Long-term amelioration of feline mucopolysaccharidosis VI after AAV-mediated liver gene transfer

Molecular Therapy

Volumn 19, Issue 3, 2011, Pages 461-469

  Cotugno, Gabriella ^a,b   Annunziata, Patrizia ^a,b   Tessitore, Alessandra ^a,b   O'Malley, Thomas ^c   Capalbo, Anita ^a,b   Faella, Armida ^a,b   Bartolomeo, Rosa ^a,b   O'Donnell, Patricia ^c   Wang, Ping ^c   Russo, Fabio ^a   Sleeper, Meg M ^c   Knox, Van W ^c   Fernandez, Steven ^c   Levanduski, Leah ^c   Hopwood, John ^d   De Leonibus, Elvira ^a,e   Haskins, Mark ^c   Auricchio, Alberto ^a,b  

^a TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d WOMEN S AND CHILDREN S HOSPITAL   (Australia)

^e INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSAMINOGLYCAN; N ACETYLGALACTOSAMINE 4 SULFATASE; PARVOVIRUS VECTOR; THYROXINE BINDING GLOBULIN;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS 2; ADENO ASSOCIATED VIRUS 8; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE LENGTH; CAT; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; LONG BONE; MAROTEAUX LAMY SYNDROME; MITRAL VALVE DISEASE; MOBILIZATION; MUSCULOSKELETAL SYSTEM PARAMETERS; NEWBORN; NONHUMAN; TREATMENT OUTCOME; VIRAL GENE DELIVERY SYSTEM;

FELIDAE;

EID: 79952190655     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2010.257     Document Type: Article

References (50)

