Gene therapy of skin adhesion disorders (mini review)

Current Pharmaceutical Biotechnology

Volumn 13, Issue 10, 2012, Pages 1868-1876

  Cavazza, Alessia ^a   Mavilio, Fulvio ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

Epidermolysis bullosa; Gene therapy; Genetic diseases; Retroviral vectors; Stem cells

Indexed keywords

COLLAGEN TYPE 7; COLLAGEN TYPE 7A1; COMPLEMENTARY DNA; LAMININ; LENTIVIRUS VECTOR; RETROVIRUS VECTOR; UNCLASSIFIED DRUG;

ARTICLE; EPIDERMOLYSIS BULLOSA; GENE EXPRESSION; GENE TARGETING; GENE THERAPY; GENE TRANSFER; GENE VECTOR; GENETIC TRANSDUCTION; HUMAN; KERATINOCYTE; NONHUMAN; SKIN ADHESION DEFECT; SKIN DISEASE; SKIN TRANSPLANTATION; STEM CELL TRANSPLANTATION; VIRAL GENE DELIVERY SYSTEM;

CLINICAL TRIALS AS TOPIC; EPIDERMOLYSIS BULLOSA; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; HUMANS; SKIN TRANSPLANTATION; TREATMENT OUTCOME;

EID: 84866652391     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920112802273119     Document Type: Article

References (73)

