Intraventricular brain injection of adeno-associated virus type 1 (AAV1) in neonatal mice results in complementary patterns of neuronal transduction to AAV2 and total long-term correction of storage lesions in the brains of β-glucuronidase-deficient mice

Journal of Virology

Volumn 77, Issue 12, 2003, Pages 7034-7040

  Passini, Marco A ^a,c   Watson, Deborah J ^a   Vite, Charles H ^a   Landsburg, Daniel J ^a   Feigenbaum, Alyson L ^a   Wolfe, John H ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c GENZYME CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLUCURONIDASE; CAPSID PROTEIN; CELL SURFACE RECEPTOR; VIRUS VECTOR;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS TYPE 1; ADENO ASSOCIATED VIRUS TYPE 2; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN DEVELOPMENT; CONTROLLED STUDY; GENETIC TRANSDUCTION; HUMAN; LYSOSOME STORAGE DISEASE; MOUSE; MUCOPOLYSACCHARIDOSIS TYPE 7; NERVE CELL; NERVE CONDUCTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEROTYPE; TARGET ORGAN; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

ANIMALS; ANIMALS, NEWBORN; BRAIN; DEPENDOVIRUS; FLUORESCENT ANTIBODY TECHNIQUE; GENE THERAPY; GENETIC VECTORS; GLUCURONIDASE; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; INJECTIONS, INTRAVENTRICULAR; MICE; MICE, INBRED C3H; MUCOPOLYSACCHARIDOSES; NEURONS; SEROTYPING; TRANSDUCTION, GENETIC;

EID: 0038618702     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.12.7034-7040.2003     Document Type: Article

References (44)

