The pharmacological chaperone AT2220 increases the specific activity and lysosomal delivery of mutant acid alpha-glucosidase, and promotes glycogen reduction in a transgenic mouse model of pompe disease

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Khanna, Richie ^a   Powe Jr , Allan C ^a,b   Lun, Yi ^a   Soska, Rebecca ^a   Feng, Jessie ^a   Dhulipala, Rohini ^a,c   Frascella, Michelle ^a   Garcia, Anadina ^a   Pellegrino, Lee J ^a   Xu, Su ^a   Brignol, Nastry ^a   Toth, Matthew J ^a,d   Do, Hung V ^a   Lockhart, David J ^a,e   Wustman, Brandon A ^a,e   Valenzano, Kenneth J ^a  

^a Amicus Therapeutics Inc   (United States)

^b VERTEX PHARMACEUTICALS   (United States)

^c Life Technologies   (United States)

^d Barth Syndrome Foundation   (United States)

^e OrPhi Therapeutics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 DEOXYNOJIRIMYCIN; ALPHA GLUCOSIDASE; AT 2220; CONCANAVALIN A; GLYCOGEN; UNCLASSIFIED DRUG; GLUCAN 1,4 ALPHA GLUCOSIDASE; ISOENZYME; MUTANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENSITOMETRY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME REPLACEMENT; GAA GENE; GENE; GENE EXPRESSION; GLYCOGEN STORAGE DISEASE TYPE 2; HYDROLYSIS; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; LYSOSOME; MALE; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN STABILITY; TISSUE DISTRIBUTION; TISSUE LEVEL; ANIMAL; BIOAVAILABILITY; BIOCATALYSIS; BIOSYNTHESIS; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; DISEASE MODEL; DRUG EFFECTS; ENZYME STABILITY; ENZYMOLOGY; GENE INACTIVATION; GENETICS; HUMAN; METABOLISM; MUTATION; ORAL DRUG ADMINISTRATION; PATHOLOGY; PROTEIN TRANSPORT; TRANSGENIC MOUSE;

1-DEOXYNOJIRIMYCIN; ADMINISTRATION, ORAL; ANIMALS; BIOCATALYSIS; BIOLOGICAL AVAILABILITY; CERCOPITHECUS AETHIOPS; COS CELLS; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM; ENZYME STABILITY; GENE KNOCKOUT TECHNIQUES; GLUCAN 1,4-ALPHA-GLUCOSIDASE; GLYCOGEN; GLYCOGEN STORAGE DISEASE TYPE II; HUMANS; ISOENZYMES; LYSOSOMES; MICE; MICE, TRANSGENIC; MUTANT PROTEINS; MUTATION; PROTEIN TRANSPORT; PROTEOLYSIS;

EID: 84904497595     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102092     Document Type: Article

References (51)

