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Published in: Journal of Inherited Metabolic Disease 6/2012

01-11-2012 | Original Article

Lysosomal delivery of therapeutic enzymes in cell models of Fabry disease

Authors: D. Marchesan, T. M. Cox, P. B. Deegan

Published in: Journal of Inherited Metabolic Disease | Issue 6/2012

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Abstract

The success of enzymatic replacement in Gaucher disease has stimulated development of targeted protein replacement for other lysosomal disorders, including Anderson-Fabry disease, which causes fatal cardiac, cerebrovascular and renal injury: deficiency of lysosomal α-Galactosidase A induces accumulation of glycosphingolipids. Endothelial cell storage was the primary endpoint in a clinical trial that led to market authorization. Two α-Galactosidase A preparations are licensed worldwide, but fatal outcomes persist, with storage remaining in many tissues. We compare mechanisms of uptake of α -Galactosidase A into cells relevant to Fabry disease, in order to investigate if the enzyme is targeted to the lysosomes in a mannose-6-phosphate receptor dependent fashion, as generally believed. α -Galactosidase A uptake was examined in fibroblasts, four different endothelial cell models, and hepatic cells in vitro. Uptake of europium-labeled human α -Galactosidase A was measured by time-resolved fluorescence. Ligand-specific uptake was quantified in inhibitor studies. Targeting to the lysosome was determined by precipitation and by confocal microscopy. The quantity and location of cation-independent mannose-6-phosphate receptors in the different cell models were investigated using confocal microscopy. Uptake and delivery of α -Galactosidase A to lysosomes in fibroblasts is mediated by the canonical mannose-6-phosphate receptor pathway, but in endothelial cells in vitro this mechanism does not operate. Moreover, this observation is supported by a striking paucity of expression of cation independent mannose-6-phosphate receptors on the plasma membrane of the four endothelial cell models and by little delivery of enzyme to lysosomes, when compared with fibroblasts. If these observations are confirmed in vivo, alternative mechanisms will be needed to explain the ready clearance of storage from endothelial cells in patients undergoing enzyme replacement therapy.
Literature
go back to reference Aden DP, Fogel A et al (1979) Controlled synthesis of HBsAg in a differentiated human liver carcinoma-derived cell line. Nature 282(5739):615–616PubMedCrossRef Aden DP, Fogel A et al (1979) Controlled synthesis of HBsAg in a differentiated human liver carcinoma-derived cell line. Nature 282(5739):615–616PubMedCrossRef
go back to reference Aerts JM, Groener JE et al (2008) Elevated globotriaosylsphingosine is a hallmark of Fabry disease. Proc Natl Acad Sci U S A 105(8):2812–2817PubMedCrossRef Aerts JM, Groener JE et al (2008) Elevated globotriaosylsphingosine is a hallmark of Fabry disease. Proc Natl Acad Sci U S A 105(8):2812–2817PubMedCrossRef
go back to reference Barbey F, Brakch N et al (2006) Cardiac and vascular hypertrophy in Fabry disease: evidence for a new mechanism independent of blood pressure and glycosphingolipid deposition. Arterioscler Thromb Vasc Biol 26(4):839–844PubMedCrossRef Barbey F, Brakch N et al (2006) Cardiac and vascular hypertrophy in Fabry disease: evidence for a new mechanism independent of blood pressure and glycosphingolipid deposition. Arterioscler Thromb Vasc Biol 26(4):839–844PubMedCrossRef
go back to reference Berger HU et al (1974) Methods of enzymatic analysis. Academic Press, New York, pp 495-496 Berger HU et al (1974) Methods of enzymatic analysis. Academic Press, New York, pp 495-496
