Mucopolysaccharidosis III (Sanfilippo Syndrome)-Disease presentation and experimental therapies

Pediatric Endocrinology Reviews

Volumn 12, Issue , 2014, Pages 133-140

  Gilkes, Janine A ^a   Heldermon, Coy D ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Gene therapy; MPS III; Mucopolysaccharidosis; Sanfilippo Syndrome; Stem cell

Indexed keywords

ACETYL COENZYME A; ACETYL COENZYME A ACETYLTRANSFERASE; ALPHA N ACETYLGLUCOSAMINIDASE; GENISTEIN; HEPARAN SULFATE;

ADULTHOOD; ARTICLE; DEATH; DEGENERATIVE DISEASE; ENZYME DEGRADATION; ENZYME REPLACEMENT; ENZYME SUBSTRATE; EXPERIMENTAL THERAPY; GENE THERAPY; GROWTH RETARDATION; HUMAN; LYSOSOME STORAGE DISEASE; MUCOPOLYSACCHARIDOSIS; NONHUMAN; NONVIRAL GENE THERAPY; PATHOPHYSIOLOGY; SANFILIPPO SYNDROME; STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; REVIEW;

ENZYME REPLACEMENT THERAPY; GENETIC THERAPY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; MUCOPOLYSACCHARIDOSIS III; THERAPIES, INVESTIGATIONAL;

EID: 84908238501     PISSN: 15654753     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (111)

1. De Ruijter, J., J Valstar, M. & A Wijburg, E Mucopolysaccharidosis type III (Sanfilippo syndrome): emerging treatment strategies. Curr. Pharm. Biotechnol. 12, (2011)923-930
2. Buhrman, D., Thakkar, K., Poe, M. & Escolar, M. L. Natural history of Sanfilippo syndrome type A. J. Inherit. Metab. Dis. (2013). doi: 10.1007/S10545-013-9661-9668
3. Van de Kamp, J. J., Niermeijer, M. F., von Figura, K. & Giesberts, M. A. Genetic heterogeneity and clinical variability in the Sanfilippo syndrome (types A, B, and C). Clin. Genet. 20, (1981)152-160
4. Valstar, M. J., Ruijter, G. J. G., van Diggelen, O. P., Poorthuis, B. J. & Wijburg, F. A. Sanfilippo syndrome: a mini-review. J. Inherit. Metab. Dis. 31, 240-252 (2008)
5. Baehner, F., Schmiedeskamp, C, Krummenauer, F., Miebach, E., Bajbouj, M., Whybra, C, Kohlschütter, A., Kampmann, C. & Beck, M. Cumulative incidence rates of the mucopolysaccharidoses in Germany. J. Inherit. Metab. Dis. 28, (2005)1011-1017
6. Yogalingam, G. & Hopwood, J. J. Molecular genetics of mucopolysaccharidosis type IIIA and IIIB: Diagnostic, clinical, and biological implications. Hum. Mutat. 18, (2001)264-281
7. Geary, M. A. & Wraith, J. E. Management of mucopolysaccharidosis type III. Arch. Dis. Child. 69, (1993)403-406
8. Bax, M. C. & Colville, G. A. Behaviour in mucopolysaccharide disorders. Arch. Dis. Child. 73, (1995)77-81
9. Meyer, A., Kossow, K., Gal, A., Miihlhausen, C, Ullrich, K., Braulke, T. & Muschol, N. Scoring Evaluation of the Natural Course of Mucopolysaccharidosis Type IIIA (Sanfilippo Syndrome Type A). Pediatrics 120, (2007)e1255-e1261
10. Muenzer, J. Mucopolysaccharidoses. Adv. Pediatr. 33, (1986)269-302
11. Blackwell, P. B. & Baker, B. M. Estimating communication competence of infants and toddlers. J. Pediatr. Health Care Off. Publ. Natl. Assoc. Pediatr. Nurse Assoc. Pract. 16, (2002)29-35
12. WHO Multicentre Growth Reference Study Group. WHO Motor Development Study: windows of achievement for six gross motor development milestones. Acta Paediatr. Oslo Nor. 1992 Suppl. 450, (2006)86-95
13. Wolañczyk, T, Banaszkiewicz, A., Mierzewska, H., Czartoryska, B. & Zdziennicka, E. [Hyperactivity and behavioral disorders in Sanfilippo A (mucopolysaccharidosis type IIIA)-case report and review of the literature]. Psychiatr. Pol. 34, (2000)831-837
