Recombinant adeno-associated virus type 2 pseudotypes: Comparing safety, specificity, and transduction efficiency in the primate striatum - Laboratory investigation

Journal of Neurosurgery

Volumn 114, Issue 3, 2011, Pages 672-680

  Sanchez, Carlos E ^a   Tierney, Travis S ^a   Gale, John T ^a   Alavian, Kambiz N ^c   Sahin, Ayguen ^a   Lee, Jeng Shin ^b   Mulligan, Richard C ^b   Carter, Bob S ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adeno associated virus; Apoptosis; Convection enhanced delivery; Gene therapy; Nonhuman primate

Indexed keywords

ADENOVIRUS VECTOR; ANTIBODY; CASPASE 2; CASPASE 3; FORMALDEHYDE; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; NEURON SPECIFIC NUCLEAR PROTEIN;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS TYPE 2; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN SIZE; BRAIN TISSUE; CAUDATE NUCLEUS; CELL DENSITY; CELL LABELING; CELL TYPE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENZYME ACTIVATION; GENETIC TRANSFECTION; GLIA; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; MACACA MULATTA; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PUTAMEN; RHESUS MONKEY; SEROTYPE; STEREOLOGY; STEREOMETRY; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; CASPASE 3; DEPENDOVIRUS; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; NEOSTRIATUM; SAFETY; STEREOTAXIC TECHNIQUES; TRANSDUCTION, GENETIC;

EID: 79952258871     PISSN: 00223085     EISSN: 19330693     Source Type: Journal    
DOI: 10.3171/2010.8.JNS091583     Document Type: Article

References (37)

