Correction of enzymatic and lysosomal storage defects in fabry mice by adenovirus-mediated gene transfer

Human Gene Therapy

Volumn 10, Issue 10, 1999, Pages 1667-1682

  Ziegler, Robin J ^a   Yew, Nelson S ^a   Li, Chester ^a   Cherry, Maribeth ^a   Berthelette, Patricia ^a   Romanczuk, Helen ^a   Ioannou, Yiannis A ^b   Zeidner, Kenneth M ^b   Desnick, Robert J ^b   Cheng, Seng H ^a  

^a GENZYME CORPORATION   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSIDASE; GLOBOTRIAOSYLCERAMIDE; GLYCOPROTEIN GP 39; GLYCOSPHINGOLIPID; MANNOSE 6 PHOSPHATE; MONOCLONAL ANTIBODY; VIRUS VECTOR;

ANIMAL CELL; ARTICLE; ENZYME ACTIVITY; FABRY DISEASE; FEMALE; FIBROBLAST; GENE THERAPY; GENE TRANSFER; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; KNOCKOUT MOUSE; LYSOSOME STORAGE DISEASE; NONHUMAN; PROTEIN EXPRESSION; VIRUS RECOMBINANT;

EID: 0033166317     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/10430349950017671     Document Type: Article

References (67)

1. AKLI, S., GUIDOTTI, J.E., VIGNE, E., PERRICAUDET, M., SANDHOFF, K., KAHN, A., and POENARU, L. (1996). Restoration of hexosaminidase A activity in human Tay-Sachs fibroblasts via adenoviral vector-mediated gene transfer. Gene Ther. 3, 769-774.
2. ARMENTANO, D., SOOKDEO, C.C., HEHIR, K., GREGORY, R.J., ST. GEORGE, J.A., PRINCE, G.A., WADSWORTH, S.C., and SMITH, A.E. (1995). Characterization of an adenovirus gene transfer vector containing an E4 deletion. Hum. Gene Ther. 6, 1343-1353.
3. ARMENTANO, D., ZABNER, J., SACKS, C., SOOKDEO, C., SMITH, M.P., ST. GEORGE, J.A., WADSWORTH, S.C., SMITH, A.E., and GREGORY, R.J. (1997). Effect of the E4 region on the persistence of transgene expression from adenovirus vectors. J. Virol. 71, 2408-2416.
4. BARTON, N.W., BRADY, R.O., DAMBROSIA, J.M., DI BISCEGLI, A.M., DOPPLET, S.H., HILL, S.C., MANKIN, H.J., MURRAY, G.J., PARKER, R.I., and ARGOFF, C.E. (1991). Replacement therapy for inherited enzyme-deficiency - macrophage-targeted glucocerebrosidase for Gaucher's disease. N. Engl. J. Med. 324, 1464-1470.
5. BISHOP, D.F., CALHOUN, D.H., BERNSTEIN, H.S., HANTZOPOULOS, P., QUINN, M., and DESNICK, R.J. (1986). Human α-galactosidase A: Nucleotide sequence of a cDNA alone encoding the mature enzyme. Proc. Natl. Acad. Sci. U.S.A. 83, 4859-4863.
6. BISHOP, D.F., KORNREICH, R., and DESNICK, R.J. (1988). Structural organization of the human α-galactosidase A gene: Further evidence for the absence of the 3′ untranslated region. Proc. Natl. Acad. Sci. U.S.A. 85, 3903-3907.
7. BRADY, R.O., GAL, A.E., BRADLEY, R.M., MARTENSSON, E., WARSHAW, A.L., and LASTER, L. (1967). Enzymatic defect in Fabry's disease: Ceramide trihexosidase deficiency. N. Engl. J. Med. 276, 1163-1167.
8. BRUDER, J.T., JIE, T., McVEY, D.L., and KOVESDI, I. (1997). Expression of gp19K increases the persistence of transgene expression from adenovirus vectors in vivo. J. Virol. 71, 9206-9213.
9. CONNELLY, S., GARDNER, J.M., LYONS, R.M., McCLELLAND, A., and KALELO, M. (1996). Sustained expression of therapeutic levels of human factor VIII in mice. Blood 87, 4671-4677.
10. CRAWLEY, A.C., BROOKS, D.A., MULLER, V.J., PETERSEN, B.A., ISAAC, E.L., BIELICKI, J., KING, B.M., BOULTER, C.D., MOORE, A.J., FAZZALARI, N.L., ANSON, D.S., BYERS, S., and HOPWOOD, J.J. (1996). Enzyme replacement therapy in a feline model of Maroteaux-Lamy syndrome. J. Clin. Invest. 97, 1864-1873.
