Gene therapy of epidermolysis bullosa

Expert Opinion on Biological Therapy

Volumn 4, Issue 9, 2004, Pages 1435-1443

  Bauer, Johann W ^a   Laimer, Martin ^a  

^a PARACELSUS MEDICAL UNIVERSITY   (Austria)

Author keywords

Aminoglycoside; Epidermolysis bullosa; Gene therapy; Non viral vector; Splicing; Viral vector

Indexed keywords

AMINOGLYCOSIDE ANTIBIOTIC AGENT; ANTIGEN; BETA4 INTEGRIN; BULLOUS PEMPHIGOID ANTIGEN 2; COLLAGEN TYPE 7; COMPLEMENTARY DNA; DESMIN; INTEGRASE; KALININ; KERATIN; LENTIVIRUS VECTOR; MATRIX METALLOPROTEINASE INHIBITOR; MIFEPRISTONE; PHIC31 INTEGRASE; RETROVIRUS VECTOR; RIBOZYME; TRANSPOSASE; UNCLASSIFIED DRUG;

CLINICAL TRIAL; COL7A1 GENE; DERMOEPIDERMAL JUNCTION; DRUG EFFICACY; ENZYME INHIBITION; EPIDERMOLYSIS BULLOSA; EXPERIMENTAL TRANSPLANTATION; GENE; GENE MUTATION; GENE THERAPY; GENETIC TRANSDUCTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; ITGB4 GENE; K14 GENE; LAMB3 GENE; NATURAL GENE THERAPY; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; RECESSIVE INHERITANCE; REVIEW; RNA SPLICING; VIRAL GENE DELIVERY SYSTEM; XENOGRAFT;

ANIMALS; AUTOANTIGENS; CELL ADHESION MOLECULES; DISEASE MODELS, ANIMAL; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; EPIDERMOLYSIS BULLOSA; GENE THERAPY; GENETIC HETEROGENEITY; GENETIC VECTORS; HUMANS; INTEGRIN BETA4; KERATIN-14; KERATINOCYTES; KERATINS; MATRIX METALLOPROTEINASES; MICE; MICE, NUDE; NON-FIBRILLAR COLLAGENS; PROTEASE INHIBITORS; RNA SPLICING; RNA, CATALYTIC; TELOMERASE;

LENTIVIRUS; UNIDENTIFIED RETROVIRUS;

EID: 4544276259     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.4.9.1435     Document Type: Review

References (64)

