On the search for skin gene therapy strategies of xeroderma pigmentosum disease

Current Gene Therapy

Volumn 7, Issue 3, 2007, Pages 163-174

  Menck, Carlos F M ^a   Armelini, Melissa G ^a   Lima Bessa, Keronninn M ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

DNA damage; DNA repair; Epidermis; Gene delivery; Keratinocytes; Sunlight; Transdermal gene transfer; Viral vectors

Indexed keywords

6 4PP DEOXYRIBODIPYRIMIDINE PHOTOLYASE; ADENOVIRUS VECTOR; BETA GALACTOSIDASE; BLOOD CLOTTING FACTOR 9; COMPLEMENTARY DNA; CPD DEOXYRIBODIPYRIMIDINE PHOTOLYASE; DEOXYRIBONUCLEASE (PYRIMIDINE DIMER); DERMATOLOGICAL AGENT; DNA; DNA VACCINE; ERYTHROPOIETIN; IMMUNOSUPPRESSIVE AGENT; KALININ; LENTIVIRUS VECTOR; LIPID EMULSION; LIPOSOME; NAKED DNA; PARVOVIRUS VECTOR; PLACEBO; POLYHISTIDINE; POLYLYSINE; RETROVIRUS VECTOR; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; XERODERMA PIGMENTOSUM GROUP A PROTEIN; XERODERMA PIGMENTOSUM GROUP C PROTEIN; XERODERMA PIGMENTOSUM GROUP D PROTEIN; XERODERMA PIGMENTOSUM GROUP V PROTEIN;

CANCER PREVENTION; CLINICAL FEATURE; CLINICAL TRIAL; DNA REPAIR; EPIDERMIS CELL; EX VIVO STUDY; GENE THERAPY; GENETIC DISORDER; GENODERMATOSIS; HAIR FOLLICLE; HEMOPHILIA; HUMAN; IN VITRO STUDY; KERATINOCYTE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; REVIEW; SKIN CANCER; SKIN CELL; SUNLIGHT; VIRAL GENE DELIVERY SYSTEM; XERODERMA PIGMENTOSUM;

ADMINISTRATION, CUTANEOUS; ANIMALS; DNA REPAIR; DNA REPAIR ENZYMES; GENE THERAPY; GENETIC VECTORS; HUMANS; LIPOSOMES; RECOMBINANT PROTEINS; SKIN; SUNLIGHT; XERODERMA PIGMENTOSUM;

ANIMALIA;

EID: 34250183843     PISSN: 15665232     EISSN: None     Source Type: Journal    
DOI: 10.2174/156652307780859017     Document Type: Review

References (93)