11. DAI, Y., SCHWARZ, E.M., GU, D., ZHANG, W., SARVETNICK, N., and VERMA, I.M. (1995). Cellular and humoral responses to adenoviral vectors containing factor IX gene: Tolerization of factor IX and vector antigens allows for long term expression. Proc. Natl. Acad. Sci. U.S.A. 92, 1401-1405.
12. DEDIEU, J.F., VIGNE, E., TORRENT, C., JULLIEN, C., MAHFOUZ, I., CAILLAUD, J.M., AUBAILLY, N., ORSINI, D., GUILLAUME, J.M., OPOLON, P., DELAERE, P., PERRICAUDET, M., and YEH, P. (1997). Long-term gene delivery into the livers of immunocompetent mice with E1/E4-defective adenoviruses. J. Virol. 71, 4626-4637.
13. DEMATTEO, R.P., CHU, G., AHN, M., CHANG, E., BARKER, C.F., and MARKMANN, J.F. (1997). Long-lasting adenovirus transgene expression in mice through neonatal intrathymic tolerance induction without the use of immunosuppression. J. Virol. 71, 5330-5335.
14. DESNICK, R.J., IOANNOU, Y.A., and ENG. C.M. (1995). α-Galactosidase A deficiency: Fabry disease. In The Metabolic and Molecular Basis of Inherited Disease. C.R. Scriver, A.L. Beaudet, W.S. Sly, and D. Valle, eds. (McGraw-Hill, New York) pp. 2741-2784.
15. DI FRANCESCO, C., CRACCO, C., TOUMANIN, R., PICCI, L., VENTURA, L., ZACCHELLO, F., DI NATALE, P., ANSON, D.S., HOPWOOD, J.J., GRAHAM, F.L., and SCARPA, M. (1997). In vitro correction of iduronate-2-sulfatase deficiency by adenovirus-mediated gene transfer. Gene Ther. 4, 442-448.
16. ENGELHARDT, J.F., YE, X., DORANZ, B., and WILSON, J.M. (1994). Ablation of E2a in recombinant adenoviruses improves trans-gene expression and decreases inflammatory responses in mouse liver. Proc. Natl. Acad. Sci. U.S.A. 91, 6196-6200.
17. GAO, G.P., YANG, Y., and WILSON, J.M. (1996). Biology of adenovirus vectors with E1 and E4 deletions for liver-directed gene therapy. J. Virol. 70, 8934-8943.
18. GIESELMANN, V. (1995). Lysosomal storage diseases. Biochim. Biophys. Acta 1270, 103-136.
19. GOTLIB, R.W., BISHOP, D.F., WANG, A.M., ZEIDNER, K.M., IOANNOU, Y.A., ADLER, D.A., DISTECHE, C.M., and DESNICK, R.J. (1996). The entire genomic sequence and cDNA expression of mouse α-galactosidase A. Biochem. Mol. Med. 57, 139-148.
20. HUARD, J., LOCHMULLER, H., ASCADI, G., JANI, A., MASSIE, B., and KARPATI, G. (1995). The route of administration is a major determinant of the transduction efficiency of rat tissues by adenoviral recombinants. Gene Ther. 2, 107-115.
21. ILAN, Y., ATTAVAR, P., TAKAHASHI, M., DAVIDSON, A., HORWITZ, M.S., GUIDA, J., CHOWDURY, N.R., and CHOWDHURY, J.R. (1996). Induction of central tolerance by intrathymic inoculation of adenoviral antigens into the host thymus permits long-term gene therapy in Gunn rats. J. Clin. Invest. 98, 2640-2647.
22. IOANNOU, Y.A., BISHOP, D.F., and DESNICK, R.J. (1992). Overexpression of human α-galactosidase A results in its intracellular aggregation, crystallization in lysosomes, and selective secretion. J. Cell Biol. 119, 1137-1150.
23. JIANG, C., O'CONNOR, S.P., ARMENTANO, D., BERTHELETTE, P.B., SCHIAVI, S.C., JEFFERSON, D.M., SMITH, A.E., WADSWORTH, S.C., and CHENG, S.H. (1996). Ability of adenovirus vectors containing different CFTR transcriptional cassettes to correct ion transport defects in CF cells. Am. J. Physiol. 271, L527-L537.