go back to reference Bishop DF, Desnick RJ (1981) Affinity purification of alpha-galactosidase A from human spleen, placenta, and plasma with elimination of pyrogen contamination. Properties of the purified splenic enzyme compared to other forms. J Biol Chem 256(3):1307–1316PubMed Bishop DF, Desnick RJ (1981) Affinity purification of alpha-galactosidase A from human spleen, placenta, and plasma with elimination of pyrogen contamination. Properties of the purified splenic enzyme compared to other forms. J Biol Chem 256(3):1307–1316PubMed
go back to reference Blom D, Speijer D et al (2003) Recombinant enzyme therapy for Fabry disease: absence of editing of human alpha-galactosidase A mRNA. Am J Hum Genet 72(1):23–31PubMedCrossRef Blom D, Speijer D et al (2003) Recombinant enzyme therapy for Fabry disease: absence of editing of human alpha-galactosidase A mRNA. Am J Hum Genet 72(1):23–31PubMedCrossRef
go back to reference Bolte S, Cordelieres FP (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224(Pt 3):213–232PubMedCrossRef Bolte S, Cordelieres FP (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224(Pt 3):213–232PubMedCrossRef
go back to reference Boutouyrie P, Laurent S et al (2002) Arterial remodelling in Fabry disease. Acta Paediatr Suppl 91(439):62–66PubMedCrossRef Boutouyrie P, Laurent S et al (2002) Arterial remodelling in Fabry disease. Acta Paediatr Suppl 91(439):62–66PubMedCrossRef
go back to reference Breunig F, Wanner C (2008) Update on Fabry disease: kidney involvement, renal progression and enzyme replacement therapy. J Nephrol 21(1):32–37PubMed Breunig F, Wanner C (2008) Update on Fabry disease: kidney involvement, renal progression and enzyme replacement therapy. J Nephrol 21(1):32–37PubMed
go back to reference Christensen EI, Zhou Q et al (2007) Distribution of alpha-galactosidase A in normal human kidney and renal accumulation and distribution of recombinant alpha-galactosidase A in Fabry mice. J Am Soc Nephrol 18(3):698–706PubMedCrossRef Christensen EI, Zhou Q et al (2007) Distribution of alpha-galactosidase A in normal human kidney and renal accumulation and distribution of recombinant alpha-galactosidase A in Fabry mice. J Am Soc Nephrol 18(3):698–706PubMedCrossRef
go back to reference Clarke JT (1981) The glycosphingolipids of human plasma lipoproteins. Can J Biochem 59(6):412–417PubMedCrossRef Clarke JT (1981) The glycosphingolipids of human plasma lipoproteins. Can J Biochem 59(6):412–417PubMedCrossRef
go back to reference Clarke JT (2007) Narrative review: Fabry disease. Ann Intern Med 146(6):425–433PubMed Clarke JT (2007) Narrative review: Fabry disease. Ann Intern Med 146(6):425–433PubMed
go back to reference Clarke JT, Stoltz JM et al (1976) Neutral glycosphingolipids of serum lipoproteins in Fabry's disease. Biochim Biophys Acta 431(2):317–325PubMedCrossRef Clarke JT, Stoltz JM et al (1976) Neutral glycosphingolipids of serum lipoproteins in Fabry's disease. Biochim Biophys Acta 431(2):317–325PubMedCrossRef
go back to reference Clarke JT, Stoltz JM et al (1980) Stability of plasma low density lipoprotein with abnormal glycolipid composition from patients with Fabry's disease. Atherosclerosis 35(2):155–163PubMedCrossRef Clarke JT, Stoltz JM et al (1980) Stability of plasma low density lipoprotein with abnormal glycolipid composition from patients with Fabry's disease. Atherosclerosis 35(2):155–163PubMedCrossRef
go back to reference Darlington GJ, Kelly JH et al (1987) Growth and hepatospecific gene expression of human hepatoma cells in a defined medium. Vitro Cell Dev Biol 23(5):349–354CrossRef Darlington GJ, Kelly JH et al (1987) Growth and hepatospecific gene expression of human hepatoma cells in a defined medium. Vitro Cell Dev Biol 23(5):349–354CrossRef
