Sialic acid deposition impairs the utility of AAV9, but not peptide-modified AAVs for brain gene therapy in a mouse model of lysosomal storage disease

Molecular Therapy

Volumn 20, Issue 7, 2012, Pages 1393-1399

  Chen, Yong Hong ^a   Claflin, Kristin ^a   Geoghegan, James C ^a   Davidson, Beverly L ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED VIRUS SEROTYPE 9; BETA GLUCURONIDASE; PARVOVIRUS VECTOR; SIALIC ACID; UNCLASSIFIED DRUG; VIROTHERAPY AGENT;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS 9; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; BRAIN FUNCTION; COGNITIVE DEFECT; CONFERENCE PAPER; CONTROLLED STUDY; ENZYME ACTIVITY; FEAR; FOOTSHOCK; FREEZING; HETEROZYGOSITY; HIPPOCAMPUS; LYSOSOME STORAGE DISEASE; MOUSE; MUCOPOLYSACCHARIDOSIS TYPE 7; NEUROPATHOLOGY; NONHUMAN; SEROTYPE; SURVIVAL RATE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIROTHERAPY; VIRUS CAPSID; VIRUS GENOME;

ADENO-ASSOCIATED VIRUS; ANIMALIA; MIRIDAE; MUS;

EID: 84863466713     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2012.100     Document Type: Conference Paper

References (46)

