A highly secreted sulphamidase engineered to cross the blood-brain barrier corrects brain lesions of mice with mucopolysaccharidoses type IIIA

EMBO Molecular Medicine

Volumn 5, Issue 5, 2013, Pages 675-690

  Sorrentino, Nicolina Cristina ^a   D'Orsi, Luca ^a   Sambri, Irene ^a   Nusco, Edoardo ^a   Monaco, Ciro ^a   Spampanato, Carmine ^a   Polishchuk, Elena ^b   Saccone, Paola ^a   De Leonibus, Elvira ^a,b   Ballabio, Andrea ^a,c,d,e   Fraldi, Alessandro ^a  

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

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

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e TEXAS CHILDREN S HOSPITAL   (United States)

Author keywords

Blood brain barrier; CNS therapy; Lysosomal storage disorders; MPS IIIA; Sulphamidase

Indexed keywords

APOLIPOPROTEIN B; ENZYME; PARVOVIRUS VECTOR; SIGNAL PEPTIDE; SULPHAMIDASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME RELEASE; FEMALE; GENE TRANSFER; LIVER; MALE; MOUSE; MUCOPOLYSACCHARIDOSIS; NONHUMAN; PRIORITY JOURNAL; SANFILIPPO SYNDROME TYPE A;

ANIMALS; APOLIPOPROTEINS B; BLOOD-BRAIN BARRIER; BRAIN; CELL LINE; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; IDURONATE SULFATASE; LIVER; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MUCOPOLYSACCHARIDOSIS III; PHENOTYPE; PROTEIN ENGINEERING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SERINE ENDOPEPTIDASES; TRANSCYTOSIS;

EID: 84877596293     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201202083     Document Type: Article

References (36)

