Lysosomal storage diseases: From pathophysiology to therapy

Annual Review of Medicine

Volumn 66, Issue , 2015, Pages 471-486

  Parenti, Giancarlo ^a,b   Andria, Generoso ^b   Ballabio, Andrea ^a,b,c,d  

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

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d TEXAS CHILDREN S HOSPITAL   (United States)

Author keywords

enzyme replacement therapy; gene therapy; pharmacological chaperone therapy; proteostasis regulators; substrate reduction therapy

Indexed keywords

CHAPERONE; ENZYME;

ARTICLE; ENZYME REPLACEMENT; GENE THERAPY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; LYSOSOME STORAGE DISEASE; PATHOPHYSIOLOGY; PATIENT CARE; PRIORITY JOURNAL; PROTEIN HOMEOSTASIS; GENETICS; LYSOSOMAL STORAGE DISEASES; METABOLISM;

ENZYME REPLACEMENT THERAPY; GENETIC THERAPY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; LYSOSOMAL STORAGE DISEASES; MOLECULAR CHAPERONES;

EID: 84921324921     PISSN: 00664219     EISSN: 1545326X     Source Type: Book Series    
DOI: 10.1146/annurev-med-122313-085916     Document Type: Article

References (91)

1. Braulke T, Bonifacino JS. 2009. Sorting of lysosomal proteins. Biochim. Biophys. Acta 1793:605-14
2. ReczekD, Schwake M, Schroder J, et al. 2007. LIMP-2 is a receptor for lysosomalmannose-6-phosphateindependent targeting of β-glucocerebrosidase. Cell 131:770-83
3. Lieberman AP, Puertollano R, Raben N, et al. 2012. Autophagy in lysosomal storage disorders. Autophagy8:719-30
4. Sancak Y, Bar-Peled L, Zoncu R, et al. 2010. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141:290-303
5. Zoncu R, Bar-Peled L, Efeyan A, et al. 2011. mTORC1 senses lysosomal amino acids through an insideout mechanism that requires the vacuolar H+-ATPase. Science 334:678-83
6. Sardiello M, Palmieri M, di Ronza A, et al. 2009. A gene network regulating lysosomal biogenesis and function. Science 325:473-77
7. Settembre C, Zoncu R, Medina DL, et al. 2012. A lysosome-To-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J. 31:1095-108
8. Fuller M, Meikle PJ, Hopwood JJ. 2006. Epidemiology of lysosomal storage diseases: an overview. In Fabry Disease: Perspectives from 5 Years of FOS, ed. A Mehta, M Beck, G Sunder-Plassmann. Oxford: Oxford PharmaGenesis. http://www.ncbi.nlm.nih.gov/pubmed/21290699
9. Nascimbeni AC, Fanin M, Masiero E, et al. 2012. The role of autophagy in the pathogenesis of glycogen storage disease type II (GSDII). Cell Death Differ. 19:1698-708
10. Shea L, Raben N. 2009. Autophagy in skeletal muscle: implications for Pompe disease. Int. J. Clin. Pharmacol. Ther. 47(Suppl. 1):S42-47
11. Settembre C, Fraldi A, Jahreiss L, et al. 2008. A block of autophagy in lysosomal storage disorders. Hum. Mol. Genet. 17:119-29
12. Lloyd-Evans E, Morgan AJ, He X, et al. 2008. Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat. Med. 14:1247-55
13. Fraldi A, Annunziata F, Lombardi A, et al. 2010. Lysosomal fusion and SNARE function are impaired by cholesterol accumulation in lysosomal storage disorders. EMBO J. 29:3607-20
14. Neudorfer O, Giladi N, Elstein D, et al. 1996. Occurrence of Parkinson's syndrome in type I Gaucher disease. QJM 89:691-94
15. Aharon-Peretz J, Rosenbaum H, Gershoni-Baruch R. 2004. Mutations in the glucocerebrosidase gene and Parkinson's disease in Ashkenazi Jews. N. Engl. J. Med. 351:1972-77
