Lipid-mediated gene delivery to the skin

European Journal of Pharmaceutical Sciences

Volumn 43, Issue 4, 2011, Pages 199-211

  Geusens, Barbara ^a   Strobbe, Tine ^a   Bracke, Stefanie ^a   Dynoodt, Peter ^a   Sanders, Niek ^b   Gele, Mireille Van ^a   Lambert, Jo ^a  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

Gene delivery; Lipid based vesicles; Skin; Topical immunization

Indexed keywords

1,2 DIOLEOYL 3 TRIMETHYLAMMONIOPROPANE; ADENOVIRUS VECTOR; CATHELICIDIN; COLLAGEN TYPE 7; COLLAGEN TYPE 7 A1; FIBROBLAST GROWTH FACTOR; KALININ; KALININ BETA 3; LIPOSOME; NANOPARTICLE; NIOSOME; PLASMID DNA; PLATELET DERIVED GROWTH FACTOR; RETROVIRUS VECTOR; SMALL INTERFERING RNA; TRANSFERSOME; UNCLASSIFIED DRUG;

ANTIGEN PRESENTING CELL; ATOPIC DERMATITIS; DIABETIC FOOT; ELECTROPORATION; FOOT ULCER; GENE TARGETING; HUMAN; HUMAN TISSUE; IMMUNIZATION; LEG ULCER; LIPID VESICLE; MELANOMA; NANOEMULSION; NONHUMAN; PRIORITY JOURNAL; PSORIASIS; REVIEW; SKIN DISEASE; STRATUM CORNEUM; TOPICAL DRUG ADMINISTRATION; VITILIGO; WOUND HEALING;

ADMINISTRATION, CUTANEOUS; ANIMALS; DNA; GENE THERAPY; GENE TRANSFER TECHNIQUES; HUMANS; LIPOSOMES; SKIN;

EID: 79959598299     PISSN: 09280987     EISSN: 18790720     Source Type: Journal    
DOI: 10.1016/j.ejps.2011.04.003     Document Type: Review

References (132)

1. W. Abraham, and D.T. Downing Interaction between corneocytes and stratum corneum lipid liposomes in vitro Biochim. Biophys. Acta 1021 1990 119
2. Z. Ahmed, R.L. Banik, H.K. Paul, Q.H. Jaigirdar, F. Begum, and S.A. Chowdhury Histopathological changes in different stages of alopecia areata Mymensingh Med. J. 19 2010 100
3. V.L. Alcon, M. Foldvari, M. Snider, P. Willson, S. Gomis, R. Hecker, L.A. Babiuk, and M.E. Baca-Estrada Induction of protective immunity in pigs after immunisation with CpG oligodeoxynucleotides formulated in a lipid-based delivery system (Biphasix) Vaccine 21 2003 1811
4. V. Alcon, M. Baca-Estrada, M. Vega-Lopez, P. Willson, L.A. Babiuk, P. Kumar, R. Hecker, and M. Foldvari Mucosal delivery of bacterial antigens and CpG oligonucleotides formulated in biphasic lipid vesicles in pigs Aaps. J. 7 2005 E566
5. V.L. Alcon, M. Baca-Estrada, M.A. Vega-Lopez, P. Willson, L.A. Babiuk, P. Kumar, and M. Foldvari Intranasal immunization using biphasic lipid vesicles as delivery systems for OmlA bacterial protein antigen and CpG oligonucleotides adjuvant in a mouse model J. Pharm. Pharmacol. 57 2005 955
6. V.L. Alcon, M.E. Baca-Estrada, A. Potter, L.A. Babiuk, P. Kumar, and M. Foldvari Biphasic lipid vesicles as a subcutaneous delivery system for protein antigens and CpG oligonucleotides Curr. Drug Deliv. 3 2006 129
7. M.Y. Alexander, and R.J. Akhurst Liposome-medicated gene transfer and expression via the skin Hum. Mol. Genet. 4 1995 2279
8. S. Babiuk, M.E. Baca-Estrada, R. Pontarollo, and M. Foldvari Topical delivery of plasmid DNA using biphasic lipid vesicles (Biphasix) J. Pharm. Pharmacol. 54 2002 1609
9. I. Badea, R. Verrall, M. Baca-Estrada, S. Tikoo, A. Rosenberg, P. Kumar, and M. Foldvari In vivo cutaneous interferon-gamma gene delivery using novel dicationic (gemini) surfactant-plasmid complexes J. Gene Med. 7 2005 1200
10. S.C. Baek, Q. Lin, P.B. Robbins, H. Fan, and P.A. Khavari Sustainable systemic delivery via a single injection of lentivirus into human skin tissue Hum. Gene Ther. 12 2001 1551
