Biochemical evidence for superior correction of neuronal storage by chemically modified enzyme in murine mucopolysaccharidosis VII

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 42, 2012, Pages 17022-17027

  Huynh, Ha T ^a   Grubb, Jeffrey H ^a,b   Vogler, Carole ^a   Sly, William S ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ULTRAGENYX PHARMACEUTICAL INC   (United States)

Author keywords

Beta glucuronidase deficiency; Glycosaminoglycans; Mannose 6 phosphate receptor; Mannose receptor

Indexed keywords

ALPHA GALACTOSIDASE; BETA GLUCURONIDASE; BETA N ACETYLHEXOSAMINIDASE; MANNOSE RECEPTOR; PERT GUS; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG CLEARANCE; DRUG EFFECT; DRUG EFFICACY; DRUG PENETRATION; ENZYME ACTIVITY; ENZYME REPLACEMENT; MOUSE; MUCOPOLYSACCHARIDOSIS TYPE 7; NONHUMAN; PRIORITY JOURNAL; TREATMENT OUTCOME;

ANIMALS; BETA-GLUCOSIDASE; BLOOD-BRAIN BARRIER; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME REPLACEMENT THERAPY; GLUCURONIDASE; GLYCOSAMINOGLYCANS; MICE; MUCOPOLYSACCHARIDOSIS VII; NEURONS;

EID: 84867653884     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1214779109     Document Type: Article

References (53)