14. MESOLELLA, M., CIMMINO, M., CANTONE, E., MARINO, A., COZZOLINO, M., DELLA CASA, R., PARENTI, G. & IENGO, M. Management of otolaryngological manifestations in mucopolysaccharidoses: our experience. Acta Otorhinolaryngol. Ital. 33, (2013)267-272
15. Moog, U., van Mierlo, I., van Schrojenstein Lantman-de Valk, H. M. J., Spaapen, L, Maaskant, M. A. & Curfs, L. M. G. Is Sanfilippo type B in your mind when you see adults with mental retardation and behavioral problems? Am. J. Med. Genet. C Semin. Med. Genet. 145C, (2007)293-301
16. Heron, B., Mikaeloff, Y., Froissart, R., Caridade, G., Maire, I., Caillaud, C, Levade, T., Chabrol, B., Feillet, F, Ogier, H., Valayannopoulos, V., Michelakakis, H., Zafeiriou, D., Lavery, L., Wraith, E., Danos, O., Heard, J.-M. & Tardieu, M. Incidence and natural history of mucopolysaccharidosis type III in France and comparison with United Kingdom and Greece. Am. J. Med. Genet. A. 155A, (2011)58-68
17. Li, H. H., Zhao, H. Z., Neufeld, E. F, Cai, Y. & Gomez-Pinilla, F. Attenuated plasticity in neurons and astrocytes in the mouse model of Sanfilippo syndrome type B. J. Neurosci. Res. 69, (2002)30-38
18. Ohmi, K., Zhao, H.-Z. & Neufeld, E. F. Defects in the Medial Entorhinal Cortex and Dentate Gyrus in the Mouse Model of Sanfilippo Syndrome Type B. PLoS ONE 6, (2011)e27461
19. Bellettato, C. M. & Scarpa, M. Pathophysiology of neuropathic lysosomal storage disorders. J. Inherit. Metab. Dis. 33, 347-362 (2010)
20. Walkley, S. U. Pathogenic cascades in lysosomal disease-Why so complex? J. Inherit. Metab. Dis. 32, (2009)181-189
21. Jolly, R. D., Johnstone, A. C, Norman, E. J., Hopwood, J. J. & Walkley, S. U. Pathology of Mucopolysaccharidosis IIIA in Huntaway Dogs. Vet. Pathol. Online 44, (2007)569-578
22. Wilkinson, F. L, Holley, R. J., Langford-Smith, K. J., Badrinath, S., Liao, A., Langford-Smith, A., Cooper, J. D., Jones, S. A., Wraith, J. E., Wynn, R. F, Merry, C. L. R. & Bigger, B. W. Neuropathology in Mouse Models of Mucopolysaccharidosis Type I, IIIA and IIIB. PLoS ONE 7, (2012)e35787
23. Ohmi, K., Greenberg, D. S., Rajavel, K. S., Ryazantsev, S., Li, H. H. & Neufeld, E. F. Activated microglia in cortex of mouse models of mucopolysaccharidoses I and IIIB. Proc. Natl. Acad. Sci. 100, (2003)1902-1907
24. Killedar, S., DiRosario, J., Divers, E., Popovich, P. G., McCarty, D. M. & Fu, H. Research Mucopolysaccharidosis IIIB, a lysosomal storage disease, triggers a pathogenic CNS autoimmune. (2010). at http://www.biomedcentral.com/content/pdf/1742-2094-7-39.pdf
25. Villani, G. R., Chierchia, A., Di Napoli, D. & Di Natale, P. Unfolded protein response is not activated in the mucopolysaccharidoses but protein disulfide isomerase 5 is deregulated. J. Inherit. Metab. Dis. 1(2012)15
26. Lieberman, A. P., Puertollano, R., Raben, N., Slaugenhaupt, S., Walkley, S. U. & Ballabio, A. Autophagy in lysosomal storage disorders. Autophagy8, (2012)0-1
27. Fukuda, T, Ewan, L., Bauer, M., Mattaliano, R. J., Zaal, K., Ralston, E., Plotz, P. H. & Raben, N. Dysfunction of endocytic and autophagic pathways in a lysosomal storage disease. Ann. Neurol. 59, (2006)700-708