1. UITTO J, PULKKINEN L: Molecular genetics of heritable blistering disorders. Arch. Dermatol. (2001) 137:1458-1461.
2. DUNNWALD M, TOMANEK-CHALKLEY A, ALEXANDRUNAS D, FISHBAUGH J, BICKENBACH JR: Isolating a pure population of epidermal stem cells for use in tissue engineering. Exp. Dermatol. (2001) 10:45-54.
3. LI A, POULIOT N, REDVERS R, KAUR P: Extensive tissue-regenerative capacity of neonatal human keratinocyte stem cells and their progeny. J. Clin. Invest. (2004) 113:390-400.
4. MORRIS RJ, LIU Y, MARLES L et al.: Capturing and profiling adult hair follicle stem cells. Nat. Biotechnol. (2004) 22:411-417.
5. TUMBAR T, GUASCH G, GRECO V et al.: Defining the epithelial stem cell niche in skin. Science (2004) 303:359-363.
6. KOLODKA TM, GARLICK JA, TAICHMAN LB: Evidence for KC 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.
7. VANDENDRIESSCHE T, COLLEN D, CHUAH MK: Gene therapy for the hemophilias. J. Thromb. Haemost. (2003) 1:1550-1558.
8. LOWENSTEIN PR: Virology and immunology of gene therapy, or virology and immunology of high MOI infection with defective viruses. Gene Ther. (2003) 10:933-998.
9. VOGEL J: The virtue of tolerance. J. Invest. Dermatol. (2003) 120:610-615.
10. IRVINE AD, MCLEAN WH: Human keratin diseases: the increasing spectrum of disease and subtlety of the phenotype-genotype correlation. Br. J. Dermatol. (1999) 140:815-828.
11. MAGIN TM, KAISER HW, LEITGEB S et al.: Supplementation of a mutant keratin by stable expression of desmin in cultured human EBS KCs. J. Cell Sci. (2000) 113:4231-4239.
12. KIRFEL J, PETERS B, GRUND C, REIFENBERG K, MAGIN TM: Ectopic expression of desmin in the epidermis of transgenic mice permits development of a normal epidermis. Differentiation (2002) 70:56-68.
13. JENSEN TG, SORENSEN CB, JENSEN UB, BOLUND L: Epidermolysis bullosa simplex keratinocytes with extended lifespan established by ectopic expression of telomerase. Exp. Dermatol. (2003) 12:71-77.
14. CAO T, LONGLEY MA, WANG XJ, ROOP DR: An inducible mouse model for epidermolysis bullosa simplex: implications for gene therapy. J Cell. Biol. (2001) 152:651-656. A first dynamic mouse model of EB.
15. POHLA-GUBO G, LAZAROVA Z, GIUDICE GJ et al.: Diminished expression of the extracellular domain of bullous pemphigoid antigen 2 (BPAG2) in the epidermal basement membrane of patients with generalized atrophic benign epidermolysis bullosa. Exp. Dermatol. (1995) 4:199-206.
16. MCGRATH JA, GATALICA B, CHRISTIANO AM et al.: Mutations in the 180-kD bullous pemphigoid antigen (BPAG2), a hemidesmosomal transmembrane collagen (COL17A1), in generalized atrophic benign epidermolysis bullosa. Nat. Genet. (1995) 11:83-86.
17. CHRISTIANO AM, PULKKINEN L, EADY RA, UTTTO J: Compound heterozygosity for nonsense and missense mutations in the LAMB3 gene in nonlethal junctional epidermolysis bullosa. J. Invest. Dermatol. (1996) 106:775-777.
18. SEITZ CS, GIUDICE GJ, BALDING SD, MARINKOVICH MP, KHAVARI PA: BP180 gene delivery in junctional epidermolysis bullosa. Gene Ther. (1999) 6:42-47.
19. DELLAMBRA E, VAILLY J, PELLEGRINI G et al.: Corrective transduction of human epidermal stem cells in laminin-5-dependent junctional epidermolysis bullosa. Hum. Gene Ther. (1998) 9:1359-1370. The first successful attempt to amend the phenotype of EB in a mouse-human xenotransplantation system.
20. VAILLY J, GAGNOUX-PALACIOS L, DELL'AMBRA E et al.: Corrective gene transfer of KCs from patients with junctional epidermolysis bullosa restores assembly of hemidesmosomes in reconstructed epithelia. Gene Ther. (1998) 5:1322-1332.
21. ROBBINS PB, LIN Q, GOODNOUGH JB, TIAN H, CHEN X, KHAVARI PA: In vivo restoration of laminin 5 beta 3 expression and function in junctional epidermolysis bullosa. Proc. Natl. Acad. Sci. USA (2001) 98:5193-5198.
22. ROBBINS PB, SHEU SM, GOODNOUGH JB, KHAVARI PA: Impact of laminin 5 beta 3 gene versus protein replacement on gene expression patterns in junctional epidermolysis bullosa. Hum. Gene Ther. (2001) 12:1443-1448. Molecular characterisation of the phenotypic correction suggesting that gene therapy is better than protein therapy.
23. ORTIZ-URDA S, THYAGARAJAN B, KEENE DR, LIN Q, CALOS MP, KHAVARI PA: PhiC31 integrase-mediated nonviral genetic correction of junctional epidermolysis bullosa. Hum. Gene Ther. (2003) 14:923-928.