1. Agrawal, N., You, H., Liu, Y., Chiriva-Internati, M., Bremner, J., Garg, T., Grizzi, F., Krishna Prasad, C., Mehta, J.L. and Hermonat. P.L. (2004) Generation of recombinant skin in vitro by adeno-associated virus type 2 vector transduction. Tissue Eng., 10: 1707-1715.
2. Alba, R., Bosch, A. and Chillon, M. (2005) Gutless adenovirus: last-generation adenovirus for gene therapy. Gene Ther., 12: S18-S27.
3. Amado, R.G. and Chen, I.S.Y. (1999) Lentiviral vectors: the promise for gene therapy within reach? Science, 285: 674-676.
4. Amoh, Y., Li, L., Katsuoka, K., Penman, S. and Hoffman, R.M. (2005a) Multipotent nestin-positive, keratin-negative hair-follicle bulge stem cells can form neurons. Proc. Natl. Acad. Sci. U.S.A., 102: 5530-5534.
5. Amoh, Y., Li, L., Campillo, R., Kawahara, K., Katsuoka, K., Penman, S. and Hoffman, R.M. (2005b) Implanted hair follicle stem cells form Schwann cells that support repair of severed peripheral nerves. Proc. Natl. Acad. Sci. U.S.A., 102: 17734-17738.
6. Armelini, M.G., Muotri, A.R., Marchetto, M.C.N., Lima-Bessa, K.M., Sarasin, A. and Menck, C.F.M. (2005) Restoring DNA repair capacity of cells from three distinct diseases by XPD-gene recombinant adenovirus. Cancer Gene Ther., 12: 389-396.
7. Armelini, M.G., Lima-Bessa K.M., Marchetto M.C.N., Muotri A.R., Chiganças V., Leite R.A., Carvalho H. and Menck C.F.M. (2007) Exploring DNA damage responses in human cells with recombinant adenoviral vectors. Hum. Exp. Toxicol., in press.
8. Arnaudeau-Bégard, C., Brellier, F., Chevallier-Lagente, O., Hoeijmakers, J., Bernerd, F., Sarasin, A. and Magnaldo, T. (2003) Genetic correction of DNA repair-deficient/cancer-prone xeroderma pigmentosum group C keratinocytes. Hum. Gene Ther., 14: 983-996.
9. Bangari, D.S. and Mittal, S.K. (2006) Current strategies and future directions for eluding adenoviral vector immunity. Curr. Gene Ther., 6: 215-226.
10. Baum, C., Schambach, A., Bohne, J. and Galla, M. (2006) Retrovirus vectors: toward the plentivirus? Mol. Ther., 13: 1050-1063.
11. Beer, S.J., Matthews, C.B., Stein, C.S., Ross, B.D., Hilfinger, J.M. and Davidson, B.L. (1998) Poly (lactic-glycolic) acid copolymer encapsulation of recombinant adenovirus reduces immunogenicity in vivo. Gene Ther., 5: 740-746.
12. Bernerd, F., Asselineau, D., Vioux, C., Chevallier-Lagente, O., Bouadjar, B., Sarasin, A. and Magnaldo, T. (2001) Clues to epidermal cancer proneness revealed by reconstruction of DNA repair-deficient xeroderma pigmentosum skin in vitro. Proc. Natl. Acad. Sci. U.S.A.,. 98: 7817-7822.
13. Bett, A.J., Haddara, W., Prevec, L. and Graham, F.L. (1994) An efficient and flexible system for construction of adenovirus vectors with insertions or deletions in early regions 1 and 3. Proc. Natl.Acad. Sci. U.S.A., 91: 8802-8806.
14. Birchall, J. C. (2006) Microneedle array technology: the time is right but is the science ready? Expert Rev. Med. Devices, 3: 1-4.
15. Blomer, U., Naldini, L., Kafri, T., Trono, D., Verma, I.M. and Gage, F.H. (1997) Highly efficient and sustained gene transfer in adult neurons with a lentivirus vector. J. Virol., 71:6641-6649.
16. Bramson, J., Dayball, K., Evelegh, C., Wan, Y.H., Page, D. and Smith, A. (2003) Enabling topical immunization via microporation: a novel method for pain-free and needle-free delivery of adenovirus-based vaccines. Gene Ther., 10: 251-260.
17. Braun-Falco, M., Doenecke, A., Smola, H. and Hallek, M. (1999) Efficient gene transfer into human keratinocytes with recombinant adeno-associated virus vectors. Gene Ther., 6: 432-441.
