Hematopoietic Stem Cell Gene Therapy Corrects Neuropathic Phenotype in Murine Model of Mucopolysaccharidosis Type II

Human Gene Therapy

Volumn 26, Issue 6, 2015, Pages 357-366

  Wakabayashi, Taichi ^a   Shimada, Yohta ^a   Akiyama, Kazumasa ^b   Higuchi, Takashi ^a   Fukuda, Takahiro ^a   Kobayashi, Hiroshi ^a   Eto, Yoshikatsu ^c   Ida, Hiroyuki ^a   Ohashi, Toya ^a  

^a JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c Institute of Neurological Disorders   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

IDURONATE 2 SULFATASE; LENTIVIRUS VECTOR; PROTEIN P62; UBIQUITIN PROTEIN LIGASE; UBIQUITINATED PROTEIN; GLYCOPROTEIN; GLYCOSAMINOGLYCAN; IDS PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BLOOD BIOCHEMISTRY; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE TARGETING; GENETIC TRANSDUCTION; GRAFT RECIPIENT; HEMATOPOIETIC STEM CELL; HUNTER SYNDROME; LYSOSOME STORAGE DISEASE; MALE; MOLECULARLY TARGETED THERAPY; MOUSE; NEUROPATHY; NONHUMAN; PHENOTYPE; STEM CELL GENE THERAPY; WILD TYPE; ANIMAL; BRAIN; C57BL MOUSE; DISEASE MODEL; GENE THERAPY; GENETICS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; KNOCKOUT MOUSE; LENTIVIRINAE; METABOLISM; MUCOPOLYSACCHARIDOSIS II; PATHOLOGY; PHYSIOLOGY; PROCEDURES;

MURINAE; MUS;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; FEMALE; GENETIC THERAPY; GLYCOPROTEINS; GLYCOSAMINOGLYCANS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; IDURONATE SULFATASE; LENTIVIRUS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUCOPOLYSACCHARIDOSIS II; TRANSDUCTION, GENETIC;

EID: 84932615222     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2014.158     Document Type: Article

References (51)