1. Fuller, M, Meikle, PJ. and Hopwood, JJ. In: Fabry Disease: Perspectives from 5 Years of FOS (eds. A. Mehta, M. Beck, and G. Sunder-Plassmann) (2006).
2. Biffi, A, De Palma, M, Quattrini, A, Del Carro, U, Amadio, S, Visigalli, I et al. (2004). Correction of metachromatic leukodystrophy in the mouse model by transplantation of genetically modified hematopoietic stem cells. J Clin Invest 113: 1118-1129. (Pubitemid 38544097)
3. Cartier, N, Hacein-Bey-Abina, S, Bartholomae, CC, Veres, G, Schmidt, M, Kutschera, I et al. (2009). Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326: 818-823.
4. Xu, S, Wang, L, El-Banna, M, Sohar, I, Sleat, DE and Lobel, P (2011). Large-volume intrathecal enzyme delivery increases survival of a mouse model of late infantile neuronal ceroid lipofuscinosis. Mol Ther 19: 1842-1848.
5. Kakkis, ED (2002). Enzyme replacement therapy for the mucopolysaccharide storage disorders. Expert Opin Investig Drugs 11: 675-685. (Pubitemid 34520617)
6. O'Connor, LH, Erway, LC, Vogler, CA, Sly, WS, Nicholes, A, Grubb, J et al. (1998). Enzyme replacement therapy for murine mucopolysaccharidosis type VII leads to improvements in behavior and auditory function. J Clin Invest 101: 1394-1400. (Pubitemid 28166837)
7. Chang, M, Cooper, JD, Sleat, DE, Cheng, SH, Dodge, JC, Passini, MA et al. (2008). Intraventricular enzyme replacement improves disease phenotypes in a mouse model of late infantile neuronal ceroid lipofuscinosis. Mol Ther 16: 649-656. (Pubitemid 351426165)
8. Sands, MS and Davidson, BL (2006). Gene therapy for lysosomal storage diseases. Mol Ther 13: 839-849.
9. Fratantoni, JC, Hall, CW and Neufeld, EF (1968). Hurler and Hunter syndromes: mutual correction of the defect in cultured fibroblasts. Science 162: 570-572.
10. Macauley, SL and Sands, MS (2009). Promising CNS-directed enzyme replacement therapy for lysosomal storage diseases. Exp Neurol 218: 5-8.
11. Liu, G, Martins, I, Wemmie, JA, Chiorini, JA and Davidson, BL (2005). Functional correction of CNS phenotypes in a lysosomal storage disease model using adeno-associated virus type 4 vectors. J Neurosci 25: 9321-9327. (Pubitemid 41464744)
12. Foust, KD, Nurre, E, Montgomery, CL, Hernandez, A, Chan, CM and Kaspar, BK (2009). Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 27: 59-65.
13. Cearley, CN, Vandenberghe, LH, Parente, MK, Carnish, ER, Wilson, JM and Wolfe, JH (2008). Expanded repertoire of AAV vector serotypes mediate unique patterns of transduction in mouse brain. Mol Ther 16: 1710-1718.
14. Fu, H, Dirosario, J, Killedar, S, Zaraspe, K and McCarty, DM (2011). Correction of neurological disease of mucopolysaccharidosis IIIB in adult mice by rAAV9 trans-bloodbrain barrier gene delivery. Mol Ther 19: 1025-1033.
15. Chen, YH, Chang, M and Davidson, BL (2009). Molecular signatures of disease brain endothelia provide new sites for CNS-directed enzyme therapy. Nat Med 15: 1215-1218.
16. Büning, H, Perabo, L, Coutelle, O, Quadt-Humme, S and Hallek, M (2008). Recent developments in adeno-associated virus vector technology. J Gene Med 10: 717-733. (Pubitemid 352003915)
17. Grifman, M, Trepel, M, Speece, P, Gilbert, LB, Arap, W, Pasqualini, R et al. (2001). Incorporation of tumor-targeting peptides into recombinant adeno-associated virus capsids. Mol Ther 3: 964-975. (Pubitemid 32611306)
18. Work, LM, Büning, H, Hunt, E, Nicklin, SA, Denby, L, Britton, N et al. (2006). Vascular bed-targeted in vivo gene delivery using tropism-modified adeno-associated viruses. Mol Ther 13: 683-693.
19. Sly, WS, Quinton, BA, McAlister, WH and Rimoin, DL (1973). Beta glucuronidase deficiency: report of clinical, radiologic, and biochemical features of a new mucopolysaccharidosis. J Pediatr 82: 249-257.
20. Neufeld, EF and Muenzer, J. In: Part 16: Lysosomal Storage Disoders (eds Beaudet Valle, Vogelshtein, Kinnzler, Antonarakis, Balabio) (Schriver, Online, 2011).
21. Shen, S, Bryant, KD, Brown, SM, Randell, SH and Asokan, A (2011) Terminal N-linked galactose is the primary receptor for adeno-associated virus 9. J Biol Chem 286: 13532-13540.
22. Bell, CL, Vandenberghe, LH, Bell, P, Limberis, MP, Gao, GP, Van Vliet, K et al. (2011). The AAV9 receptor and its modification to improve in vivo lung gene transfer in mice. J Clin Invest 121: 2427-2435.
23. Karolewski, BA and Wolfe, JH (2006). Genetic correction of the fetal brain increases the lifespan of mice with the severe multisystemic disease mucopolysaccharidosis type VII. Mol Ther 14: 14-24. (Pubitemid 43899484)
24. Daly, TM, Ohlemiller, KK, Roberts, MS, Vogler, CA and Sands, MS (2001). Prevention of systemic clinical disease in MPS VII mice following AAV-mediated neonatal gene transfer. Gene Ther 8: 1291-1298. (Pubitemid 32834297)