18. Braun-Falco, M., Eisenried, A., Buning, H. and Ring, J. (2005) Recombinant adeno-associated virus type 2-mediated gene transfer into human keratinocytes is influenced by both the ubiquitin/proteasome pathway and epidermal growth factor receptor tyrosine kinase. Arch. Dermatol. Res., 296: 528-535.
19. Cheng, L., Ziegelhoffer, P.R. and Yang, N.S. (1993) In vivo promoter activity and transgene expression in mammalian somatic tissues evaluated by using particle bombardment. Proc. Natl. Acad. Sci. U.S.A., 90: 4455-4459.
20. Cleaver, J.E. (1968) Defective repair replication of DNA in xeroderma pigmentosum. Nature, 218: 652-656.
21. Cleaver, J.E. (2005) Cancer in xeroderma pigmentosum and related disorders of DNA repair. Nat. Rev. Cancer, 5: 564-573.
22. Costa, R.M.A., Chiganças, V., Galhardo, R.S., Carvalho, H. and Menck, C.F.M. (2003) The eukaryotic nucleotide excision repair pathway. Biochimie, 85: 1083-1099.
23. Coulman, S.A., Barrow, D., Anstey, A., Gateley, C., Morrissey, A., Wilke, N., Allender, C., Brain, K. and Birchall, J.C. (2006) Minimally invasive cutaneous delivery of macromolecules and plasmid DNA via microneedles. Curr. Drug Deliv., 3: 65-75.
24. Croyle, M.A., Chirmule, N., Zhang, Y. and Wilson, J.M. (2001) "Stealth" adenoviruses blunt cell-mediated and humoral immune responses against the virus and allow for significant gene expression upon readministration in the lung. J. Virol., 75: 4792-4801.
25. Dellambra, E., Pellegrini, G., Guerra, L., Ferrari, G., Zambruno, G., Mavilio, F. and De Luca, M. (2000) Toward epidermal stem cell-mediated ex vivo gene therapy of junctional epidermolysis bullosa. Hum. Gene Ther., 11: 2283-2287.
26. Domashenko, A., Gupta, S. and Cotsarelis, G. (2000) Efficient delivery of transgenes to human hair follicle progenitor cells using topical lipoplex. Nat. Biotechnol., 18: 420-423.
27. Donahue, B.A., McArthur, J.G., Spratt, S.K., Bohl, D., Lagarde, C., Sanchez, L., Kaspar, B.A., Sloan, B.A., Lee, Y.L., Danos, O. and Snyder, R.O. (1999) Selective uptake and sustained expression of AAV vectors following subcutaneous delivery. J. Gene Med., 1: 31-42.
28. Drabick, J.J., Glasspool-Malone, J., King, A. and Malone, R.W. (2001) Cutaneous transfection and immune responses to intradermal nucleic acid vaccination are significantly enhanced by in vivo electropermeabilization. Mol. Ther., 3: 249-255.
29. Dumaz, N., Drougard, C., Quilliet, X., Mezzina, M., Sarasin, A. and Daya-Grosjean, L. (1998) Recovery of the normal p53 response after UV treatment in DNA repair-deficient fibroblasts by retroviral-mediated correction with the XPD gene. Carcinogenesis, 19: 1701-1704.
30. Fasbender, A., Zabnerm, J., Chillon, M., Moninger, T.O., Puga, A.P., Davidson, B.L. and Welsh, M.J. (1997) Complexes of adenovirus with polycationic polymers and cationic lipids increase the efficiency of gene transfer in vitro and in vivo. J. Biol. Chem., 272: 6479-6489.
31. Foldvari, M., Babiuk, S., Badea, I. (2006) DNA delivery for vaccination and therapeutics through the skin. Curr. Drug Deliv., 3: 17-28.
32. Frechet, M., Bergoglio, V., Chevallier-Lagente, O., Sarasin, A. and Magnaldo, T. (2006) Complementation assays adapted for DNA repair-deficient keratinocytes. Methods Mol. Biol., 314: 9-23.
33. Friedberg, E.C., Lehmann, A.R. and Fuchs, R.P.P. (2005) Trading places: how do DNA polymerases switch during translesion DNA synthesis? Mol. Cell, 18:499-505.
34. Gao, G., Vandenberghe, L.H., Alvira, M.R., Lu, Y., Calcedo, R., Zhou, X. and Wilson, J.M. (2004) Clades of Adeno-associated viruses are widely disseminated in human tissues. J. Virol., 78: 6381-6388.
35. Gao, G., Vandenberghe L.H. and Wilson J.M. (2005) New recombinant serotypes of AAV vectors. Curr. Gene Ther., 5: 285-297.