go back to reference Deegan PB, Baehner AF et al (2006) Natural history of Fabry disease in females in the Fabry outcome survey. J Med Genet 43(4):347–352PubMedCrossRef Deegan PB, Baehner AF et al (2006) Natural history of Fabry disease in females in the Fabry outcome survey. J Med Genet 43(4):347–352PubMedCrossRef
go back to reference DeLisser HM, Yan HC et al (1993) Platelet/endothelial cell adhesion molecule-1 (CD31)-mediated cellular aggregation involves cell surface glycosaminoglycans. J Biol Chem 268(21):16037–16046PubMed DeLisser HM, Yan HC et al (1993) Platelet/endothelial cell adhesion molecule-1 (CD31)-mediated cellular aggregation involves cell surface glycosaminoglycans. J Biol Chem 268(21):16037–16046PubMed
go back to reference Desnick RJ, Ioannou YA, Eng CM (2001) α-Galactosidase A deficiency: Fabry disease. In: Scriver CR, Beaudet AL, Sly WS, Valle D, eds. The metabolic and molecular bases of inherited disease. New York: McGraw-Hill, 8th ed. Vol. 3:3733–74 Desnick RJ, Ioannou YA, Eng CM (2001) α-Galactosidase A deficiency: Fabry disease. In: Scriver CR, Beaudet AL, Sly WS, Valle D, eds. The metabolic and molecular bases of inherited disease. New York: McGraw-Hill, 8th ed. Vol. 3:3733–74
go back to reference Elleder M (1985) Fabry's disease: absence of storage as a feature of liver sinus endothelium. Acta Histochem 77(1):33–36PubMedCrossRef Elleder M (1985) Fabry's disease: absence of storage as a feature of liver sinus endothelium. Acta Histochem 77(1):33–36PubMedCrossRef
go back to reference Elleder M (2003) Sequelae of storage in Fabry disease--pathology and comparison with other lysosomal storage diseases. Acta Paediatr Suppl 92(443):46–53, discussion 45PubMed Elleder M (2003) Sequelae of storage in Fabry disease--pathology and comparison with other lysosomal storage diseases. Acta Paediatr Suppl 92(443):46–53, discussion 45PubMed
go back to reference Elleder M, Ledvinova J et al (1990) An atypical ultrastructural pattern in Fabry's disease: a study on its nature and incidence in 7 cases. Ultrastruct Pathol 14(6):467–474PubMedCrossRef Elleder M, Ledvinova J et al (1990) An atypical ultrastructural pattern in Fabry's disease: a study on its nature and incidence in 7 cases. Ultrastruct Pathol 14(6):467–474PubMedCrossRef
go back to reference Elsea SH, Lucas RE (2002) The mousetrap: what we can learn when the mouse model does not mimic the human disease. ILAR J 43(2):66–79PubMed Elsea SH, Lucas RE (2002) The mousetrap: what we can learn when the mouse model does not mimic the human disease. ILAR J 43(2):66–79PubMed
go back to reference Eng CM, Guffon N et al (2001) Safety and efficacy of recombinant human alpha-galactosidase A–replacement therapy in Fabry's disease. N Engl J Med 345(1):9–16PubMedCrossRef Eng CM, Guffon N et al (2001) Safety and efficacy of recombinant human alpha-galactosidase A–replacement therapy in Fabry's disease. N Engl J Med 345(1):9–16PubMedCrossRef
go back to reference Fellgiebel A, Muller MJ et al (2006) CNS manifestations of Fabry's disease. Lancet Neurol 5(9):791–795PubMedCrossRef Fellgiebel A, Muller MJ et al (2006) CNS manifestations of Fabry's disease. Lancet Neurol 5(9):791–795PubMedCrossRef
go back to reference Ghosh P, Dahms NM et al (2003) Mannose 6-phosphate receptors: new twists in the tale. Nat Rev Mol Cell Biol 4(3):202–212PubMedCrossRef Ghosh P, Dahms NM et al (2003) Mannose 6-phosphate receptors: new twists in the tale. Nat Rev Mol Cell Biol 4(3):202–212PubMedCrossRef
go back to reference Ginsberg L, Manara R et al (2006) Magnetic resonance imaging changes in Fabry disease. Acta Paediatr Suppl 95(451):57–62PubMedCrossRef Ginsberg L, Manara R et al (2006) Magnetic resonance imaging changes in Fabry disease. Acta Paediatr Suppl 95(451):57–62PubMedCrossRef
go back to reference Grabowski GA, Hopkin RJ (2003) Enzyme therapy for lysosomal storage disease: principles, practice, and prospects. Annu Rev Genomics Hum Genet 4:403–436PubMedCrossRef Grabowski GA, Hopkin RJ (2003) Enzyme therapy for lysosomal storage disease: principles, practice, and prospects. Annu Rev Genomics Hum Genet 4:403–436PubMedCrossRef