16. Dehay B, Martinez-Vicente M, Caldwell GA, et al. 2013. Lysosomal impairment in Parkinson's disease. Mov. Disord. 28:725-32
17. Dehay B, Martinez-Vicente M, Ramirez A, et al. 2012. Lysosomal dysfunction in Parkinson disease: ATP13A2 gets into the groove. Autophagy 8:1389-91
18. Settembre C, Fraldi A, Medina DL, Ballabio A. 2013. Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat. Rev. Mol. Cell Biol. 14:283-96
19. SlyWS, Fischer HD. 1982. The phosphomannosyl recognition system for intracellular and intercellular transport of lysosomal enzymes. J. Cell. Biochem. 18:67-85
20. BartonNW, Brady RO, Dambrosia JM, et al. 1991. Replacement therapy for inherited enzyme deficiency-macrophage-Targeted glucocerebrosidase for Gaucher's disease. N. Engl. J. Med. 324:1464-70
21. Barton NW, Furbish FS, Murray GJ, et al. 1990. Therapeutic response to intravenous infusions of glucocerebrosidase in a patient with Gaucher disease. Proc. Natl. Acad. Sci. USA 87:1913-16
22. Eng CM, Guffon N, WilcoxWR, et al. 2001. Safety and efficacy of recombinant human a-galactosidase A replacement therapy in Fabry's disease. N. Engl. J. Med. 345:9-16
23. Schiffmann R, Kopp JB, Austin HA 3rd, et al. 2001. Enzyme replacement therapy in Fabry disease: a randomized controlled trial. JAMA 285:2743-49
24. Van den Hout H, Reuser AJ, Vulto AG, et al. 2000. Recombinant human α-glucosidase from rabbit milk in Pompe patients. Lancet 356:397-98
25. Kakkis ED, Muenzer J, Tiller GE, et al. 2001. Enzyme-replacement therapy in mucopolysaccharidosis I. N. Engl. J. Med. 344:182-88
26. Muenzer J, Wraith JE, Beck M, et al. 2006. A phase II/III clinical study of enzyme replacement therapy with idursulfase in mucopolysaccharidosis II (Hunter syndrome). Genet. Med. 8:465-73
27. Harmatz P, Giugliani R, Schwartz I, 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, openlabel extension study. J. Pediatr. 148:533-39
28. Brady RO. 2006. Enzyme replacement for lysosomal diseases. Annu. Rev. Med. 57:283-96
29. Lachmann RH. 2011. Enzyme replacement therapy for lysosomal storage diseases. Curr. Opin. Pediatr. 23:588-93
30. Wraith JE. 2006. Limitations of enzyme replacement therapy: current and future. J. Inherit. Metab. Dis. 29:442-47
31. Parenti G, Andria G. 2011. Pompe disease: from new views on pathophysiology to innovative therapeutic strategies. Curr. Pharm. Biotechnol. 12:902-15
32. Prater SN, Banugaria SG, DeArmey SM, et al. 2012. The emerging phenotype of long-Term survivors with infantile Pompe disease. Genet. Med. 14:800-10
33. Wyatt K, Henley W, Anderson L, et al. 2012. The effectiveness and cost-effectiveness of enzyme and substrate replacement therapies: a longitudinal cohort study of people with lysosomal storage disorders. Health Technol. Assess. 16(39):1-543
34. Anson DS, McIntyre C, Byers S. 2011. Therapies for neurological disease in the mucopolysaccharidoses. Curr. Gene Ther. 11:132-43
35. Begley DJ, Pontikis CC, Scarpa M. 2008. Lysosomal storage diseases and the blood-brain barrier. Curr. Pharm. Des. 14:1566-80
36. Grubb JH, Vogler C, Levy B, et al. 2008. Chemically modifiedβ-glucuronidase crosses blood-brain barrier and clears neuronal storage in murine mucopolysaccharidosis VII. Proc. Natl. Acad. Sci. USA 105:2616-21