36. Ginsburg, D.S. and Calos, M.P. (2005) Site-specific integration with phiC31 integrase for prolonged expression of therapeutic genes; Adv. Genet., 54: 179-187.
37. Glasspool-Malone, J., Somiari, S., Drabick, J.J. and Malone, R.W. (2000) Efficient nonviral cutaneous transfection. Mol. Ther., 2: 140-146.
38. Gonçalves, M.A., de Vries, A.A. (2006) Adenovirus: from foe to friend. Rev. Med. Virol., 16: 167-186.
39. Halbert C.L., Standaert, T.A., Aitken, M.L., Alexander, I.E., Russell, D.W. and Miller, A.D. (1997) Transduction by adeno-associated virus vectors in the rabbit airway: efficiency, persistence, and readministration. J. Virol., 71: 5932-5941.
40. Hengge, U.R. and Mirmohammadsadegh, A. (2000) Adeno-associated virus expresses transgenes in hair follicles and epidermis. Mol. Ther., 2: 188-194.
41. Hengge, U.R. (2005) Progress and prospects of skin gene therapy: a ten year history. Clin. Dermatol., 23: 107-114.
42. Hengge, U.R. and Bardenheuer, W. (2004) Gene therapy and the skin. Am. J. Med. Genet. C. Semin. Med. Genet., 131C: 93-100.
43. Hoffman, R.M. (2006) The hair follicle and its stem cells as drug delivery targets. Expert Opin. Drug Deliv., 3: 437-443.
44. Hopewell, J.W. (1990) The skin: its structure and response to ionizing radiation. Int. J. Radiat. Biol., 57: 751-773.
45. Jalkanen, M., Rapraeger, A. and Bernfield, M. (1988) Mouse mammary epithelial cells produce basement membrane and cell surface heparan sulfate proteoglycans containing distinct core proteins. J. Cell Biol., 106: 953-962.
46. Jiang, H., Couto, L.B., Patarroyo-White, S., Liu, T., Nagy, D., Vargas, J.A., Zhou, S., Scallan, C.D., Sommer, J., Vijay, S., Mingozzi, F., High, K.A. and Pierce, G.F. (2006) Effects of transient immunosuppression on adeno-associated, virus-mediated, liver-directed gene transfer in rhesus macaques and implications for human gene therapy. Blood, 108: 3321-3328.
47. Kafri, T., Blomer, U., Peterson, D.A., Gage, F.H. and Verma, I.M. (1997) Sustained expression of genes delivered directly into liver and muscle by lentiviral vectors. Nat. Genet., 17: 314-317.
48. Kaplan, J.M., Pennington, S.E., St George, J.A., Woodworth, L.A., Fasbender, A., Marshall, J., Cheng, S.H., Wadsworth, S.C., Gregory, R.J. and Smith, A.E. (1998) Potentiation of gene transfer to the mouse lung by complexes of adenovirus vector and polycations improves therapeutic potential. Hum. Gene Ther., 9: 1469-1479.
49. Karmali P.P. and Chaudhuri, A. (2007) Cationic liposomes as non-viral carriers of gene medicines: resolved issues, open questions, and future promises. Med. Res. Rev., in press.
50. Kashiwakura, Y., Tamayose, K., Iwabuchi, K., Hirai, Y., Shimada, T., Matsumoto, K., Nakamura, T., Watanabe, M., Oshimi, K. and Daida, H. (2005) Hepatocyte growth factor receptor is a coreceptor for adeno-associated virus type 2 infection. J. Virol., 79: 609-614.
51. Kraemer, K.H. and DiGiovanna, J.J. (2002) Topical enzyme therapy for skin diseases? J. Am. Acad. Dermatol., 46: 463-466.
52. Kraemer, K.H., Lee, M.M. and Scotto, J. (1987) Xeroderma pigmentosum. Cutaneous, ocular, and neurologic abnormalities in 830 published cases. Arch. Dermatol., 123: 241-256.
53. Le Bec, C. and Douar, A.M. (2006) Gene therapy progress and prospects - vectorology: design and production of expression cassettes in AAV vectors. Gene Ther., 13: 805-813.
54. Lehmann, A.R. (2003) DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie, 85: 1101-1111.
55. Li, L. and Hoffman, R.M. (1995) The feasibility of targeted selective gene therapy of the hair follicle. Nat. Med., 1: 705-706.
56. Lima-Bessa, K.M., Chigancas, V., Stary, A., Kannouche, P., Sarasin, A., Armelini, M.G., de Fatima Jacysyn, J., Amarante-Mendes, G.P., Cordeiro-Stone, M., Cleaver, J.E. and Menck C.F. (2006) Adenovirus mediated transduction of the human DNA polymerase eta cDNA. DNA Repair, 5: 925-934.