1. Uitto, J.; Christiano, A. M., Molecular genetics of the cutaneous basement membrane zone. Perspectives on epidermolysis bullosa and other blistering skin diseases. J. Clin. Invest., 1992, 90(3), 687-692.
2. Uitto, J.; Richard, G. Progress in epidermolysis bullosa: from eponyms to molecular genetic classification. Clin. Dermatol., 2005, 23(1), 33-40.
3. Uitto, J.; Pulkkinen, L. The genodermatoses: candidate diseases for gene therapy. Hum. Gene. Ther., 2000, 11(16), 2267-2275.
4. Hengge, U. R. Gene therapy progress and prospects: the skin--easily accessible, but still far away. Gene. Ther., 2006, 13(22), 1555-1563.
5. Uitto, J. Progress in heritable skin diseases: translational implications of mutation analysis and prospects of molecular therapies*. Acta Derm. Venereol., 2009, 89(3), 228-235.
6. Tamai, K.; Kaneda, Y.; Uitto, J. Molecular therapies for heritable blistering diseases. Trends Mol. Med., 2009, 15(7), 285-292.
7. Pellegrini, G.; Rama, P.; Mavilio, F.; De Luca, M. Epithelial stem cells in corneal regeneration and epidermal gene therapy. J. Pathol., 2009, 217(2), 217-228.
8. Morgan, J. R.; Barrandon, Y.; Green, H.; Mulligan, R. C. Expression of an exogenous growth hormone gene by transplantable human epidermal cells. Science, 1987, 237 1476-1479.
9. Fakharzadeh, S. S.; Zhang, Y.; Sarkar, R.; Kazazian, H. H. Jr. Correction of the coagulation defect in hemophilia A mice through factor VIII expression in skin. Blood, 2000, 95(9), 2799-2805.
10. Garlick, J. A.; Katz, A. B.; Fenjves, E. S.; Taichman, L. B. Retrovirus-mediated transduction of cultured epidermal keratinocytes. J. Invest. Dermatol., 1991, 97 824-829.
11. Mathor, M. B.; Ferrari, G.; Dellambra, E.; Cilli, M.; Mavilio, F.; Cancedda, R.; De Luca, M., Clonal analysis of stably transduced human epidermal stem cells in culture. Proc. Natl. Acad. Sci. USA, 1996, 93 10371-10376.
12. White, S. J.; Page, S. M.; Margaritis, P.; Brownlee, G. G. Longterm expression of human clotting factor IX from retrovirally transduced primary human keratinocytes in vivo. Hum. Gene Ther., 1998, 9 1187-1195.
13. Fenjves, E. S.; Yao, S. N.; Kurachi, K.; Taichman, L. B. Loss of expression of a retrovirus-transduced gene in human keratinocytes. J. Invest. Dermatol., 1996, 106 576-578.
14. Gerrard, A. J.; Hudson, D. L.; Brownlee, G. G.; Watt, F. M. Towards gene therapy for haemophilia B using primary human keratinocytes. Nat. Genet., 1993, 3 180-183.
15. Kolodka, T. M.; Garlick, J. A.; Taichman, L. B. Evidence for keratinocyte stem cells in vitro: long term engraftment and persistence of transgene expression from retrovirus-transduced keratinocytes. Proc. Natl. Acad. Sci. USA, 1998, 95 4356-4361.
16. Gambardella, L.; Barrandon, Y. The multifaceted adult epidermal stem cell. Curr. Opin. Cell Biol., 2003, 15(6), 771-777.
17. Blanpain, C.; Horsley, V.; Fuchs, E. Epithelial stem cells: turning over new leaves. Cell, 2007, 128(3), 445-458.
18. Levy, L.; Broad, S.; Zhu, A. J.; Carroll, J. M.; Khazaal, I.; Peault, B.; Watt, F. M. Optimised retroviral infection of human epidermal keratinocytes: long-term expression of transduced integrin gene following grafting on to SCID mice. Gene. Ther., 1998, 5(7), 913-922.
19. Mathor, M. B.; Ferrari, G.; Dellambra, E.; Cilli, M.; Mavilio, F.; Cancedda, R.; De Luca, M. Clonal analysis of stably transduced human epidermal stem cells in culture. Proc. Natl. Acad. Sci. USA, 1996, 93(19), 10371-10376.
20. White, S. J.; Page, S. M.; Margaritis, P.; Brownlee, G. G. Longterm expression of human clotting factor IX from retrovirally transduced primary human keratinocytes in vivo. Hum. Gene. Ther., 1998, 9(8), 1187-1195.