1. Neufeld, E and Muenzer, J (2001). The mucopolysaccharidoses. In: Scriver. McGraw-Hill: New York.
2. Hopwood, JJ and Morris, CP (1990). The mucopolysaccharidoses. Diagnosis, molecular genetics and treatment. Mol Biol Med 7: 381-404.
3. Harmatz, P, Giugliani, R, Schwartz, I, Guffon, N, Teles, EL, Miranda, MC et al. (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.
4. Desnick, RJ and Schuchman, EH (2002). Enzyme replacement and enhancement therapies: lessons from lysosomal disorders. Nat Rev Genet 3: 954-966. (Pubitemid 35423507)
5. Dahms, NM, Lobel, P and Kornfeld, S (1989). Mannose 6-phosphate receptors and lysosomal enzyme targeting. J Biol Chem 264: 12115-12118. (Pubitemid 19191089)
6. Schlander, M and Beck, M (2009). Expensive drugs for rare disorders: to treat or not to treat? The case of enzyme replacement therapy for mucopolysaccharidosis VI. Curr Med Res Opin 25: 1285-1293.
7. Pitz, S, Ogun, O, Arash, L, Miebach, E and Beck, M (2009). Does enzyme replacement therapy infuence the ocular changes in type VI mucopolysaccharidosis? Graefes Arch Clin Exp Ophthalmol 247: 975-980.
8. McGill, JJ, Inwood, AC, Coman, DJ, Lipke, ML, de Lore, D, Swiedler, SJ et al. (2010). Enzyme replacement therapy for mucopolysaccharidosis VI from 8 weeks of age - A sibling control study. Clin Genet 77: 492-498.
9. Crawley, AC, Niedzielski, KH, Isaac, EL, Davey, RC, Byers, S and Hopwood, JJ (1997). Enzyme replacement therapy from birth in a feline model of mucopolysaccharidosis type VI. J Clin Invest 99: 651-662. (Pubitemid 27097666)
10. Yoshida, M, Noguchi, J, Ikadai, H, Takahashi, M and Nagase, S (1993). Arylsulfatase B-defcient mucopolysaccharidosis in rats. J Clin Invest 91: 1099-1104.
11. Yogalingam, G, Litjens, T, Bielicki, J, Crawley, AC, Muller, V, Anson, DS et al. (1996). Feline mucopolysaccharidosis type VI. Characterization of recombinant N-acetylgalactosamine 4-sulfatase and identifcation of a mutation causing the disease. J Biol Chem 271: 27259-27265. (Pubitemid 26367277)
12. Evers, M, Saftig, P, Schmidt, P, Hafner, A, McLoghlin, DB, Schmahl, W et al. (1996). Targeted disruption of the arylsulfatase B gene results in mice resembling the phenotype of mucopolysaccharidosis VI. Proc Natl Acad Sci USA 93: 8214-8219. (Pubitemid 26269536)
13. Tessitore, A, Faella, A, O'Malley, T, Cotugno, G, Doria, M, Kunieda, T et al. (2008). Biochemical, pathological, and skeletal improvement of mucopolysaccharidosis VI after gene transfer to liver but not to muscle. Mol Ther 16: 30-37.
14. Cotugno, G, Tessitore, A, Capalbo, A, Annunziata, P, Strisciuglio, C, Faella, A et al. (2010). Different serum enzyme levels are required to rescue the various systemic features of the mucopolysaccharidoses. Hum Gene Ther 21: 555-569.
15. Gao, G P, Alvira, MR, Wang, L, Calcedo, R, Johnston, J and Wilson, JM (2002). Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc Natl Acad Sci USA 99: 11854-11859. (Pubitemid 34994488)
16. Gao, G, Lu, Y, Calcedo, R, Grant, RL, Bell, P, Wang, L et al. (2006). Biology of AAV serotype vectors in liver-directed gene transfer to nonhuman primates. Mol Ther 13: 77-87. (Pubitemid 41763485)
17. Nathwani, AC, Gray, JT, McIntosh, J, Ng, CY, Zhou, J, Spence, Y et al. (2007). Safe and effcient transduction of the liver after peripheral vein infusion of self-complementary AAV vector results in stable therapeutic expression of human FIX in nonhuman primates. Blood 109: 1414-1421. (Pubitemid 46239572)
18. Xu, L, Mango, RL, Sands, MS, Haskins, ME, Ellinwood, NM and Ponder, KP (2002). Evaluation of pathological manifestations of disease in mucopolysaccharidosis VII mice after neonatal hepatic gene therapy. Mol Ther 6: 745-758. (Pubitemid 36054308)