57. Lima-Bessa, K.M. and Menck, C.F. (2005) Skin cancer: lights on genome lesions. Curr. Biol., 15: R58-R61.
58. Lotti, F. and Mavilio, F. (2003) The choice of a suitable lentivirus vector transcriptional targeting. Methods Mol. Biol., 229: 17-27.
59. Magnaldo, T. (2004) Xeroderma pigmentosum: from genetics to hopes and realities of cutaneous gene therapy. Expert Opin. Biol. Ther., 4: 169-179.
60. Magnaldo, T. and Sarasin, A. (2004) Xeroderma pigmentosum: from symptoms and genetics to gene-based skin therapy. Cells Tissues Organs, 177: 189-198.
61. Marchetto, M.C.N., Correa, R.G., Menck, C.F.M. and Muotri, A.R. (2006) Functional lentiviral vectors for xeroderma pigmentosum gene therapy. J. Biotechnol., 126: 424-430.
62. Marchetto, M.C.N., Muotri, A.R., Burns, D.K., Friedberg, E.C. and Menck, C.F.M. (2004) Gene transduction in skin cells: preventing cancer in xeroderma pigmentosum mice. Proc. Natl. Acad. Sci. U.S.A., 101: 17759-17764.
63. Meira, L.B., Reis, A.M., Cheo, D.L., Nahari, D., Burns, D.K. and Friedberg, E.C. (2001) Cancer predisposition in mutant mice defective in multiple genetic pathways: uncovering important genetic interactions. Mutat. Res., 477: 51-58.
64. Meyers, C., Mane, M., Kokorina, N., Alam, S. and Hermonat, P.L. (2000) Ubiquitous human adeno-associated virus type 2 autonomously replicates in differentiating keratinocytes of a normal skin model. Virology, 272: 338-346.
65. Muotri, A.R., Marchetto, M.C.N., Zerbini, L.F.C., Libermann, T.A., Ventura, A.M., Sarasin, A. and Menck, C.F.M. (2002) Complementation of the DNA repair deficiency in human xeroderma pigmentosum group A and C cells by recombinant adenovirus-mediated gene transfer. Hum. Gene Ther., 13: 1833-1844.
66. Naldini, L., Blomer, U., Gage, F.H., Trono, D. and Verma, I.M. (1996) Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc. Natl. Aca. Sci. U.S.A., 93: 11382-11388.
67. Ortiz-Urda, S., Thyagarajan, B., Keene, D.R., Lin, Q., Fang, M., Calos, M.P. and Khavari, P.A. (2002) Stable nonviral genetic correction of inherited human skin disease. Nat. Med., 8: 1166-1170.
68. Price, A., Limberis, M., Gruneich, J.A., Wilson, J.M. and Diamond, S.L. (2005) Targeting viral-mediated transduction to the lung airway epithelium with the anti-inflammatory cationic lipid dexamethasonespermine. Mol. Ther., 12: 502-509.
69. Qing, K., Mah, C., Hansen, J., Zhou, S., Dwarki, V. and Srivastava, A. (1999) Human fibroblast growth factor receptor 1 is a co-receptor for infection by adeno-associated virus 2. Nat. Med., 5: 71-77.
70. Quilliet, X., Chevallier-Lagente, O., Eveno, E., Stojkovic, T., Destee, A., Sarasin, A. and Mezzina, M. (1996) Long-term complementation of DNA repair deficient human primary fibroblasts by retroviral transduction of the XPD gene. Mutat. Res., 364: 161-169.
71. Ritter, T., Lehmann, M. and Volk, H.D. (2002) Improvements in gene therapy: averting the immune response to adenoviral vectors. BioDrugs, 16: 3-10.
72. Rux, J.J. and Burnett, R.M. (2004) Adenovirus structure.Hum. Gene Ther., 15: 1167-1176.
73. Sailaja, G., HogenEsch, H., North, A., Hays, J. and Mittal, S.K. (2002) Encapsulation of recombinant adenovirus into alginate microspheres circumvents vector-specific immune response. Gene Ther., 9: 1722-1729.
74. Snoeys, J., Mertens, G., Lievens, J., van Berkel, T., Collen, D., Biessen, E.A. and De Geest. B. (2006) Lipid emulsions potently increase transgene expression in hepatocytes after adenoviral transfer. Mol. Ther., 13: 98-107.