24. JOOSS, K., YANG, Y., and WILSON, J.M. (1996). Cyclophosphamide diminishes inflammation and prolongs transgene expression following delivery of adenoviral vectors to mouse liver and lung. Hum. Gene Ther. 7, 1555-1566.
25. JOOSS, K., TURKA, L.A., and WILSON, J.M. (1998). Blunting of immune responses to adenoviral vectors in mouse liver and lung with CTLA4Ig. Gene Ther. 5, 309-319.
26. KAPLAN, J.M., and SMITH, A.E. (1997). Transient immunosuppression with deoxyspergualin improves longevity of transgene expression and ability to readminister adenoviral vector to the mouse lung. Hum. Gene Ther. 8, 1095-1104.
27. KAY, M.A., HOLTERMAN, A.X., MEUSE, L., GOWN, A., OCHS, H.D., LINSLEY, P.S., and WILSON, C.B. (1995). Long-term hepatic adenovirus-mediated gene expression in mice following CTLA4Ig administration. Nature Genet. 11, 191-197.
28. KAY, M.A., MEUSE, L., GOWN, A.M., LINSLEY, P., HOLLENBAUCH, D., ARUFFO, A., OCHS, H.D., and WILSON, C.B. (1997). Transient immunomodulation with anti-CD40 ligand antibody and CTLA4Ig enhances persistence and secondary adenovirus-mediated gene transfer into mouse liver. Proc. Natl. Acad. Sci. U.S.A. 94, 4686-4691.
29. KORNFELD, S., and MELLMAN, I. (1989). The biogenesis of lysosomes. Annu. Rev. Cell. Biol. 5, 483-525.
30. LIEBER, A., HE, C.Y., KIRILLOVA, I., and KAY, M.A. (1996). Recombinant adenvoiruses with large deletions generated by Cre-mediated excision exhibit different biological properties compared with first-generation vectors in vitro and in vivo. J. Virol. 70, 8944-8960.
31. MAYES, J.S., SCHEERER, J.B., SIFERS, R.N., and DONALDSON, M.L. (1981). Differential assay for lysosomal α-galactosidases in human tissues and its application to Fabry's disease. Clin. Chim. Acta 112, 247-251.
32. MEDIN, J.A., TUDOR, M., SIMOVITCH, R., QUIRK, I.M., JACOBSON, S., MURRAY, G.J., and O'BRADY, R.O. (1996). Correction in trans for Fabry disease: Expression, secretion, and uptake of α-galactosidase A in patient-derived cells driven by a high-liter recombinant retroviral vector. Proc. Natl. Acad. Sci. U.S.A. 93, 7917-7922.
33. MICHOU, A., SANTORO, L., CHRIST, M., JULLIARD, V., PAVIRANI, A., and MEHTALI, M. (1997). Adenovirus-mediated gene transfer: Influence of transgene, mouse strain and type of immune response on persistence of transgene expression. Gene Ther. 4, 473-482.
34. MORRAL, N., O'NEAL, W., ZHOU, H., LANGSTON, C., and BEAUDET, A. (1997). Immune responses to reporter proteins and high viral dose limit duration of expression with adenoviral vectors: Comparison of E2a wild type and E2a deleted vectors. Hum. Gene Ther. 8, 1275-1286.
35. MOULLIER, P., BOHL, D., HEARD, J.M., and DANOS, O. (1993). Correction of lysosomal storage in the liver and spleen of MPS VII mice by implantation of genetically modified skin fibroblasts. Nature Genet. 4, 154-159.
36. MOULLIER, P., BOHL, D., CARDOSO, J., HEARD, J.M., and DANOS, O. (1995). Long-term delivery of a lysosomal enzyme by genetically modified fibroblasts in dogs. Nature Med. 1, 353-357.
37. NEUFELD, E.F. (1991). Lysosomal storage diseases. Annu. Rev. Biochem. 60, 257-280.
38. NOELLE, R.J., ROY, M., SHEPHERD, D.M., STAMENKOVIC, I., LEDBETTER, J.A., and ARUFFO, A. (1992). A 39 kDa protein on activated helper T cells binds CD40 and transduces the signal for cognate activation of B cells. Proc. Natl. Acad. Sci. U.S.A. 89, 6550-6554.
39. O'CONNOR, L.H., ERWAY, L.C., VOGLER, C.A., SLY, W.S., NICHOLES, A., GRUBB, J., HOLMBERG, S.W., LEVY, B., and SANDS, M.S. (1998). Enzyme replacement therapy for murine mucopolysaccharidosis type VII leads to improvements in behavior and auditory function. J. Clin. Invest. 101, 1394-1400.