11. J. Banchereau, and R.M. Steinman Dendritic cells and the control of immunity Nature 392 1998 245
12. B. Baroli Penetration of nanoparticles and nanomaterials in the skin: fiction or reality? J. Pharm. Sci. 99 2010 21
13. B.W. Barry Novel mechanisms and devices to enable successful transdermal drug delivery Eur. J. Pharm. Sci. 14 2001 101
14. I. Baumgartner, N. Chronos, A. Comerota, T. Henry, J.P. Pasquet, F. Finiels, A. Caron, J.F. Dedieu, R. Pilsudski, and P. Delaere Local gene transfer and expression following intramuscular administration of FGF-1 plasmid DNA in patients with critical limb ischemia Mol. Ther. 17 2009 914
15. A.D. Bins, A. Jorritsma, M.C. Wolkers, C.F. Hung, T.C. Wu, T.N. Schumacher, and J.B. Haanen A rapid and potent DNA vaccination strategy defined by in vivo monitoring of antigen expression Nat. Med. 11 2005 899
16. J.C. Birchall, C. Marichal, L. Campbell, A. Alwan, J. Hadgraft, and M. Gumbleton Gene expression in an intact ex-vivo skin tissue model following percutaneous delivery of cationic liposome-plasmid DNA complexes Int. J. Pharm. 197 2000 233
17. J.A. Bouwstra, and M. Ponec The skin barrier in healthy and diseased state Biochim. Biophys. Acta 1758 2006 2080
18. J.A. Bouwstra, P.L. Honeywell-Nguyen, G.S. Gooris, and M. Ponec Structure of the skin barrier and its modulation by vesicular formulations Prog. Lipid Res. 42 2003 1
19. M.B. Brown, G.P. Martin, S.A. Jones, and F.K. Akomeah Dermal and transdermal drug delivery systems: current and future prospects Drug Deliv. 13 2006 175
20. M. Carretero, M.J. Escamez, F. Prada, I. Mirones, M. Garcia, A. Holguin, B. Duarte, O. Podhajcer, J.L. Jorcano, F. Larcher, and M. Del Rio Skin gene therapy for acquired and inherited disorders Histol. Histopathol. 21 2006 1233
21. G. Cevc, and G. Blume Lipid vesicles penetrate into intact skin owing to the transdermal osmotic gradients and hydration force Biochim. Biophys. Acta 1104 1992 226
22. G. Cevc, and G. Blume New, highly efficient formulation of diclofenac for the topical, transdermal administration in ultradeformable drug carriers, Transfersomes Biochim. Biophys. Acta 1514 2001 191
23. G. Cevc, D. Gebauer, J. Stieber, A. Schatzlein, and G. Blume Ultraflexible vesicles, Transfersomes, have an extremely low pore penetration resistance and transport therapeutic amounts of insulin across the intact mammalian skin Biochim. Biophys. Acta 1368 1998 201
24. J.Y. Cheng, H.N. Huang, W.C. Tseng, T.L. Li, Y.L. Chan, K.C. Cheng, and C.J. Wu Transcutaneous immunization by lipoplex-patch based DNA vaccines is effective vaccination against Japanese encephalitis virus infection J. Controlled Release 135 2009 242
25. K.A. Choate, and P.A. Khavari Direct cutaneous gene delivery in a human genetic skin disease Hum. Gene Ther. 8 1997 1659
26. M.J. Choi, and H.I. Maibach Liposomes and niosomes as topical drug delivery systems Skin Pharmacol. Physiol. 18 2005 209
27. S.N. Ciotti, and N. Weiner Follicular liposomal delivery systems J. Liposome Res. 12 2002 143
28. D. Cosco, C. Celia, F. Cilurzo, E. Trapasso, and D. Paolino Colloidal carriers for the enhanced delivery through the skin Expert Opin. Drug Deliv. 5 2008 737
