Gene therapies for inherited skin disorders

Seminars in Cutaneous Medicine and Surgery

Volumn 33, Issue 2, 2014, Pages 83-90

  Abdul Wahab, Alya ^a   Qasim, Waseem ^b   McGrath, John A ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 7; LENTIVIRUS VECTOR; NUCLEASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; RETROVIRUS VECTOR; SERINE PROTEINASE INHIBITOR; SMALL INTERFERING RNA; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; ZINC FINGER NUCLEASE; ZINC FINGER PROTEIN;

ARTICLE; CELL CULTURE; CELL TRANSPLANTATION; DISEASE MODEL; DISEASE SEVERITY; DRUG DOSE ESCALATION; DRUG SAFETY; EPIDERMOLYSIS BULLOSA; EPIDERMOLYSIS BULLOSA DYSTROPHICA; EX VIVO STUDY; GENE DELIVERY SYSTEM; GENE EDITING; GENE GUN; GENE REPLACEMENT THERAPY; GENE TARGETING; GENE THERAPY; HUMAN; IN VIVO STUDY; KERATINOCYTE; LAMELLAR ICHTHYOSIS; MEDICAL RESEARCH; MOUSE; NETHERTON DISEASE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PACHYNOCHIA CONGENITA; PHASE 1 CLINICAL TRIAL (TOPIC); PHENOTYPE; REVERTANT; SKIN DISEASE; TRANSPOSON; VIRAL GENE DELIVERY SYSTEM; X LINKED ICHTHYOSIS; XERODERMA PIGMENTOSUM; GENE VECTOR; GENETICS; METHODOLOGY; REVIEW;

GENE TARGETING; GENETIC THERAPY; GENETIC VECTORS; HUMANS; RNA, SMALL INTERFERING; SKIN DISEASES, GENETIC; ZINC FINGERS;

EID: 84907939314     PISSN: 10855629     EISSN: 15580768     Source Type: Journal    
DOI: 10.12788/j.sder.0085     Document Type: Article

References (111)

1. Blaese RM, Culver KW, Miller AD, et al. T lymphocyte-directed gene therapy for ADA-SCID: initial trial results after 4 years. Science. 1995;270(5235):475-480.
2. Cavazzana-Calvo M, Hacein-Bey S, de Saint Basile G, et al. Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science. 2000;288(5466): 669-672.
3. Woodley D T, Keene DR, 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 2004; 10(2): 318-326
4. Woodley DT, Krueger GG, Jorgensen CM, et al. 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.
5. Gache Y, Baldeschi C, Del Rio M, et al. Construction of skin equivalents for gene therapy of recessive dystrophic epidermolysis bullosa. Human Gene Ther. 2004;15(10):921-933.
6. Titeux M, Pendaries V, Zanta-Boussif MA, et al. 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.
7. Baldeschi C, Gache Y, Rattenholl A, et al. Genetic correction of canine dystrophic epidermolysis bullosa mediated by retroviral vectors. Hum Mol Genet. 2003;12(15):1897-1905.
8. Ortiz-Urda S, Thyagarajan B, Keene DR, et al. Stable nonviral genetic correction of inherited human skin disease. Nat Med, 2002;8(10):1166-1170.
9. Murauer EM, Gache Y, Gratz IA et al. Functional Correction of Type VII Collagen Expression in Dystrophic Epidermolysis Bullosa. J Invest Dermatol. 2010; 131(1): 74-83
10. Ortiz-Urda S, Thyagarajan B, Keene DR et al. PhiC31 integrase-mediated nonviral genetic correction of junctional epidermolysis bullosa." Hum Gen Therapy 200314(9): 923-928.
11. Ortiz-Urda S, Thyagarajan B, Keene DR et al. 2002). Stable nonviral genetic correction of inherited human skin disease. Nat Med. 2002 8(10): 1166-1170.