go back to reference Graham J, Ford T et al (1994) The preparation of subcellular organelles from mouse liver in self-generated gradients of iodixanol. Anal Biochem 220(2):367–373PubMedCrossRef Graham J, Ford T et al (1994) The preparation of subcellular organelles from mouse liver in self-generated gradients of iodixanol. Anal Biochem 220(2):367–373PubMedCrossRef
go back to reference Gubler MC, Lenoir G et al (1978) Early renal changes in hemizygous and heterozygous patients with Fabry's disease. Kidney Int 13(3):223–235PubMedCrossRef Gubler MC, Lenoir G et al (1978) Early renal changes in hemizygous and heterozygous patients with Fabry's disease. Kidney Int 13(3):223–235PubMedCrossRef
go back to reference Hasholt L, Wandall A et al (1988) Enzyme replacement in Fabry endothelial cells and fibroblasts: uptake experiments and electron microscopical studies. Clin Genet 33(5):360–371PubMedCrossRef Hasholt L, Wandall A et al (1988) Enzyme replacement in Fabry endothelial cells and fibroblasts: uptake experiments and electron microscopical studies. Clin Genet 33(5):360–371PubMedCrossRef
go back to reference Haslett C, Guthrie LA et al (1985) Modulation of multiple neutrophil functions by preparative methods or trace concentrations of bacterial lipopolysaccharide. Am J Pathol 119(1):101–110PubMed Haslett C, Guthrie LA et al (1985) Modulation of multiple neutrophil functions by preparative methods or trace concentrations of bacterial lipopolysaccharide. Am J Pathol 119(1):101–110PubMed
go back to reference Hilz MJ, Kolodny EH et al (2004) Reduced cerebral blood flow velocity and impaired cerebral autoregulation in patients with Fabry disease. J Neurol 251(5):564–570PubMedCrossRef Hilz MJ, Kolodny EH et al (2004) Reduced cerebral blood flow velocity and impaired cerebral autoregulation in patients with Fabry disease. J Neurol 251(5):564–570PubMedCrossRef
go back to reference Kalliokoski RJ, Kalliokoski KK et al (2006) Structural and functional changes in peripheral vasculature of Fabry patients. J Inherit Metab Dis 29(5):660–666PubMedCrossRef Kalliokoski RJ, Kalliokoski KK et al (2006) Structural and functional changes in peripheral vasculature of Fabry patients. J Inherit Metab Dis 29(5):660–666PubMedCrossRef
go back to reference Karen JK, Hale EK et al (2005) Angiokeratoma corporis diffusum (Fabry disease). Dermatol Online J 11(4):8PubMed Karen JK, Hale EK et al (2005) Angiokeratoma corporis diffusum (Fabry disease). Dermatol Online J 11(4):8PubMed
go back to reference Keller H, Niggli V (1995) Effects of cytochalasin D on shape and fluid pinocytosis in human neutrophils as related to cytoskeletal changes (actin, alpha-actinin and microtubules). Eur J Cell Biol 66(2):157–164PubMed Keller H, Niggli V (1995) Effects of cytochalasin D on shape and fluid pinocytosis in human neutrophils as related to cytoskeletal changes (actin, alpha-actinin and microtubules). Eur J Cell Biol 66(2):157–164PubMed
go back to reference Keslova-Veselikova J, Hulkova H et al (2008) Replacement of alpha-galactosidase A in Fabry disease: effect on fibroblast cultures compared with biopsied tissues of treated patients. Virchows Arch 452(6):651–665PubMedCrossRef Keslova-Veselikova J, Hulkova H et al (2008) Replacement of alpha-galactosidase A in Fabry disease: effect on fibroblast cultures compared with biopsied tissues of treated patients. Virchows Arch 452(6):651–665PubMedCrossRef
go back to reference Knowles BB, Howe CC et al (1980) Human hepatocellular carcinoma cell lines secrete the major plasma proteins and hepatitis B surface antigen. Science 209(4455):497–499PubMedCrossRef Knowles BB, Howe CC et al (1980) Human hepatocellular carcinoma cell lines secrete the major plasma proteins and hepatitis B surface antigen. Science 209(4455):497–499PubMedCrossRef