37. HuynhHT, Grubb JH, Vogler C, SlyWS. 2012. Biochemical evidence for superior correction of neuronal storage by chemically modified enzyme in murine mucopolysaccharidosis VII. Proc. Natl. Acad. Sci. USA 109:17022-27
38. Boado RJ, Zhang Y, Zhang Y, et al. 2008. Genetic engineering, expression, and activity of a chimeric monoclonal antibody-Avidin fusion protein for receptor-mediated delivery of biotinylated drugs in humans. Bioconjug. Chem. 19:731-39
39. Osborn MJ, McElmurry RT, Peacock B, et al. 2008. Targeting of the CNS in MPS-IH using a nonviral transferrin-α-L-iduronidase fusion gene product. Mol. Ther. 16:1459-66
40. Zhou QH, Boado RJ, Lu JZ, et al. 2012. Brain-penetrating IgG-iduronate 2-sulfatase fusion protein for the mouse. Drug Metab. Dispos. 40:329-35
41. Bockenhoff A, Cramer S, Wolte P, et al. 2014. Comparison of five peptide vectors for improved brain delivery of the lysosomal enzyme arylsulfatase A. J. Neurosci. 34:3122-29
42. Meng Y, Sohar I, Sleat DE, et al. 2014. Effective intravenous therapy for neurodegenerative disease with a therapeutic enzyme and a peptide that mediates delivery to the brain. Mol. Ther. 22:547-53
43. Sorrentino NC, D'Orsi L, Sambri I, et al. 2013. A highly secreted sulphamidase engineered to cross the blood-brain barrier corrects brain lesions of mice with mucopolysaccharidoses type IIIA. EMBO Mol. Med. 5:675-90
44. Kakkis E, McEntee M, Vogler C, et al. 2004. Intrathecal enzyme replacement therapy reduces lysosomal storage in the brain and meninges of the canine model of MPS I. Mol. Genet. Metab. 83:163-74
45. Dickson P, McEntee M, Vogler C, et al. 2007. Intrathecal enzyme replacement therapy: successful treatment of brain disease via the cerebrospinal fluid. Mol. Genet. Metab. 91:61-68
46. Auclair D, Finnie J, White J, et al. 2010. Repeated intrathecal injections of recombinant human 4-sulphatase remove dural storage in mature mucopolysaccharidosis VI cats primed with a short-course tolerisation regimen. Mol. Genet. Metab. 99:132-41
47. Auclair D, Finnie J, Walkley SU, et al. 2012. Intrathecal recombinant human 4-sulfatase reduces accumulation of glycosaminoglycans in dura of mucopolysaccharidosis VI cats. Pediatr. Res. 71:39-45
48. Munoz-Rojas MV, Vieira T, Costa R, et al. 2008. Intrathecal enzyme replacement therapy in a patient with mucopolysaccharidosis type I and symptomatic spinal cord compression. Am. J. Med. Genet. A 146A:2538-44
49. Zhu Y, Li X, Kyazike J, et al. 2004. Conjugation of mannose 6-phosphate-containing oligosaccharides to acid α-glucosidase improves the clearance of glycogen in Pompe mice. J. Biol. Chem. 279:50336-41
50. Tiels P, Baranova E, Piens K, et al. 2012. A bacterial glycosidase enables mannose-6-phosphate modification and improved cellular uptake of yeast-produced recombinant human lysosomal enzymes. Nat. Biotechnol. 30:1225-31
51. Zhou Q, Stefano JE, Harrahy J, et al. 2011. Strategies for Neoglycan conjugation to human acid α-glucosidase. Bioconjug. Chem. 22:741-51
52. Maga JA, Zhou J, Kambampati R, et al. 2013. Glycosylation-independent lysosomal targeting of acid α-glucosidase enhances muscle glycogen clearance in Pompe mice. J. Biol. Chem. 288:1428-38
53. Hsu J, Northrup L, Bhowmick T, Muro S. 2012. Enhanced delivery of α-glucosidase for Pompe disease by ICAM-1-Targeted nanocarriers: comparative performance of a strategy for three distinct lysosomal storage disorders. Nanomedicine 8:731-39