19. Liu, Y, Xu, L, Hennig, AK, Kovacs, A, Fu, A, Chung, S et al. (2005). Liver-directed neonatal gene therapy prevents cardiac, bone, ear, and eye disease in mucopolysaccharidosis I mice. Mol Ther 11: 35-47. (Pubitemid 40011997)
20. Ma, X, Liu, Y, Tittiger, M, Hennig, A, Kovacs, A, Popelka, S et al. (2007). Improvements in mucopolysaccharidosis I mice after adult retroviral vector-mediated gene therapy with immunomodulation. Mol Ther 15: 889-902. (Pubitemid 46621647)
21. Ill, CR, Yang, CQ, Bidlingmaier, SM, Gonzales, JN, Burns, DS, Bartholomew, RM et al. (1997). Optimization of the human factor VIII complementary DNA expression plasmid for gene therapy of hemophilia A. Blood Coagul Fibrinolysis 8 Suppl 2: S23-S30. (Pubitemid 28140910)
22. Loeb, JE, Cordier, WS, Harris, ME, Weitzman, MD and Hope, TJ (1999). Enhanced expression of transgenes from adeno-associated virus vectors with the woodchuck hepatitis virus posttranscriptional regulatory element: implications for gene therapy. Hum Gene Ther 10: 2295-2305. (Pubitemid 29459840)
23. Cosma, MP, Pepe, S, Annunziata, I, Newbold, RF, Grompe, M, Parenti, G et al. (2003). The multiple sulfatase defciency gene encodes an essential and limiting factor for the activity of sulfatases. Cell 113: 445-456. (Pubitemid 36588748)
24. Sleeper, MM, Kusiak, CM, Shofer, FS, O'Donnell, P, Bryan, C, Ponder, KP et al. (2008). Clinical characterization of cardiovascular abnormalities associated with feline mucopolysaccharidosis I and VI. J Inherit Metab Dis 31: 424-431.
25. Dangel, JH (1998). Cardiovascular changes in children with mucopolysaccharide storage diseases and related disorders-clinical and echocardiographic fndings in 64 patients. Eur J Pediatr 157: 534-538. (Pubitemid 28311476)
26. Herati, RS, Knox, VW, O'Donnell, P, D'Angelo, M, Haskins, ME and Ponder, KP (2008). Radiographic evaluation of bones and joints in mucopolysaccharidosis I and VII dogs after neonatal gene therapy. Mol Genet Metab 95: 142-151.
27. Nuttall, JD, Brumfeld, LK, Fazzalari, NL, Hopwood, JJ and Byers, S (1999). Histomorphometric analysis of the tibial growth plate in a feline model of mucopolysaccharidosis type VI. Calcif Tissue Int 65: 47-52. (Pubitemid 29293527)
28. Abreu, S, Hayden, J, Berthold, P, Shapiro, IM, Decker, S, Patterson, D et al. (1995). Growth plate pathology in feline mucopolysaccharidosis VI. Calcif Tissue Int 57: 185-190.
29. Harmatz, P, Giugliani, R, Schwartz, IV, Guffon, N, Teles, EL, Miranda, MC et al. (2008). Long-term follow-up of endurance and safety outcomes during enzyme replacement therapy for mucopolysaccharidosis VI: Final results of three clinical studies of recombinant human N-acetylgalactosamine 4-sulfatase. Mol Genet Metab 94: 469-475.
30. Harmatz, P, Ketteridge, D, Giugliani, R, Guffon, N, Teles, EL, Miranda, MC et al. (2005). Direct comparison of measures of endurance, mobility, and joint function during enzyme-replacement therapy of mucopolysaccharidosis VI (Maroteaux-Lamy syndrome): results after 48 weeks in a phase 2 open-label clinical study of recombinant human N-acetylgalactosamine 4-sulfatase. Pediatrics 115: e681-e689. (Pubitemid 43843141)
31. Harmatz, P, Whitley, CB, Waber, L, Pais, R, Steiner, R, Plecko, B et al. (2004). Enzyme replacement therapy in mucopolysaccharidosis VI (Maroteaux-Lamy syndrome). J Pediatr 144: 574-580. (Pubitemid 38594756)
32. Cooper, M, Nayak, S, Hoffman, BE, Terhorst, C, Cao, O and Herzog, RW (2009). Improved induction of immune tolerance to factor IX by hepatic AAV-8 gene transfer. Hum Gene Ther 20: 767-776.
33. Koeberl, DD, Sun, BD, Damodaran, TV, Brown, T, Millington, DS, Benjamin, DK Jr et al. (2006). Early, sustained effcacy of adeno-associated virus vector-mediated gene therapy in glycogen storage disease type Ia. Gene Ther 13: 1281-1289. (Pubitemid 44264082)
