Long-term correction of Sandhoff disease following intravenous delivery of rAAV9 to mouse neonates

Molecular Therapy

Volumn 23, Issue 3, 2015, Pages 414-422

  Walia, Jagdeep S ^a,b,c   Altaleb, Naderah ^b   Bello, Alexander ^b,d   Kruck, Christa ^b   LaFave, Matthew C ^e   Varshney, Gaurav K ^e   Burgess, Shawn M ^e   Chowdhury, Biswajit ^b   Hurlbut, David ^a   Hemming, Richard ^b   Kobinger, Gary P ^b,d   Triggs Raine, Barbara ^b,c  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

^c Manitoba Institute of Child Health   (Canada)

^d PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^e NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; BETA N ACETYLHEXOSAMINIDASE; COMPLEMENTARY DNA; GANGLIOSIDE GM2; PARVOVIRUS VECTOR; BETA N ACETYLHEXOSAMINIDASE BETA CHAIN;

ADENO ASSOCIATED VIRUS 9; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEATH; DRUG BLOOD LEVEL; DRUG BRAIN LEVEL; DRUG EFFICACY; DRUG MECHANISM; DRUG MONITORING; ENCEPHALITIS; ENZYME ACTIVITY; EXPERIMENTAL STUDY; FEMALE; HEXB GENE; HUMAN; HUMAN CELL; LIPID STORAGE; LIVER TUMOR; LUNG TUMOR; MALE; MOTOR PERFORMANCE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROLOGIC DISEASE; NEWBORN; NONHUMAN; PHENOTYPE; SANDHOFF DISEASE; SURVIVAL TIME; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS RECOMBINANT; ADMINISTRATION AND DOSAGE; ADVERSE EFFECTS; AGE; ANIMAL; BRAIN; DEPENDOPARVOVIRUS; DISEASE MODEL; ENZYMOLOGY; GENE EXPRESSION; GENE THERAPY; GENE VECTOR; GENETICS; INFLAMMATION; INTRAVENOUS DRUG ADMINISTRATION; KNOCKOUT MOUSE; LACTOSE OPERON; LIVER NEOPLASMS; LUNG NEOPLASMS; LYSOSOME; METABOLISM; MORTALITY; MOTOR ACTIVITY; PATHOLOGY; PROCEDURES; SURVIVAL ANALYSIS;

ADENO-ASSOCIATED VIRUS 9; MUS;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BETA-HEXOSAMINIDASE BETA CHAIN; BRAIN; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; FEMALE; G(M2) GANGLIOSIDE; GENE EXPRESSION; GENETIC THERAPY; GENETIC VECTORS; INFLAMMATION; INJECTIONS, INTRAVENOUS; LAC OPERON; LIVER NEOPLASMS; LUNG NEOPLASMS; LYSOSOMES; MALE; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; SANDHOFF DISEASE; SURVIVAL ANALYSIS;

EID: 84924049143     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.240     Document Type: Article

References (50)