28. Villani, G. R. D., Domenico, C. D., Musella, A., Cecere, F, Napoli, D. D. & Natale, P. D. Mucopolysaccharidosis IIIB: Oxidative damage and cytotoxic cell involvement in the neuronal pathogenesis. Brain Res. 1279, (2009)99-108
29. Villani, G. R. D., Gargiulo, N., Faraonio, R., Castaldo, S., Gonzalez y Reyero, E. & Di Natale, P. Cytokines, neurotrophins, and oxidative stress in brain disease from mucopolysaccharidosis IIIB. J. Neurosci. Res. 85, (2007)612-622
30. Tamagawa, K., Morimatsu, Y., Fujisawa, K., Hara, A. & Taketomi, T. Neuropathological study and chemico-pathoiogical correlation in sibling cases of Sanfilippo syndrome type B. Brain Dev. 7, (1985)599-609
31. McGlynn, R., Dobrenis, K. & Walkley, S. U. Differential subcellular localization of cholesterol, gangliosides, and glycosaminoglycans in murine models of mucopolysaccharide storage disorders. J. Comp. Neurol. 480, (2004)415-426
32. Vitry, S., Bruyère, J., Hocquemiller, M., Bigou, S., Ausseil, J., Colle, M.-A., Prévost, M.-C. & Heard, J. M. Storage Vesicles in Neurons Are Related to Golgi Complex Alterations in Mucopolysaccharidosis IIIB. Am. J. Pathol. 177, (2010)2984-2999
33. Constantopoulos, G., Iqbal, K. & Dekaban, A. S. Mucopolysaccharidosis Types IH, IS, II and IIIA: Glycosaminoglycans and Lipids of Isolated Brain Cells and Other Fractions from Autopsied Tissues. J. Neurochem. 34, (1980)1399-1411
34. Ginsberg, S. D., Galvin, J. E., Lee, V. M., Rorke, L. B., Dickson, D. W., Wolfe, J. H., Jones, M. Z. & Trojanowski, J. Q. Accumulation of intracellular amyloid-beta peptide (A beta 1-40) in mucopolysaccharidosis brains. J. Neuropathol. Exp. Neurol. 58, (1999)815-824
35. Ohmi, K., Kudo, L. C, Ryazantsev, S., Zhao, H.-Z., Karsten, S. L. & Neufeld, E. F. Sanfilippo syndrome type B, a lysosomal storage disease, is also a tauopathy. Proc. Natl. Acad. Sci. 106, (2009)8332-8337
36. Winder-Rhodes, S. E., Garcia-Reitbock, P., Ban, M., Evans, J. R., Jacques, T. S., Kemppinen, A., Foltynie, T., Williams-Gray, C. H., Chinnery, P. F, Hudson, G., Burn, D. J., Allcock, L. M., Sawcer, S. J., Barker, R. A. & Spillantini, M. G. Genetic and pathological links between Parkinson's disease and the lysosomal disorder Sanfilippo syndrome. Mov. Disord. 27, (2012)312-315
37. Hamano, K., Hayashi, M., Shioda, K., Fukatsu, R. & Mizutani, S. Mechanisms of neurodegeneration in mucopolysaccharidoses II and IIIB: analysis of human brain tissue. Acta Neuropathol. (Berl.) 115, (2008)547-559
38. Naughton, B. J., Duncan, F. J., Murrey, D., Ware, T., Meadows, A., McCarty, D. M. & Fu, H. Amyloidosis, Synucleinopathy, and Prion Encephalopathy in a Neuropathic Lysosomal Storage Disease: The CNS-Biomarker Potential of Peripheral Blood. PloS One 8, (2013)e80142
39. Huang, Y. & Mucke, L. Alzheimer mechanisms and therapeutic strategies. Cell 148, (2012)1204-1222
40. De Felice, F. G. & Ferreira, S. T. Beta-amyloid production, aggregation, and clearance as targets for therapy in Alzheimer's disease. Cell. Mol. Neurobiol. 22, (2002)545-563
41. Manzoni, C. & Lewis, P. A. Dysfunction of the autophagy/lysosomal degradation pathway is a shared feature of the genetic synucleinopathies. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 27, (2013)3424-3429
42. Dickson, D. W. Parkinson's disease and parkinsonism: neuropathology. Cold Spring Harb. Perspect. Med. 2, (2012)