75. Spirito, F., Capt A., Del Rio, M., Larcher, F., Guaguere, E., Danos, O. and Meneguzzi, G. (2006) Sustained phenotypic reversion of junctional epidermolysis bullosa dog keratinocytes: establishment of an immunocompetent animal model for cutaneous genetherapy. Biochem. Biophys. Res. Commun., 339: 769-778.
76. Steel, J.C., Cavanagh, H.M., Burton, M.A., Dingwall, D.J. and Kalle, W.H. (2005) Modification of liposomal concentration in liposome/ adenoviral complexes allows significant protection of adenoviral vectors from neutralising antibody, in vitro. J. Virol. Methods, 126: 31-36.
77. Summerford, C., Bartlett, J.S. and Samulski, R.J. (1999) AlphaVbeta5 integrin: a co-receptor for adeno-associated virus type 2 infection. Nat. Med., 5: 78-82.
78. Tanaka, K. Kamiuchi, S., Ren, Y., Yonemasu, R., Ichikawa, M., Murai, H., Yoshino, M., Takeuchi, S., Saijo, M., Nakatsu, Y., Miyauchi-Hashimoto, H. and Horio, T. (2001) UV-induced skin carcinogenesis in xeroderma pigmentosum group A (XPA) gene-knockout mice with nucleotide excision repair-deficiency. Mutat. Res., 447: 31-40.
79. Thomas, C.E., Ehrhardt, A. and Kay, M.A. (2003) Progress and problems with the use of viral vectors for gene therapy. Nat. Genet., 4: 346-358.
80. Udvardi, A., Kufferath, I., Grutsch, H., Zatloukal, K., Volc-Platzer, B. (1999) Uptake of exogenous DNA via the skin. J. Mol. Med., 77: 744-750.
81. Uitto, J. and Christiano, A.M. (1994) Molecular basis for the dystrophic form of epidermolysis bullosa: mutations in the type VII collagen gene. Arch. Dermatol. Res., 287: 16-22.
82. Volpers, C. and Kochanek, S. (2004) Adenoviral vectors for gene transfer and therapy. J. Gene Med., 6: 164-171.
83. Weaver, J.C. (1993) Electroporation: a general phenomenon for manipulating cells and tissues. J. Cell. Biochem., 51: 426-435.
84. Woodley, D.T., Keene, D.R., Atha, T., Huang, Y., Ram, R., Kasahara, N. and Chen, M. (2004) Intradermal injection of lentiviral vectors corrects regenerated human dystrophic epidermolysis bullosa skin tissue in vivo. Mol. Ther., 10: 318-326.
85. Wu, Z., Asokan, A. and Samulski, R.J. (2006) Adeno-associated virus serotypes: vector toolkit for human gene therapy. Mol. Ther., 14: 316-327.
86. Yang, C.H., Shen, S.C., Lee, J.C., Wu, P.C., Hsueh, S.F., Lu, C.Y., Meng, C.T., Hong, H.S. and Yang, L.C. (2004) Seeing the gene therapy: application of gene gun technique to transfect and decolour pigmented rat skin with human agouti signalling protein cDNA. Gene Ther., 11: 1033-1039.
87. Yarosh, D., Klein, J., O'Connor, A., Hawk, J., Rafal, E. and Wolf, P. (2001) Effect of topically applied T4 endonuclease V in liposomes on skin cancer in xeroderma pigmentosum: a randomised study. Xeroderma Pigmentosum Study Group. Lancet, 357: 926-929.
88. Yarosh, D.B. (2004) DNA repair, immunosuppression, and skin cancer. Cutis, 74: 10-13.
89. Young, L.S., Searle, P.F., Onion, D. and Mautner, V. (2006) Viral gene therapy strategies: from basic science to clinical application. J. Pathol., 208: 299-318.
90. Yotnda, P., Chen, D.H,, Chiu, W., Piedra, P.A., Davis, A., Templeton, N.S. and Brenner M.K. (2002) Bilamellar cationic liposomes protect adenovectors from preexisting humoral immune responses. Mol. Ther., 5: 233-241.
91. Zhang, L., Nolan, E., Kreitschitz, S. and Rabussay, D.P. (2002) Enhanced delivery of naked DNA to the skin by non-invasive in vivo electroporation. Biochim. Biophys. Acta, 1572: 1-9.
92. Zhang, L., Widera, G. and Rabussay, D. (2004) Enhancement of the effectiveness of electroporation-augmented cutaneous DNA vaccination by a particulate adjuvant. Bioelectrochemistry, 63: 369-373.
93. Zhang, X. and Godbey, W.T. (2006) Viral vectors for gene delivery in tissue engineering. Adv. Drug Deliv. Rev., 58: 515-534.