Gene therapy for the CNS using AAVs: The impact of systemic delivery by AAV9

Journal of Controlled Release

Volumn 241, Issue , 2016, Pages 94-109

  Saraiva, Joana ^a   Nobre, Rui Jorge ^a,b   Pereira de Almeida, Luis ^a,c  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

AAV9; Adeno associated virus (AAV); Central nervous system; Gene therapy; Systemic administration

Indexed keywords

GENE EXPRESSION; GENE TRANSFER; MEDICAL APPLICATIONS; NEURONS; VIRUSES;

AAV9; ADENO-ASSOCIATED VIRUS; CENTRAL NERVOUS SYSTEMS; INSERTIONAL MUTAGENESIS; LYSOSOMAL STORAGE DISORDER; MOTOR NEURON DISEASE; SYSTEMIC ADMINISTRATION; TRANSGENE EXPRESSION;

GENE THERAPY;

ALPHA N ACETYLGLUCOSAMINIDASE; AROMATIC LEVO AMINO ACID DECARBOXYLASE; ASPARTOACYLASE; COLLAPSIN RESPONSE MEDIATOR PROTEIN ASSOCIATED MOLECULE ASSOCIATED GUANOSINE TRIPHOSPHATASE; CYCLIC NUCLEOTIDE GATED CHANNEL; CYCLIC NUCLEOTIDE GATED CHANNEL BETA 3; GENE THERAPY AGENT; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLUCAN 1,4 ALPHA GLUCOSIDASE; GLUTAMATE DECARBOXYLASE; GUANOSINE TRIPHOSPHATASE; MANNITOL; MICRORNA; NADH DEHYDROGENASE 4; NERVE GROWTH FACTOR; NEURTURIN; PARVOVIRUS VECTOR; PROTEIN TYROSINE KINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; RETINAL PIGMENT EPITHELIUM SPECIFIC PROTEIN; RETINOSCHISIN 1; SHORT HAIRPIN RNA; SOLUBLE FMS LIKE TYROSINE KINASE 1; SURVIVAL MOTOR NEURON PROTEIN; TRIPEPTIDYL PEPTIDASE I; UNCLASSIFIED DRUG; CAPSID PROTEIN;

ADENO ASSOCIATED VIRUS 9; AGE RELATED MACULAR DEGENERATION; ALZHEIMER DISEASE; AROMATIC LEVO AMINO ACID DECARBOXYLASE DEFICIENCY; BLOOD BRAIN BARRIER; CANAVAN DISEASE; CENTRAL NERVOUS SYSTEM DISEASE; CHOROIDEREMIA; COLOR BLINDNESS; DEGENERATIVE DISEASE; DRUG DOSE ESCALATION; EYE DISEASE; FOCUSED ULTRASOUND; GENE SILENCING; GLYCOGEN STORAGE DISEASE; GLYCOGEN STORAGE DISEASE TYPE 2; HUMAN; HUNTINGTON CHOREA; INTRATHECAL DRUG ADMINISTRATION; INTRAUTERINE DRUG ADMINISTRATION; INTRAVASCULAR DRUG ADMINISTRATION; INTRAVENOUS DRUG ADMINISTRATION; LEBER HEREDITARY OPTIC NEUROPATHY; LYSOSOME STORAGE DISEASE; MENTAL DISEASE; MICROBUBBLE; MOTOR NEURON DISEASE; NEURONAL CEROID LIPOFUSCINOSIS; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RETINOSCHISIS; REVIEW; RNAI THERAPEUTICS; SANFILIPPO SYNDROME; SPINAL MUSCULAR ATROPHY; SUBRETINAL DRUG ADMINISTRATION; ULTRASOUND; VIRAL GENE THERAPY; VIRAL TROPISM; VIRUS CAPSID; VIRUS RECOMBINANT; X CHROMOSOME LINKED DISORDER; X LINKED RETINOSCHISIS; ADMINISTRATION AND DOSAGE; ANIMAL; CLINICAL TRIAL (TOPIC); DEPENDOPARVOVIRUS; GENE THERAPY; GENE TRANSFER; GENE VECTOR; GENETICS; PROCEDURES;

ANIMALS; CAPSID PROTEINS; CENTRAL NERVOUS SYSTEM DISEASES; CLINICAL TRIALS AS TOPIC; DEPENDOVIRUS; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; HUMANS;

EID: 84988451695     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2016.09.011     Document Type: Review

References (133)

1. [1] Murlidharan, G., Samulski, R.J., Asokan, A., Biology of adeno-associated viral vectors in the central nervous system. Front. Mol. Neurosci., 7, 2014, 76.
