Adenoassociated virus serotype 9-mediated gene therapy for X-linked adrenoleukodystrophy

Molecular Therapy

Volumn 23, Issue 5, 2015, Pages 824-834

  Gong, Yi ^a   Mu, Dakai ^a   Prabhakar, Shilpa ^a   Moser, Ann ^b   Musolino, Patricia ^a   Ren, JiaQian ^a   Breakefield, Xandra O ^a   Maguire, Casey A ^a   Eichler, Florian S ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b Hugo Moser Kennedy   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER A1; PARVOVIRUS VECTOR; VERY LONG CHAIN FATTY ACID; ABC TRANSPORTER; ABCD1 PROTEIN, HUMAN; FATTY ACID; GLUTATHIONE PEROXIDASE; GLUTATHIONE PEROXIDASE 1;

ADENO ASSOCIATED VIRUS 9; ADRENOLEUKODYSTROPHY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL CULTURE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENDOTHELIUM CELL; FIBROBLAST; GENE LOCATION; GLIA CELL; GLIAL CELL CULTURE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OLIGODENDROGLIA; PEROXISOME; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; X LINKED ADRENOLEUKODYSTROPHY; ADMINISTRATION AND DOSAGE; ANIMAL; BRAIN; CELL CULTURE; CLASSIFICATION; DEPENDOPARVOVIRUS; DISEASE MODEL; GENE EXPRESSION; GENE THERAPY; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; GLIA; KNOCKOUT MOUSE; METABOLISM; PROTEIN TRANSPORT; REPORTER GENE; SEROTYPE; TUMOR CELL LINE;

MUS;

ADRENOLEUKODYSTROPHY; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BRAIN; CELL LINE, TUMOR; CELLS, CULTURED; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; FATTY ACIDS; FIBROBLASTS; GENE EXPRESSION; GENES, REPORTER; GENETIC THERAPY; GENETIC VECTORS; GLUTATHIONE PEROXIDASE; HUMANS; MALE; MICE; MICE, KNOCKOUT; NEUROGLIA; PROTEIN TRANSPORT; SEROGROUP; TRANSDUCTION, GENETIC;

EID: 84929049006     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2015.6     Document Type: Article

References (45)