1. Bankiewicz KS, Eberling JL, Kohutnicka M, Jagust W, Pivirotto P, Bringas J, et al: Convection-enhanced delivery of AAV vector in parkinsonian monkeys; in vivo detection of gene expression and restoration of dopaminergic function using pro-drug approach. Exp Neurol 164:2-14, 2000 (Pubitemid 30490717)
2. Bankiewicz KS, Forsayeth J, Eberling JL, Sanchez-Pernaute R, Pivirotto P, Bringas J, et al: Long-term clinical improvement in MPTP-lesioned primates after gene therapy with AAV-hAADC. Mol Ther 14:564-570, 2006 (Pubitemid 44296090)
3. Bobo RH, Laske DW, Akbasak A, Morrison PF, Dedrick RL, Oldfield EH: Convection-enhanced delivery of macromolecules in the brain. Proc Natl Acad Sci U S A 91:2076-2080, 1994 (Pubitemid 24092045)
4. Broekman ML, Comer LA, Hyman BT, Sena-Esteves M: Adeno-associated virus vectors serotyped with AAV8 capsid are more efficient than AAV-1 or -2 serotypes for widespread gene delivery to the neonatal mouse brain. Neuroscience 138:501-510, 2006 (Pubitemid 43255560)
5. Burger C, Gorbatyuk OS, Velardo MJ, Peden CS, Williams P, Zolotukhin S, et al: Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol Ther 10:302-317, 2004 (Pubitemid 39117875)
6. Cunningham J, Pivirotto P, Bringas J, Suzuki B, Vijay S, Sanftner L, et al: Biodistribution of adeno-associated virus type-2 in nonhuman primates after convection-enhanced delivery to brain. Mol Ther 16:1267-1275, 2008 (Pubitemid 351866058)
7. Eberling JL, Jagust WJ, Christine CW, Starr P, Larson P, Bankiewicz KS, et al: Results from a phase I safety trial of hAADC gene therapy for Parkinson disease. Neurology 70:1980-1983, 2008
8. Emborg ME, Carbon M, Holden JE, During MJ, Ma Y, Tang C, et al: Subthalamic glutamic acid decarboxylase gene therapy: changes in motor function and cortical metabolism. J Cereb Blood Flow Metab 27:501-509, 2007
9. Forsayeth JR, Eberling JL, Sanftner LM, Zhen Z, Pivirotto P, Bringas J, et al: A dose-ranging study of AAV-hAADC therapy in Parkinsonian monkeys. Mol Ther 14:571-577, 2006 (Pubitemid 44296089)
10. Gao GP, Alvira MR, Wang L, Calcedo R, Johnston J, Wilson JM: Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc Natl Acad Sci U S A 99:11854-11859, 2002 (Pubitemid 34994488)
11. Hadaczek P, Forsayeth J, Mirek H, Munson K, Bringas J, Pivirotto P, et al: Transduction of nonhuman primate brain with adeno-associated virus serotype 1: vector trafficking and immune response. Hum Gene Ther 20:225-237, 2009
12. Hadaczek P, Kohutnicka M, Krauze MT, Bringas J, Pivirotto P, Cunningham J, et al: Convection-enhanced delivery of adeno-associated virus type 2 (AAV2) into the striatum and transport of AAV2 within monkey brain. Hum Gene Ther 17:291-302, 2006
13. Hamilton JF, Morrison PF, Chen MY, Harvey-White J, Pernaute RS, Phillips H, et al: Heparin coinfusion during convection-enhanced delivery (CED) increases the distribution of the glial-derived neurotrophic factor (GDNF) ligand family in rat striatum and enhances the pharmacological activity of neurturin. Exp Neurol 168:155-161, 2001 (Pubitemid 32195267)
14. Harding TC, Dickinson PJ, Roberts BN, Yendluri S, Gonzalez-Edick M, Lecouteur RA, et al: Enhanced gene transfer efficiency in the murine striatum and an orthotopic glioblastoma tumor model, using AAV-7- and AAV-8-pseudotyped vectors. Hum Gene Ther 17:807-820, 2006 (Pubitemid 44681451)
15. Hildinger M, Auricchio A, Gao G, Wang L, Chirmule N, Wilson JM: Hybrid vectors based on adeno-associated virus serotypes 2 and 5 for muscle-directed gene transfer. J Virol 75:6199-6203, 2001 (Pubitemid 32553151)
16. Kaplitt MG, Feigin A, Tang C, Fitzsimons HL, Mattis P, Lawlor PA, et al: 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, 2007 (Pubitemid 46935946)
17. Kells AP, Hadaczek P, Yin D, Bringas J, Varenika V, Forsayeth J, et al: Efficient gene therapy-based method for the delivery of therapeutics to primate cortex. Proc Natl Acad Sci U S A 106:2407-2411, 2009
18. Klein RL, Dayton RD, Leidenheimer NJ, Jansen K, Golde TE, Zweig RM: Efficient neuronal gene transfer with AAV8 leads to neurotoxic levels of tau or green fluorescent proteins. Mol Ther 13:517-527, 2006 (Pubitemid 43257619)
19. Klein RL, Dayton RD, Tatom JB, Henderson KM, Henning PP: AAV8, 9, Rh10, Rh43 vector gene transfer in the rat brain: effects of serotype, promoter and purification method. Mol Ther 16:89-96, 2008
20. Lawlor PA, Bland RJ, Mouravlev A, Young D, During MJ: Efficient gene delivery and selective transduction of glial cells in the mammalian brain by AAV serotypes isolated from nonhuman primates. Mol Ther 17:1692-1702, 2009
21. Lieberman DM, Laske DW, Morrison PF, Bankiewicz KS, Oldfield EH: Convection-enhanced distribution of large molecules in gray matter during interstitial drug infusion. J Neurosurg 82:1021-1029, 1995
22. Mandel RJ, Manfredsson FP, Foust KD, Rising A, Reimsnider S, Nash K, et al: Recombinant adeno-associated viral vectors as therapeutic agents to treat neurological disorders. Mol Ther 13:463-483, 2006 (Pubitemid 43257615)
23. Marks WJ Jr, Ostrem JL, Verhagen L, Starr PA, Larson PS, Bakay RA, et al: 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, 2008
24. McBride JL, Boudreau RL, Harper SQ, Staber PD, Monteys AM, Martins I, et al: Artificial miRNAs mitigate shRNA-mediated toxicity in the brain: implications for the therapeutic development of RNAi. Proc Natl Acad Sci U S A 105:5868-5873, 2008 (Pubitemid 351758464)
25. McFarland NR, Lee JS, Hyman BT, McLean PJ: Comparison of transduction efficiency of recombinant AAV serotypes 1, 2, 5, and 8 in the rat nigrostriatal system. J Neurochem 109:838-845, 2009
26. McPhee SW, Janson CG, Li C, Samulski RJ, Camp AS, Francis J, et al: Immune responses to AAV in a phase I study for Canavan disease. J Gene Med 8:577-588, 2006 (Pubitemid 43827251)
27. Passini MA, Watson DJ, Wolfe JH: Gene delivery to the mouse brain with adeno-associated virus. Methods Mol Biol 246:225-236, 2004
28. Paterna JC, Feldon J, Büeler H: Transduction profiles of recombinant adeno-associated virus vectors derived from serotypes 2 and 5 in the nigrostriatal system of rats. J Virol 78:6808-6817, 2004 (Pubitemid 38781518)
29. Paxinos G, Haung XF, Petrides M, Toga AW: The Rhesus Monkey Brain in Stereotaxic Coordinates, ed. 2. San Diego: Academic Press, 2008
30. Rabinowitz JE, Rolling F, Li C, Conrath H, Xiao W, Xiao X, et al: Cross-packaging of a single adeno-associated virus (AAV) type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity. J Virol 76:791-801, 2002 (Pubitemid 34033377)
31. Reimsnider S, Manfredsson FP, Muzyczka N, Mandel RJ: Time course of transgene expression after intrastriatal pseudotyped rAAV2/1, rAAV2/2, rAAV2/5, and rAAV2/8 transduction in the rat. Mol Ther 15:1504-1511, 2007 (Pubitemid 47103062)
32. Sanchez CE, Gale J, Tierney TS, Mulligan RC, Carter BS: AAV2-mediated gene delivery to the non-human primate striatum: development of a multi-catheter injection system for reproducible single-measure intraoperative convection en hanced delivery. Presented at the Annual Meeting of the Congress of Neurological Surgeons, Orlando, Florida, Sep tem ber 20-25, 2008 (Poster) (http://2008.cns.org/posterbrowser.aspx) [Accessed August 24, 2010]
33. Sands MS, Davidson BL: Gene therapy for lysosomal storage diseases. Mol Ther 13:839-849, 2006
34. Taymans JM, Vandenberghe LH, Haute CV, Thiry I, Deroose CM, Mortelmans L, et al: Comparative analysis of adeno-associated viral vector serotypes 1, 2, 5, 7, and 8 in mouse brain. Hum Gene Ther 18:195-206, 2007 (Pubitemid 46626459)
35. Tierney TS, Pradilla G, Wang PP, Clatterbuck RE, Tamargo RJ: Intracranial delivery of the nitric oxide donor diethylenetriamine/nitric oxide from a controlled-release polymer: toxicity in cynomolgus monkeys. Neurosurgery 58:952-960, 2006 (Pubitemid 43772440)
36. West MJ, Slomianka L, Gundersen HJ: Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497, 1991
37. Worgall S, Sondhi D, Hackett NR, Kosofsky B, Kekatpure MV, Neyzi N, et al: 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, 2008 (Pubitemid 351748791)