54. Hsu J, Bhowmick T, Burks SR, et al. 2014. Enhancing biodistribution of therapeutic enzymes in vivo by modulating surface coating and concentration of ICAM-1-Targeted nanocarriers. J. Biomed. Nanotechnol. 10:345-54
55. Koeberl DD, Austin S, Case LE, et al. 2014. Adjunctive albuterol enhances the response to enzyme replacement therapy in late-onset Pompe disease. FASEB J. 28:2171-76
56. Farah BL, Madden L, Li S, et al. 2014. Adjunctive β2-Agonist treatment reduces glycogen independently of receptor-mediated acid α-glucosidase uptake in the limb muscles of mice with Pompe disease. FASEB J. 28:2272-80
57. Ponder KP. 2008. Immune response hinders therapy for lysosomal storage diseases. J. Clin. Investig. 118:2686-89
58. Banugaria SG, Prater SN, Patel TT, et al. 2013. Algorithm for the early diagnosis and treatment of patients with cross reactive immunologic material-negative classic infantile Pompe disease: a step towards improving the efficacy of ERT. PLOS ONE 8:e67052
59. Banugaria SG, Prater SN, McGann JK, et al. 2013. Bortezomib in the rapid reduction of high sustained antibody titers in disorders treated with therapeutic protein: lessons learned from Pompe disease. Genet. Med. 15:123-31
60. Zimran A, Brill-Almon E, Chertkoff R, et al. 2011. Pivotal trial with plant cell-expressed recombinant glucocerebrosidase, taliglucerase alfa, a novel enzyme replacement therapy for Gaucher disease. Blood 118:5767-73
61. Reggi S, Marchetti S, Patti T, et al. 2005. Recombinant human acid β-glucosidase stored in tobacco seed is stable, active and taken up by human fibroblasts. Plant Mol. Biol. 57:101-13
62. Martiniuk F, Reggi S, Tchou-Wong KM, et al. 2013. Production of a functional human acid maltase in tobacco seeds: biochemical analysis, uptake by human GSDII cells, and in vivo studies in GAA knockout mice. Appl. Biochem. Biotechnol. 171:916-26
63. Patti T, Bembi B, Cristin P, et al. 2012. Endosperm-specific expression of human acid beta-glucosidase in a waxy rice. Rice 5:34
64. Orchard PJ, Blazar BR, Wagner J, et al. 2007. Hematopoietic cell therapy for metabolic disease. J. Pediatr. 151:340-46
65. Boelens JJ, Prasad VK, Tolar J, et al. 2010. Current international perspectives on hematopoietic stem cell transplantation for inherited metabolic disorders. Pediatr. Clin. North Am. 57:123-45
66. Parenti G, Fecarotta S, Moracci M, Andria G. 2014. Pharmacological chaperone therapy for lysosomal storage diseases. Future Med. Chem. 6:1031-45
67. Parenti G. 2009. Treating lysosomal storage diseases with pharmacological chaperones: from concept to clinics. EMBO Mol. Med. 1:268-79
68. Valenzano KJ, Khanna R, Powe AC, et al. 2011. Identification and characterization of pharmacological chaperones to correct enzyme deficiencies in lysosomal storage disorders. Assay Drug Dev. Technol. 9:213-35
69. Shen JS, Edwards NJ, Hong YB, Murray GJ. 2008. Isofagomine increases lysosomal delivery of exogenous glucocerebrosidase. Biochem. Biophys. Res. Commun. 369:1071-75
70. Porto C, Cardone M, Fontana F, et al. 2009. The pharmacological chaperone N-butyldeoxynojirimycin enhances enzyme replacement therapy in Pompe disease fibroblasts. Mol. Ther. 17:964-71
71. Porto C, Pisani A, Rosa M, et al. 2012. Synergy between the pharmacological chaperone 1-deoxygalactonojirimycin and the human recombinant alpha-galactosidase A in cultured fibroblasts from patients with Fabry disease. J. Inherit. Metab. Dis. 35:513-20
