A preclinical study evaluating AAVrh10-based gene therapy for sanfilippo syndrome

Human Gene Therapy

Volumn 27, Issue 5, 2016, Pages 363-375

  Winner, Leanne K ^a   Beard, Helen ^a   Hassiotis, Sofia ^a   Lau, Adeline A ^a   Luck, Amanda J ^a   Hopwood, John J ^a   Hemsley, Kim M ^a  

^a SOUTH AUSTRALIAN HEALTH AND MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GANGLIOSIDE GM3; HEPARAN SULFATE; N SULFOGLUCOSAMINE SULFOHYDROLASE; PARVOVIRUS VECTOR; RECOMBINANT ENZYME; RECOMBINANT N SULFOGLUCOSAMINE SULFOHYDROLASE; UBIQUITIN; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; DNA BINDING PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; HIGH MOBILITY GROUP PROTEIN; HYDROLASE; IXR1 PROTEIN, S CEREVISIAE; N-SULFOGLUCOSAMINE SULFOHYDROLASE; NEUTRALIZING ANTIBODY; SACCHAROMYCES CEREVISIAE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRAIN REGION; CATABOLISM; CELL INCLUSION; CONTROLLED STUDY; EVALUATION STUDY; FEMALE; GENE; GENE VECTOR; HEMISPHERE; IMMUNOHISTOCHEMISTRY; IRES GENE; MALE; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; SANFILIPPO SYNDROME; SGSH GENE; SUMF1 GENE; VIRAL GENE THERAPY; ADMINISTRATION AND DOSAGE; ANIMAL; AUTOPHAGY; BRAIN; CLASSIFICATION; DEPENDOPARVOVIRUS; DISEASE MODEL; ENDOSOME; ENZYME ACTIVATION; GENE THERAPY; GENETIC TRANSDUCTION; GENETICS; HUMAN; IMMUNOLOGY; LYSOSOME; METABOLISM; PROCEDURES; STANDARDS;

ANIMALS; ANTIBODIES, NEUTRALIZING; AUTOPHAGY; BIOMARKERS; BRAIN; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; ENDOSOMES; ENZYME ACTIVATION; FEMALE; G(M3) GANGLIOSIDE; GENETIC THERAPY; GENETIC VECTORS; GLIAL FIBRILLARY ACIDIC PROTEIN; HEPARITIN SULFATE; HIGH MOBILITY GROUP PROTEINS; HUMANS; HYDROLASES; LYSOSOMES; MALE; MICE; MUCOPOLYSACCHARIDOSIS III; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSDUCTION, GENETIC;

EID: 84964790995     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2015.170     Document Type: Article

References (51)