21. Fine, J. D.; Eady, R. A.; Bauer, E. A.; Bauer, J. W.; Bruckner-Tuderman, L.; Heagerty, A.; Hintner, H.; Hovnanian, A.; Jonkman, M. F.; Leigh, I.; McGrath, J. A.; Mellerio, J. E.; Murrell, D. F.; Shimizu, H.; Uitto, J.; Vahlquist, A.; Woodley, D.; Zambruno, G., The classification of inherited epidermolysis bullosa (EB): Report of the Third International Consensus Meeting on Diagnosis and Classification of EB. J. Am. Acad. Dermatol., 2008, 58(6), 931-950.
22. Fine, J. D. Inherited epidermolysis bullosa: recent basic and clinical advances. Curr. Opin. Pediatr., 2010, 22(4), 453-458.
23. Christiano, A. M.; Uitto, J. Molecular complexity of the cutaneous basement membrane zone. Revelations from the paradigms of epidermolysis bullosa. Exp. Dermatol., 1996, 5, 1-11.
24. Pulkkinen, L.; Uitto, J. Hemidesmosomal variants of epidermolysis bullosa. Mutations in the alpha6beta4 integrin and the 180-kD bullous pemphigoid antigen/type XVII collagen genes. Exp. Dermatol., 1998, 7(2-3), 46-64.
25. Koss-Harnes, D.; Hoyheim, B.; Anton-Lamprecht, I.; Gjesti, A.; Jorgensen, R. S.; Jahnsen, F. L.; Olaisen, B.; Wiche, G.; Gedde-Dahl, T. Jr. A site-specific plectin mutation causes dominant epidermolysis bullosa simplex Ogna: two identical de novo mutations. J. Invest. Dermatol., 2002, 118(1), 87-93.
26. Chen, M.; Kasahara, N.; Keene, D. R.; Chan, L.; Hoeffler, W. K.; Finlay, D.; Barcova, M.; Cannon, P. M.; Mazurek, C.; Woodley, D. T. Restoration of type VII collagen expression and function in dystrophic epidermolysis bullosa. Nat. Genet., 2002, 32(4), 670-675.
27. Dellambra, E.; Vailly, J.; Pellegrini, G.; Bondanza, S.; Golisano, O.; Macchia, C.; Zambruno, G.; Meneguzzi, G.; De Luca, M. Corrective transduction of human epidermal stem cells in laminin-5-dependent junctional epidermolysis bullosa. Hum. Gene Ther., 1998, 9 1359-1370.
28. Robbins, P. B.; Lin, Q.; Goodnough, J. B.; Tian, H.; Chen, X.; Khavari, P. A. In vivo restoration of laminin 5 beta 3 expression and function in junctional epidermolysis bullosa. Proc. Natl. Acad. Sci. USA, 2001, 98(9), 5193-198.
29. Gache, Y.; Baldeschi, C.; Del Rio, M.; Gagnoux-Palacios, L.; Larcher, F.; Lacour, J. P.; Meneguzzi, G. Construction of skin equivalents for gene therapy of recessive dystrophic epidermolysis bullosa. Hum. Gene Ther., 2004, 15(10), 921-933.
30. Goto, M.; Sawamura, D.; Ito, K.; Abe, M.; Nishie, W.; Sakai, K.; Shibaki, A.; Akiyama, M.; Shimizu, H. Fibroblasts show more potential as target cells than keratinocytes in COL7A1 gene therapy of dystrophic epidermolysis bullosa. J. Invest. Dermatol., 2006, 126(4), 766-772.
31. Siprashvili, Z.; Nguyen, N. T.; Bezchinsky, M. Y.; Marinkovich, M. P.; Lane, A. T.; Khavari, P. A. Long-term type VII collagen restoration to human epidermolysis bullosa skin tissue. Hum. Gene. Ther., 2010, 21(10), 1299-1310.
32. Baldeschi, C.; Gache, Y.; Rattenholl, A.; Bouille, P.; Danos, O.; Ortonne, J. P.; Bruckner-Tuderman, L.; Meneguzzi, G. Genetic correction of canine dystrophic epidermolysis bullosa mediated by retroviral vectors. Hum. Mol. Genet., 2003, 12(15), 1897-1905.
33. 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. Correction of junctional epidermolysis bullosa by transplantation of genetically modified epidermal stem cells. Nat. Med., 2006, 12(12), 1397-1402.