24. ORTIZ-URDAS, LIN Q, YANT SR, KEENE D, KAY MA, KHAVARI PA: Sustainable correction of junctional epidermolysis bullosa via transposon-mediated nonviral gene transfer. Gene Ther. (2003) 10:1099-1104.
25. DELLAMBRA E, PRISLEI S, SALVATI AL et al.: Gene correction of integrin beta4-dependent pyloric atresia-junctional epidermolysis bullosa keratinocytes establishes a role for beta4 tyrosines 1422 and 1440 in hemidesmosome assembly. J. Biol. Chem. (2001) 276:41336-41342.
26. SAT E, LEUNG KH, BRUCKNER-TUDERMAN L, CHEAH KS: Tissue-specific expression and long-term deposition of human collagen VII in the skin of transgenic mice: implications for gene therapy. Gene Ther. (2000) 7:1631-1639.
27. MECKLENBECK S, COMPTON SH, MEJIA JE et al.: A microinjected COL7A1-PAC vector restores synthesis of intact procollagen VII in a dystrophic epidermolysis bullosa keratinocyte cell line. Hum. Gene Ther. (2002) 13:1655-1662.
28. CHEN M, KASAHARA N, KEENE DR et al.: Restoration of type VII collagen expression and function in dystrophic epidermolysis bullosa. Nat. Genet. (2002) 32:670-675. A fust DEB phenotype using full-length type VII collagen in a lentiviral vector.
29. ORTIZ-URDA S, THYAGARAJAN B, KEENE DR et al.: Stable nonviral genetic correction of inherited human skin disease. Nat. Med. (2002) 8:1166-1170. Using PhiC31 integrase, the full-length type VII collagen cDNA was shown to repair regenerated human skin tissue from a RDEB patient.
30. 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) 111:251-255.
31. 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) 121:1021-1028.
32. BALDESCHI C, CACHE Y, RATTENHOLL A et al.: Genetic correction of canine dystrophic epidermolysis bullosa mediated by retroviral vectors. Hum. Mol. Genet. (2003) 12:1897-1905.
33. PETERS B, KIRFEL J, BUESSOW H, VIDAL M, MAGIN TM: Complete cytolysis and neonatal lethality in keratin 5 knockout mice reveal its fundamental role in skin integrity and in epidermolysis bullosa simplex. Mol. Biol. Cell (2001) 12:1775-1786.
34. LLOYD C, YU QC, CHENG J et al.: The basal keratin network of stratified squamous epithelia: defining K15 function in the absence of K14. J. Cell. Biol. (1995) 129:1329-1344.
35. RYAN M, LEE K, MIYASHITA Y, CARTER WG: Targeted disruption of the LAMA3 gene in mice reveals abnormalities in survival and late stage differentiation of epithelial cells. J. Cell. Biol. (1999) 145:1309-1323.
36. MENG X, KLEMENT JF, LEPERI DA et al.: Targeted inactivation of murine gamma2-chain gene recapitulates human junctional epidermolysis bullosa. J Invest. Dermatol. (2003) 121:720-731.
37. GEORGE-LABOUESSE E, MESSADEQ N, YEHIA G, CADALBERT L, DIERICH A, LE MEUR M: Absence of integrin alpha 6 leads to epidermolysis bullosa and neonatal death in mice. Nat. Genet. (1996) 13:370-373.
38. VAN DER NEUT R, KRIMPENFORT P, CALAFAT J, NIESSEN CM, SONNENBERG A: Epithelial detachment due to absence of hemidesmosomes in integrin beta4 null mice. Nat. Genet. (1996) 13:366-369.
39. HEINONEN S, MÄNNIKÖ M, KLEMENT JF, WHITAKER-MENEZES D, MURPHY GF, UITTO J: Targeted inactivation of the type VII collagen gene (COL7A1) in mice results in severe blistering phenotype: a model for recessive dystrophic epidermolysis bullosa. J. Cell. Sci. (1999) 112:3641-3648.
40. SPIRITO F, CHARLESWORTH A, UNDER K, ORTONNE JP, BAIRD J, MENEGUZZI G: Animal models for skin blistering conditions: absence of laminin 5 causes hereditary junctional mechanobullous disease in the Belgian horse. J. Invest. Dermotol. (2002) 119:684-691.
41. PALAZZI X, MARCHAL T, CHABANNE L, SPADAFORA A, MAGNOL JP, MENEGUZZI G: Inherited dystrophic epidermolysis bullosa in inbred dogs: a spontaneous animal model for somatic gene therapy. J. Invest. Dermatol. (2000) 115:135-137.
42. JONKMAN MF, SCHEFFER H, STULP R et al.: Revenant mosaicism in epidermolysis bullosa caused by mitotic gene conversion. Cell (1997) 88:543-551. An experiment of nature shows that cDNA gene therapy is a feasible approach.
43. DARLING TN, YEE C, BAUER JW, HINTNER H, YANCEY KB: Revenant mosaicism: partial correction of a germ-line mutation in COL17A1 by a frame-restoring mutation. J. Clin. Invest (1999) 103:1371-1377.