72. Benjamin ER, Khanna R, Schilling A, et al. 2012. Co-Administration with the pharmacological chaperone AT1001 increases recombinant human α-galactosidase A tissue uptake and improves substrate reduction in Fabry mice. Mol. Ther. 20:717-26
73. Khanna R, Flanagan JJ, Feng J, et al. 2012. The pharmacological chaperoneAT2220 increases recombinant human acidα-glucosidase uptake and glycogen reduction in amousemodel of Pompe disease. PLOS ONE 7:e40776
74. Parenti G, Fecarotta S, la Marca G, et al. 2014. A chaperone enhances blood α-glucosidase activity in Pompe disease patients treated with enzyme replacement therapy. Mol. Ther. 22:2004-12
75. Mu TW, Ong DS, Wang YJ, et al. 2008. Chemical and biological approaches synergize to ameliorate protein-folding diseases. Cell 134:769-81
76. Song W, Wang F, Savini M, et al. 2013. TFEB regulates lysosomal proteostasis. Hum. Mol. Genet. 22:1994-2009
77. Ong DS, Wang YJ, Tan YL. 2013. FKBP10 depletion enhances glucocerebrosidase proteostasis in Gaucher disease fibroblasts. Chem. Biol. 20:403-15
78. Platt FM, Jeyakumar M. 2008. Substrate reduction therapy. Acta Paediatr. 97(Suppl.): 88-93
79. Schiffmann R. 2010. Agalsidase treatment for Fabry disease: uses and rivalries. Genet. Med. 12:684-85
80. Cox T, Lachmann R, Hollak C, et al. 2000. Novel oral treatment of Gaucher's disease with N-butyldeoxynojirimycin (OGT 918) to decrease substrate biosynthesis. Lancet 355:1481-85
81. Patterson MC, Vecchio D, Prady H, et al. 2007. Miglustat for treatment of Niemann-Pick C disease: a randomised controlled study. Lancet Neurol. 6:765-72
82. Lukina E, Watman N, Arreguin EA, et al. 2010. Improvement in hematological, visceral, and skeletal manifestations of Gaucher disease type 1 with oral eliglustat tartrate (Genz-112638) treatment: 2-year results of a phase 2 study. Blood 116:4095-98
83. Piotrowska E, Jakobkiewicz-Banecka J, Tylki-Szymanska A, et al. 2008. Genistin-rich soy isoflavone extract in substrate reduction therapy for Sanfilippo syndrome: an open-label, pilot study in 10 pediatric patients. Curr. Ther. Res. Clin. Exp. 69:166-79
84. Sands MS, Davidson BL. 2006. Gene therapy for lysosomal storage diseases. Mol. Ther. 13:839-49
85. Biffi A, Montini E, Lorioli L, et al. 2013. Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science 341:1233158
86. RabenN, Schreiner C, Baum R, et al. 2010. Suppression of autophagy permits successful enzyme replacement therapy in a lysosomal storage disorder-murine Pompe disease. Autophagy 6:1078-89
87. Medina DL, Fraldi A, Bouche V, et al. 2011. Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev. Cell 21:421-30
88. Spampanato C, Feeney E, Li L, et al. 2013. Transcription factor EB (TFEB) is a new therapeutic target for Pompe disease. EMBO Mol. Med. 5:691-706
89. Williams IM, Wallom KL, Smith DA, et al. 2014. Improved neuroprotection using miglustat, curcumin and ibuprofen as a triple combination therapy in Niemann-Pick disease type C1 mice. Neurobiol. Dis. 67:9-17
90. Kirkegaard T, Roth AG, Petersen NH, et al. 2010. Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-Associated lysosomal pathology. Nature 463:549-53
91. Petersen NH, Kirkegaard T. 2010. HSP70 and lysosomal storage disorders: novel therapeutic opportunities. Biochem. Soc. Trans. 38:1479-83