Widespread AAV1- and AAV2-mediated transgene expression in the nonhuman primate brain: implications for Huntington's disease

Molecular Therapy Methods and Clinical Development

Volumn 3, Issue , 2016, Pages 16037-

  Hadaczek, Piotr ^a   Stanek, Lisa ^b   Ciesielska, Agnieszka ^a   Sudhakar, Vivek ^a   Samaranch, Lluis ^a   Pivirotto, Philip ^a   Bringas, John ^a   O'Riordan, Catherine ^b   Mastis, Bryan ^b   San Sebastian, Waldy ^a   Forsayeth, John ^a   Cheng, Seng H ^b   Bankiewicz, Krystof S ^a   Shihabuddin, Lamya S ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SANOFI   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; GREEN FLUORESCENT PROTEIN; ENDOTOXIN; ENHANCED GREEN FLUORESCENT PROTEIN; GADOTERIDOL;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; CAUDATE NUCLEUS; CONTROLLED STUDY; CORPUS STRIATUM; GENE EXPRESSION; HUNTINGTON CHOREA; MALE; MEDIUM SPINY NEURON; NONHUMAN; PRIORITY JOURNAL; PUTAMEN; RHESUS MONKEY; SEROTYPE; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; ADENO ASSOCIATED VIRUS 1; ADENO ASSOCIATED VIRUS 2; ANIMAL CELL; ASTROCYTE; COLUMN CHROMATOGRAPHY; HELA CELL LINE; NUCLEAR MAGNETIC RESONANCE IMAGING; POLYMERASE CHAIN REACTION; TRANSIENT TRANSFECTION; ULTRACENTRIFUGATION; WESTERN BLOTTING;

EID: 85015168703     PISSN: None     EISSN: 23290501     Source Type: Journal    
DOI: 10.1038/mtm.2016.37     Document Type: Article

References (64)

1. 1 Peel, AL, Klein, RL, Adeno-associated virus vectors: activity and applications in the CNS. J Neurosci Methods 98 (2000), 95–104.
2. 2 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 (2009), 225–237.
3. 3 Davidson, BL, Stein, CS, Heth, JA, Martins, I, Kotin, RM, Derksen, TA, et al. 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 U S A 97 (2000), 3428–3432.
4. 4 Samaranch, L, Salegio, EA, San Sebastian, W, Kells, AP, Bringas, JR, Forsayeth, J, et al. Strong cortical and spinal cord transduction after AAV7 and AAV9 delivery into the cerebrospinal fluid of nonhuman primates. Hum Gene Ther 24 (2013), 526–532.
5. 5 Merienne, N, Le Douce, J, Faivre, E, Déglon, N, Bonvento, G, Efficient gene delivery and selective transduction of astrocytes in the mammalian brain using viral vectors. Front Cell Neurosci, 7, 2013, 106.
6. 6 Dodiya, HB, Bjorklund, T, Stansell, J 3rd, Mandel, RJ, Kirik, D, Kordower, JH, Differential transduction following basal ganglia administration of distinct pseudotyped AAV capsid serotypes in nonhuman primates. Mol Ther 18 (2010), 579–587.
7. 7 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 (2007), 195–206.
8. 8 Sanchez, CE, Tierney, TS, Gale, JT, Alavian, KN, Sahin, A, Lee, JS, et al. Recombinant adeno-associated virus type 2 pseudotypes: comparing safety, specificity, and transduction efficiency in the primate striatum. Laboratory investigation. J Neurosurg 114 (2011), 672–680.
9. 9 Zhang, HS, Kim, E, Lee, S, Ahn, IS, Jang, JH, Transduction of striatum and cortex tissues by adeno-associated viral vectors produced by herpes simplex virus- and baculovirus-based methods. J Virol Methods 179 (2012), 276–280.
10. 10 Ciesielska, A, Hadaczek, P, Mittermeyer, G, Zhou, S, Wright, JF, Bankiewicz, KS, et al. Cerebral infusion of AAV9 vector-encoding non-self proteins can elicit cell-mediated immune responses. Mol Ther 21 (2013), 158–166.