29. G. Cotsarelis The hair follicle as a target for gene therapy Ann. Dermatol. Venereol. 129 2002 841
30. Z. Cui, and R.J. Mumper Topical immunization using nanoengineered genetic vaccines J. Controlled Release 81 2002 173
31. Z. Cui, W. Fountain, M. Clark, M. Jay, and R.J. Mumper Novel ethanol-in-fluorocarbon microemulsions for topical genetic immunization Pharm. Res. 20 2003 16
32. A. Domashenko, S. Gupta, and G. Cotsarelis Efficient delivery of transgenes to human hair follicle progenitor cells using topical lipoplex Nat. Biotechnol. 18 2000 420
33. G.M. El Maghraby, and A.C. Williams Vesicular systems for delivering conventional small organic molecules and larger macromolecules to and through human skin Expert Opin. Drug Deliv. 6 2009 149
34. M.M. Elsayed, O.Y. Abdallah, V.F. Naggar, and N.M. Khalafallah Lipid vesicles for skin delivery of drugs: reviewing three decades of research Int. J. Pharm. 332 2007 1
35. S.A. Eming, J.S. Whitsitt, L. He, T. Krieg, J.R. Morgan, and J.M. Davidson Particle-mediated gene transfer of PDGF isoforms promotes wound repair J. Invest. Dermatol. 112 1999 297
36. K. Epbaria, and N. Weiner Liposomes as a drug delivery system Adv. Drug Deliv. Syst. 5 1990 287
37. H. Fan, Q. Lin, G.R. Morrissey, and P.A. Khavari Immunization via hair follicles by topical application of naked DNA to normal skin Nat. Biotechnol. 17 1999 870
38. J.Y. Fang, C.T. Hong, W.T. Chiu, and Y.Y. Wang Effect of liposomes and niosomes on skin permeation of enoxacin Int. J. Pharm. 219 2001 61
39. M. Fresta, and G. Puglisi Application of liposomes as potential cutaneous drug delivery systems. In vitro and in vivo investigation with radioactively labelled vesicles J. Drug Target. 4 1996 95
40. X. Gao, and L. Huang Cationic liposome-mediated gene transfer Gene Ther. 2 1995 710
41. B. Geusens, N. Sanders, T. Prow, M. Van Gele, and J. Lambert Cutaneous short-interfering RNA therapy Expert Opin. Drug Deliv. 6 2009 1333
42. S. Ghazizadeh, R. Harrington, and L. Taichman In vivo transduction of mouse epidermis with recombinant retroviral vectors: implications for cutaneous gene therapy Gene Ther. 6 1999 1267
43. K. Ghoreschi, P. Thomas, S. Breit, M. Dugas, R. Mailhammer, W. van Eden, R. van der Zee, T. Biedermann, J. Prinz, M. Mack, U. Mrowietz, E. Christophers, D. Schlondorff, G. Plewig, C.A. Sander, and M. Rocken Interleukin-4 therapy of psoriasis induces Th2 responses and improves human autoimmune disease Nat. Med. 9 2003 40
44. R. Gonzalez, L. Hutchins, J. Nemunaitis, M. Atkins, and P.O. Schwarzenberger Phase 2 trial of Allovectin-7 in advanced metastatic melanoma Melanoma Res. 16 2006 521
45. D.A. Greenhalgh, J.A. Rothnagel, and D.R. Roop Epidermis: an attractive target tissue for gene therapy J. Invest. Dermatol. 103 1994 63S
46. L.C. Heller, M.J. Jaroszeski, D. Coppola, and R. Heller Comparison of electrically mediated and liposome-complexed plasmid DNA delivery to the skin Genet. Vaccines Ther. 6 2008 16
47. U.R. Hengge, and A. Mirmohammadsadegh Adeno-associated virus expresses transgenes in hair follicles and epidermis Mol. Ther. 2 2000 188
48. U.R. Hengge, E.F. Chan, R.A. Foster, P.S. Walker, and J.C. Vogel Cytokine gene expression in epidermis with biological effects following injection of naked DNA Nat. Genet. 10 1995 161