12. Mecklenbeck S, Compton SH, Mejia JE et al, microinjected COL7A1-PAC vector restores synthesis of intact procollagen VII in a dystrophic epidermolysis bullosa keratinocyte cell line. Hum Gen Therapy 2002; 13(13): 1655-1662.
13. Osborn MJ, Starker CG, McElroy AN et al. TALEN-based gene correction for epidermolysis bullosa. Mol Ther 2013 21(6): 1151-1159.
14. Seitz CS, Giudice GJ, Balding SD et al. BP180 gene delivery in junctional epidermolysis bullosa. Gene Ther. 1999 6(1): 42-47.
15. Mavilio F, Pellegrini G, Ferrari S, et al. Correction of junctional epidermolysis bullosa by transplantation of genetically modified epidermal stem cells. Nat Med. 2006;12(12):1397-1402.
16. Di Nunzio F, Maruggi G, Ferrari S, et al. Correction of laminin-5 deficiency in human epidermal stem cells by transcriptionally targeted lentiviral vectors. Mol Ther. 2008;16(12):1977-1985.
17. Arnaudeau-Begard C, Brellier F, Chevallier-Lagente O, et al. Genetic correction of DNA repair-deficient/cancer-prone xeroderma pigmentosum group C keratinocytes. Hum Gene Ther. 2003;14(10):983-996.
18. Marchetto MC, Muotri AR, Burns DK, Friedberg EC, Menck CF. Gene transduction in skin cells: preventing cancer in xeroderma pigmentosum mice. Proc Natl Acad Sci USA. 2004;101(51):17759-17764.
19. Marchetto MC, Correa RG, Menck CF, Muotri AR. Functional lentiviral vectors for xeroderma pigmentosum gene therapy. J Biotechnol. 2006;126(4):424-430.
20. Warrick E, Garcia M, Chagnoleau C, et al. Preclinical corrective gene transfer in xeroderma pigmentosum human skin stem cells. Mol Ther. 2012;20(4):798-807.
21. Dupuy A, Valton J, Leduc S, et al. Targeted gene therapy of xeroderma pigmentosum cells using meganuclease and TALEN. PLoS One. 2013;8(11):e78678.
22. Di WL, Larcher F, Semenova E, et al. Ex-vivo gene therapy restores LEKTI activity and corrects the architecture of Netherton syndrome-derived skin grafts. Mol Ther. 2011;19(2):408-416.
23. Freiberg RA, Choate KA, Deng H, Alperin ES, Shapiro LJ, Khavari PA. A model of corrective gene transfer in X-linked ichthyosis. Hum Mol Genet. 1997;6(6):927-933.
24. Atkinson SD, McGilligan VE, Liao H, et al. Development of allele-specific therapeutic siRNA for keratin 5 mutations in epidermolysis bullosa simplex. J Invest Dermatol. 2011;131(10):2079-2086.
25. Leachman SA, Hickerson RP, Schwartz ME, et al. First-in-human mutation-targeted siRNA phase Ib trial of an inherited skin disorder. Mol Ther. 2010;18(2):442-446.
26. Choate KA, Medalie DA, Morgan JR and P. A. Khavari. Corrective gene transfer in the human skin disorder lamellar ichthyosis. Nat Med. 1996; 2(11): 1263-1267
27. Tang S, van Rij R, Silvera D, Andino R. Toward a poliovirus-based simian immunodeficiency virus vaccine: correlation between genetic stability and immunogenicity. J Virol. 1997;71(10):7841-7850.
28. Bramson J, Dayball K, Evelegh C, Wan YH, Page D, Smith A. Enabling topical immunization via microporation: a novel method for pain-free and needle-free delivery of adenovirus-based vaccines. Gen Ther. 2003;10(3):251-260.
29. Rheinwald JG, Green H. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell. 1975;6(3):331-343.
30. Carsin H, Ainaud P, Le Bever H, et al. Cultured epithelial autografts in extensive burn coverage of severely traumatized patients: a five year single-center experience with 30 patients. Burns. 2000;26(4): 379-387.
