Comparison of endovascular and intraventricular gene therapy with adeno-associated virus-α-L-iduronidase for hurler disease

Neurosurgery

Volumn 74, Issue 1, 2014, Pages 99-111

  Janson, Christopher G ^a,b   Romanova, Liudmila G ^a   Leone, Paola ^b   Nan, Zhenhong ^a   Belur, Lalitha ^a   Scott Mclvor, R ^a   Low, Walter ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

AAV; Blood brain barrier; Gene therapy; Hurler disease; Mannitol; Mucopolysaccharidosis

Indexed keywords

BRAIN ENZYME; GANGLIOSIDE GM3; GLYCOSAMINOGLYCAN; GREEN FLUORESCENT PROTEIN; LEVO IDURONIDASE; MANNITOL; PARVOVIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CELL INCLUSION; CONTROLLED STUDY; DISEASE MARKER; DRUG EFFICACY; ENDOVASCULAR GENE THERAPY; ENZYME ACTIVITY; EPENDYMA; GENE EXPRESSION; HEMISPHERE; HUMAN; HUMAN CELL; HURLER SYNDROME; IMMUNOHISTOCHEMISTRY; INTRAVENTRICULAR GENE THERAPY; MOUSE; NERVE CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE ASSAY; TRANSGENIC MOUSE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS PARTICLE; WILD TYPE;

ANIMALS; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; GENETIC THERAPY; GENETIC VECTORS; HUMANS; IDURONIDASE; INJECTIONS, INTRA-ARTERIAL; INJECTIONS, INTRAVENTRICULAR; MICE; MICE, TRANSGENIC; MUCOPOLYSACCHARIDOSIS I;

EID: 84891829278     PISSN: 0148396X     EISSN: None     Source Type: Journal    
DOI: 10.1227/NEU.0000000000000157     Document Type: Article

References (56)

