CNS-directed gene therapy for the treatment of neurologic and somatic mucopolysaccharidosis type II (Hunter syndrome)

JCI Insight

Volumn 1, Issue 9, 2016, Pages

  Motas, Sandra ^a   Haurigot, Virginia ^a,b   Garcia, Miguel ^a,b   Marcó, Sara ^a   Ribera, Albert ^a,b   Roca, Carles ^a,b   Sánchez, Xavier ^a   Sánchez, Víctor ^a   Molas, Maria ^a,b   Bertolin, Joan ^a   Maggioni, Luca ^a,b   León, Xavier ^a,b   Ruberte, Jesús ^a,b   Bosch, Fatima ^a,b  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85055607758     PISSN: None     EISSN: 23793708     Source Type: Journal    
DOI: 10.1172/jci.insight.86696     Document Type: Article

References (86)

1. Neufeld EF, Muenzer J. The mucopolysaccharidoses. In: Scriver CR, et al., eds. The Metabolic and Molecular Basis of Inherited Disease. New York, New York, USA: McGraw-Hill, Medical Publishing Division; 2001:3421–3454.
2. Wraith JE, et al. Mucopolysaccharidosis type II (Hunter syndrome): a clinical review and recommendations for treatment in the era of enzyme replacement therapy. Eur J Pediatr. 2008;167(3):267–277.
3. Muenzer J. Overview of the mucopolysaccharidoses. Rheumatology (Oxford). 2011;50(suppl 5):v4–v12.
4. Okuyama T, et al. Japan Elaprase Treatment (JET) study: idursulfase enzyme replacement therapy in adult patients with attenuated Hunter syndrome (Mucopolysaccharidosis II, MPS II). Mol Genet Metab. 2010;99(1):18–25.
5. Yamada Y, et al. Mucopolysaccharidosis type II (Hunter disease): 13 gene mutations in 52 Japanese patients and carrier detection in four families. Hum Genet. 1993;92(2):110–114.
6. Schwartz IV, et al. A clinical study of 77 patients with mucopolysaccharidosis type II. Acta Paediatr. 2007;96(455):63–70.
7. Martin R, et al. Recognition and diagnosis of mucopolysaccharidosis II (Hunter syndrome). Pediatrics. 2008;121(2):e377–e386.
8. Al Sawaf S, Mayatepek E, Hoffmann B. Neurological findings in Hunter disease: pathology and possible therapeutic effects reviewed. J Inherit Metab Dis. 2008;31(4):473–480.
9. Enns GM, Huhn SL. Central nervous system therapy for lysosomal storage disorders. Neurosurg. 2008;24(3–4):E12.
10. Yamada Y, et al. Treatment of MPS VII (Sly disease) by allogeneic BMT in a female with homozygous A619V mutation. Bone Marrow Transplant. 1998;21(6):629–634.
11. Peters C1, Steward CG; National Marrow Donor Program; International Bone Marrow Transplant Registry, Working Party on Inborn Errors, European Bone Marrow Transplant Group. Hematopoietic cell transplantation for inherited metabolic diseases: an overview of outcomes and practice guidelines. Bone Marrow Transplant. 2003;31(4):229–239.
12. Peters C, et al. Outcome of unrelated donor bone marrow transplantation in 40 children with Hurler syndrome. Blood. 1996;87(11):4894–4902.
13. Podetz-Pedersen KM, et al. The American Society of Gene & Cell Therapy Abstracts from the 16th Annual Meeting, Salt Lake City, Utha: “Prevention of Neurocognitive Deficit by Ex Vivo Lentiviral Transduction of Hematopoietic Stem Cells in a Murine Model of Mucop. Mol Ther. 2013;21(supplement 1):S191.
14. Prasad VK, Kurtzberg J. Transplant outcomes in mucopolysaccharidoses. Semin Hematol. 2010;47(1):59–69.
15. Seto T, et al. Brain magnetic resonance imaging in 23 patients with mucopolysaccharidoses and the effect of bone marrow transplantation. Ann Neurol. 2001;50(1):79–92.
16. Vellodi A, Young E, Cooper A, Lidchi V, Winchester B, Wraith JE. Long-term follow-up following bone marrow transplantation for Hunter disease. J Inherit Metab Dis. 1999;22(5):638–648.