31. Hefton JM, Madden MR, Finkelstein JL, Shires GT. Grafting of burn patients with allografts of cultured epidermal cells. Lancet. 1983;2(8347):428-430.
32. Barrandon Y, Green H. Three clonal types of keratinocyte with different capacities for multiplication. Proc Natl Acad Sci USA. 1987;84(8): 2302-2306.
33. Rochat A, Kobayashi K, and Barrandon Y, Location of stem cells of human hair follicles by clonal analysis. Cell. 1994;76(6):1063-1073.
34. Gallico GG 3rd, O'Connor NE, Compton CC, Kehinde O, Green H. Permanent coverage of large burn wounds with autologous cultured human epithelium. N Engl J Med. 1984;311(7):448-451.
35. Jones PH and Watt FM. Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell. 1993;73(4): 713-724.
36. Kaur P, Li A. Adhesive properties of human basal epidermal cells: an analysis of keratinocyte stem cells, transit amplifying cells, and postmitotic differentiating cells. J Invest Dermatol. 2000;114(3):413-420.
37. Lin HY, Yang LT. Differential response of epithelial stem cell populations in hair follicles to TGF-beta signaling. Dev Biol. 2013;373(2): 394-406.
38. Bose A, Teh MT, Mackenzie IC, Waseem A. Keratin k15 as a biomarker of epidermal stem cells. Int J Mol Sci. 2013;14(10):19385-19398.
39. Nowak JA, Polak L, Pasolli HA, Fuchs E. Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell. 2008;3(1):33-43.
40. Jensen KB, Watt FM. Single-cell expression profiling of human epidermal stem and transit-amplifying cells: Lrig1 is a regulator of stem cell quiescence. Proc Natl Acad Sci USA. 2006;103(32):11958-11963.
41. Nijhof JG, Braun KM, Giangreco A, et al. The cell-surface marker MTS24 identifies a novel population of follicular keratinocytes with characteristics of progenitor cells. Development. 2006;133(15):3027-3037.
42. Goto M, Sawamura D, Ito K, et al. 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.
43. Armelini MG, Muotri AR, Marchetto MC, de Lima-Bessa KM, Sarasin A, Menck CF. Restoring DNA repair capacity of cells from three distinct diseases by XPD gene-recombinant adenovirus. Cancer Gene Ther. 2005;12(4):389-396.
44. Chen M, Kasahara N, Keene DR, et al. Restoration of type VII collagen expression and function in dystrophic epidermolysis bullosa. Nat Genet. 2002;32(4):670-675.
45. Wagner JE, Ishida-Yamamoto A, McGrath JA, et al. Bone marrow transplantation for recessive dystrophic epidermolysis bullosa. N Engl J Med. 2010;363(7):629-639.
46. Cartier N, Hacein-Bey-Abina S, Bartholomae CC, et al. Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science. 2009;326(5954):818-823.
47. Gaspar HB, Cooray S, Gilmour KC, et al. Hematopoietic stem cell gene therapy for adenosine deaminase-deficient severe combined immunodeficiency leads to long-term immunological recovery and metabolic correction. Sci Transl Med. 2011;3(97):97ra80.
48. Thomas CE, Ehrhardt A, and Kay MA. Progress and problems with the use of viral vectors for gene therapy. Nat Rev Genet. 2003;4(5):346-358.
49. Ginn SL, Alexander IE, Edelstein ML, Abedi MR, Wixon J. Gene therapy clinical trials worldwide to 2012-an update. J Gene Med. 2013;15(2):65-77.
50. Fenjves ES, Yao SN, Kurachi K, Taichman LB. Loss of expression of a retrovirustransduced gene in human keratinocytes. J Invest Dermatol. 1996;106(3):576-578.
51. Choate KA, Khavari PA. Sustainability of keratinocyte gene transfer and cell survival in vivo. Hum Gene Ther. 1997;8(8):895-901.
52. Hacein-Bey-Abina S, von Kalle C, Schmidt M, et al. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N Engl J Med. 2003;348(3):255-256.