1. Neufeld EF, Muenzer J (2001) The Metabolic and Molecular Bases of Inherited Disease, eds Scriver CR, Beaudet AL, Sly WS, Valle D. (McGraw-Hill, New York), pp 3421-3451.
2. Sly WS, Quinton BA, McAlister WH, Rimoin DL (1973) Beta glucuronidase deficiency: Report of clinical, radiologic, and biochemical features of a new mucopolysaccharidosis. J Pediatr 82:249-257.
3. Beutler E, et al. (1991) Enzyme replacement therapy for Gaucher disease. Blood 78:1183-1189.
4. Thurberg BL, et al. (2002) Globotriaosylceramide accumulation in the Fabry kidney is cleared from multiple cell types after enzyme replacement therapy. Kidney Int 62:1933-1946. (Pubitemid 35366149)
5. Eng CM, et al. (2001) A phase 1/2 clinical trial of enzyme replacement in Fabry disease: Pharmacokinetic, substrate clearance, and safety studies. Am J Hum Genet 68:711-722. (Pubitemid 32202764)
6. Wilcox WR, et al.; International Fabry Disease Study Group (2004) Long-term safety and efficacy of enzyme replacement therapy for Fabry disease. Am J Hum Genet 75:65-74.
7. Thurberg BL, et al. (2006) Characterization of pre- and post-treatment pathology after enzyme replacement therapy for Pompe disease. Lab Invest 86:1208-1220. (Pubitemid 44789911)
8. Zhu Y, et al. (2005) Carbohydrate-remodelled acid alpha-glucosidase with higher affinity for the cation-independent mannose 6-phosphate receptor demonstrates improved delivery to muscles of Pompe mice. Biochem J 389:619-628. (Pubitemid 41117321)
9. Zhu Y, et al. (2004) Conjugation of mannose 6-phosphate-containing oligosaccharides to acid alpha-glucosidase improves the clearance of glycogen in Pompe mice. J Biol Chem 279:50336-50341. (Pubitemid 39577850)
10. Kakkis ED, et al. (2001) Enzyme-replacement therapy in mucopolysaccharidosis I. N Engl J Med 344:182-188. (Pubitemid 32064139)
11. Muenzer J, et al. (2011) Long-term, open-labeled extension study of idursulfase in the treatment of Hunter syndrome. Genet Med 13:95-101.
12. Harmatz P, et al.; MPS VI Phase 3 Study Group (2006) Enzyme replacement therapy for mucopolysaccharidosis VI: A phase 3, randomized, double-blind, placebo-controlled, multinational study of recombinant human N-acetylgalactosamine 4-sulfatase (recombinant human arylsulfatase B or rhASB) and follow-on, open-label extension study. J Pediatr 148:533-539.
13. Brady RO (2006) Enzyme replacement for lysosomal diseases. Annu Rev Med 57:283-296.
14. Frisella WA, et al. (2001) Intracranial injection of recombinant adeno-associated virus improves cognitive function in a murine model of mucopolysaccharidosis type VII. Mol Ther 3:351-358. (Pubitemid 32514651)
15. Liu G, et al. (2007) Adeno-associated virus type 5 reduces learning deficits and restores glutamate receptor subunit levels in MPS VII mice CNS. Mol Ther 15:242-247. (Pubitemid 46111872)
16. Daly TM, Vogler C, Levy B, Haskins ME, 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. (Pubitemid 29117908)
17. Sferra TJ, et al. (2004) Widespread correction of lysosomal storage following intrahepatic injection of a recombinant adeno-associated virus in the adult MPS VII mouse. Mol Ther 10:478-491. (Pubitemid 39186111)
18. Cardone M, et al. (2006) Correction of Hunter syndrome in the MPSII mouse model by AAV2/8-mediated gene delivery. Hum Mol Genet 15:1225-1236.
19. Porteus MH, Connelly JP, Pruett SM (2006) A look to future directions in gene therapy research for monogenic diseases. PLoS Genet 2:e133.
20. Macauley SL, Sands MS (2009) Promising CNS-directed enzyme replacement therapy for lysosomal storage diseases. Exp Neurol 218:5-8.
21. Chang M, et al. (2008) Intraventricular enzyme replacement improves disease phenotypes in a mouse model of late infantile neuronal ceroid lipofuscinosis. Mol Ther 16:649-656. (Pubitemid 351426165)
22. Xu S, et al. (2011) Large-volume intrathecal enzyme delivery increases survival of a mouse model of late infantile neuronal ceroid lipofuscinosis. Mol Ther 19:1842-1848.
23. Vogler C, et al. (1993) Enzyme replacement with recombinant beta-glucuronidase in the newborn mucopolysaccharidosis type VII mouse. Pediatr Res 34:837-840. (Pubitemid 23352657)
24. Vogler C, et al. (1998) Murine mucopolysaccharidosis type VII: The impact of therapies on the clinical course and pathology in a murine model of lysosomal storage disease. J Inherit Metab Dis 21:575-586. (Pubitemid 28391509)
25. O'Connor LH, et al. (1998) Enzyme replacement therapy for murine mucopolysaccharidosis type VII leads to improvements in behavior and auditory function. J Clin Invest 101:1394-1400. (Pubitemid 28166837)
26. Urayama A, Grubb JH, Sly WS, Banks WA (2004) Developmentally regulated mannose 6-phosphate receptor-mediated transport of a lysosomal enzyme across the blood-brain barrier. Proc Natl Acad Sci USA 101:12658-12663. (Pubitemid 39122079)