17. Giugliani R, et al. Mucopolysaccharidosis I, II, and VI: Brief review and guidelines for treatment. Genet Mol Biol. 2010;33(4):589–604.
18. Valayannopoulos V, Wijburg FA. Therapy for the mucopolysaccharidoses. Rheumatology (Oxford). 2011;50(suppl 5):v49–v59.
19. Muenzer J, et al. Long-term, open-labeled extension study of idursulfase in the treatment of Hunter syndrome. Genet Med. 2011;13(2):95–101.
20. Muenzer J, et al. A phase II/III clinical study of enzyme replacement therapy with idursulfase in mucopolysaccharidosis II (Hunter syndrome). Genet Med. 2006;8(8):465–473.
21. Muenzer J, Gucsavas-Calikoglu M, McCandless SE, Schuetz TJ, Kimura A. A phase I/II clinical trial of enzyme replacement therapy in mucopolysaccharidosis II (Hunter syndrome). Mol Genet Metab. 2007;90(3):329–337.
22. Muenzer J, et al. A phase I/II study of intrathecal idursulfase-IT in children with severe mucopolysaccharidosis II. Genet Med. 2016;18(1):73–81.
23. Bainbridge JW, et al. Effect of gene therapy on visual function in Leber’s congenital amaurosis. N Engl J Med. 2008;358(21):2231–2239.
24. Rivera VM, et al. Long-term pharmacologically regulated expression of erythropoietin in primates following AAV-mediated gene transfer. Blood. 2005;105(4):1424–1430.
25. Hauswirth WW, et al. Treatment of leber congenital amaurosis due to RPE65 mutations by ocular subretinal injection of adeno-associated virus gene vector: short-term results of a phase I trial. Hum Gene Ther. 2008;19(10):979–990.
26. Maguire AM, et al. Safety and efficacy of gene transfer for Leber’s congenital amaurosis. N Engl J Med. 2008;358(21):2240–2248.
27. Niemeyer GP, et al. Long-term correction of inhibitor-prone hemophilia B dogs treated with liver-directed AAV2-mediated factor IX gene therapy. Blood. 2009;113(4):797–806.
28. Nathwani AC, et al. Long-term safety and efficacy of factor IX gene therapy in hemophilia B. N Engl J Med. 2014;371(21):1994–2004.
29. Wolf DA, Banerjee S, Hackett PB, Whitley CB, McIvor RS, Low WC. Gene therapy for neurologic manifestations of mucopolysaccharidoses. Expert Opin Drug Deliv. 2015;12(2):283–296.
30. Lisowski L, Tay SS, Alexander IE. Adeno-associated virus serotypes for gene therapeutics. Curr Opin Pharmacol. 2015;24:59–67.
31. Callejas D, et al. Treatment of diabetes and long-term survival after insulin and glucokinase gene therapy. Diabetes. 2013;62(5):1718–1729.
32. Bainbridge JW, et al. Long-term effect of gene therapy on Leber’s congenital amaurosis. N Engl J Med. 2015;372(20):1887–1897.
33. Testa F, et al. Three-year follow-up after unilateral subretinal delivery of adeno-associated virus in patients with Leber congenital Amaurosis type 2. Ophthalmology. 2013;120(6):1283–1291.
34. Gaudet D, et al. Efficacy and long-term safety of alipogene tiparvovec (AAV1-LPLS447X) gene therapy for lipoprotein lipase deficiency: an open-label trial. Gene Ther. 2013;20(4):361–369.
35. Jacobson SG, et al. Gene therapy for leber congenital amaurosis caused by RPE65 mutations: safety and efficacy in 15 children and adults followed up to 3 years. Arch Ophthalmol. 2012;130(1):9–24.
36. Buchlis G, et al. Factor IX expression in skeletal muscle of a severe hemophilia B patient 10 years after AAV-mediated gene transfer. Blood. 2012;119(13):3038–3041.
37. Simonelli F, et al. Gene therapy for Leber’s congenital amaurosis is safe and effective through 1.5 years after vector administration. Mol Ther. 2010;18(3):643–650.
38. Haurigot V, et al. Whole body correction of mucopolysaccharidosis IIIA by intracerebrospinal fluid gene therapy. J Clin Invest. 2013;123(8):3254–3271.
39. Gray SJ, Nagabhushan Kalburgi S, McCown 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.
40. Ribera A, et al. Biochemical, histological and functional correction of mucopolysaccharidosis type IIIB by intra-cerebrospinal fluid gene therapy. Hum Mol Genet. 2015;24(7):2078–2095.