1. Hirschhorn R, Reuser AJJ (2001) Glycogen storage disease type II: Acid α-glucosidase (acid maltase) deficiency. In: Scriver C, Beaudet A, Sly W, Valle D, editors. The metabolic and molecular bases of inherited disease. New York: McGraw-Hill. pp. 3389-3420.
2. van der Ploeg AT, Reuser AJJ (2008) Pompe's disease. Lancet 372: 1342-1353.
3. Raben N, Jatkar T, Lee A, Lu N, Dwivedi S, et al. (2002) Glycogen stored in skeletal but not in cardiac muscle in acid α-glucosidase mutant (Pompe) mice is highly resistant to transgene-encoded human enzyme. Mol Ther 6: 601-608. (Pubitemid 35363692)
4. Kishnani PS, Howell RR (2004) Pompe disease in infants and children. J Pediatr 144: S35-43. (Pubitemid 38591273)
5. Hagemans ML, Winkel LP, Hop WC, Reuser AJ, Van Doorn PA, et al. (2005) Disease severity in children and adults with Pompe disease related to age and disease duration. Neurology 64: 2139-2141. (Pubitemid 40881011)
6. Van den Hout JM, Kamphoven JH, Winkel LP, Arts WF, De Klerk JB, et al. (2004) Long-term intravenous treatment of Pompe disease with recombinant human α-glucosidase from milk. Pediatrics 113: e448-457.
7. Nicolino M, Byrne B, Wraith JE, Leslie N, Mandel H, et al. (2009) Clinical outcomes after long-term treatment with alglucosidase alfa in infants and children with advanced Pompe disease. Genet Med 11: 210-219.
8. Chen L-R, Chen C-A, Chiu S-N, Chien Y-H, Lee N-C, et al. (2009) Reversal of cardiac dysfunction after enzyme replacement in patients with infantile-onset Pompe disease. J Pediatr 155: 271-275.
9. Kishnani PS, Hwu WL, Mandel H, Nicolino M, Yong F, et al. (2006) A retrospective, multinational, multicenter study on the natural history of infantile-onset Pompe disease. J Pediatr 148: 671-676.
10. Kishnani PS, Nicolino M, Voit T, Rogers RC, Tsai AC, et al. (2006) Chinese hamster ovary cell-derived recombinant human acid α-glucosidase in infantile-onset Pompe disease. J Pediatr 149: 89-97. (Pubitemid 44081924)
11. Kishnani PS, Steiner RD, Bali D, Berger K, Byrne BJ, et al. (2006) Pompe disease diagnosis and management guideline. Genet Med 8: 267-288. (Pubitemid 44297314)
12. Strothotte S, Strigl-Pill N, Grunert B, Kornblum C, Eger K, et al. (2010) Enzyme replacement therapy with alglucosidase alfa in 44 patients with late-onset glycogen storage disease type 2: 12-month results of an observational clinical trial. J Neurol 257: 91-97.
13. van der Ploeg AT, Clemens PR, Corzo D, Escolar DM, Florence J, et al. (2010) A randomized study of alglucosidase alfa in late-onset Pompe's disease. N Engl J Med 362: 1396-1406.
14. Raben N, Danon M, Gilbert AL, Dwivedi S, Collins B, et al. (2003) Enzyme replacement therapy in the mouse model of Pompe disease. Mol Genet Metab 80: 159-169. (Pubitemid 37272242)
15. Cardone M, Porto C, Tarallo A, Vicinanza M, Rossi B, et al. (2008) Abnormal mannose-6-phosphate receptor trafficking impairs recombinant α-glucosidase uptake in Pompe disease fibroblasts. Pathogenetics 1: 6.
16. Kishnani PS, Goldenberg PC, DeArmey SL, Heller J, Benjamin D, et al. (2010) Cross-reactive immunologic material status affects treatment outcomes in Pompe disease infants. Mol Genet Metab 99: 26-33.
17. de Vries JM, van der Beek NAME, Kroos MA, Özkan L, van Doorn PA, et al. (2010) High antibody titer in an adult with Pompe disease affects treatment with alglucosidase alfa. Mol Genet Metab 101: 338-345.
18. Fukuda T, Roberts A, Ahearn M, Zaal K, Ralston E, et al. (2006) Autophagy and lysosomes in Pompe disease. Autophagy 2: 318-320. (Pubitemid 44342381)