1. Matalon R, Dorfman A. Hurler's syndrome, an alpha-L-iduronidase deficiency. Biochem Biophys Res Comm. 1972;47(4):959-964.
2. Bach G, Friedman R, Weissman B, Neufeld EF. The defect in Hurler and Scheie syndromes: deficiency of alpha-L-iduronidase. Proc Natl Acad Sci U S A. 1972;69 (8):2048-2051.
3. Clarke JTR. Hurler's disease. In: NORD Guide to Rare Disorders. Philadelphia, PA: Lippincott; 2003.
4. Staba SL, Escolar ML, Poe M, et al. Cord blood transplants from unrelated donors in patients with Hurler's syndrome. N Engl J Med. 2004;350(19):1960- 1969.
5. Unger ER, Sung JH, Manivel JC, et al. Male donor-derived cells in the brains of female sex-mismatched bone marrow transplant recipients: Y-chromosome specific in situ hybridization study. J Neuropath Exper Neurol. 1993;52(5):460-470.
6. Dekaban AS, Constantopoulos G. Mucopolysaccharidosis types I, IV, IIIA, V: pathological and biochemical abnormalities in the neural and mesenchymal elements of the brain. Acta Neuropath. 1977;39(1):1-7.
7. MacBrinn M, Okada S, Woollacott M, et al. Beta-galactosidase deficiency in the Hurler syndrome. N Engl J Med. 1969;281(7):338-343.
8. 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(4):415-426.
9. Love S, Louis D, Ellison D, eds. Greenfield's Neuropathology, 8th ed. London, UK: Hodder Arnold; 2008:544-547.
10. Traas AM, Wang P, Ma X, et al. Correction of clinical manifestations of canine mucopolysaccharidosis I with neonatal retroviral vector gene therapy. Mol Ther. 2007;15(8):1423-1431.
11. Janson CG, McPhee SW, Leone P, et al. Viral-based gene transfer to the mammalian CNS for functional genomic studies. Trends Neurosci. 2001;24(12):706-712.
12. Ohmi K, Greenberg DS, Rajavel KS, Ryazanysev S, Li HH, Neufeld EF. Activated microglia in cortex of mouse models of mucopolysaccharidoses I and IIIB. Proc Natl Acad Sci U S A. 2003;100(4):1902-1907.
13. Haskins ME, Aguirre GD, Jezyk PF, Desnick RJ, Patterson DF. The pathology of the feline model of mucopolysaccharidosis I. Am J Path. 1983;112(1):27-36.
14. Spellacy E, Shull RM, Constantopoulos G, Neufled EF. A canine model of human alpha-L-iduronidase deficiency. Proc Natl Acad Sci U S A. 1983;80(19):6091-6095.
15. Di Pasquale G, Davidson BL, Stein CS, et al. Identification of PDGFR as a receptor for AAV-5 transduction. Nat Med. 2003;9(10):1306-1312.
16. Boutin S, Monteilhet V, Veron P, et al. Prevalence of serum IgG and neutralizing factors against adeno-associated virus (AAV) types 1,2,5,6,8, and 9 in the healthy population: implications for gene therapy using AAV vectors. Hum Gene Ther. 2010;21(6):704-712.
17. Rapoport SI, Hori M, Klatzo I. Reversible osmotic opening of the blood-brain barrier. Science. 1971;173(4001):1026-1028.
18. Rapoport SI, Fredericks WR, Ohno K, Pettigrew KD. Quantitative aspects of reversible osmotic opening of the blood-brain barrier. Am J Physiol. 1980;238(5): R421-R431.
19. Neuwelt EA, Frenkel EP, Diehl J, Vu LH, Rapoport S, Hill S. Reversible osmotic blood-brain barrier disruption in humans: implications for the chemotherapy of malignant brain tumors. Neurosurgery. 1980;7(1):44-52.
20. Doran SE, Ren XD, Betz AL, et al. Gene expression from recombinant viral vectors in the central nervous system after blood-brain barrier disruption. Neurosurgery. 1995;36(5):965-970.
21. Nilaver G, Muldoon LL, Kroll RA, et al. Delivery of herpesvirus and adenovirus to nude rat intracerebral tumors after osmotic blood-brain barrier disruption. Proc Natl Acad Sci U S A. 1995;92(21):9829-9833.
22. Muldoon LL, Nilaver G, Kroll RA, et al. Comparison of intracerebral inoculation and osmotic blood-brain barrier disruption for delivery of adenovirus, herpesvirus, and iron oxide particles to the brain. Am J Path. 1995;147(6):1840-1851.
23. Liu R, Martuza RL, Rabkin SD. Intracarotid delivery of oncolytic HSV vector G47Delta to metastatic breast cancer in the brain. Gene Ther. 2005;12(8):647-654.
24. Leone P, Janson CG, Bilaniuk L, et al. Aspartoacylase gene transfer to the mammalian central nervous system with therapeutic implications for Canavan disease. Ann Neurol. 2000;48(1):27-38.
25. Ghodsi A, Stein C, Derksen T, Martins I, Anderson RD, Davidson BL. Systemic hyperosmolality improves beta-glucuronidase distribution and pathology in murine MPS VII brain following intraventricular gene transfer. Exp Neurol. 1999;160(1):109-116.
26. Burger C, Nguyen FN, Deng J, Mandel RJ. Systemic mannitol-induced hyperosmolality amplifies rAAV2-mediated striatal transduction to a greater extent than local co-infusion. Mol Ther. 2005;11(2):327-331.
27. Janson C, McPhee S, Bilaniuk L, et al. Clinical protocol: gene therapy of Canavan disease: AAV2 vector for neurosurgical delivery of aspartoacylase gene (ASPA) to the human brain. Hum Gene Ther. 2002;13(11):1391-1412.
28. Leone P, Shera D, McPhee SW, et al. Long-term follow-up of gene therapy for Canavan disease. Sci Transl Med. 2012;4(165):165ra163.
29. Davidson BL, Stein CS, Heth JA, et al. 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 U S A. 2000;97(7):3428-3432.
30. Scott HS, Anson DS, Orsborn A M, et al. Human alpha-L-iduronidase: cDNA isolation and expression. Proc Natl Acad Sci U S A. 1991;88(21):9695-9699.
