AAV9-mediated expression of a non-self protein in nonhuman primate central nervous system triggers widespread neuroinflammation driven by antigen-presenting cell transduction

Molecular Therapy

Volumn 22, Issue 2, 2014, Pages 329-337

  Samaranch, Lluis ^a   Sebastian, Waldy San ^a   Kells, Adrian P ^a   Salegio, Ernesto A ^a,b   Heller, Gregory ^a   Bringas, John R ^a   Pivirotto, Philip ^a   Dearmond, Stephen ^a   Forsayeth, John ^a   Bankiewicz, Krystof S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC LEVO AMINO ACID DECARBOXYLASE; CALBINDIN; GREEN FLUORESCENT PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PARVOVIRUS VECTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; ASTROCYTE; ATAXIA; CELL ACTIVATION; CENTRAL NERVOUS SYSTEM; CISTERNA MAGNA; GENE EXPRESSION; IMMUNE RESPONSE; MACACA FASCICULARIS; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PURKINJE CELL; SIGNAL TRANSDUCTION; TRANSGENE; UPREGULATION; VIRAL GENE DELIVERY SYSTEM; ADMINISTRATION AND DOSAGE; ANIMAL; CORPUS STRIATUM; DEPENDOPARVOVIRUS; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; HUMAN; IMMUNOLOGY; INFLAMMATION; METABOLISM; NERVE CELL; PATHOLOGY; RAT; REPORTER GENE;

ADENO-ASSOCIATED VIRUS; ANIMALIA; PRIMATES; RATTUS; SCYPHOZOA;

ANIMALS; ANTIGEN-PRESENTING CELLS; CENTRAL NERVOUS SYSTEM; CORPUS STRIATUM; DEPENDOVIRUS; GENE EXPRESSION; GENES, REPORTER; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HUMANS; INFLAMMATION; NEURONS; RATS; TRANSDUCTION, GENETIC; TRANSGENES;

EID: 84893307092     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.266     Document Type: Article

References (26)

1. Forsayeth, JR, Eberling, JL, Sanftner, LM, Zhen, Z, Pivirotto, P, Bringas, J et al. (2006). A dose-ranging study of AAV-hAADC therapy in Parkinsonian monkeys. Mol Ther 14: 571-577.
2. 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.
3. 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.
4. 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.
5. Haurigot, V, Marcó, S, Ribera, A, Garcia, M, Ruzo, A, Villacampa, P, et al. (2013). Whole body correction of mucopolysaccharidosis IIIA by intracerebrospinal fluid gene therapy. J Clin Invest 123: 3254-3271.
6. 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.
7. Ciesielska, A, Hadaczek, P, Mittermeyer, G, Zhou, S, Wright, JF, Bankiewicz, KS et al. (2013). Cerebral infusion of AAV9 vector-encoding non-self proteins can elicit cellmediated immune responses. Mol Ther 21: 158-166.
8. Hadaczek, P, Forsayeth, J, Mirek, H, Munson, K, Bringas, J, Pivirotto, P et al. (2009). Transduction of nonhuman primate brain with adeno-associated virus serotype 1: vector trafficking and immune response. Hum Gene Ther 20: 225-237.
9. Bankiewicz, KS, Eberling, JL, Kohutnicka, M, Jagust, W, Pivirotto, P, Bringas, J et al. (2000). Convection-enhanced delivery of AAV vector in parkinsonian monkeys; in vivo detection of gene expression and restoration of dopaminergic function using prodrug approach. Exp Neurol 164: 2-14.
10. Bobo, RH, Laske, DW, Akbasak, A, Morrison, PF, Dedrick, RL and Oldfield, EH (1994). Convection-enhanced delivery of macromolecules in the brain. Proc Natl Acad Sci USA 91: 2076-2080.
11. Bartlett, JS, Samulski, RJ and McCown, TJ (1998). Selective and rapid uptake of adeno-associated virus type 2 in brain. Hum Gene Ther 9: 1181-1186.
12. Ciesielska, A, Mittermeyer, G, Hadaczek, P, Kells, AP, Forsayeth, J and Bankiewicz, KS (2009). Anterograde axonal transport of AAV2-GDNF in rat basal ganglia. Molecular Therapy: 1-6.
13. 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.
14. Barski, JJ, Hartmann, J, Rose, CR, Hoebeek, F, Mörl, K, Noll-Hussong, M et al. (2003). Calbindin in cerebellar Purkinje cells is a critical determinant of the precision of motor coordination. J Neurosci 23: 3469-3477.
15. Aalbers, CJ, Tak, PP and Vervoordeldonk, MJ (2011). Advancements in adenoassociated viral gene therapy approaches: exploring a new horizon. F1000 Med Rep 3: 17.
16. Manning, WC, Zhou, S, Bland, MP, Escobedo, JA and Dwarki, V (1998). Transient immunosuppression allows transgene expression following readministration of adenoassociated viral vectors. Hum Gene Ther 9: 477-485.
17. Treleaven, CM, Tamsett, TJ, Bu, J, Fidler, JA, Sardi, SP, Hurlbut, GD et al. (2012). Gene transfer to the CNS is efficacious in immune-primed mice harboring physiologically relevant titers of anti-AAV antibodies. Mol Ther 20: 1713-1723.
18. Dodiya, HB, Bjorklund, T, Stansell, J 3rd, Mandel, RJ, Kirik, D and Kordower, JH (2010). Differential transduction following basal ganglia administration of distinct pseudotyped AAV capsid serotypes in nonhuman primates. Mol Ther 18: 579-587.
19. McBride, JL, Pitzer, MR, Boudreau, RL, Dufour, B, Hobbs, T, Ojeda, SR et al. (2011). Preclinical safety of RNAi-mediated HTT suppression in the rhesus macaque as a potential therapy for Huntington′s disease. Mol Ther 19: 2152- 2162.
20. Klein, RL, Dayton, RD, Leidenheimer, NJ, Jansen, K, Golde, TE and Zweig, RM (2006). Efficient neuronal gene transfer with AAV8 leads to neurotoxic levels of tau or green fluorescent proteins. Mol Ther 13: 517-527.
21. Gray, SJ, Foti, SB, Schwartz, JW, Bachaboina, L, Taylor-Blake, B, Coleman, J et al. (2011). Optimizing promoters for recombinant adeno-associated virus-mediated gene expression in the peripheral and central nervous system using self-complementary vectors. Hum Gene Ther 22: 1143-1153.
22. 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.
23. Matsushita, T, Elliger, S, Elliger, C, Podsakoff, G, Villarreal, L, Kurtzman, GJ et al. (1998). Adeno-associated virus vectors can be efficiently produced without helper virus. Gene Ther 5: 938-945.
24. Wright, JF, Qu, G, Tang, C and Sommer, JM (2003). Recombinant adeno-associated virus: formulation challenges and strategies for a gene therapy vector. Curr Opin Drug Discov Devel 6: 174-178.
25. Fiandaca, MS, Forsayeth, JR, Dickinson, PJ and Bankiewicz, KS (2008). Image-guided convection-enhanced delivery platform in the treatment of neurological diseases. Neurotherapeutics 5: 123-127.
26. Krauze, MT, Saito, R, Noble, C, Tamas, M, Bringas, J, Park, JW et al. (2005). Refluxfree cannula for convection-enhanced high-speed delivery of therapeutic agents. J Neurosurg 103: 923-929.