49. R.P. Hickerson, F.J. Smith, R.E. Reeves, C.H. Contag, D. Leake, S.A. Leachman, L.M. Milstone, W.H. McLean, and R.L. Kaspar Single-nucleotide-specific siRNA targeting in a dominant-negative skin model J. Invest. Dermatol. 128 2008 594
50. U. Hoffman, Y. Tokura, T. Nishijima, M. Takigawa, and R. Paus Hair cycle-dependent changes in skin immune functions: anagen-associated depression of sensitization for contact hypersensitivity in mice J. Invest. Dermatol. 106 1996 598
51. H.E. Hofland, J.A. Bouwstra, H.E. Bodde, F. Spies, and H.E. Junginger Interactions between liposomes and human stratum corneum in vitro: freeze fracture electron microscopical visualization and small angle X-ray scattering studies Br. J. Dermatol. 132 1995 853
52. P.L. Honeywell-Nguyen, and J.A. Bouwstra Vesicles as a tool for transdermal and dermal delivery Drug Discov. Today: Technol. 2 2005 67
53. P.L. Honeywell-Nguyen, H.W.W. Groenink, and J.A. Bouwstra Elastic vesicles as a tool for dermal and transdermal delivery Drug Discov. Today: Technol. 2 2005 67
54. T. Ishimoto, Y. Takei, Y. Yuzawa, K. Hanai, S. Nagahara, Y. Tarumi, S. Matsuo, and K. Kadomatsu Downregulation of monocyte chemoattractant protein-1 involving short interfering RNA attenuates hapten-induced contact hypersensitivity Mol. Ther. 16 2008 387
55. S.C. Jayaraman, C. Ramachandran, and N. Weiner Topical delivery of erythromycin from various formulations: an in vivo hairless mouse study J. Pharm. Sci. 85 1996 1082
56. M.G. Jeschke, and D. Klein Liposomal gene transfer of multiple genes is more effective than gene transfer of a single gene Gene Ther. 11 2004 847
57. M.G. Jeschke, R.E. Barrow, H.K. Hawkins, M.T. Chrysopoulo, J.R. Perez-Polo, and D.N. Herndon Effect of multiple gene transfers of insulin like growth factor I complementary DNA gene constructs in rats after thermal injury Arch. Surg. 134 1999 1137
58. M.G. Jeschke, R.E. Barrow, H.K. Hawkins, K. Yang, R.L. Hayes, B.J. Lichtenbelt, J.R. Perez-Polo, and D.N. Herndon IGF-I gene transfer in thermally injured rats Gene Ther. 6 1999 1015
59. M.G. Jeschke, R.E. Barrow, H.K. Hawkins, Z. Tao, J.R. Perez-Polo, and D.N. Herndon Biodistribution and feasibility of non-viral IGF-I gene transfers in thermally injured skin Lab. Invest. 80 2000 151
60. M.G. Jeschke, T. Schubert, and D. Klein Exogenous liposomal IGF-I cDNA gene transfer leads to endogenous cellular and physiological responses in an acute wound Am. J. Physiol. Regul. Integr. Comp. Physiol. 286 2004 R958
61. J. Kanitakis Anatomy, histology and immunohistochemistry of normal human skin Eur. J. Dermatol. 12 2002 390
62. S. Kawakami, A. Sato, M. Nishikawa, F. Yamashita, and M. Hashida Mannose receptor-mediated gene transfer into macrophages using novel mannosylated cationic liposomes Gene Ther. 7 2000 292
63. P.A. Khavari Genetic correction of inherited epidermal disorders Hum. Gene Ther. 11 2000 2277
64. P.A. Khavari, O. Rollman, and A. Vahlquist Cutaneous gene transfer for skin and systemic diseases J. Intern. Med. 252 2002 1
65. Y. Kikuchi, K. Tamai, and Y. Kaneda Cutaneous gene delivery J. Dermatol. Sci. 50 2008 87
66. S.I. Kim, K.S. Kim, H.S. Kim, D.S. Kim, Y. Jang, K.H. Chung, and Y.S. Park Inhibitory effect of the salmosin gene transferred by cationic liposomes on the progression of B16BL6 tumors Cancer Res. 63 2003 6458