2. [2] Maguire, C.A., Ramirez, S.H., Merkel, S.F., Sena-Esteves, M., Breakefield, X.O., Gene therapy for the nervous system: challenges and new strategies. Neurotherapeutics: the journal of the American Society for Experimental NeuroTherapeutics 11 (2014), 817–839.
3. [3] Conceicao, M., Mendonca, L., Nobrega, C., Gomes, C., Costa, P., Hirai, H., Moreira, J.N., Lima, M.C., Manjunath, N., Pereira de Almeida, L., Intravenous administration of brain-targeted stable nucleic acid lipid particles alleviates Machado-Joseph disease neurological phenotype. Biomaterials 82 (2016), 124–137.
4. [4] Alvarez-Erviti, L., Seow, Y., Yin, H., Betts, C., Lakhal, S., Wood, M.J., Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat. Biotechnol. 29 (2011), 341–345.
5. [5] Choudhury, S.R., Hudry, E., Maguire, C.A., Sena-Esteves, M., Breakefield, X.O., Grandi, P., Viral vectors for therapy of neurologic diseases. Neuropharmacology, 2016 http://www.sciencedirect.com/science/article/pii/S002839081630048X.
6. [6] Nobre, R.J., Almeida, L.P., Gene therapy for Parkinson's and Alzheimer's diseases: from the bench to clinical trials. Curr. Pharm. Des. 17 (2011), 3434–3445.
7. [7] Nobrega, C., Nascimento-Ferreira, I., Onofre, I., Albuquerque, D., Hirai, H., Deglon, N., de Almeida, L.P., Silencing mutant ataxin-3 rescues motor deficits and neuropathology in Machado-Joseph disease transgenic mice. PLoS One, 8, 2013, e52396.
8. [8] Nobrega, C., Nascimento-Ferreira, I., Onofre, I., Albuquerque, D., Deglon, N., de Almeida, L.P., RNA interference mitigates motor and neuropathological deficits in a cerebellar mouse model of Machado-Joseph disease. PLoS One, 9, 2014, e100086.
9. [9] Alves, S., Nascimento-Ferreira, I., Auregan, G., Hassig, R., Dufour, N., Brouillet, E., Pedroso de Lima, M.C., Hantraye, P., Pereira de Almeida, L., Deglon, N., Allele-specific RNA silencing of mutant ataxin-3 mediates neuroprotection in a rat model of Machado-Joseph disease. PLoS One, 3, 2008, e3341.
10. [10] Revilla, S., Ursulet, S., Alvarez-Lopez, M.J., Castro-Freire, M., Perpina, U., Garcia-Mesa, Y., Bortolozzi, A., Gimenez-Llort, L., Kaliman, P., Cristofol, R., Sarkis, C., Sanfeliu, C., Lenti-GDNF gene therapy protects against Alzheimer's disease-like neuropathology in 3xTg-AD mice and MC65 cells. CNS Neurosci. Ther. 20 (2014), 961–972.
11. [11] Ralph, G.S., Radcliffe, P.A., Day, D.M., Carthy, J.M., Leroux, M.A., Lee, D.C., Wong, L.F., Bilsland, L.G., Greensmith, L., Kingsman, S.M., Mitrophanous, K.A., Mazarakis, N.D., Azzouz, M., Silencing mutant SOD1 using RNAi protects against neurodegeneration and extends survival in an ALS model. Nat. Med. 11 (2005), 429–433.
12. [12] Cunha-Santos, J., Duarte-Neves, J., Carmona, V., Guarente, L., Pereira de Almeida, L., Cavadas, C., Caloric restriction blocks neuropathology and motor deficits in Machado-Joseph disease mouse models through SIRT1 pathway. Nat. Commun., 7, 2016, 11445.
13. [13] Kells, A.P., Hadaczek, P., Yin, D., Bringas, J., Varenika, V., Forsayeth, J., Bankiewicz, K.S., Efficient gene therapy-based method for the delivery of therapeutics to primate cortex. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 2407–2411.
14. [14] Atchison, R.W., Casto, B.C., Hammon, W.M., Adenovirus-associated defective virus particles. Science 149 (1965), 754–756.
15. [15] Balakrishnan, B., Jayandharan, G.R., Basic biology of adeno-associated virus (AAV) vectors used in gene therapy. Current gene therapy 14 (2014), 86–100.