go back to reference Lee K, Jin X et al (2003) A biochemical and pharmacological comparison of enzyme replacement therapies for the glycolipid storage disorder Fabry disease. Glycobiology 13(4):305–313PubMedCrossRef Lee K, Jin X et al (2003) A biochemical and pharmacological comparison of enzyme replacement therapies for the glycolipid storage disorder Fabry disease. Glycobiology 13(4):305–313PubMedCrossRef
go back to reference Li Q, Lau A et al (2004) A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J Neurosci 24(16):4070–4081PubMedCrossRef Li Q, Lau A et al (2004) A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J Neurosci 24(16):4070–4081PubMedCrossRef
go back to reference Lin Y, Weisdorf D, Solovey A, Hebbel RP (2000a) Origins of circulating endothelial outgrowth from blood. J Clin Invest 105:71–77PubMedCrossRef Lin Y, Weisdorf D, Solovey A, Hebbel RP (2000a) Origins of circulating endothelial outgrowth from blood. J Clin Invest 105:71–77PubMedCrossRef
go back to reference Lin Y, Weisdorf DJ et al (2000b) Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest 105(1):71–77PubMedCrossRef Lin Y, Weisdorf DJ et al (2000b) Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest 105(1):71–77PubMedCrossRef
go back to reference Lin Y, Chang L et al (2002) Use of blood outgrowth endothelial cells for gene therapy for hemophilia A. Blood 99(2):457–462PubMedCrossRef Lin Y, Chang L et al (2002) Use of blood outgrowth endothelial cells for gene therapy for hemophilia A. Blood 99(2):457–462PubMedCrossRef
go back to reference Mayes JS, Scheerer JB et al (1981) Differential assay for lysosomal alpha-galactosidases in human tissues and its application to Fabry's disease. Clin Chim Acta 112(2):247–251PubMedCrossRef Mayes JS, Scheerer JB et al (1981) Differential assay for lysosomal alpha-galactosidases in human tissues and its application to Fabry's disease. Clin Chim Acta 112(2):247–251PubMedCrossRef
go back to reference Medin JA, Tudor M et al (1996) Correction in trans for Fabry disease: expression, secretion and uptake of alpha-galactosidase A in patient-derived cells driven by a high-titer recombinant retroviral vector. Proc Natl Acad Sci U S A 93(15):7917–7922PubMedCrossRef Medin JA, Tudor M et al (1996) Correction in trans for Fabry disease: expression, secretion and uptake of alpha-galactosidase A in patient-derived cells driven by a high-titer recombinant retroviral vector. Proc Natl Acad Sci U S A 93(15):7917–7922PubMedCrossRef
go back to reference Moore DF, Scott LT et al (2001) Regional cerebral hyperperfusion and nitric oxide pathway dysregulation in Fabry disease: reversal by enzyme replacement therapy. Circulation 104(13):1506–1512PubMedCrossRef Moore DF, Scott LT et al (2001) Regional cerebral hyperperfusion and nitric oxide pathway dysregulation in Fabry disease: reversal by enzyme replacement therapy. Circulation 104(13):1506–1512PubMedCrossRef
go back to reference Moore DF, Kaneski CR et al (2007) The cerebral vasculopathy of Fabry disease. J Neurol Sci 257(1–2):258–263PubMedCrossRef Moore DF, Kaneski CR et al (2007) The cerebral vasculopathy of Fabry disease. J Neurol Sci 257(1–2):258–263PubMedCrossRef
go back to reference Nguyen TT, Gin T et al (2005) Ophthalmological manifestations of Fabry disease: a survey of patients at the Royal Melbourne Fabry Disease Treatment Centre. Clin Experiment Ophthalmol 33(2):164–168PubMedCrossRef Nguyen TT, Gin T et al (2005) Ophthalmological manifestations of Fabry disease: a survey of patients at the Royal Melbourne Fabry Disease Treatment Centre. Clin Experiment Ophthalmol 33(2):164–168PubMedCrossRef