1. Mosser J, Douar AM, Sarde CO, Kioschis P, Feil R, Moser H, et al. (1993). Putative X-linked adrenoleukodystrophy gene shares unexpected homology with ABC transporters. Nature 361: 726-730
2. Moser AB, Kreiter N, Bezman L, Lu, S, Raymond GV, Naidu S, et al. (1999). Plasma very long chain fatty acids in 3, 000 peroxisome disease patients and 29, 000 controls. Ann Neurol 45: 100-110
3. Valianpour F, Selhorst JJ, van Lint LE, van Gennip AH, Wanders RJ and Kemp S. (2003). Analysis of very long-chain fatty acids using electrospray ionization mass spectrometry. Mol Genet Metab 79: 189-196
4. Ferrer I, Aubourg P and Pujol A. (2010). General aspects and neuropathology of X-linked adrenoleukodystrophy. Brain Pathol 20: 817-830
5. Singh I and Pujol A. (2010). Pathomechanisms underlying X-adrenoleukodystrophy: a three-hit hypothesis. Brain Pathol 20: 838-844
6. 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
7. Mingozzi F and High KA. (2011). Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet 12: 341-355
8. Kaplitt MG, Feigin A, Tang C, Fitzsimons HL, Mattis P, Lawlor PA, et al. (2007). Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label phase I trial. Lancet 369: 2097-2105
9. Marks WJ Jr, Ostrem JL, Verhagen L, Starr PA, Larson PS, Bakay RA, et al. (2008). Safety and tolerability of intraputaminal delivery of CERE-120 (adeno-associated virus serotype 2-neurturin) to patients with idiopathic Parkinson's disease: an open-label phase I trial. Lancet Neurol 7: 400-408
10. Worgall S, Sondhi D, Hackett NR, Kosofsky B, Kekatpure MV, Neyzi N, et al. (2008). Treatment of late infantile neuronal ceroid lipofuscinosis by CNS administration of a serotype 2 adeno-associated virus expressing CLN2 cDNA. Hum Gene Ther 19: 463-474
11. Maguire AM, High KA, Auricchio A, Wright JF, Pierce EA, Testa F, et al. (2009). Age-dependent effects of RPE65 gene therapy for Leber's congenital amaurosis: a phase 1 dose-escalation trial. Lancet 374: 1597-1605
12. Nathwani AC, Tuddenham EG, Rangarajan S, Rosales C, McIntosh J, Linch DC, et al. (2011). Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N Engl J Med 365: 2357-2365
13. Davidson BL, Stein CS, Heth JA, Martins I, Kotin RM, Derksen TA, et al. (2000). Recombinant adeno-associated virus type 2, 4, and 5 vectors: transduction of variant cell types and regions in the mammalian central nervous system. Proc Natl Acad Sci USA 97: 3428-3432
14. Taymans JM, Vandenberghe LH, Haute CV, Thiry I, Deroose CM, Mortelmans L, et al. (2007). Comparative analysis of adeno-associated viral vector serotypes 1, 2, 5, 7, and 8 in mouse brain. Hum Gene Ther 18: 195-206
15. Tarantal AF and Lee CC. (2010). Long-term luciferase expression monitored by bioluminescence imaging after adeno-associated virus-mediated fetal gene delivery in rhesus monkeys (Macaca mulatta). Hum Gene Ther 21: 143-148
16. Manfredsson FP, Rising AC and Mandel RJ. (2009). AAV9: a potential blood-brain barrier buster. Mol Ther 17: 403-405
17. 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
18. 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
19. 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
20. Maguire CA, Meijer DH, LeRoy SG, Tierney LA, Broekman ML, Costa FF, et al. (2008). Preventing growth of brain tumors by creating a zone of resistance. Mol Ther 16: 1695-1702
21. Maguire CA, Balaj L, Sivaraman S, Crommentuijn MH, Ericsson M, Mincheva- Nilsson L, et al. (2012). Microvesicle-associated AAV vector as a novel gene delivery system. Mol Ther 20: 960-971
22. Hubbard WC, Moser AB, Tortorelli S, Liu A, Jones D and Moser H. (2006). Combined liquid chromatography-tandem mass spectrometry as an analytical method for high throughput screening for X-linked adrenoleukodystrophy and other peroxisomal disorders: preliminary findings. Mol Genet Metab 89: 185-187
23. Fourcade S, López-Erauskin J, Galino J, Duval C, Naudi A, Jove M, et al. (2008). Early oxidative damage underlying neurodegeneration in X-adrenoleukodystrophy. Hum Mol Genet 17: 1762-1773
24. Meijer DH, Maguire CA, LeRoy SG and Sena-Esteves M. (2009). Controlling brain tumor growth by intraventricular administration of an AAV vector encoding IFN-beta. Cancer Gene Ther 16: 664-671
25. Yamazaki Y, Hirai Y, Miyake K and Shimada T. (2014). Targeted gene transfer into ependymal cells through intraventricular injection of AAV1 vector and long-term enzyme replacement via the CSF. Sci Rep 4: 5506