16. [16] Sonntag, F., Schmidt, K., Kleinschmidt, J.A., A viral assembly factor promotes AAV2 capsid formation in the nucleolus. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 10220–10225.
17. [17] Gao, G., Vandenberghe, L.H., Alvira, M.R., Lu, Y., Calcedo, R., Zhou, X., Wilson, J.M., Clades of adeno-associated viruses are widely disseminated in human tissues. J. Virol. 78 (2004), 6381–6388.
18. [18] Summerford, C., Samulski, R.J., Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J. Virol. 72 (1998), 1438–1445.
19. [19] Nonnenmacher, M., Weber, T., Intracellular transport of recombinant adeno-associated virus vectors. Gene Ther. 19 (2012), 649–658.
20. [20] Lisowski, L., Tay, S.S., Alexander, I.E., Adeno-associated virus serotypes for gene therapeutics. Curr. Opin. Pharmacol. 24 (2015), 59–67.
21. [21] Berns, K.I., Pinkerton, T.C., Thomas, G.F., Hoggan, M.D., Detection of adeno-associated virus (AAV)-specific nucleotide sequences in DNA isolated from latently infected Detroit 6 cells. Virology 68 (1975), 556–560.
22. [22] Weitzman, M.D., Kyostio, S.R., Kotin, R.M., Owens, R.A., Adeno-associated virus (AAV) Rep proteins mediate complex formation between AAV DNA and its integration site in human DNA. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 5808–5812.
23. [23] Balague, C., Kalla, M., Zhang, W.W., Adeno-associated virus Rep78 protein and terminal repeats enhance integration of DNA sequences into the cellular genome. J. Virol. 71 (1997), 3299–3306.
24. [24] Xiao, X., Xiao, W., Li, J., Samulski, R.J., A novel 165-base-pair terminal repeat sequence is the sole cis requirement for the adeno-associated virus life cycle. J. Virol. 71 (1997), 941–948.
25. [25] Collaco, R.F., Cao, X., Trempe, J.P., A helper virus-free packaging system for recombinant adeno-associated virus vectors. Gene 238 (1999), 397–405.
26. [26] Dong, B., Nakai, H., Xiao, W., Characterization of genome integrity for oversized recombinant AAV vector. Molecular therapy: the journal of the American Society of Gene Therapy 18 (2010), 87–92.
27. [27] Samulski, R.J., Berns, K.I., Tan, M., Muzyczka, N., Cloning of adeno-associated virus into pBR322: rescue of intact virus from the recombinant plasmid in human cells. Proc. Natl. Acad. Sci. U. S. A. 79 (1982), 2077–2081.
28. [28] Zincarelli, C., Soltys, S., Rengo, G., Rabinowitz, J.E., Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Molecular therapy: the journal of the American Society of Gene Therapy 16 (2008), 1073–1080.
29. [29] Aschauer, D.F., 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.
30. [30] Taymans, J.M., Vandenberghe, L.H., Haute, C.V., Thiry, I., Deroose, C.M., Mortelmans, L., Wilson, J.M., Debyser, Z., Baekelandt, V., Comparative analysis of adeno-associated viral vector serotypes 1, 2, 5, 7, and 8 in mouse brain. Hum. Gene Ther. 18 (2007), 195–206.
31. [31] Cearley, C.N., Wolfe, J.H., Transduction characteristics of adeno-associated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain. Molecular therapy: the journal of the American Society of Gene Therapy 13 (2006), 528–537.
32. [32] Davidson, B.L., Stein, C.S., Heth, J.A., Martins, I., Kotin, R.M., Derksen, T.A., Zabner, J., Ghodsi, A., Chiorini, J.A., 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.
33. [33] Wang, C., Wang, C.M., Clark, K.R., Sferra, T.J., Recombinant AAV serotype 1 transduction efficiency and tropism in the murine brain. Gene Ther. 10 (2003), 1528–1534.
34. [34] Castle, M.J., Perlson, E., Holzbaur, E.L., Wolfe, J.H., Long-distance axonal transport of AAV9 is driven by dynein and kinesin-2 and is trafficked in a highly motile Rab7-positive compartment. Molecular therapy: the journal of the American Society of Gene Therapy 22 (2014), 554–566.
35. [35] Zhang, H., Yang, B., Mu, X., Ahmed, S.S., Su, Q., He, R., Wang, H., Mueller, C., Sena-Esteves, M., Brown, R., Xu, Z., Gao, G., Several rAAV vectors efficiently cross the blood-brain barrier and transduce neurons and astrocytes in the neonatal mouse central nervous system. Molecular therapy: the journal of the American Society of Gene Therapy 19 (2011), 1440–1448.