1. Meikle PJ, Hopwood JJ, Clague AE, et al. Prevalence of lysosomal storage disorders. JAMA. 1999; 281: 249-254.
2. Neufeld EF, Muenzer J. The mucopolysaccharidoses. In: The Metabolic and Molecular Bases of Inherited Diseases. CR Scriver, ed. (McGraw-Hill, New York, NY). 2001; pp. 3421-3452.
3. Valstar MJ, Neijs S, Bruggenwirth HT, et al. Mucopolysaccharidosis type IIIA: Clinical spectrum and genotype-phenotype correlations. Ann Neurol. 2010; 68: 876-887.
4. Boelens JJ, Prasad VK, Tolar J, et al. Current international perspectives on hematopoietic stem cell transplantation for inherited metabolic disorders. Pediatr Clin North Am. 2010; 57: 123-145.
5. Sivakumur P, Wraith JE. Bone marrow transplantation in mucopolysaccharidosis type IIIA: A comparison of an early treated patient with his untreated sibling. J Inherit Metab Dis. 1999; 22: 849-850.
6. Lau AA, Hannouche H, Rozaklis T, et al. Allogeneic stem cell transplantation does not improve neurological deficits in mucopolysaccharidosis type IIIA mice. Exp Neurol. 2010; 225: 445-454.
7. Brady RO, Pentchev PG, Gal AE, et al. Replacement therapy for inherited enzyme deficiency. Use of purified glucocerebrosidase in Gaucher;s disease. N Engl J Med. 1974; 291: 989-993.
8. Schiffmann R, Murray GJ, Treco D, et al. Infusion of alpha-galactosidase A reduces tissue globotriaosylceramide storage in patients with Fabry disease. Proc Natl Acad Sci USA. 2000; 97: 365-370.
9. Harmatz P, Whitley CB, Waber L, et al. Enzyme replacement therapy in mucopolysaccharidosis VI (Maroteaux-Lamy syndrome). J Pediatr. 2004; 144: 574-580.
10. Sondhi D, Johnson L, Purpura K, et al. Long-Term expression and safety of administration of AAVrh.10hCLN2 to the brain of rats and nonhuman primates for the treatment of late infantile neuronal ceroid lipofuscinosis. Hum Gene Ther Methods. 2012; 23: 324-335.
11. Worgall S, Sondhi D, Hackett NR, et al. Treatment of late infantile neuronal ceroid lipofuscinosis by CNS administration of a serotype 2 adenoassociated virus expressing CLN2 cDNA. Hum Gene Ther. 2008; 19: 463-474.
12. Crawley AC, Gliddon BL, Auclair D, et al. Characterization of a C57BL/6 congenic mouse strain of mucopolysaccharidosis type IIIA. Brain Res. 2006; 1104: 1-17.
13. Cosma MP, Pepe S, Annunziata I, et al. The multiple sulfatase deficiency gene encodes an essential and limiting factor for the activity of sulfatases. Cell. 2003; 113: 445-456.
14. Fraldi A, Hemsley KM, Crawley A, et al. Functional correction of CNS lesions in a MPS-IIIA mouse model by intracerebral AAV-mediated delivery of sulfamidase and SUMF1 genes. Hum Mol Genet. 2007; 16: 2693-2702.
15. Cressant A, Desmaris N, Verot L, et al. Improved behavior and neuropathology in the mouse model of Sanfilippo type IIIB disease after adenoassociated virus-mediated gene transfer in the striatum. J Neurosci. 2004; 24: 10229-10239.
16. Passini MA, Watson DJ, Vite CH, et al. 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 beta-glucuronidasedeficient mice. J Virol. 2003; 77: 7034-7040.
17. Bartlett JS, Samulski RJ, McCown TJ. Selective and rapid uptake of adeno-Associated virus type 2 in brain. Hum Gene Ther. 1998; 9: 1181-1186.
18. Cearley CN, Wolfe JH. Transduction characteristics of adeno-Associated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain. Mol Ther. 2006; 13: 528-537.
19. Weinberg MS, Blake BL, Samulski RJ, et al. The influence of epileptic neuropathology and prior peripheral immunity on CNS transduction by rAAV2 and rAAV5. Gene Ther. 2011; 18: 961-968.
20. Cearley CN, Wolfe JH. A single injection of an adenoassociated virus vector into nuclei with divergent connections results in widespread vector distribution in the brain and global correction of a neurogenetic disease. J Neurosci. 2007; 27: 9928-9940.
21. Redgrave P, Rodriguez M, Smith Y, et al. Goaldirected and habitual control in the basal ganglia: Implications for Parkinson;s disease. Nat Rev Neurosci. 2010; 11: 760-772.
22. Sesack SR, Grace AA. Cortico-basal ganglia reward network: Microcircuitry. Neuropsychopharmacology. 2010; 35: 27-47.
23. Pan WX, Mao T, Dudman JT. Inputs to the dorsal striatum of the mouse reflect the parallel circuit architecture of the forebrain. Front Neuroanat. 2010; 4: 147.
24. Sondhi D, Hackett NR, Peterson DA, et al. Enhanced survival of the LINCL mouse following CLN2 gene transfer using the rh.10 rhesus macaque-derived adeno-Associated virus vector. Mol Ther. 2007; 15: 481-491.
25. Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates. 2nd edition. (Academic Press, San Diego, CA), 2001.
26. Lau AA, Hopwood JJ, Kremer EJ, et al. SGSH gene transfer in mucopolysaccharidosis type IIIA mice using canine adenovirus vectors. Mol Genet Metab. 2010; 100: 168-175.