19. Moreland RJ, Jin X, Zhang XK, Decker RW, Albee KL, et al. (2005) Lysosomal acid α-glucosidase consists of four different peptides processed from a single chain precursor. J Biol Chem 280: 6780-6791. (Pubitemid 40341233)
20. Wisselaar HA, Kroos MA, Hermans MM, van Beeumen J, Reuser AJ (1993) Structural and functional changes of lysosomal acid α-glucosidase during intracellular transport and maturation. J Biol Chem 268: 2223-2231. (Pubitemid 23033637)
21. Hasilik A, Neufeld EF (1980) Biosynthesis of lysosomal enzymes in fibroblasts. Phosphorylation of mannose residues. J Biol Chem 255: 4946-4950. (Pubitemid 10049708)
22. Bijvoet AG, Kroos MA, Pieper FR, Van der Vliet M, De Boer HA, et al. (1998) Recombinant human acid α-glucosidase: High level production in mouse milk, biochemical characteristics, correction of enzyme deficiency in GSDII KO mice. Hum Mol Genet 7: 1815-1824. (Pubitemid 28464158)
23. Fan J-Q (2008) A counterintuitive approach to treat enzyme deficiencies: Use of enzyme inhibitors for restoring mutant enzyme activity. Biol Chem 389: 1-11.
24. Okumiya T, Kroos MA, Vliet LV, Takeuchi H, Van der Ploeg AT, et al. (2007) Chemical chaperones improve transport and enhance stability of mutant α-glucosidases in glycogen storage disease type II. Mol Genet Metab 90: 49-57. (Pubitemid 44856297)
25. Parenti G, Zuppaldi A, Gabriela Pittis M, Rosaria Tuzzi M, Annunziata I, et al. (2007) Pharmacological enhancement of mutated α-glucosidase activity in fibroblasts from patients with Pompe disease. Mol Ther 15: 508-514.
26. Flanagan JJ, Rossi B, Tang K, Wu X, Mascioli K, et al. (2009) The pharmacological chaperone 1-deoxynojirimycin increases the activity and lysosomal trafficking of multiple mutant forms of acid α-glucosidase. Hum Mutat 30: 1683-1692.
27. Sawkar AR, Cheng WC, Beutler E, Wong CH, Balch WE, et al. (2002) Chemical chaperones increase the cellular activity of N370S β-glucosidase: A therapeutic strategy for Gaucher disease. Proc Natl Acad Sci U S A 99: 15428-15433. (Pubitemid 35403951)
28. Tropak MB, Reid SP, Guiral M, Withers SG, Mahuran D (2004) Pharmacological enhancement of β-hexosaminidase activity in fibroblasts from adult Tay-Sachs and Sandhoff patients. J Biol Chem 279: 13478-13487. (Pubitemid 38468872)
29. Fan J-Q (2003) A contradictory treatment for lysosomal storage disorders: Inhibitors enhance mutant enzyme activity. Trends Pharmacol Sci 24: 355-360.
30. Shimmoto M, Kase R, Itoh K, Utsumi K, Ishii S, et al. (1997) Generation and characterization of transgenic mice expressing a human mutant α-galactosidase with an R301Q substitution causing a variant form of Fabry disease. FEBS Lett 417: 89-91. (Pubitemid 27490479)
31. Ishii S, Yoshioka H, Mannen K, Kulkarni AB, Fan JQ (2004) Transgenic mouse expressing human mutant α-galactosidase A in an endogenous enzyme deficient background: A biochemical animal model for studying active-site specific chaperone therapy for Fabry disease. Biochim Biophys Acta 1690: 250-257. (Pubitemid 39423620)
32. Khanna R, Soska R, Lun Y, Feng J, Frascella M, et al. (2010) The pharmacological chaperone 1-deoxygalactonojirimycin reduces tissue globotriaosylceramide levels in a mouse model of Fabry disease. Mol Ther 18: 23-33.
33. Gordon JW, Scangos GA, Plotkin DJ, Barbosa JA, Ruddle FH (1980) Genetic transformation of mouse embryos by microinjection of purified DNA. Proc Natl Acad Sci USA 77: 7380-7384. (Pubitemid 11131133)
34. Raben N, Nagaraju K, Lee E, Kessler P, Byrne B, et al. (1998) Targeted disruption of the acid α-glucosidase gene in mice causes an illness with critical features of both infantile and adult human glycogen storage disease type II. J Biol Chem 273: 19086-19092. (Pubitemid 28366303)