36. [36] Yang, B., Li, S., Wang, H., Guo, Y., Gessler, D.J., Cao, C., Su, Q., Kramer, J., Zhong, L., Ahmed, S.S., Zhang, H., He, R., Desrosiers, R.C., Brown, R., Xu, Z., Gao, G., Global CNS transduction of adult mice by intravenously delivered rAAVrh.8 and rAAVrh.10 and nonhuman primates by rAAVrh.10. Molecular therapy: the journal of the American Society of Gene Therapy 22 (2014), 1299–1309.
37. [37] Miyake, N., Miyake, K., Yamamoto, M., Hirai, Y., Shimada, T., Global gene transfer into the CNS across the BBB after neonatal systemic delivery of single-stranded AAV vectors. Brain Res. 1389 (2011), 19–26.
38. [38] Lentz, T.B., Gray, S.J., Samulski, R.J., Viral vectors for gene delivery to the central nervous system. Neurobiol. Dis. 48 (2012), 179–188.
39. [39] Hadaczek, P., Eberling, J.L., Pivirotto, P., Bringas, J., Forsayeth, J., Bankiewicz, K.S., Eight years of clinical improvement in MPTP-lesioned primates after gene therapy with AAV2-hAADC. Molecular therapy: the journal of the American Society of Gene Therapy 18 (2010), 1458–1461.
40. [40] Leone, P., Shera, D., McPhee, S.W., Francis, J.S., Kolodny, E.H., Bilaniuk, L.T., Wang, D.J., Assadi, M., Goldfarb, O., Goldman, H.W., Freese, A., Young, D., During, M.J., Samulski, R.J., Janson, C.G., Long-term follow-up after gene therapy for canavan disease. Sci. Transl. Med. 4 (2012), 163–165.
41. [41] Bessis, N., GarciaCozar, F.J., Boissier, M.C., Immune responses to gene therapy vectors: influence on vector function and effector mechanisms. Gene Ther. 11:Suppl. 1 (2004), S10–S17.
42. [42] Murrey, D.A., Naughton, B.J., Duncan, F.J., Meadows, A.S., Ware, T.A., Campbell, K.J., Bremer, W.G., Walker, C.M., Goodchild, L., Bolon, B., La Perle, K., Flanigan, K.M., McBride, K.L., McCarty, D.M., Fu, H., Feasibility and safety of systemic rAAV9-hNAGLU delivery for treating mucopolysaccharidosis IIIB: toxicology, biodistribution, and immunological assessments in primates. Human gene therapy. Clinical development 25 (2014), 72–84.
43. [43] McCarty, D.M., Young, S.M. Jr., Samulski, R.J., Integration of adeno-associated virus (AAV) and recombinant AAV vectors. Annu. Rev. Genet. 38 (2004), 819–845.
44. [44] Miyake, K., Miyake, N., Yamazaki, Y., Shimada, T., Hirai, Y., Serotype-independent method of recombinant adeno-associated virus (AAV) vector production and purification. Journal of Nippon Medical School = Nippon Ika Daigaku zasshi 79 (2012), 394–402.
45. [45] Ferrari, F.K., Samulski, T., Shenk, T., Samulski, R.J., Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors. J. Virol. 70 (1996), 3227–3234.
46. [46] McCarty, D.M., Monahan, P.E., Samulski, R.J., Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther. 8 (2001), 1248–1254.
47. [47] Ehlert, E.M., Eggers, R., Niclou, S.P., Verhaagen, J., Cellular toxicity following application of adeno-associated viral vector-mediated RNA interference in the nervous system. BMC Neurosci., 11, 2010, 20.
48. [48] Martin, J.N., Wolken, N., Brown, T., Dauer, W.T., Ehrlich, M.E., Gonzalez-Alegre, P., Lethal toxicity caused by expression of shRNA in the mouse striatum: implications for therapeutic design. Gene Ther. 18 (2011), 666–673.
49. [49] Grimm, D., Streetz, K.L., Jopling, C.L., Storm, T.A., Pandey, K., Davis, C.R., Marion, P., Salazar, F., Kay, M.A., Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441 (2006), 537–541.
50. [50] McBride, J.L., Boudreau, R.L., Harper, S.Q., Staber, P.D., Monteys, A.M., Martins, I., Gilmore, B.L., Burstein, H., Peluso, R.W., Polisky, B., Carter, B.J., Davidson, B.L., Artificial miRNAs mitigate shRNA-mediated toxicity in the brain: implications for the therapeutic development of RNAi. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 5868–5873.