1. Muenzer J, Wraith JE, Beck M, et al. A phase II/III clinical study of enzyme replacement therapy with idursulfase in mucopolysaccharidosis II (Hunter syndrome). Genet Med 2006;8:465-473.
2. Okuyama T, Tanaka A, Suzuki Y, 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;99:18-25.
3. Muenzer J, Beck M, Eng CM, et al. Long-term, open-labeled extension study of idursulfase in the treatment of Hunter syndrome. Genet Med 2011;13:95-101.
4. Manara R, Priante E, Grimaldi M, et al. Brain and spine MRI features of Hunter disease: frequency, natural evolution and response to therapy. J Inherit Metab Dis 2011;34:763-780.
5. Malatack JJ, Consolini DM, Bayever E. The status of hematopoietic stem cell transplantation in lysosomal storage disease. Pediatr Neurol 2003;29:391-403.
6. Sano R, Tessitore A, Ingrassia A, et al. Chemokine-induced recruitment of genetically modified bone marrow cells into the CNS of GM1-gangliosidosis mice corrects neuronal pathology. Blood 2005;106:2259-2268.
7. Shapiro EG, Lockman LA, Balthazor M, et al. Neuropsychological outcomes of several storage diseases with and without bone marrow transplantation. J Inherit Metab Dis 1995;18:413-429.
8. Vellodi A, Young E, Cooper A, et al. Long-term follow-up following bone marrow transplantation for Hunter disease. J Inherit Metab Dis 1999;22:638-648.
9. Guffon N, Bertrand Y, Forest I, et al. Bone marrow transplantation in children with Hunter syndrome: outcome after 7 to 17 years. J Pediatr 2009;154:733-737.
10. Akiyama K, Shimada Y, Higuchi T, et al. Enzyme augmentation therapy enhances the therapeutic efficacy of bone marrow transplantation in mucopolysaccharidosis type II mice. Mol Genet Metab 2014;111:139-146.
11. Cartier N, Hacein-Bey-Abina S, Bartholomae CC, et al. Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 2009;326:818-823.
12. Biffi A, Montini E, Lorioli L, et al. Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science 2013;341:1233158.
13. Aiuti A, Biasco L, Scaramuzza S, et al. Lentiviral hematopoietic stem cell gene therapy in patients with Wiskott-Aldrich syndrome. Science 2013;341:1233151.
14. Drakopoulou E, Papanikolaou E, Anagnou NP. The ongoing challenge of hematopoietic stem cell-based gene therapy for β-thalassemia. Stem Cells Int 2011;2011:987980.
15. Visigalli I, Delai S, Politi LS, et al. Gene therapy augments the efficacy of hematopoietic cell transplantation and fully corrects mucopolysaccharidosis type I phenotype in the mouse model. Blood 2010;116:5130-5139.
16. Langford-Smith A, Wilkinson FL, Langford-Smith KJ, et al. Hematopoietic stem cell and gene therapy corrects primary neuropathology and behavior in mucopolysaccharidosis IIIA mice. Mol Ther 2012;20:1610-1621.
17. Garcia AR, Pan J, Lamsa JC, et al. The characterization of a murine model of mucopolysaccharidosis II (Hunter syndrome). J Inherit Metab Dis 2007;30:924-934.
18. Kobayashi H, Carbonaro D, Pepper K, et al. Neonatal gene therapy of MPS I mice by intravenous injection of a lentiviral vector. Mol Ther 2005;11:776-789.
19. Kimura T, Koya RC, Anselmi L, et al. Lentiviral vectors with CMV or MHCII promoters administered in vivo: immune reactivity versus persistence of expression. Mol Ther 2007;15:1390-1399.
20. Falahati R, Zhang J, Flebbe-Rehwaldt L, et al. Chemoselection of allogeneic HSC after murine neonatal transplantation without myeloablation or post-transplant immunosuppression. Mol Ther 2012;20:2180-2189.
21. Higuchi T, Shimizu H, Fukuda 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;107:122-128.
22. Shimada Y, Wakabayashi T, Akiyama K, et al. A method for measuring disease-specific iduronic acid from the nonreducing end of glycosaminoglycan in mucopolysaccharidosis type II mice. Accepted.
23. Shimada Y, Fukuda T, Aoki K, et al. A protocol for immunoaffinity separation of the accumulated ubiquitin-protein conjugates solubilized with sodium dodecyl sulfate. Anal Biochem 2008;377:77-82.
24. Shimada Y, Nishimura E, Hoshina H, et al. Proteasome inhibitor bortezomib enhances the activity of multiple mutant forms of lysosomal α-glucosidase in Pompe disease. JIMD Rep 2015;18:33-39.
25. Ohashi T, Iizuka S, Shimada Y, et al. Administration of anti-CD3 antibodies modulates the immune response to an infusion of α-glucosidase in mice. Mol Ther 2012;20:1924-1931.