1. Alisky, J. M., S. M. Hughes, S. L. Sauter, D. Jolly, T. W. Dubensky, P. D. Staber, J. A. Chiorini, and B. L. Davidson. 2000. Transduction of murine cerebellar neurons with recombinant FIV and AAV5 vectors. Neuroreport 1:2669-2673.
2. Auricchio, A., G. Kobinger, V. Anand, M. Hildinger, E. O'Connor, A. M. Maguire, J. M. Wilson, and J. Bennett. 2001. Exchange of surface proteins impacts on viral vector cellular specificity and transduction characteristics: the retina as a model. Hum. Mol. Genet. 10:3075-3081.
3. Bantel-Schaal, U., H. Delius, R. Schmidt, and H. Van Hausen. 1999. Human adeno-associated virus type 5 is only distantly related to other known primate helper-dependent parvovirus. J. Virol. 73:939-947.
4. Barthel, L. K., and P. A. Raymond. 2000. In situ hybridization studies of retinal neurons. Methods Enzymol. 316:579-590.
5. Bartlett, J. S., R. J. Samulski, and T. J. McCown. 1998. Selective and rapid uptake of adeno-associated virus type 2 in brain. Hum. Gene Ther. 9:1181-1186.
6. Bartlett, J. S., R. Wilcher, and R. J. Samulski. 2000. Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors. J. Virol. 74: 2777-2785.
7. Birkenmeier, E. H., M. T. Davisson, W. G. Bearner, R. E. Ganschow, C. A. Vogler, B. Gwynn, K. A. Lyford, L. M. Maltais, and C. J. Wawrzyniak. 1989. Murine mucopolysaccharidosis VII: characterization of a mouse with β-glucuronidase deficiency. J. Clin. Investig. 83:1258-1266.
8. Bosch, A., E. Perret, N. Desmaris, and J. M. Heard. 2000. Long-term and significant correction of brain lesions in adult mucopolysaccharidosis type VII mice using recombinant AAV vectors. Mol. Ther. 1:63-70.
9. Brooks, A. I., C. S. Stein, S. M. Hughes, J. Heth, P. M. McCray, S. L. Sauter, J. C. Johnston, D. A. Cory-Slechta, H. J. Federoff, and B. L. Davidson. 2002. Functional correction of established central nervous system deficits in an animal model of lysosomal storage disease with feline immunodeficiency virus-based vectors. Proc. Natl. Acad. Sci. USA 99:6216-6221.
10. Casal, M. L., and J. H. Wolfe. 2001. In utero transplantation of fetal liver cells in the mucopolysaccharidosis type VII mouse results in low-level chimerism, but overexpression of β-glucuronidase can delay onset of clinical signs. Blood 97:1625-1634.
11. Chao, H., Y. Liu, J. Rabinowitz, C. Li, R. J. Samulski, and C. E. Walsh. 2000. Several log increase in therapeutic transgene delivery by distinct adeno-associated viral serotype vectors. Mol. Ther. 2:619-623.
12. Chiorini, J. A., L. Yang, Y. Liu, B. Safer, and R. M. Kotin. 1997. Cloning of adeno-associated virus type-4 (AAV4) and generation of recombinant AAV4 particles. J. Virol. 71:6823-6833.
13. Chiorini, J. A., F. Kim, L. Yang, and R. M. Kotin. 1999. Cloning and characterizing of adeno-associated virus type-5. J. Virol. 73:1309-1319.
14. Davidson, B. L., C. S. Stein, J. A. Heth, I. Martins, R. M. Kotin, T. A. Derksen, J. Zabner, A. Ghodsi, and J. A. Chiorini. 2000. Recombinant adeno-associated virus type 2, 4, and 5 vectors: transduction of variant cell types and regions in the mammalian central nervous system. Proc. Natl. Acad. Sci. USA 97:3428-3432.
15. Donsante, A., C. Vogler, N. Muzyczka, J. M. Crawford, J. Barker, T. Flotte, M. Campbell-Thompson, T. Daly, and M. S. Sands. 2001. Observed incidence of tumorigenesis in long-term rodent studies of rAAV vectors. Gene Ther. 8:1343-1346.
16. Duan, D., Z. Yan, Y. Yue, W. Ding, and J. F. Engelhardt. 2001. Enhancement of muscle gene delivery with pseudotyped adeno-associated virus type 5 correlates with myoblast differentiation. J. Virol. 75:7662-7671.
17. Elliger, S., C. Elliger, C. Aguilar, N. Raju, and G. Watson. 1999. Elimination of lysosomal storage in brains of MPS VII mice treated with intrathecal administration of an adeno-associated virus vector. Gene Ther. 6:1175-1178.
18. Frisella, W. A., L. H. O'Connor, C. A. Vogler, M. Roberts, S. Walkley, B. Levy, T. M. Daly, and M. S. Sands. 2001. Intracranial injection of recombinant adeno-associated virus improves cognitive function in a murine model of mucopolysaccharidosis type VII. Mol. Ther. 3:351-358.
19. Gao, G. P., M. R. Alivira, L. Wang, R. Caleedo, J. Johnston, and J. M. Wilson. 2002. Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc. Natl. Acad. Sci. USA 99:11854-11859.
20. Hildinger, M., A. Auricchio, G. P. Gao, L. Wang, N. Chirmule, and J. M. Wilson. 2001. Hybrid vectors based on adeno-associated virus serotypes 2 and 5 for muscle-directed gene transfer. J. Virol. 75:6199-6203.
21. Levy, B., N. Galvin, C. Vogler, E. H. Birkenmeier; and W. S. Sly. 1996. Neuropathology of murine mucopolysaccharidosis type VII. Acta Neuropathol. 92:562-568.
22. Meikle, P. J., J. J. Hopwood, A. E. Clague, and W. F. Carey. 1999. Prevalence of lysosomal storage disorders. JAMA 20:249-254.
23. Neufeld, E. F. 1991. Lysosomal storage diseases Annu. Rev. Biochem. 60: 257-280.