51. [51] Boudreau, R.L., Martins, I., Davidson, B.L., Artificial microRNAs as siRNA shuttles: improved safety as compared to shRNAs in vitro and in vivo. Molecular therapy: the journal of the American Society of Gene Therapy 17 (2009), 169–175.
52. [52] Kotterman, M.A., Schaffer, D.V., Engineering adeno-associated viruses for clinical gene therapy. Nat. Rev. Genet. 15 (2014), 445–451.
53. [53] Zhong, L., Li, B., Mah, C.S., Govindasamy, L., Agbandje-McKenna, M., Cooper, M., Herzog, R.W., Zolotukhin, I., Warrington, K.H. Jr., Weigel-Van Aken, K.A., Hobbs, J.A., Zolotukhin, S., Muzyczka, N., Srivastava, A., Next generation of adeno-associated virus 2 vectors: point mutations in tyrosines lead to high-efficiency transduction at lower doses. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 7827–7832.
54. [54] Choi, V.W., McCarty, D.M., Samulski, R.J., AAV hybrid serotypes: improved vectors for gene delivery. Current gene therapy 5 (2005), 299–310.
55. [55] Rabinowitz, J.E., Bowles, D.E., Faust, S.M., Ledford, J.G., Cunningham, S.E., Samulski, R.J., Cross-dressing the virion: the transcapsidation of adeno-associated virus serotypes functionally defines subgroups. J. Virol. 78 (2004), 4421–4432.
56. [56] Maheshri, N., Koerber, J.T., Kaspar, B.K., Schaffer, D.V., Directed evolution of adeno-associated virus yields enhanced gene delivery vectors. Nat. Biotechnol. 24 (2006), 198–204.
57. [57] Grimm, D., Lee, J.S., Wang, L., Desai, T., Akache, B., Storm, T.A., Kay, M.A., In vitro and in vivo gene therapy vector evolution via multispecies interbreeding and retargeting of adeno-associated viruses. J. Virol. 82 (2008), 5887–5911.
58. [58] Yla-Herttuala, S., Endgame: glybera finally recommended for approval as the first gene therapy drug in the European union. Molecular therapy: the journal of the American Society of Gene Therapy 20 (2012), 1831–1832.
59. [59] High, K.H., Nathwani, A., Spencer, T., Lillicrap, D., Current status of haemophilia gene therapy. Haemophilia: the official journal of the World Federation of Hemophilia 20:Suppl. 4 (2014), 43–49.
60. [60] Duarte-Neves, J., Goncalves, N., Cunha-Santos, J., Simoes, A.T., den Dunnen, W.F., Hirai, H., Kugler, S., Cavadas, C., Pereira de Almeida, L., Neuropeptide Y mitigates neuropathology and motor deficits in mouse models of Machado-Joseph disease. Hum. Mol. Genet. 24 (2015), 5451–5463.
61. [61] Simoes, A.T., Goncalves, N., Koeppen, A., Deglon, N., Kugler, S., Duarte, C.B., Pereira de Almeida, L., Calpastatin-mediated inhibition of calpains in the mouse brain prevents mutant ataxin 3 proteolysis, nuclear localization and aggregation, relieving Machado-Joseph disease. Brain J. Neurol. 135 (2012), 2428–2439.
62. [62] Vite, C.H., Passini, M.A., Haskins, M.E., Wolfe, J.H., Adeno-associated virus vector-mediated transduction in the cat brain. Gene Ther. 10 (2003), 1874–1881.
63. [63] Benkhelifa-Ziyyat, S., Besse, A., Roda, M., Duque, S., Astord, S., Carcenac, R., Marais, T., Barkats, M., Intramuscular scAAV9-SMN injection mediates widespread gene delivery to the spinal cord and decreases disease severity in SMA mice. Molecular therapy: the journal of the American Society of Gene Therapy 21 (2013), 282–290.
64. [64] Ojala, D.S., Amara, D.P., Schaffer, D.V., Adeno-associated virus vectors and neurological gene therapy. The Neuroscientist: a review journal bringing neurobiology, neurology and psychiatry 21 (2015), 84–98.
65. [65] Abbott, N.J., Patabendige, A.A., Dolman, D.E., Yusof, S.R., Begley, D.J., Structure and function of the blood-brain barrier. Neurobiol. Dis. 37 (2010), 13–25.