43. Kumar, K. R., Djarmati-Westenberger, A. & Grùnewald, A. Genetics of Parkinson's disease. Semin. Neurol. 31, (2011)433-440
44. Fu, H., Bartz, J. D., Stephens, R. L., Jr & McCarty, D. M. Peripheral nervous system neuropathology and progressive sensory impairments in a mouse model of Mucopolysaccharidosis IIIB. PloS One 7, (2012) e45992
45. Capila, I. & Linhardt, R. J. Heparin-protein interactions. Angew. Chem. Int. Ed Engl. 41, (2002)391-412
46. Bishop, J. R., Schuksz, M. & Esko, J. D. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446, (2007)1030-1037
47. Bernfield, M., Gotte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincecum, J. & Zako, M. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, (1999)729-777
48. Hacker, U., Nybakken, K. & Perrimon, N. Heparan sulphate proteoglycans: the sweet side of development. Nat. Rev. Mol. Cell Biol. 6, (2005)530-541
49. Jackson, R. L., Busch, S. J. & Cardin, A. D. Glycosaminoglycans: molecular properties, protein interactions, and role in physiological processes. Physiol. Rev. 71, (1991)481-539
50. Dawson, G., Fuller, M., Helmsley, K. M. & Hopwood, J. J. Abnormal Gangliosides are Localized in Lipid Rafts in Sanfilippo (MPS3a) Mouse Brain. Neurochem. Res. 37, (2012)1372-1380
51. Walkley, S. U. Secondary accumulation of gangliosides in lysosomal storage disorders, in Semin. Cell Dev. Biol. 15, (2004)433-444
52. Avila, J. L. & Convit, J. Inhibition of leucocytic lysosomal enzymes by glycosaminoglycans in vitro. Biochem. J. 152, (1975)57-64
53. Walkley, S. U., Siegel, D. A. & Dobrenis, K. GM2 ganglioside and pyramidal neuron dendritogenesis. Neurochem. Res. 20, (1995)1287-1299
54. Ryazantsev, S., Yu, W.-H., Zhao, H.-Z., Neufeld, E. F. & Ohmi, K. Lysosomal Accumulation of SCMAS (Subunit c of Mitochondrial ATP Synthase) in Neurons of the Mouse Model of Mucopolysaccharidosis III B. Mol. Genet. Metab. 90, (2007)393-401
55. Fraldi, A., Annunziata, F., Lombardi, A., Kaiser, H.-J., Medina, D. L., Spampanato, C, Fedele, A. O., Polishchuk, R., Sorrentino, N. C. & Simons, K. Lysosomal fusion'and SNARE function are impaired by cholesterol accumulation in lysosomal storage disorders. EMBO J. 29, (2010)3607-3620
56. Walkley, S. U. & Vanier, M. T. Secondary lipid accumulation in lysosomal disease. Biochim. Biophys. Acta 1793, (2009)726-736
57. Simons, K. & Gruenberg, J. Jamming the endosomal system: lipid rafts and lysosomal storage diseases. Trends Cell Biol. 10, (2000)459-462
58. Ausseil, J., Desman's, N., Bigou, S., Attali, R., Corbineau, S., Vitry, S., Parent, M., Cheillan, D., Fuller, M., Maire, I., Vanier, M.-T. & Heard, J.-M. Early Neurodegeneration Progresses Independently of Microglial Activation by Heparan Sulfate in the Brain of Mucopolysaccharidosis IIIB Mice. PLoS ONE 3, (2008)e2296
59. Crawley, A. C, Gliddon, B. L., Auclair, D., Brodie, S. L., Hirte, C, King, B. M., Fuller, M., Hemsley, K. M. & Hopwood, J. J. Characterization of a C57BL/6 congenic mouse strain of mucopolysaccharidosis type IIIA. Brain Res. 1104, (2006)1-17
60. DiRosario, J., Divers, E., Wang, C, Etter, J., Charrier, A., Jukkola, P., Auer, H., Best, V., Newsom, D. L., McCarty, D. M. & Fu, H. Innate and adaptive immune activation in the brain of MPS IIIB mouse model. J. Neurosci. Res. 87, (2009)978-990