1. Atwal JK, Chen Y, Chiu C, Mortensen DL, Meilandt WJ, Liu Y, Heise CE, Hoyte K, Luk W, Lu Y, et al (2011) A therapeutic antibody targeting BACE1 inhibits amyloid-beta production in vivo. Sci Transl Med 3: 84ra43
2. Bhattacharyya R, Gliddon B, Beccari T, Hopwood JJ, Stanley P (2001) A novel missense mutation in lysosomal sulfamidase is the basis of MPS III A in a spontaneous mouse mutant. Glycobiology 11: 99- 103
3. Bhaumik M, Muller VJ, Rozaklis T, Johnson L, Dobrenis K, Bhattacharyya R, Wurzelmann S, Finamore P, Hopwood JJ, Walkley SU, et al (1999) A mouse model for mucopolysaccharidosis type III A (Sanfilippo syndrome). Glycobiology 9: 1389- 1396
4. Blanz J, Stroobants S, Lullmann-Rauch R, Morelle W, Ludemann M, D'Hooge R, Reuterwall H, Michalski JC, Fogh J, Andersson C, et al (2008) Reversal of peripheral and central neural storage and ataxia after recombinant enzyme replacement therapy in alpha-mannosidosis mice. Hum Mol Genet 17: 3437- 3445
5. Boren J, Lee I, Zhu W, Arnold K, Taylor S, Innerarity TL (1998) Identification of the low density lipoprotein receptor-binding site in apolipoprotein B100 and the modulation of its binding activity by the carboxyl terminus in familial defective apo-B100. J Clin Invest 101: 1084- 1093
6. Brady RO, Schiffmann R (2004) Enzyme-replacement therapy for metabolic storage disorders. Lancet Neurol 3: 752- 756
7. Brown MS, Goldstein JL (1986) A receptor-mediated pathway for cholesterol homeostasis. Science 232: 34- 47
8. Brunetti-Pierri N, Ng P (2011) Helper-dependent adenoviral vectors for liver-directed gene therapy. Hum Mol Genet 20: R7- R13
9. Chen YH, Chang M, Davidson BL (2009) Molecular signatures of disease brain endothelia provide new sites for CNS-directed enzyme therapy. Nat Med 15: 1215- 1218
10. Crawley AC, Gliddon BL, Auclair D, Brodie SL, Hirte C, King BM, Fuller M, Hemsley KM, Hopwood JJ (2006) Characterization of a C57BL/6 congenic mouse strain of mucopolysaccharidosis type IIIA. Brain Res 1104: 1- 17
11. Fraldi A, Annunziata F, Lombardi A, Kaiser HJ, Medina DL, Spampanato C, Fedele AO, Polishchuk R, Sorrentino NC, Simons K, et al (2010) Lysosomal fusion and SNARE function are impaired by cholesterol accumulation in lysosomal storage disorders. EMBO J 29: 3607- 3620
12. Fraldi A, Hemsley K, Crawley A, Lombardi A, Lau A, Sutherland L, Auricchio A, Ballabio A, Hopwood JJ (2007) 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: 2693- 2702
13. Gliddon BL, Hopwood JJ (2004) Enzyme-replacement therapy from birth delays the development of behavior and learning problems in mucopolysaccharidosis type IIIA mice. Pediatr Res 56: 65- 72
14. Grubb JH, Vogler C, Levy B, Galvin N, Tan Y, Sly WS (2008) Chemically modified beta-glucuronidase crosses blood-brain barrier and clears neuronal storage in murine mucopolysaccharidosis VII. Proc Natl Acad Sci USA 105: 2616- 2621
15. Hemsley KM, Beard H, King BM, Hopwood JJ (2008) Effect of high dose, repeated intra-CSF injection of sulphamidase on neuropathology in MPS IIIA mice. Genes Brain Behav 7: 740- 753
16. Hemsley KM, Hopwood JJ (2005) Development of motor deficits in a murine model of mucopolysaccharidosis type IIIA (MPS-IIIA). Behav Brain Res 158: 191- 199
17. Hemsley KM, King B, Hopwood JJ (2007) Injection of recombinant human sulfamidase into the CSF via the cerebellomedullary cistern in MPS IIIA mice. Mol Genet Metab 90: 313- 328
18. Langford-Smith A, Langford-Smith KJ, Jones SA, Wynn RF, Wraith JE, Wilkinson FL, Bigger BW (2011) Female mucopolysaccharidosis IIIA mice exhibit hyperactivity and a reduced sense of danger in the open field test. PLoS ONE 6: e25717
19. Lau AA, Hopwood JJ, Kremer EJ, Hemsley KM (2010) SGSH gene transfer in mucopolysaccharidosis type IIIA mice using canine adenovirus vectors. Mol Genet Metab 100: 168- 175
20. Mingozzi F, High KA (2011) Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet 12: 341- 355
21. Nathwani AC, Tuddenham EG, Rangarajan S, Rosales C, McIntosh J, Linch DC, Chowdary P, Riddell A, Pie AJ, Harrington C, et al (2011) Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N Engl J Med 365: 2357- 2365
22. Pardridge WM (2002a) Drug and gene delivery to the brain: the vascular route. Neuron 36: 555- 558
23. Pardridge WM (2002b) Targeting neurotherapeutic agents through the blood-brain barrier. Arch Neurol 59: 35- 40
24. Pardridge WM (2005) Molecular biology of the blood-brain barrier. Mol Biotechnol 30: 57- 70
25. Polito VA, Cosma MP (2009) IDS crossing of the blood-brain barrier corrects CNS defects in MPSII mice. Am J Hum Genet 85: 296- 301
26. Rozaklis T, Beard H, Hassiotis S, Garcia AR, Tonini M, Luck A, Pan J, Lamsa JC, Hopwood JJ, Hemsley KM (2011) Impact of high-dose, chemically modified sulfamidase on pathology in a murine model of MPS IIIA. Exp Neurol 230: 123- 130
27. Ruzo A, Garcia M, Ribera A, Villacampa P, Haurigot V, Marco S, Ayuso E, Anguela XM, Roca C, Agudo J, et al (2012) Liver production of sulfamidase reverses peripheral and ameliorates CNS pathology in mucopolysaccharidosis IIIA mice. Mol Ther: J Am Soc Gene Ther 20: 254- 266
28. Savas PS, Hemsley KM, Hopwood JJ (2004) Intracerebral injection of sulfamidase delays neuropathology in murine MPS-IIIA. Mol Genet Metab 82: 273- 285
29. Settembre C, Fraldi A, Jahreiss L, Spampanato C, Venturi C, Medina D, de Pablo R, Tacchetti C, Rubinsztein DC, Ballabio A (2008) A block of autophagy in lysosomal storage disorders. Hum Mol Genet 17: 119- 129
30. Spencer B, Marr RA, Gindi R, Potkar R, Michael S, Adame A, Rockenstein E, Verma IM, Masliah E (2011) Peripheral delivery of a CNS targeted, metalo-protease reduces abeta toxicity in a mouse model of Alzheimer's disease. PLoS ONE 6: e16575
31. Spencer BJ, Verma IM (2007) Targeted delivery of proteins across the blood-brain barrier. Proc Natl Acad Sci USA 104: 7594- 7599
32. Stefansson S, Chappell DA, Argraves KM, Strickland DK, Argraves WS (1995) Glycoprotein 330/low density lipoprotein receptor-related protein-2 mediates endocytosis of low density lipoproteins via interaction with apolipoprotein B100. J Biol Chem 270: 19417- 19421
33. Urayama A, Grubb JH, Sly WS, Banks WA (2004) Developmentally regulated mannose 6-phosphate receptor-mediated transport of a lysosomal enzyme across the blood-brain barrier. Proc Natl Acad Sci USA 101: 12658- 12663
34. Urayama A, Grubb JH, Sly WS, Banks WA, (2008) Mannose 6-phosphate receptor-mediated transport of sulfamidase across the blood-brain barrier in the newborn mouse. Mol Ther 16: 1261- 1266
35. Vogler C, Levy B, Grubb JH, Galvin N, Tan Y, Kakkis E, Pavloff N, Sly WS (2005) Overcoming the blood-brain barrier with high-dose enzyme replacement therapy in murine mucopolysaccharidosis VII. Proc Natl Acad Sci USA 102: 14777- 14782
36. Yu YJ, Zhang Y, Kenrick M, Hoyte K, Luk W, Lu Y, Atwal J, Elliott JM, Prabhu S, Watts RJ, et al (2011) Boosting brain uptake of a therapeutic antibody by reducing its affinity for a transcytosis target. Sci Transl Med 3: 84ra44