66. [66] Fu, H., Muenzer, J., Samulski, R.J., Breese, G., Sifford, J., Zeng, X., McCarty, D.M., Self-complementary adeno-associated virus serotype 2 vector: global distribution and broad dispersion of AAV-mediated transgene expression in mouse brain. Molecular therapy: the journal of the American Society of Gene Therapy 8 (2003), 911–917.
67. [67] Burger, C., Nguyen, F.N., Deng, J., Mandel, R.J., Systemic mannitol-induced hyperosmolality amplifies rAAV2-mediated striatal transduction to a greater extent than local co-infusion. Molecular therapy: the journal of the American Society of Gene Therapy 11 (2005), 327–331.
68. [68] McCarty, D.M., DiRosario, J., Gulaid, K., Muenzer, J., Fu, H., Mannitol-facilitated CNS entry of rAAV2 vector significantly delayed the neurological disease progression in MPS IIIB mice. Gene Ther. 16 (2009), 1340–1352.
69. [69] Berger, S., Schurer, L., Hartl, R., Messmer, K., Baethmann, A., Reduction of post-traumatic intracranial hypertension by hypertonic/hyperoncotic saline/dextran and hypertonic mannitol. Neurosurgery 37 (1995), 98–107 discussion 107-108.
70. [70] van Hengel, P., Nikken, J.J., de Jong, G.M., Hesp, W.L., van Bommel, E.F., Mannitol-induced acute renal failure. Neth. J. Med. 50 (1997), 21–24.
71. [71] Choi, J.J., Pernot, M., Small, S.A., Konofagou, E.E., Noninvasive, transcranial and localized opening of the blood-brain barrier using focused ultrasound in mice. Ultrasound Med. Biol. 33 (2007), 95–104.
72. [72] Marquet, F., Tung, Y.S., Teichert, T., Ferrera, V.P., Konofagou, E.E., Noninvasive, transient and selective blood-brain barrier opening in non-human primates in vivo. PLoS One, 6, 2011, e22598.
73. [73] Samiotaki, G., Vlachos, F., Tung, Y.S., Konofagou, E.E., A quantitative pressure and microbubble-size dependence study of focused ultrasound-induced blood-brain barrier opening reversibility in vivo using MRI. Magn. Reson. Med. 67 (2012), 769–777.
74. [74] Hsu, P.H., Wei, K.C., Huang, C.Y., Wen, C.J., Yen, T.C., Liu, C.L., Lin, Y.T., Chen, J.C., Shen, C.R., Liu, H.L., Noninvasive and targeted gene delivery into the brain using microbubble-facilitated focused ultrasound. PLoS One, 8, 2013, e57682.
75. [75] Marquet, F., Teichert, T., Wu, S.Y., Tung, Y.S., Downs, M., Wang, S., Chen, C., Ferrera, V., Konofagou, E.E., Real-time, transcranial monitoring of safe blood-brain barrier opening in non-human primates. PLoS One, 9, 2014, e84310.
76. [76] Downs, M.E., Buch, A., Sierra, C., Karakatsani, M.E., Chen, S., Konofagou, E.E., Ferrera, V.P., Long-term safety of repeated blood-brain barrier opening via focused ultrasound with microbubbles in non-human primates performing a cognitive task. PLoS One, 10, 2015, e0125911.
77. [77] Foust, K.D., Nurre, E., Montgomery, C.L., Hernandez, A., Chan, C.M., Kaspar, B.K., Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat. Biotechnol. 27 (2009), 59–65.
78. [78] Duque, S., Joussemet, B., Riviere, C., Marais, T., Dubreil, L., Douar, A.M., Fyfe, J., Moullier, P., Colle, M.A., Barkats, M., Intravenous administration of self-complementary AAV9 enables transgene delivery to adult motor neurons. Molecular therapy: the journal of the American Society of Gene Therapy 17 (2009), 1187–1196.
79. [79] Gray, S.J., Matagne, V., Bachaboina, L., Yadav, S., Ojeda, S.R., Samulski, R.J., Preclinical differences of intravascular AAV9 delivery to neurons and glia: a comparative study of adult mice and nonhuman primates. Molecular therapy: the journal of the American Society of Gene Therapy 19 (2011), 1058–1069.
80. [80] Manfredsson, F.P., Rising, A.C., Mandel, R.J., AAV9: a potential blood-brain barrier buster. Molecular therapy: the journal of the American Society of Gene Therapy 17 (2009), 403–405.