go back to reference Parkkila S, Parkkila AK et al (1993) Competitive time-resolved immunofluorometric assay for quantifying carbonic anhydrase VI in saliva. Clin Chem 39(10):2154–2157PubMed Parkkila S, Parkkila AK et al (1993) Competitive time-resolved immunofluorometric assay for quantifying carbonic anhydrase VI in saliva. Clin Chem 39(10):2154–2157PubMed
go back to reference Prabakaran T, Nielsen R et al (2011) Receptor-Mediated Endocytosis of alpha-Galactosidase A in Human Podocytes in Fabry Disease. PLoS One 6(9):e25065PubMedCrossRef Prabakaran T, Nielsen R et al (2011) Receptor-Mediated Endocytosis of alpha-Galactosidase A in Human Podocytes in Fabry Disease. PLoS One 6(9):e25065PubMedCrossRef
go back to reference Rafii S, Lyden D (2003) Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 9(6):702–712PubMedCrossRef Rafii S, Lyden D (2003) Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 9(6):702–712PubMedCrossRef
go back to reference Sakuraba H, Murata-Ohsawa M et al (2006) Comparison of the effects of agalsidase alfa and agalsidase beta on cultured human Fabry fibroblasts and Fabry mice. J Hum Genet 51(3):180–188PubMedCrossRef Sakuraba H, Murata-Ohsawa M et al (2006) Comparison of the effects of agalsidase alfa and agalsidase beta on cultured human Fabry fibroblasts and Fabry mice. J Hum Genet 51(3):180–188PubMedCrossRef
go back to reference Schiffmann R, Murray GJ et al (2000) Infusion of alpha-galactosidase A reduces tissue globotriaosylceramide storage in patients with Fabry disease. Proc Natl Acad Sci U S A 97(1):365–370PubMedCrossRef Schiffmann R, Murray GJ et al (2000) Infusion of alpha-galactosidase A reduces tissue globotriaosylceramide storage in patients with Fabry disease. Proc Natl Acad Sci U S A 97(1):365–370PubMedCrossRef
go back to reference Schiffmann R, Kopp JB et al (2001) Enzyme replacement therapy in Fabry disease: a randomized controlled trial. Jama 285(21):2743–2749PubMedCrossRef Schiffmann R, Kopp JB et al (2001) Enzyme replacement therapy in Fabry disease: a randomized controlled trial. Jama 285(21):2743–2749PubMedCrossRef
go back to reference Schiffmann R, Rapkiewicz A et al (2006) Pathological findings in a patient with Fabry disease who died after 2.5 years of enzyme replacement. Virchows Arch 448(3):337–343PubMedCrossRef Schiffmann R, Rapkiewicz A et al (2006) Pathological findings in a patient with Fabry disease who died after 2.5 years of enzyme replacement. Virchows Arch 448(3):337–343PubMedCrossRef
go back to reference Shen JS, Meng XL et al (2007) Establishment and characterization of Fabry disease endothelial cells with an extended lifespan. Mol Genet Metab 92(1–2):137–144PubMedCrossRef Shen JS, Meng XL et al (2007) Establishment and characterization of Fabry disease endothelial cells with an extended lifespan. Mol Genet Metab 92(1–2):137–144PubMedCrossRef
go back to reference Sheppard MN, Cane P et al (2010) A detailed pathologic examination of heart tissue from three older patients with Anderson-Fabry disease on enzyme replacement therapy. Cardiovasc Pathol 19(5):293–301PubMedCrossRef Sheppard MN, Cane P et al (2010) A detailed pathologic examination of heart tissue from three older patients with Anderson-Fabry disease on enzyme replacement therapy. Cardiovasc Pathol 19(5):293–301PubMedCrossRef
go back to reference Sleat DE, Wang Y et al (2006) Identification and validation of mannose 6-phosphate glycoproteins in human plasma reveal a wide range of lysosomal and non-lysosomal proteins. Mol Cell Proteomics 5(10):1942–1956PubMedCrossRef Sleat DE, Wang Y et al (2006) Identification and validation of mannose 6-phosphate glycoproteins in human plasma reveal a wide range of lysosomal and non-lysosomal proteins. Mol Cell Proteomics 5(10):1942–1956PubMedCrossRef
go back to reference Sodi A, Ioannidis AS et al (2007) Ocular manifestations of Fabry's disease: data from the Fabry outcome survey. Br J Ophthalmol 91(2):210–214PubMedCrossRef Sodi A, Ioannidis AS et al (2007) Ocular manifestations of Fabry's disease: data from the Fabry outcome survey. Br J Ophthalmol 91(2):210–214PubMedCrossRef