61. Savas, P. S., Hemsley, K. M. & Hopwood, J. J. Intracerebral injection of sulfamidase delays neuropathology in murine MPS-IIIA. Mol. Genet. Metab. 82, (2004)273-285
62. Brady, R. O. Enzyme Replacement for Lysosomal Diseases. Annu. Rev. Med. 57, (2006)283-296
63. Neufeld, E. F. in Fabry Dis. Perspect. 5 Years FOS (Mehta, A., Beck, M. & Sunder-Plassmann, G.) (Oxford PharmaGenesis, 2006). at http://www.ncbi.nlm.nih.gov/books/NBK11588/
64. Vogler, C, Levy, B., Galvin, N. J., Thorpe, C, Sands, M. S., Barker, J. E., Baty, J., Birkenmeier, E. H. & Sly, W. S. Enzyme replacement in murine mucopolysaccharidosis type VII: neuronal and glial response to beta-glucuronidase requires early initiation of enzyme replacement therapy. Pediatr. Res.45, (1999)838-844
65. Yu, W. H., Zhao, K. W., Ryazantsev, S., Rozengurt, N. & Neufeld, E. F. Short-term enzyme replacement in the murine model of Sanfilippo syndrome type B. Mol. Genet. Metab. 71, (2000)573-580
66. Kan, S.-H., Troitskaya, L. A., Sinow, C. S., Haitz, K., Todd, A. K., Di Stefano, A., Le, S. Q., Dickson, P. I. & Tippin, B. L Insulin-like growth factor II peptide fusion enables uptake and lysosomal delivery of a-N-acetylglucosaminidase to mucopolysaccharidosis type IIIB fibroblasts. Biochem. J. 458, (2014)281-289
67. Synageva BioPharma(TM) to Present at the 32(nd) Annual J.P. Morgan Healthcare Conference-WSJ.com. at http://online.wsj.com/article/PR-CO-20140102-904257.html
68. Hemsley, K. M., King, B. & Hopwood, J. J. Injection of recombinant human sulfamidase into the CSF via the cerebellomedullary cistern in MPS IIIA mice. Mol. Genet. Metab. 90, (2007)313-328
69. Hemsley, K. M., Norman, E. J., Crawley, A. C, Auclair, D., King, B., Fuller, M., Lang, D. L., Dean, C. J., Jolly, R. D. & Hopwood, J. J. Effect of cisternal sulfamidase delivery in MPS IIIA Huntaway dogs-a proof of principle study. Mol. Genet. Metab. 98, (2009)383-392
70. Felice, B. R., Wright, T. L., Boyd, R. B., Butt, M. T., Pfeifer, R. W., Pan, J., Ruiz, J. A., Heartlein, M. W. & Calias, P. Safety evaluation of chronic intrathecal administration of idursulfase-IT in cynomolgus monkeys. Toxicol. Pathol. 39, (2011)879-892
71. Vera, M., Le, S., Kan, S.-H., Garban, H., Naylor, D., Mlikotic, A., Kaitila, I., Harmatz, P., Chen, A. & Dickson, P. Immune response to intrathecal enzyme replacement therapy in mucopolysaccharidosis I patients. Pediatr. Res. 74, (2013) 712-720
72. Muenzer, J. Overview of the mucopolysaccharidoses. Rheumatology 50, (2011)v4-v12
73. Peters, C, Steward, C. G., National Marrow Donor Program, International Bone Marrow Transplant Registry Et Working Party on Inborn Errors, European Bone Marrow Transplant Group. Hematopoietic cell transplantation for inherited metabolic diseases: an overview of outcomes and practice guidelines. Bone Marrow Transplant. 31, (2003)229-239
74. Krivit, W, Sung, J. H., Shapiro, E. G. & Lockman, L. A. Microglia: the effector cell for reconstitution of the central nervous system following bone marrow transplantation for lysosomal and peroxisomal storage diseases. Cell Transplant. 4, (1995)385-392
75. Shapiro, E. G., Lockman, L. A., Balthazor, M. & Krivit, W. Neuropsychological outcomes of several storage diseases with and without bone marrow transplantation. J. Inherit. Metab. Dis. 18, (1995)413-429