35. Khanna R, Flanagan JJ, Feng J, Soska R, Frascella M, et al. (2012) The pharmacological chaperone AT2220 increases recombinant human acid α-glucosidase uptake and glycogen reduction in a mouse model of Pompe disease. PLoS ONE 7: e40776.
36. Lynch CM, Johnson J, Vaccaro C, Thurberg BL (2005) High-resolution light microscopy (HRLM) and digital analysis of Pompe disease pathology. J Histochem Cytochem 53: 63-73. (Pubitemid 40130121)
37. Takikita S, Myerowitz R, Zaal K, Raben N, Plotz PH (2009) Murine muscle cell models for Pompe disease and their use in studying therapeutic approaches. Mol Genet Metab 96: 208-217.
38. Steet RA, Chung S, Wustman B, Powe A, Do H, et al. (2006) The iminosugar isofagomine increases the activity of N370S mutant acid β-glucosidase in Gaucher fibroblasts by several mechanisms. Proc Natl Acad Sci U S A 109: 13813-13818. (Pubitemid 44413990)
39. Reuser AJJ, Kroos MA, Ponne NJ, Wolterman RA, Loonen MCB, et al. (1984) Uptake and stability of human and bovine acid α-glucosidase in cultured fibroblasts and skeletal muscle cells from glycogenosis type II patients. Exp Cell Res 155: 178-189. (Pubitemid 15213279)
40. Zhu Y, Li X, McVie-Wylie A, Jiang C, Thurberg BL, et al. (2005) Carbohydrate-remodelled acid α-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)
41. Hawes ML, Kennedy W, O'Callaghan MW, Thurberg BL (2007) Differential muscular glycogen clearance after enzyme replacement therapy in a mouse model of Pompe disease. Mol Genet Metab 91: 343-351. (Pubitemid 47043513)
42. DeRuisseau LR, Fuller DD, Qiu K, DeRuisseau KC, Donnelly WH, et al. (2009) Neural deficits contribute to respiratory insufficiency in Pompe disease. Proc Natl Acad Sci U S A 106: 9419-9424.
43. neo Pompe disease mice. J Neuropathol Exp Neurol 67: 803-818.
44. Lee C-J, Fan X, Guo X, Medin JA (2011) Promoter-specific lentivectors for long-term, cardiac-directed therapy of Fabry disease. J Cardiol 57: 115-122.
45. Kikuchi T, Yang HW, Pennybacker M, Ichihara N, Mizutani M, et al. (1998) Clinical and metabolic correction of Pompe disease by enzyme therapy in acid maltase-deficient quail. J Clin Invest 101: 827-833. (Pubitemid 28096080)
46. Huie ML, Chen AS, Tsujino S, Shanske S, DiMauro S, et al. (1994) Aberrant splicing in adult onset glycogen storage disease type II (GSDII): Molecular identification of an IVS1 (-13t->g) mutation in a majority of patients and a novel IVS10 (+1gt->ct) mutation. Hum Mol Genet 3: 2231-2236.
47. Hermans MM, De Graaff E, Kroos MA, Mohkamsing S, Eussen BJ, et al. (1994) The effect of a single base pair deletion (delta t525) and a c1634t missense mutation (pro545leu) on the expression of lysosomal α-glucosidase in patients with glycogen storage disease type II. Hum Mol Genet 3: 2213-2218.
48. Raben N, Plotz P, Byrne BJ (2002) Acid α-glucosidase deficiency (glycogenosis type II, Pompe disease). Curr Mol Med 2: 145-166. (Pubitemid 34649837)
49. Montalvo AL, Bembi B, Donnarumma M, Filocamo M, Parenti G, et al. (2006) Mutation profile of the GAA gene in 40 italian patients with late onset glycogen storage disease type II. Hum Mutat 27: 999-1006. (Pubitemid 44454052)
50. Pittis M, Donnarumma M, Montalvo ALE, Dominissini S, Kroos M, et al. (2008) Molecular and functional characterization of eight novel GAA mutations in italian infants with Pompe disease. Hum Mutat 29: E27-E36.
51. Porto C, Cardone M, Fontana F, Rossi B, Tuzzi MR, et al. (2009) The pharmacological chaperone N-butyldeoxynojirimycin enhances enzyme replacement therapy in Pompe disease fibroblasts. Mol Ther 17: 964-971.