67. A. Kim, E.H. Lee, S.H. Choi, and C.K. Kim In vitro and in vivo transfection efficiency of a novel ultradeformable cationic liposome Biomaterials 25 2004 305
68. K.S. Kim, H.S. Kim, J.S. Park, Y.G. Kwon, and Y.S. Park Inhibition of B16BL6 tumor progression by coadministration of recombinant angiostatin K1-3 and endostatin genes with cationic liposomes Cancer Gene Ther. 11 2004 441
69. V. Kinet, N.Q. Nguyen, C. Sabatel, S. Blacher, A. Noel, J.A. Martial, and I. Struman Antiangiogenic liposomal gene therapy with 16K human prolactin efficiently reduces tumor growth Cancer Lett. 284 2009 222
70. G. Krueger, and C.N. Ellis Psoriasis-recent advances in understanding its pathogenesis and treatment J. Am. Acad. Dermatol. 53 2005 S94
71. S.A. Leachman, R.P. Hickerson, P.R. Hull, F.J. Smith, L.M. Milstone, E.B. Lane, S.J. Bale, D.R. Roop, W.H. McLean, and R.L. Kaspar Therapeutic siRNAs for dominant genetic skin disorders including pachyonychia congenita J. Dermatol. Sci. 51 2008 151
72. E.H. Lee, A. Kim, Y.K. Oh, and C.K. Kim Effect of edge activators on the formation and transfection efficiency of ultradeformable liposomes Biomaterials 26 2005 205
73. L. Li, and R.M. Hoffman Model of selective gene therapy of hair growth: liposome targeting of the active Lac-Z gene to hair follicles of histocultured skin In Vitro Cell. Dev. Biol. Anim. 31 1995 11
74. L. Li, and R.M. Hoffman Topical liposome delivery of molecules to hair follicles in mice J. Dermatol. Sci. 14 1997 101
75. L. Li, V. Lishko, and R.M. Hoffman Liposome targeting of high molecular weight DNA to the hair follicles of histocultured skin: a model for gene therapy of the hair growth processes In Vitro Cell. Dev. Biol. Anim. 29A 1993 258
76. J. Li, X. Li, Y. Zhang, X.K. Zhou, H.S. Yang, X.C. Chen, Y.S. Wang, Y.Q. Wei, L.J. Chen, H.Z. Hu, and C.Y. Liu Gene therapy for psoriasis in the K14-VEGF transgenic mouse model by topical transdermal delivery of interleukin-4 using ultradeformable cationic liposome J. Gene Med. 12 2010 481
77. Y. Lu, S. Kawakami, F. Yamashita, and M. Hashida Development of an antigen-presenting cell-targeted DNA vaccine against melanoma by mannosylated liposomes Biomaterials 28 2007 3255
78. S. Mahor, A. Rawat, P.K. Dubey, P.N. Gupta, K. Khatri, A.K. Goyal, and S.P. Vyas Cationic transfersomes based topical genetic vaccine against hepatitis B Int. J. Pharm. 340 2007 13
79. A. Manosroi, N. Khositsuntiwong, F. Gotz, R.G. Werner, and J. Manosroi Transdermal enhancement through rat skin of luciferase plasmid DNA loaded in elastic nanovesicles J. Liposome Res. 19 2009 91
80. J. Manosroi, N. Khositsuntiwong, W. Manosroi, F. Gotz, R.G. Werner, and A. Manosroi Enhancement of transdermal absorption, gene expression and stability of tyrosinase plasmid (pMEL34)-loaded elastic cationic niosomes: Potential application in vitiligo treatment J Pharm Sci. 99 2010 3533
81. M.C. Marchetto, A.R. Muotri, D.K. Burns, E.C. Friedberg, and C.F. Menck Gene transduction in skin cells: preventing cancer in xeroderma pigmentosum mice Proc. Natl. Acad. Sci. USA 101 2004 17759
82. D.J. Margolis, T. Cromblehome, M. Herlyn, P. Cross, L. Weinberg, J. Filip, and K. Propert Clinical protocol. Phase I trial to evaluate the safety of H5.020CMV.PDGF-b and limb compression bandage for the treatment of venous leg ulcer: trial A Hum. Gene Ther. 15 2004 1003