11. 11 Samaranch, L, San Sebastian, W, Kells, AP, Salegio, EA, Heller, G, Bringas, JR, et al. AAV9-mediated expression of a non-self protein in nonhuman primate central nervous system triggers widespread neuroinflammation driven by antigen-presenting cell transduction. Mol Ther 22 (2014), 329–337.
12. 12 Harper, SQ, Staber, PD, He, X, Eliason, SL, Martins, IH, Mao, Q, et al. RNA interference improves motor and neuropathological abnormalities in a Huntington's disease mouse model. Proc Natl Acad Sci USA 102 (2005), 5820–5825.
13. 13 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 USA 105 (2008), 5868–5873.
14. 14 Franich, NR, Fitzsimons, HL, Fong, DM, Klugmann, M, During, MJ, Young, D, AAV vector-mediated RNAi of mutant huntingtin expression is neuroprotective in a novel genetic rat model of Huntington's disease. Mol Ther 16 (2008), 947–956.
15. 15 Boudreau, RL, McBride, JL, Martins, I, Shen, S, Xing, Y, Carter, BJ, et al. Nonallele-specific silencing of mutant and wild-type huntingtin demonstrates therapeutic efficacy in Huntington's disease mice. Mol Ther 17 (2009), 1053–1063.
16. 16 Stanek, LM, Sardi, SP, Mastis, B, Richards, AR, Treleaven, CM, Taksir, T, et al. Silencing mutant huntingtin by adeno-associated virus-mediated RNA interference ameliorates disease manifestations in the YAC128 mouse model of Huntington's disease. Hum Gene Ther 25 (2014), 461–474.
17. 17 Han, I, You, Y, Kordower, JH, Brady, ST, Morfini, GA, Differential vulnerability of neurons in Huntington's disease: the role of cell type-specific features. J Neurochem 113 (2010), 1073–1091.
18. 18 Vonsattel, JP, Huntington disease models and human neuropathology: similarities and differences. Acta Neuropathol 115 (2008), 55–69.
19. 19 Wang, N, Gray, M, Lu, XH, Cantle, JP, Holley, SM, Greiner, E, et al. Neuronal targets for reducing mutant huntingtin expression to ameliorate disease in a mouse model of Huntington's disease. Nat Med 20 (2014), 536–541.
20. 20 Foust, KD, Nurre, E, Montgomery, CL, Hernandez, A, Chan, CM, Kaspar, BK, Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 27 (2009), 59–65.
21. 21 Gray, SJ, Matagne, V, Bachaboina, L, Yadav, S, Ojeda, SR, Samulski, RJ, Preclinical differences of intravascular AAV9 delivery to neurons and glia: a comparative study of adult mice and nonhuman primates. Mol Ther 19 (2011), 1058–1069.
22. 22 Dufour, BD, Smith, CA, Clark, RL, Walker, TR, McBride, JL, Intrajugular vein delivery of AAV9-RNAi prevents neuropathological changes and weight loss in Huntington's disease mice. Mol Ther 22 (2014), 797–810.
23. 23 Richardson, RM, Kells, AP, Martin, AJ, Larson, PS, Starr, PA, Piferi, PG, et al. Novel platform for MRI-guided convection-enhanced delivery of therapeutics: preclinical validation in nonhuman primate brain. Stereotact Funct Neurosurg 89 (2011), 141–151.
24. 24 Richardson, RM, Gimenez, F, Salegio, EA, Su, X, Bringas, J, Berger, MS, et al. T2 imaging in monitoring of intraparenchymal real-time convection-enhanced delivery. Neurosurgery 69 (2011), 154–163 discussion 163.
25. 25 Richardson, RM, Kells, AP, Rosenbluth, KH, Salegio, EA, Fiandaca, MS, Larson, PS, et al. Interventional MRI-guided putaminal delivery of AAV2-GDNF for a planned clinical trial in Parkinson's disease. Mol Ther 19 (2011), 1048–1057.
26. 26 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 (2000), 2–14.
27. 27 Rosenbluth, KH, Luz, M, Mohr, E, Mittermeyer, S, Bringas, J, Bankiewicz, KS, Design of an in-dwelling cannula for convection-enhanced delivery. J Neurosci Methods 196 (2011), 118–123.