34. Hacein-Bey-Abina, S.; Von Kalle, C.; Schmidt, M.; McCormack, M. P.; Wulffraat, N.; Leboulch, P.; Lim, A.; Osborne, C. S.; Pawliuk, R.; Morillon, E.; Sorensen, R.; Forster, A.; Fraser, P.; Cohen, J. I.; De Saint Basile, G.; Alexander, I.; Wintergerst, U.; Frebourg, T.; Aurias, A.; Stoppa-Lyonnet, D.; Romana, S.; Radford-Weiss, I.; Gross, F.; Valensi, F.; Delabesse, E.; Macintyre, E.; Sigaux, F.; Soulier, J.; Leiva, L. E.; Wissler, M.; Prinz, C.; Rabbitts, T. H.; Le Deist, F.; Fischer, A.; Cavazzana-Calvo, M. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science, 2003, 302(5644), 415-419.
35. McCormack, M. P.; Rabbitts, T. H. Activation of the T-cell oncogene LMO2 after gene therapy for X-linked severe combined immunodeficiency. N. Engl. J. Med., 2004, 350 (9), 913-922.
36. Hacein-Bey-Abina, S.; Garrigue, A.; Wang, G. P.; Soulier, J.; Lim, A.; Morillon, E.; Clappier, E.; Caccavelli, L.; Delabesse, E.; Beldjord, K.; Asnafi, V.; MacIntyre, E.; Dal Cortivo, L.; Radford, I.; Brousse, N.; Sigaux, F.; Moshous, D.; Hauer, J.; Borkhardt, A.; Belohradsky, B. H.; Wintergerst, U.; Velez, M. C.; Leiva, L.; Sorensen, R.; Wulffraat, N.; Blanche, S.; Bushman, F. D.; Fischer, A.; Cavazzana-Calvo, M. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J. Clin. Invest., 2008, 118(9), 3132-3142.
37. Howe, S. J.; Mansour, M. R.; Schwarzwaelder, K.; Bartholomae, C.; Hubank, M.; Kempski, H.; Brugman, M. H.; Pike-Overzet, K.; Chatters, S. J.; de Ridder, D.; Gilmour, K. C.; Adams, S.; Thornhill, S. I.; Parsley, K. L.; Staal, F. J.; Gale, R. E.; Linch, D. C.; Bayford, J.; Brown, L.; Quaye, M.; Kinnon, C.; Ancliff, P.; Webb, D. K.; Schmidt, M.; von Kalle, C.; Gaspar, H. B.; Thrasher, A. J. Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J. Clin. Invest., 2008, 118(9), 3143-3150.
38. Coffin, J. M.; Huges, S. H.; Varmus, H. E. Retroviruses. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, 1997.
39. Bushman, F.; Lewinski, M.; Ciuffi, A.; Barr, S.; Leipzig, J.; Hannenhalli, S.; Hoffmann, C. Genome-wide analysis of retroviral DNA integration. Nat. Rev. Microbiol., 2005, 3(11), 848-858.
40. Cattoglio, C.; Facchini, G.; Sartori, D.; Antonelli, A.; Miccio, A.; Cassani, B.; Schmidt, M.; von Kalle, C.; Howe, S.; Thrasher, A. J.; Aiuti, A.; Ferrari, G.; Recchia, A.; Mavilio, F. Hot spots of retroviral integration in human CD34+ hematopoietic cells. Blood 2007, 110(6), 1770-1778.
41. Recchia, A.; Bonini, C.; Magnani, Z.; Urbinati, F.; Sartori, D.; Muraro, S.; Tagliafico, E.; Bondanza, A.; Stanghellini, M. T.; Bernardi, M.; Pescarollo, A.; Ciceri, F.; Bordignon, C.; Mavilio, F. Retroviral vector integration deregulates gene expression but has no consequence on the biology and function of transplanted T cells. Proc. Natl. Acad. Sci. USA, 2006, 103(5), 1457-1462.
42. Maruggi, G.; Porcellini, S.; Facchini, G.; Perna, S. K.; Cattoglio, C.; Sartori, D.; Ambrosi, A.; Schambach, A.; Baum, C.; Bonini, C.; Bovolenta, C.; Mavilio, F.; Recchia, A. Transcriptional enhancers induce insertional gene deregulation independently from the vector type and design. Mol. Ther., 2009, 17(5), 851-856.
43. Aiuti, A.; Cassani, B.; Andolfi, G.; Mirolo, M.; Biasco, L.; Recchia, A.; Urbinati, F.; Valacca, C.; Scaramuzza, S.; Aker, M.; Slavin, S.; Cazzola, M.; Sartori, D.; Ambrosi, A.; Di Serio, C.; Roncarolo, M. G.; Mavilio, F.; Bordignon, C. Multilineage hematopoietic reconstitution without clonal selection in ADA-SCID patients treated with stem cell gene therapy. J. Clin. Invest., 2007, 117(8), 2233-2240.
44. Zufferey, R.; Dull, T.; Mandel, R. J.; Bukovsky, A.; Quiroz, D.; Naldini, L.; Trono, D. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J. Virol., 1998, 72(12), 9873-9880.