1. Sandhoff, K, Andreae, U and Jatzkewitz, H (1968). Deficient hexosaminidase activity in an exceptional case of Tay-Sachs disease with additional storage of kidney globoside in visceral organs. Pathol Eur 3: 278-285.
2. Gravel, RA, Triggs-Raine, BL and Mahuran, DJ (1991). Biochemistry and genetics of Tay-Sachs disease. Can J Neurol Sci 18(suppl. 3): 419-423.
3. Myrianthopoulos, NC (1962). Some Epidemiologic and Genetic Aspects of Tay Sachs Disease. Academic Press: New York.
4. Andermann, E, Scriver, CR, Wolfe, LS, Dansky, L and Andermann, F (1977). Genetic variants of Tay-Sachs disease: Tay-Sachs disease and Sandhoff's disease in French Canadians, juvenile Tay-Sachs disease in Lebanese Canadians, and a Tay-Sachs screening program in the French-Canadian population. Prog Clin Biol Res 18: 161-188.
5. Lowden, JA, Ives, EJ, Keene, DL, Burton, AL, Skomorowski, MA and Howard, F (1978). Carrier detection in Sandhoff disease. Am J Hum Genet 30: 38-45.
6. Kaya, N, Al-Owain, M, Abudheim, N, Al-Zahrani, J, Colak, D, Al-Sayed, M et al. (2011). GM2 gangliosidosis in Saudi Arabia: multiple mutations and considerations for future carrier screening. Am J Med Genet A 155A: 1281-1284.
7. Cantor, RM, Roy, C, Lim, JS and Kaback, MM (1987). Sandhoff disease heterozygote detection: a component of population screening for Tay-Sachs disease carriers. II. Sandhoff disease gene frequencies in American Jewish and non-Jewish populations. Am J Hum Genet 41: 16-26.
8. Kleiman, FE, de Kremer, RD, de Ramirez, AO, Gravel, RA and Argaraña, CE (1994). Sandhoff disease in Argentina: high frequency of a splice site mutation in the HEXB gene and correlation between enzyme and DNA-based tests for heterozygote detection. Hum Genet 94: 279-282.
9. Conzelmann, E and Sandhoff, K (1983). Partial enzyme deficiencies: residual activities and the development of neurological disorders. Dev Neurosci 6: 58-71.
10. Miklyaeva, EI, Dong, W, Bureau, A, Fattahie, R, Xu, Y, Su, M et al. (2004). Late onset Tay-Sachs disease in mice with targeted disruption of the Hexa gene: behavioral changes and pathology of the central nervous system. Brain Res 1001: 37-50.
11. Phaneuf, D, Wakamatsu, N, Huang, JQ, Borowski, A, Peterson, AC, Fortunato, SR et al. (1996). Dramatically different phenotypes in mouse models of human Tay-Sachs and Sandhoff diseases. Hum Mol Genet 5: 1-14.
12. Sango, K, Yamanaka, S, Hoffmann, A, Okuda, Y, Grinberg, A, Westphal, H et al. (1995). Mouse models of Tay-Sachs and Sandhoff diseases differ in neurologic phenotype and ganglioside metabolism. Nat Genet 11: 170-176.
13. Gulinello, M, Chen, F and Dobrenis, K (2008). Early deficits in motor coordination and cognitive dysfunction in a mouse model of the neurodegenerative lysosomal storage disorder, Sandhoff disease. Behav Brain Res 193: 315-319.
14. Hoogerbrugge, PM, Brouwer, OF, Bordigoni, P, Ringden, O, Kapaun, P, Ortega, JJ et al. (1995). Allogeneic bone marrow transplantation for lysosomal storage diseases. The European Group for Bone Marrow Transplantation. Lancet 345: 1398-1402.
15. Tsuji, D, Akeboshi, H, Matsuoka, K, Yasuoka, H, Miyasaki, E, Kasahara, Y et al. (2011). Highly phosphomannosylated enzyme replacement therapy for GM2 gangliosidosis. Ann Neurol 69: 691-701.
16. Cachón-González, MB, Wang, SZ, Lynch, A, Ziegler, R, Cheng, SH and Cox, TM (2006). Effective gene therapy in an authentic model of Tay-Sachs-related diseases. Proc Natl Acad Sci USA 103: 10373-10378.
17. Cachón-González, MB, Wang, SZ, McNair, R, Bradley, J, Lunn, D, Ziegler, R et al. (2012). Gene transfer corrects acute GM2 gangliosidosis-potential therapeutic contribution of perivascular enzyme flow. Mol Ther 20: 1489-1500.
18. Cachón-González, MB, Wang, SZ, Ziegler, R, Cheng, SH and Cox, TM (2014). Reversibility of neuropathology in Tay-Sachs-related diseases. Hum Mol Genet 23: 730-748.
19. Clarke, JT, Mahuran, DJ, Sathe, S, Kolodny, EH, Rigat, BA, Raiman, JA et al. (2011). An open-label Phase I/II clinical trial of pyrimethamine for the treatment of patients affected with chronic GM2 gangliosidosis (Tay-Sachs or Sandhoff variants). Mol Genet Metab 102: 6-12.
20. Ashe, KM, Bangari, D, Li, L, Cabrera-Salazar, MA, Bercury, SD, Nietupski, JB et al. (2011). Iminosugar-based inhibitors of glucosylceramide synthase increase brain glycosphingolipids and survival in a mouse model of Sandhoff disease. PLoS ONE 6: e21758.
21. Büning, H, Perabo, L, Coutelle, O, Quadt-Humme, S and Hallek, M (2008). Recent developments in adeno-associated virus vector technology. J Gene Med 10: 717-733.
22. Gray, SJ, Matagne, V, Bachaboina, L, Yadav, S, Ojeda, SR and Samulski, RJ (2011). Preclinical differences of intravascular AAV9 delivery to neurons and glia: a comparative study of adult mice and nonhuman primates. Mol Ther 19: 1058-1069.
23. Foust, KD, Nurre, E, Montgomery, CL, Hernandez, A, Chan, CM and Kaspar, BK (2009). Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 27: 59-65.