28. 28 Aschauer, DF, Kreuz, S, Rumpel, S, Analysis of transduction efficiency, tropism and axonal transport of AAV serotypes 1, 2, 5, 6, 8 and 9 in the mouse brain. PLoS One, 8, 2013, e76310.
29. 29 Clark, KR, Liu, X, McGrath, JP, Johnson, PR, Highly purified recombinant adeno-associated virus vectors are biologically active and free of detectable helper and wild-type viruses. Hum Gene Ther 10 (1999), 1031–1039.
30. 30 Burnham, B, Nass, S, Kong, E, Mattingly, M, Woodcock, D, Song, A, et al. Analytical Ultracentrifugation as an Approach to Characterize Recombinant Adeno-Associated Viral Vectors. Hum Gene Ther Methods 26 (2015), 228–242.
31. 31 Bartus, RT, Kordower, JH, Johnson, EM Jr, Brown, L, Kruegel, BR, Chu, Y, et al. Post-mortem assessment of the short and long-term effects of the trophic factor neurturin in patients with α-synucleinopathies. Neurobiol Dis 78 (2015), 162–171.
32. 32 McCown, TJ, Adeno-Associated Virus (AAV) Vectors in the CNS. Curr Gene Ther 11 (2011), 181–188.
33. 33 Morton, AJ, Howland, DS, Large genetic animal models of Huntington's Disease. J Huntingtons Dis 2 (2013), 3–19.
34. 34 Vonsattel, JP, Keller, C, Cortes Ramirez, EP, Huntington's disease - neuropathology. Handb Clin Neurol 100 (2011), 83–100.
35. 35 Vonsattel, JP, Myers, RH, Stevens, TJ, Ferrante, RJ, Bird, ED, Richardson, EP Jr, Neuropathological classification of Huntington's disease. J Neuropathol Exp Neurol 44 (1985), 559–577.
36. 36 Watakabe, A, Ohtsuka, M, Kinoshita, M, Takaji, M, Isa, K, Mizukami, H, et al. Comparative analyses of adeno-associated viral vector serotypes 1, 2, 5, 8 and 9 in marmoset, mouse and macaque cerebral cortex. Neurosci Res 93 (2015), 144–157.
37. 37 Markakis, EA, Vives, KP, Bober, J, Leichtle, S, Leranth, C, Beecham, J, et al. Comparative transduction efficiency of AAV vector serotypes 1-6 in the substantia nigra and striatum of the primate brain. Mol Ther 18 (2010), 588–593.
38. 38 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 (2004), 302–317.
39. 39 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 (2006), 291–302.
40. 40 Kaspar, BK, Erickson, D, Schaffer, D, Hinh, L, Gage, FH, Peterson, DA, Targeted retrograde gene delivery for neuronal protection. Mol Ther 5 (2002), 50–56.
41. 41 Passini, MA, Macauley, SL, Huff, MR, Taksir, TV, Bu, J, Wu, IH, et al. AAV vector-mediated correction of brain pathology in a mouse model of Niemann-Pick A disease. Mol Ther 11 (2005), 754–762.
42. 42 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 USA 106 (2009), 2407–2411.
43. 43 Hollis, ER 2nd, Kadoya, K, Hirsch, M, Samulski, RJ, Tuszynski, MH, Efficient retrograde neuronal transduction utilizing self-complementary AAV1. Mol Ther 16 (2008), 296–301.
44. 44 Castle, MJ, Gershenson, ZT, Giles, AR, Holzbaur, EL, Wolfe, JH, Adeno-associated virus serotypes 1, 8, and 9 share conserved mechanisms for anterograde and retrograde axonal transport. Hum Gene Ther 25 (2014), 705–720.
45. 45 San Sebastian, W, Richardson, RM, Kells, AP, Lamarre, C, Bringas, J, Pivirotto, P, et al. Safety and tolerability of magnetic resonance imaging-guided convection-enhanced delivery of AAV2-hAADC with a novel delivery platform in nonhuman primate striatum. Hum Gene Ther 23 (2012), 210–217.