41. Hinderer C, et al. Neonatal systemic AAV induces tolerance to CNS gene therapy in MPS I dogs and nonhuman primates. Mol Ther. 2015;23(8):1298–1307.
42. Samaranch L, et al. Adeno-associated virus serotype 9 transduction in the central nervous system of nonhuman primates. Hum Gene Ther. 2012;23(4):382–389.
43. Higuchi T, et al. Enzyme replacement therapy (ERT) procedure for mucopolysaccharidosis type II (MPS II) by intraventricular administration (IVA) in murine MPS II. Mol Genet Metab. 2012;107(1–2):122–128.
44. Sardiello M, et al. A gene network regulating lysosomal biogenesis and function. Science. 2009;325(5939):473–477.
45. Tomatsu S, et al. Keratan sulphate levels in mucopolysaccharidoses and mucolipidoses. J Inherit Metab Dis. 2005;28(2):187–202.
46. Rowan DJ, Tomatsu S, Grubb JH, Montaño AM, Sly WS. Assessment of bone dysplasia by micro-CT and glycosaminoglycan levels in mouse models for mucopolysaccharidosis type I, IIIA, IVA, and VII. J Inherit Metab Dis. 2013;36(2):235–246.
47. Hamano K, Hayashi M, Shioda K, Fukatsu R, Mizutani S. Mechanisms of neurodegeneration in mucopolysaccharidoses II and IIIB: analysis of human brain tissue. Acta Neuropathol. 2008;115(5):547–559.
48. Constantopoulos G, Iqbal K, Dekaban AS. Mucopolysaccharidosis types IH, IS, II, and IIIA: glycosaminoglycans and lipids of isolated brain cells and other fractions from autopsied tissues. J Neurochem. 1980;34(6):1399–1411.
49. Eng LF, Ghirnikar RS. GFAP and astrogliosis. Brain Pathol. 1994;4(3):229–237.
50. Streit WJ, Kreutzberg GW. Lectin binding by resting and reactive microglia. J Neurocytol. 1987;16(2):249–260.
51. Hunter C. A rare disease in two brothers. Proc R Soc Med. 1917;10(Sect study dis child):104–116.
52. Ruzo A, 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(12):1237–1246.
53. Ohmi K, Greenberg DS, Rajavel KS, Ryazantsev 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.
54. Ruzo A, et al. Liver production of sulfamidase reverses peripheral and ameliorates CNS pathology in mucopolysaccharidosis IIIA mice. Mol Ther. 2012;20(2):254–266.
55. Fraldi A, et al. Functional correction of CNS lesions in an MPS-IIIA mouse model by intracerebral AAV-mediated delivery of sulfamidase and SUMF1 genes. Hum Mol Genet. 2007;16(22):2693–2702.
56. DiRosario J, et al. Innate and adaptive immune activation in the brain of MPS IIIB mouse model. J Neurosci Res. 2009;87(4):978–990.
57. Archer LD, Langford-Smith KJ, Bigger BW, Fildes JE. Mucopolysaccharide diseases: a complex interplay between neuroinflammation, microglial activation and adaptive immunity. J Inherit Metab Dis. 2014;37(1):1–12.
58. Resnick JM, Whitley CB, Leonard AS, Krivit W, Snover DC. Light and electron microscopic features of the liver in mucopolysaccharidosis. Hum Pathol. 1994;25(3):276–286.
59. Bailey K, Crawley J. Anxiety-related behaviors in mice. In: Buccafusco JJ, ed. Methods of Behavior Analysis in Neuroscience. 2nd ed. Boca Raton, Florida, USA: CRC Press/Taylor & Francis; 2009:Chapter 5.
60. Polito VA, Cosma MP. IDS crossing of the blood-brain barrier corrects CNS defects in MPSII mice. Am J Hum Genet. 2009;85(2):296–301.
61. Cardone M, et al. Correction of Hunter syndrome in the MPSII mouse model by AAV2/8-mediated gene delivery. Hum Mol Genet. 2006;15(7):1225–1236.
62. Vogler C, et al. Overcoming the blood-brain barrier with high-dose enzyme replacement therapy in murine mucopolysaccharidosis VII. Proc Natl Acad Sci U S A. 2005;102(41):14777–14782.