24. O'Connor, L. H., L. C. Erway, C. A. Vogler, W. S. Sly, A. Nicholes, J. Grubb, S. W. Holmberg, B. Levy, and M. S. Sands. 1998. Enzyme replacement therapy for murine mucopolysaccharidosis type VII leads to improvements in behavior and auditory function. J. Clin. Investig. 101:1394-1400.
25. Passini, M. A., and J. H. Wolfe. 2001. Widespread gene delivery and structure-specific patterns of expression in the brain from an adeno-associated virus vector following intraventricular injections of neonatal mice. J. Virol. 75:12382-12392.
26. Passini, M. A., E. B. Lee, G. G. Heuer, and J. H. Wolfe. 2002. Distribution of a lysosomal enzyme in the adult brain by axonal transport and by cells of the rostral migratory stream. J. Neurosci. 22:6437-6446.
27. Rabinowitz, J. E., F. Rolling, C. Li, H. Conrath, W. Xiao, A. Xiao, and R. J. Samulski. 2002. Cross-packaging of a single adeno-associated virus (AAV) type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity. J. Virol. 76:791-801.
28. Ross, C. J., M. Ralph, and P. L. Chang. 2000. Somatic gene therapy for a neurodegenerative disease using microencapsulated recombinant cells. Exp. Neurol. 166:276-286.
29. Rutledge, E. A., C. L. Halbert, and D. W. Russell. 1998. Infectious clones and vectors derived from adeno-associated virus (AAV) serotypes other than AAV type 2. J. Virol. 72:309-319.
30. Sando, G. N., and E. F. Neufeld. 1977. Recognition and receptor-mediated uptake of a lysosomal enzyme, alpha-L-iduronidase, by cultured human fibroblasts. Cell 12:619-627.
31. Sciver, C. R., A. L. Beaudet, W. S. Sly, and D. Valle. 2001. Metabolic basis of inherited disease, 8th ed., p. 3369-3894. McGraw-Hill Book Co., New York, N.Y.
32. Sferra, T. J., G. Qu, D. McNeely, R. Rennard, K. R. Clark, W. D. Lo, and P. R. Johnson. 2000. Recombinant adeno-associated virus-mediated correction of lysosomal storage within the central nervous system of the adult mucopolysaccharidosis type VII mouse. Hum. Gene Ther. 11:507-519.
33. Skorupa, A. F., K. J. Fisher, J. M. Wilson, M. K. Parente, and J. H. Wolfe. 1999. Sustained production of β-glucuronidase from localized sites after AAV vector gene transfer results in widespread distribution of enzyme and reversal of lysosomal storage lesions in a large volume of brain in mucopolysaccharidosis VII mice. Exp. Neurol. 160:17-27.
34. Sly, W. S., B. A. Quinton, W. J. McAlister, and D. J. Rimoin. 1973. Beta glucuronidase deficiency: report of clinical, radiologic, and biochemical features of a new mucopolysaccharidosis. J. Pediatr. 82:249-257.
35. Snyder, E. Y., R. M. Taylor, and J. H. Wolfe. 1995. Neural progenitor cell engraftment corrects lysosomal storage throughout the MPS VII mouse brain. Nature 374:367-370.
36. Summerford, C., and R. J. Samulski. 1998. Membrane-associated heparin sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J. Virol. 72:1438-1445.
37. Taylor, R. M., and J. H. Wolfe. 1997. Decreased lysosomal storage in the adult MPS VII mouse brain in the vicinity of grafts of retroviral vector-corrected fibroblasts secreting high levels of β-glucuronidase. Nat. Med. 3:771-774.
38. Vogler, C., E. H. Birkenmeier, W. S. Sly, B. Levy, C. Pegors, J. W. Kyle, and W. G. Beamer. 1990. A murine model of mucopolysaccharidosis VII. Am. J. Pathol. 136:207-217.
39. Walters, R. W., S. M. P. Yi, S. Keshavjee, K. E. Brown, M. J. Welsh, J. A. Chiorini, and J. Zabner. 2001. Binding of adeno-associated virus type 5 to 2,3 sialic acid is required for gene transfer. J. Biol. Chem. 276:20610-20616.
40. Watson, D. J., and J. H. Wolfe. 2002. Lentiviral vectors for gene transfer to the central nervous system: applications in lysosomal storage disease animal models, p. 383-403. In C. Machida (ed.), Viral vectors for gene therapy: methods and protocols. Humana Press, Inc., Totowa, N.J.
41. Wolfe, J. H., J. W. Kyle, M. S. Sands, W. S. Sly, D. G. Markowitz, and M. K. Parente. 1995. High levels of expression and export of β-glucuronidase from murine mucopolysaccharidosis VII cells corrected by a double-copy retrovirus vector. Gene Ther. 2:70-78.
42. Wolfe, J. H., and M. S. Sands. 1996. Murine mucopolysaccharidosis type VII: a model for somatic gene therapy of the central nervous system, p. 263-274. In R. R. Lowenstein and L. W. Enquist (ed.), Protocols for gene transfer in neuroscience: towards gene therapy of neurological disorders. John Wiley & Sons, Ltd., London, United Kingdom.
43. Xiao, W., N. Chirmule, S. C. Berta, B. McCullough, G. P. Gao, and J. M. Wilson. 1999. Gene therapy based on adeno-associated virus type 1. J. Virol. 73:3994-4003.
44. Zabner, J., M. Seiler, R. Walters, R. Kotin, W. Fulgeras, B. L. Davidson, and J. A. Chiorini. 2000. Adeno-associated virus type 5 (AAV5) but not AAV2 binds to the apical surface of airway epithelia and facilitates gene transfer. J. Virol. 74:3852-3858.