46. 46 Hadaczek, P, Eberling, JL, Pivirotto, P, Bringas, J, Forsayeth, J, Bankiewicz, KS, Eight years of clinical improvement in MPTP-lesioned primates after gene therapy with AAV2-hAADC. Mol Ther 18 (2010), 1458–1461.
47. 47 Wang, C, Wang, CM, Clark, KR, Sferra, TJ, Recombinant AAV serotype 1 transduction efficiency and tropism in the murine brain. Gene Ther 10 (2003), 1528–1534.
48. 48 Yang, GS, Schmidt, M, Yan, Z, Lindbloom, JD, Harding, TC, Donahue, BA, et al. Virus-mediated transduction of murine retina with adeno-associated virus: effects of viral capsid and genome size. J Virol 76 (2002), 7651–7660.
49. 49 Summerford, C, Samulski, RJ, Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J Virol 72 (1998), 1438–1445.
50. 50 Wu, Z, Miller, E, Agbandje-McKenna, M, Samulski, RJ, Alpha2,3 and alpha2,6 N-linked sialic acids facilitate efficient binding and transduction by adeno-associated virus types 1 and 6. J Virol 80 (2006), 9093–9103.
51. 51 McBride, JL, Pitzer, MR, Boudreau, RL, Dufour, B, Hobbs, T, Ojeda, SR, et al. Preclinical safety of RNAi-mediated HTT suppression in the rhesus macaque as a potential therapy for Huntington's disease. Mol Ther 19 (2011), 2152–2162.
52. 52 Parent, A, Hazrati, LN, Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Brain Res Rev 20 (1995), 91–127.
53. 53 Haber, SN, Knutson, B, The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35 (2010), 4–26.
54. 54 McFarland, NR, Haber, SN, Thalamic relay nuclei of the basal ganglia form both reciprocal and nonreciprocal cortical connections, linking multiple frontal cortical areas. J Neurosci 22 (2002), 8117–8132.
55. 55 Künzle, H, Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis. Brain Res 88 (1975), 195–209.
56. 56 Hadaczek, P, Yamashita, Y, Mirek, H, Tamas, L, Bohn, MC, Noble, C, et al. The “perivascular pump” driven by arterial pulsation is a powerful mechanism for the distribution of therapeutic molecules within the brain. Mol Ther 14 (2006), 69–78.
57. 57 Forsayeth, J, Bankiewicz, KS, Transduction of antigen-presenting cells in the brain by AAV9 warrants caution in preclinical studies. Mol Ther, 23, 2015, 612.
58. 58 San Sebastian, W, Kells, AP, Bringas, J, Samaranch, L, Hadaczek, P, Ciesielska, A, et al. Safety and tolerability of MRI-guided infusion of AAV2-hAADC into the mid-brain of non-human primate. Mol Ther Methods Clin Dev, 3, 2014, 14049.
59. 59 San Sebastian, W, Samaranch, L, Heller, G, Kells, AP, Bringas, J, Pivirotto, P, et al. Adeno-associated virus type 6 is retrogradely transported in the non-human primate brain. Gene Ther 20 (2013), 1178–1183.
60. 60 Xiao, X, Li, J, Samulski, RJ, Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus. J Virol 72 (1998), 2224–2232.
61. 61 Thorne, BA, Takeya, RK, Peluso, RW, Manufacturing recombinant adeno-associated viral vectors from producer cell clones. Hum Gene Ther 20 (2009), 707–714.
62. 62 Martin, J, Frederick, A, Luo, Y, Jackson, R, Joubert, M, Sol, B, et al. Generation and characterization of adeno-associated virus producer cell lines for research and preclinical vector production. Hum Gene Ther Methods 24 (2013), 253–269.
63. 63 Qu, G, Bahr-Davidson, J, Prado, J, Tai, A, Cataniag, F, McDonnell, J, et al. Separation of adeno-associated virus type 2 empty particles from genome containing vectors by anion-exchange column chromatography. J Virol Methods 140 (2007), 183–192.
64. 64 Grimm, D, Kay, MA, Kleinschmidt, JA, Helper virus-free, optically controllable, and two-plasmid-based production of adeno-associated virus vectors of serotypes 1 to 6. Mol Ther 7 (2003), 839–850.