76. Sivakumur, P. & Wraith, J. E. Bone marrow transplantation in mucopolysaccharidosis type IIIA: a comparison of an early treated patient with his untreated sibling. J. Inherit. Metab. Dis. 22, (1999)849-850
77. Heldermon, C. D., Ohlemiller, K. K., Herzog, E. D., Vogler, C, Qin, E., Wozniak, D. F, Tan, Y., Orrock, J. L. & Sands, M. S. Therapeutic Efficacy of Bone Marrow Transplant, Intracranial AAV-mediated Gene Therapy, or Both in the Mouse Model of MPS IIIB. Mol. Ther. 18, (2010)873-880
78. Langford-Smith, A., Wilkinson, F. L., Langford-Smith, K. J., Holley, R. J., Sergijenko, A., Howe, S. J., Bennett, W. R., Jones, S. A., Wraith, J., Merry, C. L., Wynn, R. F. & Bigger, B. W. Hematopoietic Stem Cell and Gene Therapy Corrects Primary Neuropathology and Behavior in Mucopolysaccharidosis IIIA Mice. Mol. Ther. 20, (2012)1610-1621
79. Lau, A. A., Hannouche, H., Rozaklis, T., Hassiotis, S., Hopwood, J. J. & Hemsley, K. M. Allogeneic stem cell transplantation does not improve neurological deficits in mucopolysaccharidosis type IIIA mice. Exp. Neurol. 225, (2010)445-454
80. Prasad, V. K., Mendizabal, A., Parikh, S. H., Szabolcs, P., Driscoll, T. A., Page, K., Lakshminarayanan, S., Allison, J., Wood, S., Semmel, D., Escolar, M. L., Martin, P. L., Carter, S. & Kurtzberg, J. Unrelated donor umbilical cord blood transplantation for inherited metabolic disorders in 159 pediatric patients from a single center: influence of cellular composition of the graft on transplantation outcomes. Blood 112, (2008)2979-2989
81. Willing, A. E., Garbuzova-Davis, S. N., Zayko, O., Derasari, H. M., Rawls, A. E., James, C. R., Mervis, R. F, Sanberg, C. D., Kuzmin-Nichols, N. & Sanberg, P. R. Repeated Administrations of Human Umbilical Cord Blood Cells Improve Disease Outcomes in a Mouse Model of Sanfilippo Syndrome Type III B. Cell Transplant. (2013). doi: 10.3727/096368913X676916
82. Husain, A. M., Escolar, M. L. & Kurtzberg, J. Neurophysiology assessment of mucopolysaccharidosis III. Clin. Neurophysiol. Off. J. Int. Fed. Clin. Neurophysiol. 117, (2006)2059-2063
83. Sands, M. S. & Davidson, B. L. Gene therapy for lysosomal storage diseases. Mol. Ther. J. Am. Soc. Gene Ther. 13, (2006)839-849
84. Daly, T. M. & Sands, M. S. Gene therapy for lysosomal storage diseases. Expert Opin. Investig. Drugs 7, (1998)1673-1682
85. Byrne, B. J., Falk, D. J., Clement, N. & Mah, C. S. Gene Therapy Approaches for Lysosomal Storage Disease: Next-Generation Treatment. Hum. Gene Ther. 23, (2012)808-815
86. Zheng, Y., Ryazantsev, S., Ohmi, K., Zhao, H. Z., Rozengurt, N., Kohn, D. B. & Neufeld, E. F. Retrovirally transduced bone marrow has a therapeutic effect on brain in the mouse model of mucopolysaccharidosis 1MB. Mol. Genet. Metab. 82, (2004)286-295
87. Ponder, K. P. & Haskins, M. E. Gene therapy for mucopolysaccharidosis. Expert Opin. Biol. Ther. 7, (2007)1333-1345
88. Fraldi, A., Hemsley, K., Crawley, A., Lombardi, A., Lau, A., Sutherland, L, Auricchio, A., Ballabio, A. & Hopwood, J. J. Functional correction of CNS lesions in an MPS-IIIA mouse model by intracerebral AAV-mediated delivery of sulfamidase and SUMF1 genes. Hum. Mol. Genet. 16, (2007)2693-2702