27. Urayama A, Grubb JH, Sly WS, Banks WA (2008) Mannose 6-phosphate receptor-mediated transport of sulfamidase across the blood-brain barrier in the newborn mouse. Mol Ther 16:1261-1266. (Pubitemid 351866057)
28. Vogler C, et al. (2005) Overcoming the blood-brain barrier with high-dose enzyme replacement therapy in murine mucopolysaccharidosis VII. Proc Natl Acad Sci USA 102:14777-14782. (Pubitemid 41457132)
29. Polito VA, et al. (2010) Correction of CNS defects in the MPSII mouse model via systemic enzyme replacement therapy. Hum Mol Genet 19:4871-4885.
30. Dunder U, et al. (2000) Enzyme replacement therapy in a mouse model of aspartyl-glycosaminuria. FASEB J 14:361-367. (Pubitemid 30086073)
31. Roces DP, et al. (2004) Efficacy of enzyme replacement therapy in alpha-mannosidosis mice: A preclinical animal study. Hum Mol Genet 13:1979-1988. (Pubitemid 39377822)
32. Matzner U, et al. (2005) Enzyme replacement improves nervous system pathology and function in a mouse model for metachromatic leukodystrophy. Hum Mol Genet 14:1139-1152. (Pubitemid 40613903)
33. Sly WS, et al. (2006) Enzyme therapy in mannose receptor-null mucopolysaccharidosis VII mice defines roles for the mannose 6-phosphate and mannose receptors. Proc Natl Acad Sci USA 103:15172-15177. (Pubitemid 44583183)
34. Grubb JH, et al. (2008) Chemically modified beta-glucuronidase crosses blood-brain barrier and clears neuronal storage in murine mucopolysaccharidosis VII. Proc Natl Acad Sci USA 105:2616-2621. (Pubitemid 351520562)
35. Rozaklis T, et al. (2011) Impact of high-dose, chemically modified sulfamidase on pathology in a murine model of MPS IIIA. Exp Neurol 230:123-130.
36. Meng Y, Sohar I, Wang L, Sleat DE, Lobel P (2012) Systemic administration of tripeptidyl peptidase I in a mouse model of late infantile neuronal ceroid lipofuscinosis: Effect of glycan modification. PLoS ONE 7:e40509.
37. Sly WS, et al. (2001) Active site mutant transgene confers tolerance to human beta-glucuronidase without affecting the phenotype of MPS VII mice. Proc Natl Acad Sci USA 98:2205-2210. (Pubitemid 32209460)
38. Sands MS, et al. (1997) Murine mucopolysaccharidosis type VII: Long term therapeutic effects of enzyme replacement and enzyme replacement followed by bone marrow transplantation. J Clin Invest 99:1596-1605. (Pubitemid 27163810)
39. Birkenmeier EH, et al. (1991) Increased life span and correction of metabolic defects in murine mucopolysaccharidosis type VII after syngeneic bone marrow transplantation. Blood 78:3081-3092.
40. Sands MS, et al. (1994) Enzyme replacement therapy for murine mucopolysaccharidosis type VII. J Clin Invest 93:2324-2331. (Pubitemid 24177142)
41. Freeman BJ, et al. (1999) Behavior and therapeutic efficacy of beta-glucuronidase-positive mononuclear phagocytes in a murine model of mucopolysaccharidosis type VII. Blood 94:2142-2150. (Pubitemid 29430432)
42. Achord DT, Brot FE, Bell CE, Sly WS (1978) Human beta-glucuronidase: In vivo clearance and in vitro uptake by a glycoprotein recognition system on reticuloendothelial cells. Cell 15:269-278. (Pubitemid 9027530)
43. Achord D, Brot F, Gonzalez-Noriega A, Sly W, Stahl P (1977) Human beta-glucuronidase. II. Fate of infused human placental beta-glucuronidase in the rat. Pediatr Res 11:816-822. (Pubitemid 8154358)
44. Tippin BL, et al. (2011) Biochemical characterization of fluorescent-labeled recombinant human alpha-L-iduronidase in vitro. Biotechnol Appl Biochem 58:391-396.
45. Nakajima M, Irimura T, Nicolson GL (1988) Heparanases and tumor metastasis. J Cell Biochem 36:157-167.
46. Bao X, et al. (2010) Endothelial heparan sulfate controls chemokine presentation in recruitment of lymphocytes and dendritic cells to lymph nodes. Immunity 33:817-829.
47. Lenaerts L, van Dam W, Persoons L, Naesens L (2012) Interaction between mouse adenovirus type 1 and cell surface heparan sulfate proteoglycans. PLoS ONE 7:e31454.
48. Olsen I, Dean MF, Muir H, Harris G (1982) Acquisition of beta-glucuronidase activity by deficient fibroblasts during direct contact with lymphoid cells. J Cell Sci 55:211-231. (Pubitemid 12025329)
49. Dean MF, McNamara A, Jenne BM (1985) Direct transfer of beta-glucuronidase from mouse macrophages to other types of cell. J Cell Sci 79:137-149. (Pubitemid 16187517)
50. Wu YP, Proia RL (2004) Deletion of macrophage-inflammatory protein 1 alpha retards neurodegeneration in Sandhoff disease mice. Proc Natl Acad Sci USA 101:8425-8430.
51. Montaño AM, et al. (2008) Acidic amino acid tag enhances response to enzyme replacement in mucopolysaccharidosis type VII mice. Mol Genet Metab 94:178-189.
52. Glaser JH, Sly WS (1973) Beta-glucuronidase deficiency mucopolysaccharidosis: Methods for enzymatic diagnosis. J Lab Clin Med 82:969-977.
53. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275.