go back to reference Speert DP, Silverstein SC (1985) Phagocytosis of unopsonized zymosan by human monocyte-derived macrophages: maturation and inhibition by mannan. J Leukoc Biol 38(5):655–658PubMed Speert DP, Silverstein SC (1985) Phagocytosis of unopsonized zymosan by human monocyte-derived macrophages: maturation and inhibition by mannan. J Leukoc Biol 38(5):655–658PubMed
go back to reference Synnes M, Prydz K et al (1999) Fluid phase endocytosis and galactosyl receptor-mediated endocytosis employ different early endosomes. Biochim Biophys Acta 1421(2):317–328PubMedCrossRef Synnes M, Prydz K et al (1999) Fluid phase endocytosis and galactosyl receptor-mediated endocytosis employ different early endosomes. Biochim Biophys Acta 1421(2):317–328PubMedCrossRef
go back to reference Takamatsu S, Fukuta K et al (2003) Monitoring biodistribution of glycoproteins with modified sugar chains. Biochim Biophys Acta 1622(3):179–191PubMedCrossRef Takamatsu S, Fukuta K et al (2003) Monitoring biodistribution of glycoproteins with modified sugar chains. Biochim Biophys Acta 1622(3):179–191PubMedCrossRef
go back to reference Thurberg BL, Randolph Byers H et al (2004) Monitoring the 3-year efficacy of enzyme replacement therapy in fabry disease by repeated skin biopsies. J Invest Dermatol 122(4):900–908PubMedCrossRef Thurberg BL, Randolph Byers H et al (2004) Monitoring the 3-year efficacy of enzyme replacement therapy in fabry disease by repeated skin biopsies. J Invest Dermatol 122(4):900–908PubMedCrossRef
go back to reference Wagner SJ, Myrup AC (2005) Toward closed-system culture of blood origin endothelial cells. Transfusion 45(7):1201–1207PubMedCrossRef Wagner SJ, Myrup AC (2005) Toward closed-system culture of blood origin endothelial cells. Transfusion 45(7):1201–1207PubMedCrossRef
go back to reference Wang CH, Cherng WJ et al (2008) Late-outgrowth endothelial cells attenuate intimal hyperplasia contributed by mesenchymal stem cells after vascular injury. Arterioscler Thromb Vasc Biol 28(1):54–60PubMedCrossRef Wang CH, Cherng WJ et al (2008) Late-outgrowth endothelial cells attenuate intimal hyperplasia contributed by mesenchymal stem cells after vascular injury. Arterioscler Thromb Vasc Biol 28(1):54–60PubMedCrossRef
go back to reference Wilcox WR (2004) Lysosomal storage disorders: the need for better pediatric recognition and comprehensive care. J Pediatr 144(5 Suppl):S3–S14PubMed Wilcox WR (2004) Lysosomal storage disorders: the need for better pediatric recognition and comprehensive care. J Pediatr 144(5 Suppl):S3–S14PubMed
go back to reference Wilcox WR, Banikazemi M et al (2004) Long-term safety and efficacy of enzyme replacement therapyfor fabry disease. Am J Hum Genet 75(1):65–74PubMedCrossRef Wilcox WR, Banikazemi M et al (2004) Long-term safety and efficacy of enzyme replacement therapyfor fabry disease. Am J Hum Genet 75(1):65–74PubMedCrossRef
go back to reference Wu X, Robinson CE et al (1995) Cloning and characterization of the murine activin receptor like kinase-1 (ALK-1) homolog. Biochem Biophys Res Commun 216(1):78–83PubMedCrossRef Wu X, Robinson CE et al (1995) Cloning and characterization of the murine activin receptor like kinase-1 (ALK-1) homolog. Biochem Biophys Res Commun 216(1):78–83PubMedCrossRef
Metadata
Title
Lysosomal delivery of therapeutic enzymes in cell models of Fabry disease
Authors
D. Marchesan
T. M. Cox
P. B. Deegan
Publication date
01-11-2012
Publisher
Springer Netherlands
Published in
Journal of Inherited Metabolic Disease / Issue 6/2012
Print ISSN: 0141-8955
Electronic ISSN: 1573-2665
DOI
https://doi.org/10.1007/s10545-012-9472-3

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