45. Montini, E.; Cesana, D.; Schmidt, M.; Sanvito, F.; Ponzoni, M.; Bartholomae, C.; Sergi Sergi, L.; Benedicenti, F.; Ambrosi, A.; Di Serio, C.; Doglioni, C.; von Kalle, C.; Naldini, L. Hematopoietic stem cell gene transfer in a tumor-prone mouse model uncovers low genotoxicity of lentiviral vector integration. Nat. Biotechnol., 2006, 24(6), 687-696.
46. Di Nunzio, F.; Maruggi, G.; Ferrari, S.; Di Iorio, E.; Poletti, V.; Garcia, M.; Del Rio, M.; De Luca, M.; Larcher, F.; Pellegrini, G.; Mavilio, F. Correction of laminin-5 deficiency in human epidermal stem cells by transcriptionally targeted lentiviral vectors. Mol. Ther., 2008, 16(12), 1977-1985.
47. Titeux, M.; Pendaries, V.; Zanta-Boussif, M. A.; Decha, A.; Pironon, N.; Tonasso, L.; Mejia, J. E.; Brice, A.; Danos, O.; Hovnanian, A. SIN retroviral vectors expressing COL7A1 under human promoters for ex vivo gene therapy of recessive dystrophic epidermolysis bullosa. Mol. Ther., 2010, 18(8), 1509-1518.
48. Woodley, D. T.; Keene, D. R.; Atha, T.; Huang, Y.; Lipman, K.; Li, W.; Chen, M. Injection of recombinant human type VII collagen restores collagen function in dystrophic epidermolysis bullosa. Nat. Med., 2004, 10(7), 693-695.
49. Woodley, D. T.; Krueger, G. G.; Jorgensen, C. M.; Fairley, J. A.; Atha, T.; Huang, Y.; Chan, L.; Keene, D. R.; Chen, M. Normal and gene-corrected dystrophic epidermolysis bullosa fibroblasts alone can produce type VII collagen at the basement membrane zone. J. Invest. Dermatol., 2003, 121(5), 1021-1028.
50. Woodley, D. T.; Remington, J.; Huang, Y.; Hou, Y.; Li, W.; Keene, D. R.; Chen, M. Intravenously injected human fibroblasts home to skin wounds, deliver type VII collagen, and promote wound healing. Mol. Ther., 2007, 15(3), 628-635.
51. Chen, M.; O'Toole, E. A.; Muellenhoff, M.; Medina, E.; Kasahara, N.; Woodley, D. T. Development and characterization of a recombinant truncated type VII collagen "minigene". Implication for gene therapy of dystrophic epidermolysis bullosa. J. Biol. Chem., 2000, 275(32), 24429-24435.
52. Wagner, J. E.; Ishida-Yamamoto, A.; McGrath, J. A.; Hordinsky, M.; Keene, D. R.; Riddle, M. J.; Osborn, M. J.; Lund, T.; Dolan, M.; Blazar, B. R.; Tolar, J. Bone marrow transplantation for recessive dystrophic epidermolysis bullosa. N. Engl. J. Med., 2010, 363(7), 629-639.
53. Porteus, M. H.; Connelly, J. P.; Pruett, S. M. A look to future directions in gene therapy research for monogenic diseases. PLoS Genet., 2006, 2(9), e133.
54. Izsvak, Z.; Ivics, Z.; Plasterk, R. H. Sleeping Beauty, a wide hostrange transposon vector for genetic transformation in vertebrates. J. Mol. Biol., 2000, 302(1), 93-102.
55. Hackett, P. B.; Ekker, S. C.; Largaespada, D. A.; McIvor, R. S. Sleeping beauty transposon-mediated gene therapy for prolonged expression. Adv. Genet., 2005, 54 189-232.
56. Mates, L.; Chuah, M. K.; Belay, E.; Jerchow, B.; Manoj, N.; Acosta-Sanchez, A.; Grzela, D. P.; Schmitt, A.; Becker, K.; Matrai, J.; Ma, L.; Samara-Kuko, E.; Gysemans, C.; Pryputniewicz, D.; Miskey, C.; Fletcher, B.; Vandendriessche, T.; Ivics, Z.; Izsvak, Z. Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nat. Genet., 2009, 41(6), 753-761.
57. Ortiz-Urda, S.; Lin, Q.; Yant, S. R.; Keene, D.; Kay, M. A.; Khavari, P. A. Sustainable correction of junctional epidermolysis bullosa via transposon-mediated nonviral gene transfer. Gene. Ther., 2003, 10(13), 1099-104.
58. Ginsburg, D. S.; Calos, M. P. Site-specific integration with phiC31 integrase for prolonged expression of therapeutic genes. Adv. Genet., 2005, 54 179-187.