40. OHASHI, Y., WATABE, K., UEHARA, K., SLY, W.S., VOGLER, C., and ETO, Y. (1997). Adenovirus-mediated gene transfer and expression of human β-glucuronidase gene in the liver, spleen, and central nervous system in mucopolysaccharidosis type VII mice. Proc. Natl. Acad. Sci. U.S.A. 94, 1287-1292.
41. OHSHIMA, T., MURRAY, G.J., NAGLE, J.W., QUIRK, J.M., KRAUS, M.H., BARTON, N.W., BRADY, R.O., and KULKARNI, A.B. (1995). Structural organization and expression of the mouse gene encoding α-galactosidase A. Gene 166, 277-280.
42. OHSHIMA, T., MURRAY, G.J., SWAIM, W.D., LONGENECKER, G., QUIRK, J.M., CARDARELLI, C.O., SUGIMOTO, Y., PASTAN, I., GOTTESMAN, M.M., BRADY, R.O., and KULKARNI, A.B. (1997). α-Galactosidase A deficient mice: A model of Fabry disease. Proc. Natl. Acad. Sci. U.S.A. 94, 2540-2544.
43. PASTORES, G.M., SIBILLE, A.R., and GRABOWSKI, G.A. (1993). Enzyme therapy in Gaucher disease type I: Dosage efficacy and adverse effects in 33 patients treated for 6 to 24 months. Blood 82, 408-416.
44. PEETERS, M.J., PATJIN, G.A., LIEBER, A., MEUSE, L., and KAY, M.A. (1996). Adenovirus-mediated hepatic gene transfer in mice: Comparison of intravascular and biliary administration. Hum. Gene Ther. 7, 1693-1699.
45. PFEFFER, S.R. (1991). Targeting of proteins to the lysosome. Curr. Top. Microbiol. Immunol. 170, 43-63.
46. PLATT, F.M., NEISES, G.R., REINKENSMEIER, G., TOWNSEND, M.J., PERRY, V.H., PROIA, R.L., WINCHESTER, B., DWEK, R.A., and BUTTERS, T.D. (1997). Prevention of lysosomal storage in Tay-Sachs mice treated with n-butyldeoxynojirimycin. Science 276, 428-431.
47. POENARU, L. (1996). Particularities of lysosomal storage diseases gene therapy. Gene Ther. 3, 1039-1041.
48. SALVETTI, A., MOULLIER, P., CORNET, V., BROOKS, D., HOPWOOD, J.J., DANOS, O., and HEARD, J.M. (1995). In vivo delivery of human α-L-iduronidase in mice implanted with neo-organs. Hum. Gene Ther. 6, 1153-1159.
49. SCARIA, A., ST. GEORGE, J.A., GREGORY, R.J., WADSWORTH, S.C., SMITH, A.E., and KAPLAN, J.M. (1997). Antibody to CD40 ligand inhibits both humoral and cellular immune responses to adenoviral vectors and facilitates repeated administration to mouse airway. Gene Ther. 4, 611-617.
50. SCARIA, A., ST. GEORGE, J.A., JIANG, C., KAPLAN, J.M., WADSWORTH, S.C., and GREGORY, R.J. (1998). Adenovirus-mediated persistent cystic fibrosis transmembrane conductance regulator expression in mouse airway epithelium. J. Virol. 72, 7302-7309.
51. SCHEULE, R.K., ST. GEORGE, J.A., BAGLEY, R.G., MARSHALL, J., KAPLAN, J.M., AKITA, G.Y., WANG, K.X., LEE, E.R., HARRIS, D.J., JIANG, C., YEW, N.S., SMITH, A.E., and CHENG, S.H. (1997). Basis of pulmonary toxicity associated with cationic lipid-mediated gene transfer to the mammalian lung. Hum. Gene Ther. 8, 689-707.
52. SCHIEDNER, G., MORRAL, N., PARKS, R.J., WU, Y., KOOPMANS, S.C., LANGSTON, C., GRAHAM, F.L., BEAUDET, A.L., and KOCHANEK, S. (1998). Genomic DNA transfer with a high-capacity adenovirus vector results in improved in vivo gene expression and decreased toxicity. Nature Genet. 18, 180-183.
53. SHULL, R.M., KAKKIS, E.D., McENTEE, M.F., KANIA, S.A., JONAS, A.J., and NEUFELD, E.F. (1994). Enzyme replacement in a canine model of Hurler syndrome. Proc. Natl. Acad. Sci. U.S.A. 91, 12937-12941.