26. Raymond GV, Seidman R, Monteith TS, Kolodny E, Sathe S, Mahmood A, et al. (2010). Head trauma can initiate the onset of adreno-leukodystrophy. J Neurol Sci 290: 70-74
27. Musolino PL, Rapalino O, Caruso P, Caviness VS and Eichler FS. (2012). Hypoperfusion predicts lesion progression in cerebral X-linked adrenoleukodystrophy. Brain 135(Pt 9): 2676-2683
28. Fouquet F, Zhou JM, Ralston E, Murray K, Troalen F, Magal E, et al. (1997). Expression of the adrenoleukodystrophy protein in the human and mouse central nervous system. Neurobiol Dis 3: 271-285
29. Höftberger R, Kunze M, Weinhofer I, Aboul-Enein F, Voigtländer T, Oezen I, et al. (2007). Distribution and cellular localization of adrenoleukodystrophy protein in human tissues: implications for X-linked adrenoleukodystrophy. Neurobiol Dis 28: 165-174
30. Baarine M, Andréoletti P, Athias A, Nury T, Zarrouk A, Ragot K, et al. (2012). Evidence of oxidative stress in very long chain fatty acid-treated oligodendrocytes and potentialization of ROS production using RNA interferencedirected knockdown of ABCD1 and ACOX1 peroxisomal proteins. Neuroscience 213: 1-18
31. Eichler FS, Ren JQ, Cossoy M, Rietsch AM, Nagpal S, Moser AB, et al. (2008). Is microglial apoptosis an early pathogenic change in cerebral X-linked adrenoleukodystrophy?. Ann Neurol 63: 729-742
32. Dirren E, Towne CL, Setola V, Redmond De Jr, Schneider BL and Aebischer P. (2014). Intracerebroventricular injection of adeno-associated virus 6 and 9 vectors for cell type-specific transgene expression in the spinal cord. Hum Gene Ther 25: 109-120
33. von Jonquieres G, Mersmann N, Klugmann CB, Harasta AE, Lutz B, Teahan O, et al. (2013). Glial promoter selectivity following AAV-delivery to the immature brain. PLoS ONE 8: e65646
34. Murphy SR, Chang CC, Dogbevia G, Bryleva EY, Bowen Z, Hasan MT, et al. (2013). Acat1 knockdown gene therapy decreases amyloid-ß in a mouse model of Alzheimer's disease. Mol Ther 21: 1497-1506
35. Quattrocelli M, Crippa S, Montecchiani C, Camps J, Cornaglia AI, Boldrin L, et al. (2013). Long-term miR-669a therapy alleviates chronic dilated cardiomyopathy in dystrophic mice. J Am Heart Assoc 2: e000284
36. Singh I, Moser HW, Moser AB and Kishimoto Y. (1981). Adrenoleukodystrophy: impaired oxidation of long chain fatty acids in cultured skin fibroblasts an adrenal cortex. Biochem Biophys Res Commun 102: 1223-1229
37. Moser HW, Moser AB, Frayer KK, Chen W, Schulman JD, O'Neill BP, et al. (1981). Adrenoleukodystrophy: increased plasma content of saturated very long chain fatty acids. Neurology 31: 1241-1249
38. Forss-Petter S, Werner H, Berger J, Lassmann H, Molzer B, Schwab MH, et al. (1997). Targeted inactivation of the X-linked adrenoleukodystrophy gene in mice. J Neurosci Res 50: 829-843
39. Samaranch L, Salegio EA, San Sebastian W, Kells AP, Bringas JR, Forsayeth J, et al. (2013). Strong cortical and spinal cord transduction after AAV7 and AAV9 delivery into the cerebrospinal fluid of nonhuman primates. Hum Gene Ther 24: 526-532
40. Foust KD, Salazar DL, Likhite S, Ferraiuolo L, Ditsworth D, Ilieva H, et al. (2013). Therapeutic AAV9-mediated suppression of mutant SOD1 slows disease progression and extends survival in models of inherited ALS. Mol Ther 21: 2148-2159
41. Murrey DA, Naughton BJ, Duncan FJ, Meadows AS, Ware TA, Campbell KJ, et al. (2014). Feasibility and safety of systemic rAAV9-hNAGLU delivery for treating mucopolysaccharidosis IIIB: toxicology biodistribution and immunological assessments in primates. Hum Gene Ther Clin Dev 25: 72-84
42. Samaranch L, Salegio EA, San Sebastian W, Kells AP, Foust KD, Bringas JR, et al. (2012). Adeno-associated virus serotype 9 transduction in the central nervous system of nonhuman primates. Hum Gene Ther 23: 382-389
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, Nagabhushan Kalburgi S, McCown TJ and Jude Samulski R. (2013). Global CNS gene delivery and evasion of anti-AAV-neutralizing antibodies by intrathecal AAV administration in non-human primates. Gene Ther 20: 450-459
45. Mattar CN, Waddington SN, Biswas A, Johana N, Ng, XW, Fisk AS, et al. (2013). Systemic delivery of scAAV9 in fetal macaques facilitates neuronal transduction of the central and peripheral nervous systems. Gene Ther 20: 69-83