53. Ott MG, Schmidt M, Schwarzwaelder K, et al. Correction of X-linked chronic granulomatous disease by gene therapy, augmented by insertional activation of MDS1-EVI1, PRDM16 or SETBP1. Nat Med. 2006;12(4):401-409.
54. Montini E, Cesana D, Schmidt M, et al. 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.
55. Cattoglio C, Pellin D, Rizzi E, et al. High-definition mapping of retroviral integration sites identifies active regulatory elements in human multipotent hematopoietic progenitors. Blood. 2010;116(25):5507-5517.
56. Dull T, Zufferey R, Kelly M, et al. A third-generation lentivirus vector with a conditional packaging system. J Virol. 1998;72(11):8463-8471.
57. Zufferey R, Dull T, Mandel RJ, et al. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol. 1998;72(12):9873-9880.
58. Galy A, Roncarolo MG, Thrasher AJ. Development of lentiviral gene therapy for Wiskott Aldrich syndrome. Expert Opin Biol Ther. 2008;8(2):181-190.
59. Biffi A, Montini E, Lorioli L, et al. Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science. 2013;341(6148):1233158.
60. Payen E, Colomb C, Negre O, Beuzard Y, Hehir K, Leboulch P. Lentivirus Vectors in Beta-Thalassemia. Methods Enzymol. 2012;507:109-124.
61. Carbonaro DA, Jin XY, Geiger S, et al. Development of a lentiviral gene therapy for adenosine deaminase-deficient severe combined immunodeficiency (ADA-SCID). Mol Ther. 2012;20:S162-S162.
62. Aiuti A, Biasco L, Scaramuzza S, et al. Lentiviral hematopoietic stem cell gene therapy in patients with Wiskott-Aldrich syndrome. Science. 2013;341(6148):1233151.
63. Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med. 2011;365(8):725-733.
64. Carulli S, Contin R, De Rosa L, Pellegrini G, De Luca M. The long and winding road that leads to a cure for epidermolysis bullosa. Regen Med. 2013;8(4):467-481.
65. Bentz H, Morris NP, Murray LW, Sakai LY, Hollister DW, Burgeson RE. Isolation and partial characterization of a new human collagen with an extended triple-helical structural domain. Proc Natl Acad Sci USA. 1983;80(11):3168-3172
66. Chen M, O'Toole EA, Muellenhoff M, Medina E, Kasahara N, Woodley DT. 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.
67. Serrano F, Del Rio M, Larcher F, et al. A comparison of targeting performance of oncoretroviral versus lentiviral vectors on human keratinocytes. Hum Gene Ther. 2003;14(16):1579-1585.
68. Ortiz-Urda S, Lin Q, Green CL, Keene DR, Marinkovich MP, Khavari PA. Injection of genetically engineered fibroblasts corrects regenerated human epidermolysis bullosa skin tissue. J Clin Invest. 2003;111(2):251-255.
69. Gache Y, Pin D, Gagnoux-Palacios L, Carozzo C, Meneguzzi G. Correction of dog dystrophic epidermolysis bullosa by transplantation of genetically modified epidermal autografts. J Invest Dermatol. 2011;131(10):2069-2078.
70. Falabella AF, Valencia IC, Eaglstein WH, Schachner LA. Tissue-engineered skin (Apligraf) in the healing of patients with epidermolysis bullosa wounds. Arch Dermatol. 2000;136(10):1225-1230.
71. Fivenson DP, Scherschun L, Cohen LV. Apligraf in the treatment of severe mitten deformity associated with recessive dystrophic epidermolysis bullosa. Plast Reconstr Surg. 2003;112(2):584-588.
72. Fivenson DP, Scherschun L, Choucair M, Kukuruga D, Young J, Shwayder T. Graftskin therapy in epidermolysis bullosa. J Am Acad Dermatol. 2003;48(6):886-892.
73. Natsuga K, Sawamura D, Goto M, et al. Response of intractable skin ulcers in recessive dystrophic epidermolysis bullosa patients to an allogeneic cultured dermal substitute. Acta Derm Venereol. 2010;90(2):165-169.