54. SMITH, T.A., WHITE, B.S., GARDNER, J.M., KALEKO, M., and McCLELLAND, A. (1996). Transient immunosuppression permits successful repetitive intravenous administration of an adenovirus vector. Gene Ther. 3, 496-502.
55. SNYDER, R.O., MIAO, C., MEUSE, L., TUBB, J., DONAHUE, B.A., LIN, H.F., STAFFORD, D.W., PATEL, S., THOMPSON, A.R., NICHOLS, T., READ, M.S., BELLINGER, D.A., BRINKHOUS, K.M., and KAY, M.A. (1999). Correction of hemophilia B in canine and murine models using recombinant adeno-associated viral vectors. Nature Med. 5, 64-70.
56. STEIN, C.S., PEMBERTON, J.L., VAN ROOIJEN, N., and DAVIDSON, B.L. (1998). Effects of macrophage depletion and anti-CD40 ligand on transgene expression and redosing with recombinant adenovirus. Gene Ther. 5, 431-439.
57. TRIPATHY, S.K., BLACK, H.B., GOLDWASSER, E., and LEIDEN, J.M. (1996). Immune repsonses to transgene-encoded proteins limit the stability of gene expression after injection of replication-defective adenovirus vectors. Nature Med. 2, 545-550.
58. TSUJINO, S., KINOSHITA, N., TASHIRO, T., IKEDA, K., ICHIHARA, N., KIKUCHI, H., HAGIWARA, Y., MIZUTANI, M., KIKUCHI, T., and SAKURAGAWA, N. (1998). Adenovirus-mediated transfer of human acid maltase gene reduces glycogen accumulation in skeletal muscle of Japanese quail with acid maltase deficiency. Hum. Gene Ther. 9, 1609-1616.
59. VOGLER, C., SANDS, M.S., GALVIN, N., LEVY, B., THORPE, C., BARKER, J., and SLY, W.S. (1998). Murine mucopolysaccharidosis type VII: The impact of therapies on the clinical course and pathology in a murine model of lysosomal storage disease. J. Inherit. Metab. Dis. 21, 575-586.
60. VON FIGURA, K., and HASILIK, A. (1986). Lysosomal enzymes and their receptors. Annu. Rev. Biochem. 55, 167-193.
61. WANG, A.M., IOANNOU, Y.A., ZEIDNER, K.M., GOTLIB, R.W., DIKMAN, S., STEWART, C.L., and DESNICK, R.J. (1996). Fabry disease: Generation of a mouse model with α-galactosidase A defiriency. Am. J. Hum. Genet. 59, A208.
62. WATSON, G.L., SAYLES, J.N., ELLIGER, S.S., ELLIGER, C.A., RAJU, N.R., KURTZMAN, G.J., and PODSAKOFF, G.M. (1998). Treatment of lysosomal storage disease in MPS VII mice using recombinant adene-associated virus. Gene Ther. 5, 1642-1649.
63. WOLFE, J.H., SANDS, M.S., BARKER, J.E., GWYNN, B., ROWE, L.B., VOGLER, C.A., and BIRKENMEIER, E.H. (1992). Reversal of pathology in murine mucopolysaccharidosis type VII by somatic cell gene transfer. Nature (London) 360, 749-753.
64. XIAO, W., BERTA, S.C., LU, M.M., MOSCIONI, A.D., TAZELAAR, J., and WILSON, J.M. (1998). Adeno-associated virus as a vector for liver-directed gene therapy. J. Virol. 72, 10222-10226.
65. YANG, Y., NUNES, F.A., BERENCSI, K., FURTH, E.E., GONCZOL, E., and WILSON, J.M. (1994). Cellular immunity to viral antigens limits E1-deleted adenoviruses for gene therapy. Proc. Natl. Acad. Sci. U.S.A. 91, 4407-4411.
66. YANG, Y., SU, Q., GREWAL, I.S., SCHILZ, R., FLAVELL, R.A., and WILSON, J.M. (1996). Transient subversion of CD40 ligand function diminishes immune responses to adenovirus vectors in mouse liver and lung tissue. J. Virol. 70, 6370-6377.
67. ZEIDNER, K.M., DESNICK, R.J., and IOANNOU, Y.A. (1999). Quantitative determination of globotriaosylceramide by immunodetection of glycolipid-bound recombinant verotoxin B subunit. Anal. Biochem. (in press).