos K (2009) Designer adenoviruses for nanomedicine and nanodiagnostics. Trends Biotechnol 27(4):220–229. doi:10.1016/j.tibtech.2009.01.003
Stewart DJ, Hilton JD, Arnold JM, Gregoire J, Rivard A, Archer SL, Charbonneau F, Cohen E, Curtis M, Buller CE, Mendelsohn FO, Dib N, Page P, Ducas J, Plante S, Sullivan J, Macko J, Rasmussen C, Kessler PD, Rasmussen HS (2006) Angiogenic gene therapy in patients with nonrevascularizable ischemic heart disease: a phase 2 randomized, controlled trial of AdVEGF(121) (AdVEGF121) versus maximum medical treatment. Gene Ther 13(21):1503–1511. doi:10.1038/sj.gt.3302802
Sun WH, Burkholder JK, Sun J, Culp J, Turner J, Lu XG, Pugh TD, Ershler WB, Yang NS (1995) In vivo cytokine gene transfer by gene gun reduces tumor growth in mice. Proc Natl Acad Sci U S A 92(7):2889–2893
Tachibana K (1992) Transdermal delivery of insulin to alloxan-diabetic rabbits by ultrasound exposure. Pharm Res 9(7):952–954
Tachibana K, Tachibana S (1991) Transdermal delivery of insulin by ultrasonic vibration. J Pharm Pharmacol 43(4):270–271
Tachibana K, Tachibana S (1993) Use of ultrasound to enhance the local anesthetic effect of topically applied aqueous lidocaine. Anesthesiology 78(6):1091–1096
Takeuchi Y, Dotson M, Keen NT (1992) Plant transformation: a simple particle bombardment device based on flowing helium. Plant Mol Biol 18(4):835–839
Tan CY, Statham B, Marks R, Payne PA (1982) Skin thickness measurement by pulsed ultrasound: its reproducibility, validation and variability. Br J Dermatol 106(6):657–667
Tauber E, Kollaritsch H, von Sonnenburg F, Lademann M, Jilma B, Firbas C, Jelinek T, Beckett C, Knobloch J, McBride WJ, Schuller E, Kaltenbock A, Sun W, Lyons A (2008) Randomized, double-blind, placebo-controlled phase 3 trial of the safety and tolerability of IC51, an inactivated Japanese encephalitis vaccine. J Infect Dis 198(4):493–499. doi:10.1086/590116
Terrier O, Essere B, Yver M, Barthelemy M, Bouscambert-Duchamp M, Kurtz P, VanMechelen D, Morfin F, Billaud G, Ferraris O, Lina B, Rosa-Calatrava M, Moules V (2009) Cold oxygen plasma technology efficiency against different airborne respiratory viruses. J Clin Virol 45(2):119–124. doi:10.1016/j.jcv.2009.03.017
Ugen KE, Kutzler MA, Marrero B, Westover J, Coppola D, Weiner DB, Heller R (2006) Regression of subcutaneous B16 melanoma tumors after intratumoral delivery of an IL-15-expressing plasmid followed by in vivo electroporation. Cancer Gene Ther 13(10):969–974. doi:10.1038/sj.cgt.7700973
Wang B, Yu H, Yang FR, Huang M, Ma JH, Tong GZ (2012) Protective efficacy of a broadly cross-reactive swine influenza DNA vaccine encoding M2e, cytotoxic T lymphocyte epitope and consensus H3 hemagglutinin. Virol J 9:127. doi:10.1186/1743-422X-9-127
Wentworth DE, McGregor MW, Macklin MD, Neumann V, Hinshaw VS (1997) Transmission of swine influenza virus to humans after exposure to experimentally infected pigs. J Infect Dis 175(1):7–15
Williams RS, Johnston SA, Riedy M, DeVit MJ, McElligott SG, Sanford JC (1991) Introduction of foreign genes into tissues of living mice by DNA-coated microprojectiles. Proc Natl Acad Sci U S A 88(7):2726–2730
Wolchok JD, Yuan J, Houghton AN, Gallardo HF, Rasalan TS, Wang J, Zhang Y, Ranganathan R, Chapman PB, Krown SE, Livingston PO, Heywood M, Riviere I, Panageas KS, Terzulli SL, Perales MA (2007) Safety and immunogenicity of tyrosinase DNA vaccines in patients with melanoma. Mol Ther 15(11):2044–2050. doi:10.1038/sj.mt.6300290
Wong TW, Chen CH, Huang CC, Lin CD, Hui SW (2006) Painless electroporation with a new needle-free microelectrode array to enhance transdermal drug delivery. J Control Rel 110(3):557–565. doi:10.1016/j.jconrel.2005.11.003
Wong TW, Chen TY, Huang CC, Tsai JC, Hui SW (2011) Painless skin electroporation as a novel way for insulin delivery. Diabetes Technol Ther 13(9):929–935. doi:10.1089/dia.2011.0077
Wu A, Zeng Q, Kang TH, Peng S, Roosinovich E, Pai SI, Hung CF (2011) Innovative DNA vaccine for human papillomavirus (HPV)-associated head and neck cancer. Gene Ther 18(3):304–312. doi:10.1038/gt.2010.151
Yang NS, Burkholder J, Roberts B, Martinell B, McCabe D (1990) In vivo and in vitro gene transfer to mammalian somatic cells by particle bombardment. Proc Natl Acad Sci U S A 87(24):9568–9572
Yin D, Yang WG, Weissberg J, Goff CB, Chen W, Kuwayama Y, Leiter A, Xing H, Meixel A, Gaut D, Kirkbir F, Sawcer D, Vernier PT, Said JW, Gundersen MA, Koeffler HP (2012) Cutaneous papilloma and squamous cell carcinoma therapy utilizing nanosecond pulsed electric fields (nsPEF). PLoS One 7(8):e43891. doi:10.1371/journal.pone.0043891
Zhou QH, Miller DL, Carlisle RC, Seymour LW, Oupicky D (2005) Ultrasound-enhanced transfection activity of HPMA-stabilized DNA polyplexes with prolonged plasma circulation. J Control Rel 106(3):416–427. doi:10.1016/j.jconrel.2005.05.002
Zimmer C, von Gabain A, Henics T (2001) Analysis of sequence-specific binding of RNA to Hsp70 and its various homologs indicates the involvement of N- and C-terminal interactions. RNA 7(11):1628–1637
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Donate, A., Heller, R. (2017). Gene Transfer to the Skin by Physical Methods of Delivery. In: Dragicevic, N., I. Maibach, H. (eds) Percutaneous Penetration Enhancers Physical Methods in Penetration Enhancement. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-53273-7_29
Download citation
DOI: https://doi.org/10.1007/978-3-662-53273-7_29
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-662-53271-3
Online ISBN: 978-3-662-53273-7
eBook Packages: MedicineMedicine (R0)