83. F. Mavilio, G. Pellegrini, S. Ferrari, F. Di Nunzio, E. Di Iorio, A. Recchia, G. Maruggi, G. Ferrari, E. Provasi, C. Bonini, S. Capurro, A. Conti, C. Magnoni, A. Giannetti, and M. De Luca Correction of junctional epidermolysis bullosa by transplantation of genetically modified epidermal stem cells Nat. Med. 12 2006 1397
84. X. Meng, D. Sawamura, K. Tamai, K. Hanada, H. Ishida, and I. Hashimoto Keratinocyte gene therapy for systemic diseases. Circulating interleukin 10 released from gene-transferred keratinocytes inhibits contact hypersensitivity at distant areas of the skin J. Clin. Invest. 101 1998 1462
85. N. Meykadeh, A. Mirmohammadsadegh, Z. Wang, E. Basner-Tschakarjan, and U.R. Hengge Topical application of plasmid DNA to mouse and human skin J. Mol. Med. 83 2005 897
86. D. Mishra, V. Dubey, A. Asthana, D.K. Saraf, and N.K. Jain Elastic liposomes mediated transcutaneous immunization against Hepatitis B Vaccine 24 2006 4847
87. S. Mitragotri, D. Ray, J. Farrell, H. Tang, B. Yu, J. Kost, D. Blankschtein, and R. Langer Synergistic effect of low-frequency ultrasound and sodium lauryl sulfate on transdermal transport J. Pharm. Sci. 89 2000 892
88. R.A. Morgan, and W.F. Anderson Human gene therapy Annu. Rev. Biochem. 62 1993 191
89. R.S. Mueller, J. Veir, K.V. Fieseler, and S.W. Dow Use of immunostimulatory liposome-nucleic acid complexes in allergen-specific immunotherapy of dogs with refractory atopic dermatitis - a pilot study Vet. Dermatol. 16 2005 61
90. H. Nakamura, M. Aoki, K. Tamai, M. Oishi, T. Ogihara, Y. Kaneda, and R. Morishita Prevention and regression of atopic dermatitis by ointment containing NF-kB decoy oligodeoxynucleotides in NC/Nga atopic mouse model Gene Ther. 9 2002 1221
91. L.B. Nanney, S. Paulsen, M.K. Davidson, N.L. Cardwell, J.S. Whitsitt, and J.M. Davidson Boosting epidermal growth factor receptor expression by gene gun transfection stimulates epidermal growth in vivo Wound Repair Regen. 8 2000 117
92. Z. Nemes, and P.M. Steinert Bricks and mortar of the epidermal barrier Exp. Mol. Med. 31 1999 5
93. S.M. Niemiec, J.M. Latta, C. Ramachandran, N.D. Weiner, and B.J. Roessler Perifollicular transgenic expression of human interleukin-1 receptor antagonist protein following topical application of novel liposome-plasmid DNA formulations in vivo J. Pharm. Sci. 86 1997 701
94. S. Nikol, I. Baumgartner, E. Van Belle, C. Diehm, A. Visona, M.C. Capogrossi, N. Ferreira-Maldent, A. Gallino, M.G. Wyatt, L.D. Wijesinghe, M. Fusari, D. Stephan, J. Emmerich, G. Pompilio, F. Vermassen, E. Pham, V. Grek, M. Coleman, and F. Meyer Therapeutic angiogenesis with intramuscular NV1FGF improves amputation-free survival in patients with critical limb ischemia Mol. Ther. 16 2008 972
95. D.W. Osborne, A.J. Ward, and K.J. O'Neill Microemulsions as topical drug delivery vehicles: in-vitro transdermal studies of a model hydrophilic drug J. Pharm. Pharmacol. 43 1991 450
96. K. Oshikawa, A.L. Rakhmilevich, F. Shi, P.M. Sondel, N. Yang, and D.M. Mahvi Interleukin 12 gene transfer into skin distant from the tumor site elicits antimetastatic effects equivalent to local gene transfer Hum. Gene Ther. 12 2001 149