27. Hopwood JJ, Elliott H. Diagnosis of Sanfilippo A syndrome by estimation of sulfamidase activity using a radiolabelled tetrasaccharide substrate. Clin Chim Acta. 1982; 123: 241-250.
28. Hemsley KM, Luck AJ, Crawley AC, et al. Examination of intravenous and intra-CSF protein delivery for treatment of neurological disease. Eur J Neurosci. 2009; 29: 1197-1214.
29. Hemsley KM, Beard H, King BM, et al. Effect of high dose, repeated intra-CSF injection of sulphamidase on neuropathology in MPS IIIA mice. Genes Brain Behav. 2008; 7: 740-753.
30. McGlynn R, Dobrenis K, Walkley SU. Differential subcellular localization of cholesterol, gangliosides, and glycosaminoglycans in murine models of mucopolysaccharide storage disorders. J Comp Neurol. 2004; 480: 415-426.
31. Hemsley KM, King B, Hopwood JJ. Injection of recombinant human sulfamidase into the CSF via the cerebellomedullary cistern in MPS IIIA mice. Mol Genet Metab. 2007; 90: 313-328.
32. Savas PS, Hemsley KM, Hopwood JJ. Intracerebral injection of sulfamidase delays neuropathology in murineMPS-IIIA.Mol GenetMetab. 2004; 82: 273-285.
33. Komatsu M, Ichimura Y. Physiological significance of selective degradation of p62 by autophagy. FEBS Lett. 2010; 584: 1374-1378.
34. Clancy B, Darlington RB, Finlay BL. Translating developmental time across mammalian species. Neuroscience. 2001; 105: 7-17.
35. Rafi MA, Rao HZ, Luzi P, et al. Extended normal life after AAVrh10-mediated gene therapy in the mouse model of Krabbe disease. Mol Ther. 2012; 20: 2031-2042.
36. Sondhi D, Peterson DA, Edelstein AM, et al. Survival advantage of neonatal CNS gene transfer for late infantile neuronal ceroid lipofuscinosis. Exp Neurol. 2008; 213: 18-27.
37. Carty N, Lee D, Dickey C, et al. Convectionenhanced delivery and systemic mannitol increase gene product distribution of AAV vectors 5, 8, and 9 and increase gene product in the adult mouse brain. J Neurosci Methods. 2010; 194: 144-153.
38. Valles F, Fiandaca MS, Eberling JL, et al. Qualitative imaging of adeno-Associated virus serotype 2-human aromatic L-Amino acid decarboxylase gene therapy in a phase I study for the treatment of Parkinson disease. Neurosurgery. 2010; 67: 1377-1385.
39. Van der Perren A, Toelen J, Carlon M, et al. Efficient and stable transduction of dopaminergic neurons in rat substantia nigra by rAAV 2/1, 2/2, 2/5, 2/6.2, 2/.7, 2/8 and 2/9. Gene Ther. 2011; 18: 517-527.
40. Taymans JM, Vandenberghe LH, Haute CV, et al. Comparative analysis of adeno-Associated viral vector serotypes 1, 2, 5, 7, and 8 in mouse brain. Hum Gene Ther. 2007; 18: 195-206.
41. Salegio EA, Kells AP, Richardson RM, et al. Magnetic resonance imaging-guided delivery of adeno-Associated virus type 2 to the primate brain for the treatment of lysosomal storage disorders. Hum Gene Ther. 2010; 21: 1093-1103.
42. Vite CH, McGowan JC, Niogi SN, et al. Effective gene therapy for an inherited CNS disease in a large animal model. Ann Neurol. 2005; 57: 355-364.
43. McIntyre C, Byers S, Anson DS. Correction of mucopolysaccharidosis type IIIA somatic and central nervous system pathology by lentiviral-mediated gene transfer. J Gene Med. 2010; 12: 717-728.
44. Fu H, DiRosario J, Killedar S, et al. Correction of neurological disease of mucopolysaccharidosis IIIB in adult mice by rAAV9 trans-blood-brain barrier gene delivery. Mol Ther. 2011; 19: 1025-1033.
45. Ruzo A, Marcó S, García M, et al. Correction of pathological accumulation of glycosaminoglycans in central nervous system and peripheral tissues of MPSIIIA mice through systemic AAV9 gene transfer. Hum Gene Ther. 2012; 23: 1237-1246.
46. Haurigot V, Marcó S, Ribera A, et al. Whole body correction of mucopolysaccharidosis IIIA by intracerebrospinal fluid gene therapy. J Clin Invest. 2013; doi: 10.1172/JCI66778.
47. Donsante A, Miller DG, Li Y, et al. AAV vector integration sites in mouse hepatocellular carcinoma. Science. 2007; 317: 477.
48. Ruzo A, Garcia M, Ribera A, et al. Liver production of sulfamidase reverses peripheral and ameliorates CNS pathology in mucopolysaccharidosis IIIA mice. Mol Ther. 2012; 20: 254-266.
49. Sorrentino NC, D;Orsi L, Sambri I, et al. A highly secreted sulphamidase engineered to cross the blood-brain barrier corrects brain lesions of mice with mucopolysaccharidoses type IIIA. EMBO Mol Med. 2013; 5: 675-690.
50. Ellinwood NM, Ausseil J, Desmaris N, et al. Safe, efficient, and reproducible gene therapy of the brain in the dog models of Sanfilippo and Hurler syndromes. Mol Ther. 2011; 19: 251-259.
51. Tardieu M, Zérah M, Husson B, et al. Intracerebral administration of adeno-Associated viral vector serotype rh.10 carrying human SGSH and SUMF1 cDNAs in children with mucopolysaccharidosis type IIIA disease: Results of a phase I/II trial. Hum Gene Ther. 2014; 25: 506-516.