74. Abdul-Wahab A, Georgiadis C, Qasim W, Thrasher A, McGrath JA, Di W. Gene therapy for recessive dystrophic epidermolysis bullosa using COL7A1 gene corrected autologous fibroblasts. J Invest Dermatol. 2013;133:S143-S143.
75. Choate KA, Kinsella TM, Williams ML, Nolan GP, Khavari PA. Transglutaminase 1 delivery to lamellar ichthyosis keratinocytes. Hum Gene Ther. 1996;7(18):2247-2253.
76. Velez-Cruz R, Zadorin AS, Coin F, Egly JM. Sirt1 suppresses RNA synthesis after UV irradiation in combined xeroderma pigmentosum group D/Cockayne syndrome (XP-D/CS) cells. Proc Natl Acad Sci USA. 2013;110(3):E212-220.
77. Sawamura D, Ina S, Itai K, et al. In vivo gene introduction into keratinocytes using jet injection. Gene Ther. 1999;6(10):1785-1787.
78. Sun WH, Burkholder JK, Sun J, et al. In vivo cytokine gene transfer by gene gun reduces tumor growth in mice. Proc Natl Acad Sci USA. 1995;92(7):2889-2893.
79. Alexander MY, Akhurst RJ. Liposome-medicated gene transfer and expression via the skin. Hum Mol Genet. 1995;4(12):2279-2285.
80. Kebriaei P, Huls H, Jena B, et al. Infusing CD19-directed T cells to augment disease control in patients undergoing autologous hematopoietic stem-cell transplantation for advanced B-lymphoid malignancies. Hum Gene Ther. 2012;23(5):444-450.
81. Field AC, Vink C, Gabriel R, et al. Comparison of lentiviral and sleeping beauty mediated alphabeta T cell receptor gene transfer. PLoS One. 2013;8(6):e68201.
82. Hackett PB, Largaespada DA, Switzer KC, Cooper LJ. Evaluating risks of insertional mutagenesis by DNA transposons in gene therapy. Transl Res. 2013;161(4):265-283.
83. Urnov FD, Miller JC, Lee YL, et al. Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature. 2005;435(7042):646-651.
84. Yusa K, Rashid ST, Strick-Marchand H, et al. Targeted gene correction of alpha1-antitrypsin deficiency in induced pluripotent stem cells. Nature. 2011;478(7369):391-394.
85. Sebastiano V, Maeder ML, Angstman JF, et al. In situ genetic correction of the sickle cell anemia mutation in human induced pluripotent stem cells using engineered zinc finger nucleases. Stem Cells. 2011;29(11):1717-1726.
86. Connelly JP, Barker JC, Pruett-Miller S, Porteus MH. Gene correction by homologous recombination with zinc finger nucleases in primary cells from a mouse model of a generic recessive genetic disease. Mol Ther. 2010;18(6):1103-1110.
87. Yamanaka S, Takahashi K. Induction of pluripotent stem cells from mouse fibroblast cultures [in Japanese]. Tanpakushitsu Kakusan Koso. 2006;51(15):2346-2351.
88. Aasen T, Raya A, Barrero MJ, et al. Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat Biotechnol. 2008;26(11):1276-
89. Aasen T, Izpisua Belmonte JC. Isolation and cultivation of human keratinocytes from skin or plucked hair for the generation of induced pluripotent stem cells. Nat Protoc. 2010;5(2):371-382.
90. Redondo P, Prieto J, Munoz IG, et al. Molecular basis of xeroderma pigmentosum group C DNA recognition by engineered meganucleases. Nature. 2008;456(7218):107-111.
91. Caplen NJ. Gene therapy progress and prospects. Downregulating gene expression: the impact of RNA interference. Gene Ther. 2004;11(16):1241-1248.
92. Leachman SA, Kaspar RL, Fleckman P, et al. Clinical and pathological features of pachyonychia congenita. J Invest Dermatol Symp Proc. 2005;10(1):3-17.