97. N. Otberg, H. Richter, H. Schaefer, U. Blume-Peytavi, W. Sterry, and J. Lademann Variations of hair follicle size and distribution in different body sites J. Invest. Dermatol. 122 2004 14
98. Z. Paroo, and D.R. Corey Challenges for RNAi in vivo Trends Biotechnol. 22 2004 390
99. K.K. Peachman, M. Rao, and C.R. Alving Immunization with DNA through the skin Methods 31 2003 232
100. C.T. Pereira, D.N. Herndon, R. Rocker, and M.G. Jeschke Liposomal gene transfer of keratinocyte growth factor improves wound healing by altering growth factor and collagen expression J. Surg. Res. 139 2007 222
101. I. Plasencia, L. Norlen, and L.A. Bagatolli Direct visualization of lipid domains in human skin stratum corneum's lipid membranes: effect of pH and temperature Biophys. J. 93 2007 3142
102. R.J. Powell, M. Simons, F.O. Mendelsohn, G. Daniel, T.D. Henry, M. Koga, R. Morishita, and B.H. Annex Results of a double-blind, placebo-controlled study to assess the safety of intramuscular injection of hepatocyte growth factor plasmid to improve limb perfusion in patients with critical limb ischemia Circulation 118 2008 58
103. G.J. Prud'homme, Y. Glinka, A.S. Khan, and R. Draghia-Akli Electroporation-enhanced nonviral gene transfer for the prevention or treatment of immunological, endocrine and neoplastic diseases Curr. Gene Ther. 6 2006 243
104. N. Raghavachari, and W.E. Fahl Targeted gene delivery to skin cells in vivo: a comparative study of liposomes and polymers as delivery vehicles J. Pharm. Sci. 91 2002 615
105. M. Rodolfo, E.M. Cato, S. Soldati, R. Ceruti, M. Asioli, E. Scanziani, P. Vezzoni, G. Parmiani, and M.G. Sacco Growth of human melanoma xenografts is suppressed by systemic angiostatin gene therapy Cancer Gene Ther. 8 2001 491
106. J.L. Rodriguez, C.G. Miller, W.L. Garner, G.O. Till, P. Guerrero, N.P. Moore, M. Corridore, D.P. Normolle, D.J. Smith, and D.G. Remick Correlation of the local and systemic cytokine response with clinical outcome following thermal injury J. Trauma 34 1993 684
107. D. Sawamura, K. Yasukawa, K. Kodama, K. Yokota, K.C. Sato-Matsumura, T. Toshihiro, and H. Shimizu The majority of keratinocytes incorporate intradermally injected plasmid DNA regardless of size but only a small proportion of cells can express the gene product J. Invest. Dermatol. 118 2002 967
108. R.J. Scheuplein Mechanism of percutaneous absorption. II. Transient diffusion and the relative importance of various routes of skin penetration J. Invest. Dermatol. 48 1967 79
109. R.A. Schwendener, B. Ludewig, A. Cerny, and O. Engler Liposome-based vaccines Methods Mol. Biol. 605 2010 163
110. Z. Shi, D.T. Curiel, and D.C. Tang DNA-based non-invasive vaccination onto the skin Vaccine 17 1999 2136
111. C. Sinico, and A.M. Fadda Vesicular carriers for dermal drug delivery Expert Opin. Drug Deliv. 6 2009 813
112. M.G. Sotomayor, H. Yu, S. Antonia, E.M. Sotomayor, and D.M. Pardoll Advances in gene therapy for malignant melanoma Cancer Control. 9 2002 39
113. L. Speroni, J. Gasparri, A.B.V. de los, N.S. Chiaramoni, A. Smagur, S. Szala, M.C. Taira, and V.A.S. del Antitumoral effect of IL-12 gene transfected via liposomes into B16F0 cells Acta Biochim. Pol. 56 2009 249
114. A.T. Stopeck, A. Jones, E.M. Hersh, J.A. Thompson, D.M. Finucane, J.C. Gutheil, and R. Gonzalez Phase II study of direct intralesional gene transfer of allovectin-7, an HLA-B7/beta2-microglobulin DNA-liposome complex, in patients with metastatic melanoma Clin. Cancer Res. 7 2001 2285