26. Fukuda T, Shimizu J, Furuhata H, et al. Overexpression of heat shock proteins in pallido-nigral axonal spheroids of non-human aged primates. Acta Neuropathol 2005;110:145-150.
27. Lawrence R, Brown JR, Al-Mafraji K, et al. Disease-specific non-reducing end carbohydrate biomarkers for mucopolysaccharidoses. Nat Chem Biol 2012;8:197-204.
28. Lieberman AP, Puertollano R, Raben N, et al. Autophagy in lysosomal storage disorders. Autophagy 2012;8:719-730.
29. Settembre C, Fraldi A, Jahreiss L, et al. A block of autophagy in lysosomal storage disorders. Hum Mol Genet 2008;17:119-129.
30. Sibille EL, Pavlides C, Fenster RJ, et al. Impaired hippocampal-dependent learning and functional abnormalities in the hippocampus in mice lacking serotonin 1A receptors. 2000;97:14731-14736.
31. Washida K, Ihara M, Nishio K, et al. Nonhypotensive dose of telmisartan attenuates cognitive impairment partially due to peroxisome proliferator-activated receptor-γ activation in mice with chronic cerebral hypoperfusion. Stroke 2010;41:1798-1806.
32. Muenzer J, Wraith JE, Clarke LA. Mucopolysaccharidosis I: management and treatment guidelines. Pediatrics 2009;123:19-29.
33. Staba S, Escolar M, Poe M. Cord-blood transplants from unrelated donors in patients with Hurler's syndrome. N Engl J Med 2004;350:1960-1969.
34. Tanaka A, Okuyama T, Suzuki Y, et al. Long-term efficacy of hematopoietic stem cell transplantation on brain involvement in patients with mucopolysaccharidosis type II: a nationwide survey in Japan. Mol Genet Metab 2012;107:513-520.
35. Polito VA, Cosma MP. IDS crossing of the blood-brain barrier corrects CNS defects in MPSII mice. Am J Hum Genet 2009;85:296-301.
36. Polito VA, Abbondante S, Polishchuk RS, et al. Correction of CNS defects in the MPSII mouse model via systemic enzyme replacement therapy. Hum Mol Genet 2010;19:4871-4885.
37. Priller J, Flügel A, Wehner T, et al. Targeting gene-modified hematopoietic cells to the central nervous system: use of green fluorescent protein uncovers microglial engraftment. Nat Med 2001;7:1356-1361.
38. Priller J, Prinz M, Heikenwalder M, et al. Early and rapid engraftment of bone marrow-derived microglia in scrapie. J Neurosci 2006;26:11753-11762.
39. Burrell K, Hill RP, Zadeh G. High-resolution in-vivo analysis of normal brain response to cranial irradiation. PLoS One 2012;7:e38366.
40. Biffi A, De Palma M, Quattrini A, et al. Correction of metachromatic leukodystrophy in the mouse model by transplantation of genetically modified hematopoietic stem cells. J Clin Invest 2004;113:1118-1129.
41. Biffi A, Capotondo A, Fasano S, et al. Gene therapy of metachromatic leukodystrophy reverses neurological damage and deficits in mice. J Clin Invest 2006;116:3070-3082.
42. Sergijenko A, Langford-Smith A, Liao AY, et al. Myeloid/microglial driven autologous hematopoietic stem cell gene therapy corrects a neuronopathic lysosomal disease. Mol Ther 2013;21:1938-1949.
43. Suzuki Y, Ogawa S, Sakakibara Y. Chaperone therapy for neuronopathic lysosomal diseases: competitive inhibitors as chemical chaperones for enhancement of mutant enzyme activities. Perspect Medicin Chem 2009;3:7-19.
44. Conzelmann E, Sandhoff K. Partial enzyme deficiencies: residual activities and the development of neurological disorders. Dev Neurosci 6:58-71.
45. Visigalli I, Ungari S, Martino S, et al. The galactocerebrosidase enzyme contributes to the maintenance of a functional hematopoietic stem cell niche. Blood 2010;116:1857-1866.
46. Anson DS, Muller V, Bielicki J, et al. Overexpression of N-acetylgalactosamine-4-sulphatase induces a multiple sulphatase deficiency in mucopolysaccharidosis-type-VI fibroblasts. Biochem J 1993;294:657-662.
47. Capotondo A, Cesani M, Pepe S, et al. Safety of arylsulfatase A overexpression for gene therapy of metachromatic leukodystrophy. Hum Gene Ther 2007;18:821-836.
48. Wagemaker G. Lentiviral hematopoietic stem cell gene therapy in inherited metabolic disorders. Hum Gene Ther 2014;25:862-865.
49. Hacein-Bey-Abina S, Von Kalle C, Schmidt M, et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 2003;302:415-419.
50. Stein S, Ott MG, Schultze-Strasser S, et al. Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease. Nat Med 2010;16:198-204.
51. Cavazzana-Calvo M, Payen E, Negre O, et al. Transfusion independence and HMGA2 activation after gene therapy of human β-thalassaemia. Nature 2010;467:318-322.