24. Ruzo, A, Marcó, S, García, M, Villacampa, P, Ribera, A, Ayuso, E et al. (2012). Correction of pathological accumulation of glycosaminoglycans in central nervous system and peripheral tissues of MPSIIIA mice through systemic AAV9 gene transfer. Hum Gene Ther 23: 1237-1246.
25. Wu, YP and Proia, RL (2004). Deletion of macrophage-inflammatory protein 1 alpha retards neurodegeneration in Sandhoff disease mice. Proc Natl Acad Sci USA 101: 8425-8430.
26. Huang, JQ, Trasler, JM, Igdoura, S, Michaud, J, Hanal, N and Gravel, RA (1997). Apoptotic cell death in mouse models of GM2 gangliosidosis and observations on human Tay-Sachs and Sandhoff diseases. Hum Mol Genet 6: 1879-1885.
27. Wang, PR, Xu, M, Toffanin, S, Li, Y, Llovet, JM and Russell, DW (2012). Induction of hepatocellular carcinoma by in vivo gene targeting. Proc Natl Acad Sci USA 109: 11264-11269.
28. Katoh, M (2008). Cancer genomics and genetics of FGFR2 (Review). Int J Oncol 33: 233-237.
29. Moos, T and Møllgård, K (1993). Cerebrovascular permeability to azo dyes and plasma proteins in rodents of different ages. Neuropathol Appl Neurobiol 19: 120-127.
30. Daly, TM, Vogler, C, Levy, B, Haskins, ME and Sands, MS (1999). Neonatal gene transfer leads to widespread correction of pathology in a murine model of lysosomal storage disease. Proc Natl Acad Sci USA 96: 2296-2300.
31. Abo-Ouf, H, Hooper, AW, White, EJ, van Rensburg, HJ, Trigatti, BL and Igdoura, SA (2013). Deletion of tumor necrosis factor-a ameliorates neurodegeneration in Sandhoff disease mice. Hum Mol Genet 22: 3960-3975.
32. Donsante, A, Vogler, C, Muzyczka, N, Crawford, JM, Barker, J, Flotte, T et al. (2001). Observed incidence of tumorigenesis in long-term rodent studies of rAAV vectors. Gene Ther 8: 1343-1346.
33. Zhong, L, Malani, N, Li, M, Brady, T, Xie, J, Bell, P et al. (2013). Recombinant adeno-associated virus integration sites in murine liver after ornithine transcarbamylase gene correction. Hum Gene Ther 24: 520-525.
34. Bell, P, Moscioni, AD, McCarter, RJ, Wu, D, Gao, G, Hoang, A et al. (2006). Analysis of tumors arising in male B6C3F1 mice with and without AAV vector delivery to liver. Mol Ther 14: 34-44.
35. Donsante, A, Miller, DG, Li, Y, Vogler, C, Brunt, EM, Russell, DW et al. (2007). AAV vector integration sites in mouse hepatocellular carcinoma. Science 317: 477.
36. Li, H, Malani, N, Hamilton, SR, Schlachterman, A, Bussadori, G, Edmonson, SE et al. (2011). Assessing the potential for AAV vector genotoxicity in a murine model. Blood 117: 3311-3319.
37. Kao, CY, Yang, SJ, Tao, MH, Jeng, YM, Yu, IS and Lin, SW (2013). Incorporation of the factor IX Padua mutation into FIX-Triple improves clotting activity in vitro and in vivo. Thromb Haemost 110: 244-256.
38. Russell, DW (2007). AAV vectors, insertional mutagenesis, and cancer. Mol Ther 15: 1740-1743.
39. Sinici, I, Yonekawa, S, Tkachyova, I, Gray, SJ, Samulski, RJ, Wakarchuk, W et al. (2013). In cellulo examination of a beta-alpha hybrid construct of beta-hexosaminidase A subunits, reported to interact with the GM2 activator protein and hydrolyze GM2 ganglioside. PLoS ONE 8: e57908.
40. Bapat, B, Ethier, M, Neote, K, Mahuran, D and Gravel, RA (1988). Cloning and sequence analysis of a cDNA encoding the beta-subunit of mouse beta-hexosaminidase. FEBS Lett 237: 191-195.
41. Bello, A, Tran, K, Chand, A, Doria, M, Allocca, M, Hildinger, M et al. (2009). Isolation and evaluation of novel adeno-associated virus sequences from porcine tissues. Gene Ther 16: 1320-1328.
42. Kaback, MM, Shapiro, LJ, Hirsch, P and Roy, C (1977). Tay-Sachs disease heterozygote detection: a quality control study. Prog Clin Biol Res 18: 267-279.
43. Varshney, GK, Lu, J, Gildea, DE, Huang, H, Pei, W, Yang, Z et al. (2013). A large-scale zebrafish gene knockout resource for the genome-wide study of gene function. Genome Res 23: 727-735.
44. LaFave, MC, Varshney, GK, Gildea, DE, Wolfsberg, TG, Baxevanis, AD and Burgess, SM (2014). MLV integration site selection is driven by strong enhancers and active promoters. Nucleic Acids Res 42: 4257-4269.
45. Barnett, DW, Garrison, EK, Quinlan, AR, Strömberg, MP and Marth, GT (2011). BamTools: a C++ API and toolkit for analyzing and managing BAM files. Bioinformatics 27: 1691-1692.
46. Langmead, B, Trapnell, C, Pop, M and Salzberg, SL (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
47. Martin, M (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17: 10-12.
48. Quinlan, AR and Hall, IM (2010). BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842.
49. Flicek, P, Amode, MR, Barrell, D, Beal, K, Billis, K, Brent, S et al. (2014). Ensembl 2014. Nucleic Acids Res 42(Database issue): D749-D755.
50. Kinsella, RJ, Kähäri, A, Haider, S, Zamora, J, Proctor, G, Spudich, G et al. (2011). Ensembl BioMarts: a hub for data retrieval across taxonomic space. Database (Oxford) 2011: bar030.