115. L. Sun, L. Xu, H. Chang, F.A. Henry, R.M. Miller, J.M. Harmon, and T.B. Nielsen Transfection with aFGF cDNA improves wound healing J. Invest. Dermatol. 108 1997 313
116. G. Szabo The number of eccrine sweat glands in human skin Adv. Biol. Skin 3 1962 1
117. Y. Tabata, and Y. Ikada Effect of the size and surface charge of polymer microspheres on their phagocytosis by macrophage Biomaterials 9 1988 356
118. A. Tandle, D.G. Blazer 3rd, and S.K. Libutti Antiangiogenic gene therapy of cancer: recent developments J. Transl. Med. 2 2004 22
119. E. Touitou, N. Dayan, L. Bergelson, B. Godin, and M. Eliaz Ethosomes - novel vesicular carriers for enhanced delivery: characterization and skin penetration properties J. Controlled Release 65 2000 403
120. J.H. van den Berg, B. Nuijen, T.N. Schumacher, J.B. Haanen, G. Storm, J.H. Beijnen, and W.E. Hennink Synthetic vehicles for DNA vaccination J. Drug Target. 18 2010 1
121. J.H. van den Berg, K. Oosterhuis, W.E. Hennink, G. Storm, L.J. van der Aa, J.F. Engbersen, J.B. Haanen, J.H. Beijnen, T.N. Schumacher, and B. Nuijen Shielding the cationic charge of nanoparticle-formulated dermal DNA vaccines is essential for antigen expression and immunogenicity J. Controlled Release 141 2010 234
122. J.C. Vogel A direct in vivo approach for skin gene therapy Proc. Assoc. Am. Physicians 111 1999 190
123. J.C. Vogel Nonviral skin gene therapy Hum. Gene Ther. 11 2000 2253
124. B. Vora, A.J. Khopade, and N.K. Jain Proniosome based transdermal delivery of levonorgestrel for effective contraception J. Controlled Release 54 1998 149
125. K. Vrhovnik, J. Kristl, M. Sentjurc, and J. Smid-Korbar Influence of liposome bilayer fluidity on the transport of encapsulated substance into the skin as evaluated by EPR Pharm. Res. 15 1998 525
126. S.P. Vyas, R.P. Singh, S. Jain, V. Mishra, S. Mahor, P. Singh, P.N. Gupta, A. Rawat, and P. Dubey Non-ionic surfactant based vesicles (niosomes) for non-invasive topical genetic immunization against hepatitis B Int. J. Pharm. 296 2005 80
127. J. Wang, J.H. Hu, F.Q. Li, G.Z. Liu, Q.G. Zhu, J.Y. Liu, H.J. Ma, C. Peng, and F.G. Si Strong cellular and humoral immune responses induced by transcutaneous immunization with HBsAg DNA-cationic deformable liposome complex Exp. Dermatol. 16 2007 724
128. S. Watabe, K.Q. Xin, A. Ihata, L.J. Liu, A. Honsho, I. Aoki, K. Hamajima, B. Wahren, and K. Okuda Protection against influenza virus challenge by topical application of influenza DNA vaccine Vaccine 19 2001 4434
129. Watkinson, A.C., 2010, The future of transdermal drug delivery, in: Perspectives in Percutaneous Penetration, La Grande Motte, France.
130. D.T. Woodley, D.R. Keene, T. Atha, Y. Huang, R. Ram, N. Kasahara, and M. Chen Intradermal injection of lentiviral vectors corrects regenerated human dystrophic epidermolysis bullosa skin tissue in vivo Mol. Ther. 10 2004 318
131. C.J. Wraight, and P.J. White Antisense oligonucleotides in cutaneous therapy Pharmacol. Ther. 90 2001 89
132. H. Wu, C. Ramachandran, A.U. Bielinska, K. Kingzett, R. Sun, N.D. Weiner, and B.J. Roessler Topical transfection using plasmid DNA in a water-in-oil nanoemulsion Int. J. Pharm. 221 2001 23