81. [81] DiMattia, M.A., Nam, H.J., Van Vliet, K., Mitchell, M., Bennett, A., Gurda, B.L., McKenna, R., Olson, N.H., Sinkovits, R.S., Potter, M., Byrne, B.J., Aslanidi, G., Zolotukhin, S., Muzyczka, N., Baker, T.S., Agbandje-McKenna, M., Structural insight into the unique properties of adeno-associated virus serotype 9. J. Virol. 86 (2012), 6947–6958.
82. [82] Wang, D.B., Dayton, R.D., Henning, P.P., Cain, C.D., Zhao, L.R., Schrott, L.M., Orchard, E.A., Knight, D.S., Klein, R.L., Expansive gene transfer in the rat CNS rapidly produces amyotrophic lateral sclerosis relevant sequelae when TDP-43 is overexpressed. Molecular therapy: the journal of the American Society of Gene Therapy 18 (2010), 2064–2074.
83. [83] Rahim, A.A., Wong, A.M., Hoefer, K., Buckley, S.M., Mattar, C.N., Cheng, S.H., Chan, J.K., Cooper, J.D., Waddington, S.N., Intravenous administration of AAV2/9 to the fetal and neonatal mouse leads to differential targeting of CNS cell types and extensive transduction of the nervous system. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 25 (2011), 3505–3518.
84. [84] Foust, K.D., Wang, X., McGovern, V.L., Braun, L., Bevan, A.K., Haidet, A.M., Le, T.T., Morales, P.R., Rich, M.M., Burghes, A.H., Kaspar, B.K., Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat. Biotechnol. 28 (2010), 271–274.
85. [85] Nagai, M., Re, D.B., Nagata, T., Chalazonitis, A., Jessell, T.M., Wichterle, H., Przedborski, S., Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat. Neurosci. 10 (2007), 615–622.
86. [86] Colangelo, A.M., Alberghina, L., Papa, M., Astrogliosis as a therapeutic target for neurodegenerative diseases. Neurosci. Lett. 565 (2014), 59–64.
87. [87] Lowenstein, P.R., Crossing the rubicon. Nat. Biotechnol. 27 (2009), 42–44.
88. [88] Dehay, B., Dalkara, D., Dovero, S., Li, Q., Bezard, E., Systemic scAAV9 variant mediates brain transduction in newborn rhesus macaques. Sci. Report., 2, 2012, 253.
89. [89] Bevan, A.K., Duque, S., Foust, K.D., Morales, P.R., Braun, L., Schmelzer, L., Chan, C.M., McCrate, M., Chicoine, L.G., Coley, B.D., Porensky, P.N., Kolb, S.J., Mendell, J.R., Burghes, A.H., Kaspar, B.K., Systemic gene delivery in large species for targeting spinal cord, brain, and peripheral tissues for pediatric disorders. Molecular therapy: the journal of the American Society of Gene Therapy 19 (2011), 1971–1980.
90. [90] Samaranch, L., Salegio, E.A., San Sebastian, W., Kells, A.P., Foust, K.D., Bringas, J.R., Lamarre, C., Forsayeth, J., Kaspar, B.K., Bankiewicz, K.S., Adeno-associated virus serotype 9 transduction in the central nervous system of nonhuman primates. Hum. Gene Ther. 23 (2012), 382–389.
91. [91] Mattar, C.N., Waddington, S.N., Biswas, A., Johana, N., Ng, X.W., Fisk, A.S., Fisk, N.M., Tan, L.G., Rahim, A.A., Buckley, S.M., Tan, M.H., Lu, J., Choolani, M., Chan, J.K., Systemic delivery of scAAV9 in fetal macaques facilitates neuronal transduction of the central and peripheral nervous systems. Gene Ther. 20 (2013), 69–83.
92. [92] Karda, R., Buckley, S.M., Mattar, C.N., Ng, J., Massaro, G., Hughes, M.P., Kurian, M.A., Baruteau, J., Gissen, P., Chan, J.K., Bacchelli, C., Waddington, S.N., Rahim, A.A., Perinatal systemic gene delivery using adeno-associated viral vectors. Front. Mol. Neurosci., 7, 2014, 89.
93. [93] Valori, C.F., Ning, K., Wyles, M., Mead, R.J., Grierson, A.J., Shaw, P.J., Azzouz, M., Systemic delivery of scAAV9 expressing SMN prolongs survival in a model of spinal muscular atrophy. Sci. Transl. Med. 2 (2010), 35–42.