25. Balestrieri, ML and Napoli, C (2007). Novel challenges in exploring peptide ligands and corresponding tissue-specific endothelial receptors. Eur J Cancer 43: 1242-1250. (Pubitemid 46729702)
26. Hajitou, A, Pasqualini, R and Arap, W (2006). Vascular targeting: recent advances and therapeutic perspectives. Trends Cardiovasc Med 16: 80-88.
27. Burg, MA, Pasqualini, R, Arap, W, Ruoslahti, E and Stallcup, WB (1999). NG2 proteoglycan-binding peptides target tumor neovasculature. Cancer Res 59: 2869-2874. (Pubitemid 29283125)
28. Yabe, T, Hosoda-Yabe, R, Kanamaru, Y and Kiso, M (2011). A peptide found by phage display discriminates a specific structure of a trisaccharide in heparin. J Biol Chem 286: 12397-12406.
29. Wölcke, J and Weinhold, E (2001). A DNA-binding peptide from a phage display library. Nucleosides Nucleotides Nucleic Acids 20: 1239-1241. (Pubitemid 32821961)
30. Traving, C and Schauer, R (1998). Structure, function and metabolism of sialic acids. Cell Mol Life Sci 54: 1330-1349. (Pubitemid 29015295)
31. Michelfelder, S, Varadi, K, Raupp, C, Hunger, A, Körbelin, J, Pahrmann, C et al. (2011). Peptide ligands incorporated into the threefold spike capsid domain to re-direct gene transduction of AAV8 and AAV9 in vivo. PLoS ONE 6: e23101.
32. Varadi, K, Michelfelder, S, Korff, T, Hecker, M, Trepel, M, Katus, HA et al. (2011). Novel random peptide libraries displayed on AAV serotype 9 for selection of endothelial cell-directed gene transfer vectors. Gene Ther. (doi:10.1038/gt. 2011.143).
33. Frisella, WA, O'Connor, LH, Vogler, CA, Roberts, M, Walkley, S, Levy, B et al. (2001). Intracranial injection of recombinant adeno-associated virus improves cognitive function in a murine model of mucopolysaccharidosis type VII. Mol Ther 3: 351-358. (Pubitemid 32514651)
34. Renlund, M, Tietze, F and Gahl, WA (1986). Defective sialic acid egress from isolated fibroblast lysosomes of patients with Salla disease. Science 232: 759-762. (Pubitemid 16078721)
35. Tietze, F, Seppala, R, Renlund, M, Hopwood, JJ, Harper, GS, Thomas, GH et al. (1989). Defective lysosomal egress of free sialic acid (N-acetylneuraminic acid) in fibroblasts of patients with infantile free sialic acid storage disease. J Biol Chem 264: 15316-15322. (Pubitemid 19242897)
36. McCarty, DM, DiRosario, J, Gulaid, K, Killedar, S, Oosterhof, A, van Kuppevelt, TH et al. (2011). Differential distribution of heparan sulfate glycoforms and elevated expression of heparan sulfate biosynthetic enzyme genes in the brain of mucopolysaccharidosis IIIB mice. Metab Brain Dis 26: 9-19.
37. Vinogradova, MV, Michaud, L, Mezentsev, AV, Lukong, KE, El-Alfy, M, Morales, CR et al. (1998). Molecular mechanism of lysosomal sialidase deficiency in galactosialidosis involves its rapid degradation. Biochem J 330 (Pt 2): 641-650. (Pubitemid 28111957)
38. Rajotte, D, Arap, W, Hagedorn, M, Koivunen, E, Pasqualini, R and Ruoslahti, E (1998). Molecular heterogeneity of the vascular endothelium revealed by in vivo phage display. J Clin Invest 102: 430-437. (Pubitemid 28335203)
39. Kolonin, M, Pasqualini, R and Arap, W (2001). Molecular addresses in blood vessels as targets for therapy. Curr Opin Chem Biol 5: 308-313. (Pubitemid 32718528)
40. Arap, W, Kolonin, MG, Trepel, M, Lahdenranta, J, Cardó-Vila, M, Giordano, RJ et al. (2002). Steps toward mapping the human vasculature by phage display. Nat Med 8: 121-127. (Pubitemid 34155122)
41. Neuwelt, EA, Bauer, B, Fahlke, C, Fricker, G, Iadecola, C, Janigro, D et al. (2011). Engaging neuroscience to advance translational research in brain barrier biology. Nat Rev Neurosci 12: 169-182.
42. Zlokovic, BV (2011). Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat Rev Neurosci 12: 723-738.
43. Bevan, AK, Duque, S, Foust, KD, Morales, PR, Braun, L, Schmelzer, L et al. (2011). Systemic gene delivery in large species for targeting spinal cord, brain, and peripheral tissues for pediatric disorders. Mol Ther 19: 1971-1980.
44. Gray, SJ, Matagne, V, Bachaboina, L, Yadav, S, Ojeda, SR and Samulski, RJ (2011). Preclinical differences of intravascular AAV9 delivery to neurons and glia: a comparative study of adult mice and nonhuman primates. Mol Ther 19: 1058-1069.
45. Song, L and Pachter, JS (2003). Culture of murine brain microvascular endothelial cells that maintain expression and cytoskeletal association of tight junction-associated proteins. In Vitro Cell Dev Biol Anim 39: 313-320. (Pubitemid 38200254)
46. Warren, L (1959). The thiobarbituric acid assay of sialic acids. J Biol Chem 234: 1971-1975.