63. Ou L, Herzog T, Koniar BL, Gunther R, Whitley CB. High-dose enzyme replacement therapy in murine Hurler syndrome. Mol Genet Metab. 2014;111(2):116–122.
64. Wu Z, Asokan A, Samulski RJ. Adeno-associated virus serotypes: vector toolkit for human gene therapy. MolTher. 2006;14(3):316–327.
65. Xia W, et al. High levels of protein expression using different mammalian CMV promoters in several cell lines. Protein Expr Purif. 2006;45(1):115–124.
66. Manno CS, et al. Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat Med. 2006;12(3):342–347.
67. Settembre C, Fraldi A, Medina DL, Ballabio A. Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat Rev Mol Cell Biol. 2013;14(5):283–296.
68. Richard M, Arfi A, Rhinn H, Gandolphe C, Scherman D. Identification of new markers for neurodegeneration process in the mouse model of Sly disease as revealed by expression profiling of selected genes. J Neurosci Res. 2008;86(15):3285–3294.
69. Baldo G, et al. Shotgun proteomics reveals possible mechanisms for cognitive impairment in Mucopolysaccharidosis I mice. Mol Genet Metab. 2015;114(2):138–145.
70. Fu H, Bartz JD, Stephens RL, McCarty DM. Peripheral nervous system neuropathology and progressive sensory impairments in a mouse model of Mucopolysaccharidosis IIIB. PLoS One. 2012;7(9):e45992.
71. Walkley SU. Pathogenic mechanisms in lysosomal disease: a reappraisal of the role of the lysosome. Acta Paediatr. 2007;96(455):26–32.
72. McGeer PL, McGeer EG. Glial cell reactions in neurodegenerative diseases: pathophysiology and therapeutic interventions. Alzheimer Dis Assoc Disord. 1998;12(suppl 2):S1–S6.
73. Gurda BL, et al. Evaluation of AAV-mediated gene therapy for central nervous system disease in canine Mucopolysaccharidosis VII. MolTher. 2016;24(2):206–216.
74. Snyder BR, et al. Comparison of adeno-associated viral vector serotypes for spinal cord and motor neuron gene delivery. Hum Gene Ther. 2011;22(9):1129–1135.
75. 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.
76. Bevan AK, et al. Systemic gene delivery in large species for targeting spinal cord, brain, and peripheral tissues for pediatric disorders. MolTher. 2011;19(11):1971–1980.
77. Bucher T, et al. Intracisternal delivery of AAV9 results in oligodendrocyte and motor neuron transduction in the whole central nervous system of cats. Gene Ther. 2014;21(5):522–528.
78. Jackson KL, Dayton RD, Klein RL. AAV9 supports wide-scale transduction of the CNS and TDP-43 disease modeling in adult rats. Mol Ther Methods Clin Dev. 2015;2:15036.
79. Duque S, et al. Intravenous administration of self-complementary AAV9 enables transgene delivery to adult motor neurons. Mol Ther. 2009;17(7):1187–1196.
80. Donsante A, et al. Intracerebroventricular delivery of self-complementary adeno-associated virus serotype 9 to the adult rat brain. Gene Ther. 2016;23(5):401–407.
81. Klein RL, Dayton RD, Tatom JB, Henderson KM, Henning PP. AAV8, 9, Rh10, Rh43 vector gene transfer in the rat brain: effects of serotype, promoter and purification method. Mol Ther. 2008;16(1):89–96.
82. Ayuso E, et al. High AAV vector purity results in serotype- and tissue-independent enhancement of transduction efficiency. Gene Ther. 2010;17(4):503–510.
83. Reijneveld JC, Taphoorn MJ, Voest EE. A simple mouse model for leptomeningeal metastases and repeated intrathecal therapy. J Neurooncol. 1999;42(2):137–142.
84. Voznyi YV, Keulemans JL, van Diggelen OP. A fluorimetric enzyme assay for the diagnosis of MPS II (Hunter disease). J Inherit Metab Dis. 2001;24(6):675–680.
85. Voznyi YaV, et al. A fluorimetric enzyme assay for the diagnosis of Sanfilippo disease C (MPS III C). J Inherit Metab Dis. 1993;16(2):465–472.
86. van Diggelen OP, et al. A fluorimetric enzyme assay for the diagnosis of Morquio disease type A (MPS IV A). Clin Chim Acta. 1990;187(2):131–139.