44. SMITHF J, MORLEY SM, MCLEAN WH: Novel mechanism of revenant mosaicism in Dowling-Meara epidermolysis bullosa simplex. J. Invest. Dermatol. (2004) 122:73-77.
45. LACERRA G, SIERAKOWSKA H, CARESTIA C et al.: Restoration of hemoglobin A synthesis in erythroid cells from peripheral blood of thalassemic patients. Proc. Natl. Acad Sci. USA (2000) 97:9591-9596.
46. RUZZI L, PAS H, POSTERARO P et al.: A homozygous nonsense mutation in type XVII collagen gene (COL17A1) uncovers an alternatively spliced mRNA accounting for an unusually mild form of non-Herlitz junctional epidermolysis bullosa. J. Invest. Dermatol. (2001) 116:182-187.
47. MCGRATH JA, ASHTON GH, MELLERIO JE et al.: Moderation of phenotypic severity in dystrophic and junctional forms of epidermolysis bullosa through in-frame skipping of exons containing non-sense or frameshift mutations. J. Invest. Dermatol. (1999) 113:314-321.
48. HOFMANN Y, LORSON CL, STAMM S, ANDROPHY EJ, WIRTH B: Htra2-beta 1 stimulates an exonic splicing enhancer and can restore full-length SMN expression to survival motor neuron 2 (SMN2). Proc. Natl. Acad. Sci. USA (2000) 97:9618-9623.
49. LAN N, HOWREY RP, LEE SW, SMITH CA, SULLENGER BA: Ribozyme-mediated repair of sickle beta-globin mRNAs in erythrocyte precursors. Science (1998) 280:1593-1596. Targeted trans-splicing used to repair genetic diseases.
50. PUTTARAJU M, JAMISON SF, MANSFIELD SG, GARCIA-BLANCO MA, MITCHELL LG: Spliceosome-mediated RNA trans-splicing as a tool for gene therapy. Nat. Biotechnol. (1999) 17:246-252.
51. LIU X, JIANG Q, MANSFIELD SG et al.: Partial correction of endogenous DeltaF508 CFTR in human cystic fibrosis airway epithelia by spliceosome-mediated RNA trans-splicing. Nat. Biotechnol. (2002) 20:47-52.
52. CHAO H, MANSFIELD SG, BARTEL RC a al.: Phenotype correction of hemophilia A mice by spliceosome-mediated RNA trans-splicing. Nat. Med. (2003) 9:1015-1019.
53. DALLINGER G, PUTTARAJU M, MITCHELL LG et al.: Development of spliceosome-mediated RNA trans-splicing (SMaRT trade mark) for the correction of inherited skin diseases. Exp. Dermatol. (2003) 12:37-46.
54. SINGH A, URSIC D, DAVIES J: Phenotypic suppression and misreading Saccharomyces cerevisiae. Nature (1979) 277:146-148.
55. BARTON-DAVIS ER, CORDIER L, SHOTURMA DI, LELAND SE, SWEENEY HL: Aminoglycoside antibiotics restore dystrophin function to skeletal muscles of mdx mice. J. Clin. Invest (1999) 104:375-381. The application of a long known antibiotic for gene therapy.
56. WAGNER KR, HAMED S, HADLEY DW et al.: Gentamicin treatment of Duchenne and Becker muscular dystrophy due to nonsense mutations. Ann. Nuerol. (2001) 49:706-711.
57. POLITANO L, NIGRO G, NIGRO V et al.: Gentamicin administration in Duchenne patients with premature stop codon. Preliminary results. Acta Myol. (2003) 22:15-21.
58. HOWARD MT, SHIRTS BH, PETROS LM, FLANIGAN KM, GESTELAND RF, ATKINS JF: Sequence specificity of aminoglycoside-induced stop codon readthrough: potential implications for treatment of Duchenne muscular dystrophy. Ann. Neurol. (2000) 48:164-169.
59. WILSCHANSKI M, YAHAV Y, YAACOV Y et al.: Gentamicin-induced correction of CFTR function in patients with cystic fibrosis and CFTR stop mutations. N. Eng. J. Med. (2003) 349:1433-1441. In certain instances, gentamicin also works in the human system.
60. ARAKAWA M, SHIOZUKA M, NAKAYAMA Y et al.: Negamycin restores dystrophin expression in skeletal and cardiac muscles of mdx mice. J. Biochem. (Tokyo) (2003) 134:751-758.
61. BODEMER C, TCHEN SI, GHOMRASSENl S et al.: Skin expression of metalloproteinases and tissue inhibitor of metalloproteinases in sibling patients with recessive dystrophic epidermolysis and intrafamilial phenotypic variation. J. Invest. Dermatol. (2003) 121:273-279.
62. HACEIN-BEY-ABINA S, VON KALLE C, SCHMIDT M et al.: LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science (2003) 302:415-419. The insertion into a tumour-suppressor gene described here led to a transient halt of retroviral-based gene therapy trials.
63. CAVAZZANA-CALVO M, TRASHER A, MAVILIO F: The future of gene therapy. Nature (2004) 427:779-781.
64. MCLEAN I, TERRON A: Ribozyme gene therapy strategies for keratin disorders. J. Invest. Dermatol. (2002) 119:268.