31. Hartung SD, Frandsen JL, Pan D, et al. Correction of metabolic, craniofacial, and neurologic abnormalities in MPS I mice treated at birth with adeno-associated virus vector transducing the human alpha-L-iduronidase gene. Mol Ther. 2004;9(6):866-875.
32. Garcia-Rivera MF, Colvin-Wanshura LE, Nelson MS, et al. Characterization of an immunodeficient mouse model of mucopolysaccharidosis type I suitable for preclinical testing of human stem cell and gene therapy. Brain Res Bull. 2007;74 (6):429-438.
33. Hopwood JJ, Muller V, Smithson A, Baggett N. A fluorometric assay using 4-methyl-umbelliferyl alpha-L-iduronide for the estimation of alpha-L-iduronidase activity and the detection of Hurler and Scheie syndromes. Clinca Chim Acta. 1979; 92:257-265.
34. McCarty DM, Monahan PE, Samulski RJ. Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther. 2001;8(16):1248-1254.
35. McCarty DM, Fu H, Monahan PE, Toulson CE, Naik P, Samulski RJ. Adenoassociated virus terminal repeat (TR) mutant generates self-complementary vectors to overcome the rate-limiting step to transduction in vivo. Gene Therapy. 2003;10 (26):2112-2118.
36. Fu H, Muenzer J, Samulski RJ, et al. Self-complementary adeno-associated virus serotype 2 vector: global distribution and broad dispersion of AAV-mediated transgene expression in mouse brain. Mol Ther. 2003;8(6):911-917.
37. McCarty DM, DiRosario J, Gulaid K, Muenzer J, Fu H. Mannitol-facilitated CNS entry of rAAV2 vector significantly delayed the neurological disease progression in MPS-IIIB mice. Gene Ther. 2009;16(11):1340-1352.
38. Zhang H, Yang B, Mu X, et al. Several rAAV vectors efficiently cross the bloodbrain barrier and transduce neurons and astrocytes in the neonatal mouse central nervous system. Mol Ther. 2011;19(8)1440-1448.
39. Foust KD, Nurre E, Montgomery CL, Hernandez A, Chan CM, Kaspar BK. Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol. 2009;27(1):59-65.
40. Foust KD, Wang X, McGovern VL, et al. Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat Biotechnol. 2011;28(3):271-276.
41. Chen YH, Chang M, Davidson BL. Molecular signatures of disease brain endothelia provide new sites for CNS-directed enzyme therapy. Nat Med. 2009;15 (10):1215-1219.
42. Dalkara D, Byrne LC, Lee T, et al. Enhanced gene delivery to the neonatal retina through systemic administration of tyrosine-mutated AAV9. Gene Ther. 2012;19 (2):176-181.
43. Fu H, Dirosario J, Killedar S, Zaraspe K, McCarty DM. Correction of neurological disease of MPSIIIB in adult mice by rAAV9 trans-blood-brain barrier gene delivery. Mol Ther. 2011;19(6):1025-1033.
44. Gray SJ, Matagne V, Bachaboina L, Yadav S, Ojeda SR, Samulski SJ. Preclinical differences of intravascular AAV9 delivery to neurons and glia: a comparative study of adult mice and nonhuman primates. Mol Ther. 2011;19(6):1058-1069.
45. Burger C, Gorbatyuk OS, Velardo MJ, et al. Recombinant AAV viral Vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol Ther. 2004;10(12):302-317.
46. Watson G, Bastacky J, Belichenko P, et al. Intrathecal administration of AAV vectors for the treatment of lysosomal storage in the brains of MPS I mice. Gene Ther. 2006;13(11):917-925.
47. Desmaris N, Verot L, Puech JP, Caillaud C, Vanier MT, Heard JM. Prevention of neuropathology in themouse model of Hurler syndrome. Ann Neurol. 2004;56(1):68-76.
48. Ciron C, Desmaris N, Colle MA, et al. Gene therapy of the brain in the dog model of Hurler's syndrome. Ann Neurol. 2006;60(2):204-213.
49. Saunders NR, Joakim EK C, Dziegielewska KM. The neonatal blood-brain barrier is functionally effective, and immaturity does not explain differential targeting of AAV9. Nat Biotechnol. 2009;27(9):804.
50. Samaranch L, Salegio EA, San Sebastian W, et al. Adeno-associated virus serotype 9 transduction in the central nervous system of nonhuman primates. Hum Gene Ther. 2012 23(4):382-389.
51. Gray SJ, Nagabhushan Kalburgi S, McGown TJ, Jude Samulski R. Global CNS gene delivery and evasion of anti-AAV neutralizing antibodies by intrathecal AAV administration in non-human primates. Gene Ther. 2013;20(4):450-459.
52. Bevan AK, Duque S, Foust KD, et al. Systemic gene delivery in large species for targeting spinal cord, brain, and peripheral tissues for pediatric disorders. Mol Ther. 2011;19(11):1971-1980.
53. Hartung SD, Reddy RG, Whitley CB, McIvor R S. Enzymatic correction and cross-correction of mucopolysaccharidosis type I fibroblasts by adeno-associated virus-mediated transduction of the alpha-L-iduronidase gene. Hum Gene Ther. 1999;10(13):2163-2172.
54. Scott HS, Litjens T, Nelson PV, et al. Identification of mutations in the alpha-Liduronidase (IDUA) gene that cause Hurler and Scheie syndromes. Am J Hum Genet. 1993;53(5):973-986.
55. Wolf DA, Lenander AW, Nan Z, et al. Direct gene transfer to the CNS prevents emergence of neurologic disease in a murine model of mucopolysaccharidosis type I. Neurobiol Dis. 2011;43(1):123-133.
56. US Department of Health & Human Services, Office of Biotechnology Activities (OBA). Documents Interest: RAC Protoc List. 2012.