34. Franco, LM, Sun, B, Yang, X, Bird, A, Zhang, H, Schneider, A et al. (2005). Evasion of immune responses to introduced human acid alpha-glucosidase by liver-restricted expression in glycogen storage disease type II. Mol Ther 12: 876-884. (Pubitemid 41614483)
35. Mingozzi, F, Liu, YL, Dobrzynski, E, Kaufhold, A, Liu, JH, Wang, Y et al. (2003). Induction of immune tolerance to coagulation factor IX antigen by in vivo hepatic gene transfer. J Clin Invest 111: 1347-1356. (Pubitemid 36554705)
36. Litjens, T and Hopwood, JJ (2001). Mucopolysaccharidosis type VI: Structural and clinical implications of mutations in N-acetylgalactosamine-4- sulfatase. Hum Mutat 18: 282-295. (Pubitemid 32916859)
37. Flageul, M, Aubert, D, Pichard, V, Nguyen, TH, Nowrouzi, A, Schmidt, M et al. (2009). Transient expression of genes delivered to newborn rat liver using recombinant adeno-associated virus 2/8 vectors. J Gene Med 11: 689-696.
38. Pañeda, A, Vanrell, L, Mauleon, I, Crettaz, JS, Berraondo, P, Timmermans, EJ et al. (2009). Effect of adeno-associated virus serotype and genomic structure on liver transduction and biodistribution in mice of both genders. Hum Gene Ther 20: 908-917.
39. Davidoff, AM, Ng, CY, Zhou, J, Spence, Y and Nathwani, AC (2003). Sex signifcantly infuences transduction of murine liver by recombinant adeno-associated viral vectors through an androgen-dependent pathway. Blood 102: 480-488. (Pubitemid 36841964)
40. Wang, L, Calcedo, R, Wang, H, Bell, P, Grant, R, Vandenberghe, LH et al. (2010). The pleiotropic effects of natural AAV infections on liver-directed gene transfer in macaques. Mol Ther 18: 126-134.
41. Haskins, ME, Jezyk, PF and Patterson, DF (1979). Mucopolysaccharide storage disease in three families of cats with arylsulfatase B defciency: leukocyte studies and carrier identifcation. Pediatr Res 13: 1203-1210. (Pubitemid 9256283)
42. Strauch, OF, Stypmann, J, Reinheckel, T, Martinez, E, Haverkamp, W and Peters, C (2003). Cardiac and ocular pathologies in a mouse model of mucopolysaccharidosis type VI. Pediatr Res 54: 701-708. (Pubitemid 37310771)
43. Crawley, AC, Brooks, DA, Muller, VJ, Petersen, BA, Isaac, EL, Bielicki, J et al. (1996). Enzyme replacement therapy in a feline model of Maroteaux-Lamy syndrome. J Clin Invest 97: 1864-1873. (Pubitemid 26129873)
44. Byers, S, Nuttall, JD, Crawley, AC, Hopwood, JJ, Smith, K and Fazzalari, NL (1997). Effect of enzyme replacement therapy on bone formation in a feline model of mucopolysaccharidosis type VI. Bone 21: 425-431. (Pubitemid 27485311)
45. Calcedo, R, Vandenberghe, LH, Gao, G, Lin, J and Wilson, JM (2009). Worldwide epidemiology of neutralizing antibodies to adeno-associated viruses. J Infect Dis 199: 381-390.
46. Auricchio, A, Hildinger, M, O'Connor, E, Gao, GP and Wilson, JM (2001). Isolation of highly infectious and pure adeno-associated virus type 2 vectors with a single-step gravity-fow column. Hum Gene Ther 12: 71-76. (Pubitemid 32044468)
47. Xiao, W, Chirmule, N, Berta, SC, McCullough, B, Gao, G and Wilson, JM (1999). Gene therapy vectors based on adeno-associated virus type 1. J Virol 73: 3994-4003. (Pubitemid 29189844)
48. Gao, G, Qu, G, Burnham, MS, Huang, J, Chirmule, N, Joshi, B et al. (2000). Purifcation of recombinant adeno-associated virus vectors by column chromatography and its performance in vivo. Hum Gene Ther 11: 2079-2091.
49. Chang, PL, Rosa, NE and Davidson, RG (1981). Differential assay of arylsulfatase A and B activities: a sensitive method for cultured human cells. Anal Biochem 117: 382-389. (Pubitemid 12189974)
50. Meikle, PJ, Grasby, DJ, Dean, CJ, Lang, DL, Bockmann, M, Whittle, AM et al. (2006). Newborn screening for lysosomal storage disorders. Mol Genet Metab 88: 307-314. (Pubitemid 44107765)