93. Kaspar RL. Challenges in developing therapies for rare diseases including pachyonychia congenita. J Invest Derm Symp P. 2005;10(1):62-66.
94. Hickerson RP, Smith FJ, Reeves RE, et al. Single-nucleotide-specific siRNA targeting in a dominant-negative skin model. J Invest Dermatol. 2008;128(3):594-605.
95. Leachman SA, Hickerson RP, Hull PR, et al. Therapeutic siRNAs for dominant genetic skin disorders including pachyonychia congenita. J Dermatol Sci. 2008;51(3):151-157.
96. Zheng D, Giljohann DA, Chen DL, et al. Topical delivery of siRNA-based spherical nucleic acid nanoparticle conjugates for gene regulation. Proc Natl Acad Sci USA. 2012;109(30):11975-11980.
97. Pendaries V, Gasc G, Titeux M, Tonasso L, Mejia JE, Hovnanian A. siRNA-mediated allele-specific inhibition of mutant type VII collagen in dominant dystrophic epidermolysis bullosa. J Invest Dermatol. 2012;132(6):1741-1743.
98. Cao T, Longley MA, Wang XJ, Roop DR. An inducible mouse model for epidermolysis bullosa simplex: implications for gene therapy. J Cell Biol. 2001;152(3):651-656.
99. Allen EH, Atkinson SD, Liao H, et al. Allele-specific siRNA silencing for the common keratin 12 founder mutation in Meesmann epithelial corneal dystrophy. Invest Ophthalmol Vis Sci. 2013;54(1):494-502.
100. Jonkman MF, Scheffer H, Stulp R, et al. Revertant mosaicism in epidermolysis bullosa caused by mitotic gene conversion. Cell. 1997;88(4):543-551.
101. Jonkman MF, Pasmooij AM. Revertant mosaicism-patchwork in the skin. N Engl J Med. 2009;360(16):1680-1682.
102. Darling TN, Yee C, Bauer JW, Hintner H, Yancey KB. Revertant mosaicism: partial correction of a germ-line mutation in COL17A1 by a frame-restoring mutation. J Clin Invest. 1999;103(10):1371-1377.
103. Hirschhorn R. In vivo reversion to normal of inherited mutations in humans. J Med Genet. 2003;40(10):721-728.
104. Jonkman MF, Castellanos Nuijts M, van Essen AJ. Natural repair mechanisms in correcting pathogenic mutations in inherited skin disorders. Clin Exp Dermatol. 2003;28(6): 625-631.
105. Lai-Cheong JE, McGrath JA, Uitto J. Revertant mosaicism in skin: natural gene therapy. Trends Mol Med. 2011;17(3):140-148.
106. Choate KA, Lu Y, Zhou J, et al. Mitotic recombination in patients with ichthyosis causes reversion of dominant mutations in KRT10. Science. 2010;330(6000):94-97.
107. Gostynski A, Deviaene FC, Pasmooij AM, Pas HH, Jonkman MF. Adhesive stripping to remove epidermis in junctional epidermolysis bullosa for revertant cell therapy. Br J Dermatol. 2009;161(2):444-447.
108. Gostynski A, Pasmooij AM, Jonkman MF. Successful therapeutic transplantation of revertant skin in epidermolysis bullosa. J Am Acad Dermatol. 2014;70(1):98-101.
109. Tolar J, Xia L, Riddle MJ, et al. Induced pluripotent stem cells from individuals with recessive dystrophic epidermolysis bullosa. J Invest Dermatol. 2010;131(4):848-856.
110. Tolar J, Xia L, Lees CJ, et al. Keratinocytes from induced pluripotent stem cells in junctional epidermolysis bullosa. J Invest Dermatol. 2013;133(2):562-565.
111. Tolar J, McGrath JA, Xia L, et al. Patient-specific naturally gene-reverted induced pluripotent stem cells in recessive dystrophic epidermolysis bullosa. J Invest Dermatol. 2014;134(5):1246-1254.