89. Fu, H., Kang, L, Jennings, J. S., Moy, S. S., Perez, A., Dirosario, J., McCarty, D. M. & Muenzer, J. Significantly increased lifespan and improved behavioral performances by rAAV gene delivery in adult mucopolysaccharidosis IIIB mice. Gene Ther. 14, (2007)1065-1077
90. Cressant, A., Desman's, N., Verot, L, Bréjot, T., Froissart, R., Vanier, M. T, Maire, I. & Heard, J. M. Improved behavior and neuropathology in the mouse model of Sanfilippo type IIIB disease after adeno-associated virus-mediated gene transfer in the striatum. J. Neurosa. 24, 1(2004)0229-10239
91. Fu, H. Neurological Correction of Lysosomal Storage in a Mucopolysaccharidosis IIIB Mouse Model by Adeno-associated Virus-Mediated Gene Delivery. Mol. Ther. 5, (2002) 42-49
92. Haurigot, V., Marcó, S., Ribera, A., Garcia, M., Ruzo, A., Villacampa, P., Ayuso, E., Añor, S., Andaluz, A., Pineda, M., García-Fructuoso, G., Molas, M., Maggioni, L., Muñoz, S., Motas, S., Ruberte, J., Mingozzi, F, Pumarola, M. & Bosch, F. Whole body correction of mucopolysaccharidosis IIIA by intracerebrospinal fluid gene therapy. J. Clin. Invest. (2013). doi:10.1172/JCI66778
93. Heldermon, C. D., Qjn, E. Y., Ohlemiller, K. K., Herzog, E. D., Brown, J. R., Vogler, C, Hou, W., Orrock, J. L., Crawford, B. E. & Sands, M. S. Disease correction by combined neonatal intracranial AAV and systemic lentiviral gene therapy in Sanfilippo Syndrome type B mice. Gene Ther. 20, (2013)913-921
94. Mclntyre, C, Byers, S. & Anson, D. S. Correction of mucopolysaccharidosis type IIIA somatic and central nervous system pathology by lentiviral-mediated gene transfer. J. Gene Med. 12, 7(2010)17-728
95. Di Domenico, C, Viilani, G. R. D., Di Napoli, D., Nusco, E., Cali, G., Nitsch, L. & Di Natale, P. Intracranial gene delivery of LV-NAGLU vector corrects neuropathology in murine MPS IIIB. Am. J. Med. Genet. A. 149A, (2009)1209-1218
96. Ruzo, A., Marcó, S., García, M., Villacampa, P., Ribera, A., Ayuso, E., Maggioni, L., Mingozzi, R, Haurigot, V. & Bosch, F. Correction of Pathological Accumulation of Glycosaminoglycans in Central Nervous System and Peripheral Tissues of MPSIIIA Mice Through Systemic AAV9 Gene Transfer. Hum. Gene Ther. 23, (2012)1237-1246
97. Fu, H., DiRosario, J., Killedar, S., Zaraspe, K. & McCarty, D. M. Correction of Neurological Disease of Mucopolysaccharidosis IIIB in Adult Mice by rAAV9 Trans-Blood-Brain Barrier Gene Delivery. Mol. Ther. 19, 1025-1033 (2011)
98. Tardieu, M., Zerah, M., Husson, B., de Bournonville, S., Deiva, K., Adamsbaum, C, Vincent, F., Hocquemiller, M., Broissand, C, Furlan, V., Ballabio, A., Fraldi, A., Crystal, R., Baugnon, T., Roujeau, T., Heard, J. & Danos, O. Intracerebral administration of AAV rh.10 carrying human SGSH and SUMF1 cDNAs in children with MPSIIIA disease: results of a phase l/ll trial. Hum. Gene Ther. 140213093236007 (2014). doi:10.1089/hum.2013.238
99. Ellinwood, N. M., Ausseil, J., Desmaris, N., Bigou, S., Liu, S., Jens, J. K., Snella, E. M., Mohammed, E. E., Thomson, C. B., Raoul, S., Joussemet, B., Roux, F., Cherel, Y., Lajat, Y., Piraud, M., Benchaouir, R., Hermening, S., Petry, H., Froissart, R., Tardieu, M., Ciron, C, Moullier, P., Parkes, J., Kline, K. L., Maire, I., Vanier, M.-T, Heard, J.-M. & Colle, M.-A. Safe, Efficient, and Reproducible Gene Therapy of the Brain in the Dog Models of Sanfilippo and Hurler Syndromes. Mol. Ther. 19, (2011)251-259