59. Ortiz-Urda, S.; Thyagarajan, B.; Keene, D. R.; Lin, Q.; Calos, M. P.; Khavari, P. A. PhiC31 integrase-mediated nonviral genetic correction of junctional epidermolysis bullosa. Hum. Gene. Ther., 2003, 14(9), 923-928.
60. Ortiz-Urda, S.; Thyagarajan, B.; Keene, D. R.; Lin, Q.; Fang, M.; Calos, M. P.; Khavari, P. A. Stable nonviral genetic correction of inherited human skin disease. Nat. Med., 2002, 8(10), 1166-1170.
61. Epstein, E. H. Jr. The genetics of human skin diseases. Curr. Opin. Genet. Dev., 1996, 6 295-300.
62. Leachman, S. A.; Hickerson, R. P.; Schwartz, M. E.; Bullough, E. E.; Hutcherson, S. L.; Boucher, K. M.; Hansen, C. D.; Eliason, M. J.; Srivatsa, G. S.; Kornbrust, D. J.; Smith, F. J.; McLean, W. I.; Milstone, L. M.; Kaspar, R. L. First-in-human mutation-targeted siRNA phase Ib trial of an inherited skin disorder. Mol. Ther., 2010, 18(2), 442-446.
63. Petek, L. M.; Fleckman, P.; Miller, D. G. Efficient KRT14 targeting and functional characterization of transplanted human keratinocytes for the treatment of epidermolysis bullosa simplex. Mol. Ther., 2010, 18(9), 1624-1632.
64. Lombardo, A.; Genovese, P.; Beausejour, C. M.; Colleoni, S.; Lee, Y. L.; Kim, K. A.; Ando, D.; Urnov, F. D.; Galli, C.; Gregory, P. D.; Holmes, M. C.; Naldini, L. Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat. Biotechnol., 2007, 25(11), 1298-1306.
65. Porteus, M. H. Mammalian gene targeting with designed zinc finger nucleases. Mol. Ther., 2006, 13(2), 438-446.
66. Hengge, U. R. SMaRT technology enables gene expression repair in skin gene therapy. J. Invest. Dermatol., 2008, 128(3), 499-500.
67. Wally, V.; Klausegger, A.; Koller, U.; Lochmuller, H.; Krause, S.; Wiche, G.; Mitchell, L. G.; Hintner, H.; Bauer, J. W. 5' transsplicing repair of the PLEC1 gene. J. Invest. Dermatol., 2008, 128(3), 568-574.
68. Dallinger, G.; Puttaraju, M.; Mitchell, L. G.; Yancey, K. B.; Yee, C.; Klausegger, A.; Hintner, H.; Bauer, J. W. Development of spli ceosome-mediated RNA trans-splicing (SMaRT) for the correction of inherited skin diseases. Exp. Dermatol., 2003, 12(1), 37-46.
69. Murauer, E. M.; Gache, Y.; Gratz, I. K.; Klausegger, A.; Muss, W.; Gruber, C.; Meneguzzi, G.; Hintner, H.; Bauer, J. W. Functional correction of type VII collagen expression in dystrophic epidermolysis bullosa. J. Invest. Dermatol., 2010, 131(1), 74-83.
70. Wong, T.; Gammon, L.; Liu, L.; Mellerio, J. E.; Dopping-Hepenstal, P. J.; Pacy, J.; Elia, G.; Jeffery, R.; Leigh, I. M.; Navsaria, H.; McGrath, J. A. Potential of fibroblast cell therapy for recessive dystrophic epidermolysis bullosa. J. Invest. Dermatol., 2008, 128(9), 2179-2189.
71. Chino, T.; Tamai, K.; Yamazaki, T.; Otsuru, S.; Kikuchi, Y.; Nimura, K.; Endo, M.; Nagai, M.; Uitto, J.; Kitajima, Y.; Kaneda, Y. Bone marrow cell transfer into fetal circulation can ameliorate genetic skin diseases by providing fibroblasts to the skin and inducing immune tolerance. Am. J. Pathol., 2008, 173(3), 803-814.
72. Fujita, Y.; Abe, R.; Inokuma, D.; Sasaki, M.; Hoshina, D.; Natsuga, K.; Nishie, W.; McMillan, J. R.; Nakamura, H.; Shimizu, T.; Akiyama, M.; Sawamura, D.; Shimizu, H. Bone marrow transplantation restores epidermal basement membrane protein expression and rescues epidermolysis bullosa model mice. Proc. Natl. Acad. Sci. USA, 2010, 107(32), 14345-50.
73. Tolar, J.; Ishida-Yamamoto, A.; Riddle, M.; McElmurry, R. T.; Osborn, M.; Xia, L.; Lund, T.; Slattery, C.; Uitto, J.; Christiano, A. M.; Wagner, J. E.; Blazar, B. R. Amelioration of epidermolysis bullosa by transfer of wild-type bone marrow cells. Blood, 2009, 113(5), 1167-1174.