100. Malinowska, M., Wilkinson, F. L, Bennett, W., Langford-Smith, K. J., O'Leary, H. A., Jakobkiewicz-Banecka, J., Wynn, R., Wraith, J. E., Wegrzyn, G. & Bigger, B. W. Genistein reduces lysosomal storage in peripheral tissues of mucopolysaccharide IIIB mice. Mol. Genet. Metab. 98, 235-242 (2009)
101. Jakobkiewicz-Banecka, J., Wegrzyn, A. & Wegrzyn, G. Substrate deprivation therapy: a new hope for patients suffering from neuronopathic forms of inherited lysosomal storage diseases. J. Appl. Genet. 48, (2007)383-388
102. Tsai, T.-H. Concurrent measurement of unbound genistein in the blood, brain and bile of anesthetized rats using microdialysis and its pharmacokinetic application. J. Chromatogr. A1073, (2005)317-322
103. Roberts, A. L. K., Thomas, B. J., Wilkinson, A. S., Fletcher, J. M. & Byers, S. Inhibition of glycosaminoglycan synthesis using rhodamine B in a mouse model of mucopolysaccharidosis type IIIA. Pediatr. Res. 60, (2006)309-314
104. Roberts, A. L. K., Rees, M. H., Klebe, S., Fletcher, J. M. & Byers, S. Improvement in behaviour after substrate deprivation therapy with rhodamine B in a mouse model of MPS IIIA. Mol. Genet. Metab. 92, (2007)115-121
105. Piotrowska, E., Jakobkiewicz-Banecka, J., Baraiiska, S., Tylki-Szymanska, A., Czartoryska, B., Wegrzyn, A. & Wegrzyn, G. Genistein-mediated inhibition of glycosaminoglycan synthesis as a basis for gene expression-targeted isoflavone therapy for mucopolysaccharidoses. Eur. J. Hum. Genet. EJHG 14, (2006)846-852
106. Malinowska, M., Wilkinson, F. L, Langford-Smith, K. J., Langford-Smith, A., Brown, J. R., Crawford, B. E., Vanier, M. T, Grynkiewicz, G., Wynn, R. E, Wraith, J. E., Wegrzyn, G. & Bigger, B. W. Genistein Improves Neuropathology and Corrects Behaviour in a Mouse Model of Neurodegenerative Metabolic Disease. PLoS ONE 5, (2010)e14192
107. Piotrowska, E., Jakobkiewicz-Banecka, J., Tylki-Szymanska, A., Liberek, A., Maryniak, A., Malinowska, M., Czartoryska, B., Puk, E., Kloska, A., Liberek, T., Baranska, S., Wegrzyn, A. & Wegrzyn, G. Genistin-rich soy isoflavone extract in substrate reduction therapy for Sanfilippo syndrome: An open-label, pilot study in 10 pediatric patients. Curr. Ther. Res. 69, (2008)166-179
108. Delgadillo, V., O'Callaghan, M. D. M., Artuch, R., Montero, R. & Pineda, M. Genistein supplementation in patients affected by Sanfilippo disease. J. Inherit. Metab. Dis. 34, (2011)1039-1044
109. De Ruijter, J., Valstar, M. J., Narajczyk, M., Wegrzyn, G., Kulik, W., Ulst, L., Wagemans, I, van der Wal, W. M. & Wijburg, F. A. Genistein in Sanfilippo disease: A randomized controlled crossover trial. Ann. Neurol. 71, (2012)110-120
110. Piotrowska, E., Jakobkiewicz-Banecka, J., Maryniak, A., Tylki-Szymanska, A., Puk, E., Liberek, A., Wegrzyn, A., Czartoryska, B., Slominska-Wojewodzka, M. & Wegrzyn, G. Two-year follow-up of Sanfilippo Disease patients treated with a genistein-rich isoflavone extract: assessment of effects on cognitive functions and general status of patients. Med. Sci. Monit. Int. Med. J. Exp. Clin. Res. 17, (2011)CR196-202
111. Kim, K. H., Dodsworth, C, Paras, A. & Burton, B. K. High dose genistein aglycone therapy is safe in patients with mucopolysaccharidoses involving the central nervous system. Mol. Genet. Metab. 109, (2013)382-385