94. [94] Dominguez, E., Marais, T., Chatauret, N., Benkhelifa-Ziyyat, S., Duque, S., Ravassard, P., Carcenac, R., Astord, S., Pereira de Moura, A., Voit, T., Barkats, M., Intravenous scAAV9 delivery of a codon-optimized SMN1 sequence rescues SMA mice. Hum. Mol. Genet. 20 (2011), 681–693.
95. [95] Glascock, J.J., Osman, E.Y., Wetz, M.J., Krogman, M.M., Shababi, M., Lorson, C.L., Decreasing disease severity in symptomatic, Smn(−/−);SMN2(+/+), spinal muscular atrophy mice following scAAV9-SMN delivery. Hum. Gene Ther. 23 (2012), 330–335.
96. [96] Meyer, K., Ferraiuolo, L., Schmelzer, L., Braun, L., McGovern, V., Likhite, S., Michels, O., Govoni, A., Fitzgerald, J., Morales, P., Foust, K.D., Mendell, J.R., Burghes, A.H., Kaspar, B.K., Improving single injection CSF delivery of AAV9-mediated gene therapy for SMA: a dose-response study in mice and nonhuman primates. Molecular therapy: the journal of the American Society of Gene Therapy 23 (2015), 477–487.
97. [97] Hamilton, G., Gillingwater, T.H., Spinal muscular atrophy: going beyond the motor neuron. Trends Mol. Med. 19 (2013), 40–50.
98. [98] Duque, S.I., Arnold, W.D., Odermatt, P., Li, X., Porensky, P.N., Schmelzer, L., Meyer, K., Kolb, S.J., Schumperli, D., Kaspar, B.K., Burghes, A.H., A large animal model of spinal muscular atrophy and correction of phenotype. Ann. Neurol. 77 (2015), 399–414.
99. [99] Garg, S.K., Lioy, D.T., Cheval, H., McGann, J.C., Bissonnette, J.M., Murtha, M.J., Foust, K.D., Kaspar, B.K., Bird, A., Mandel, G., Systemic delivery of MeCP2 rescues behavioral and cellular deficits in female mouse models of Rett syndrome. J. Neurosci. 33 (2013), 13612–13620.
100. [100] Lioy, D.T., Garg, S.K., Monaghan, C.E., Raber, J., Foust, K.D., Kaspar, B.K., Hirrlinger, P.G., Kirchhoff, F., Bissonnette, J.M., Ballas, N., Mandel, G., A role for glia in the progression of Rett's syndrome. Nature 475 (2011), 497–500.
101. [101] Fu, H., Dirosario, J., Killedar, S., Zaraspe, K., McCarty, D.M., Correction of neurological disease of mucopolysaccharidosis IIIB in adult mice by rAAV9 trans-blood-brain barrier gene delivery. Molecular therapy: the journal of the American Society of Gene Therapy 19 (2011), 1025–1033.
102. [102] Falk, D.J., Mah, C.S., Soustek, M.S., Lee, K.Z., Elmallah, M.K., Cloutier, D.A., Fuller, D.D., Byrne, B.J., Intrapleural administration of AAV9 improves neural and cardiorespiratory function in Pompe disease. Molecular therapy: the journal of the American Society of Gene Therapy 21 (2013), 1661–1667.
103. [103] Todd, A.G., McElroy, J.A., Grange, R.W., Fuller, D.D., Walter, G.A., Byrne, B.J., Falk, D.J., Correcting neuromuscular deficits with gene therapy in Pompe disease. Ann. Neurol., 2015.
104. [104] Dufour, B.D., Smith, C.A., Clark, R.L., Walker, T.R., McBride, J.L., Intrajugular vein delivery of AAV9-RNAi prevents neuropathological changes and weight loss in Huntington's disease mice. Molecular therapy: the journal of the American Society of Gene Therapy 22 (2014), 797–810.
105. [105] Konno, A., Shuvaev, A.N., Miyake, N., Miyake, K., Iizuka, A., Matsuura, S., Huda, F., Nakamura, K., Yanagi, S., Shimada, T., Hirai, H., Mutant ataxin-3 with an abnormally expanded polyglutamine chain disrupts dendritic development and metabotropic glutamate receptor signaling in mouse cerebellar Purkinje cells. Cerebellum 13 (2014), 29–41.
106. [106] Iwata, N., Sekiguchi, M., Hattori, Y., Takahashi, A., Asai, M., Ji, B., Higuchi, M., Staufenbiel, M., Muramatsu, S., Saido, T.C., Global brain delivery of neprilysin gene by intravascular administration of AAV vector in mice. Sci. Report., 3, 2013, 1472.
107. [107] Passini, M.A., Bu, J., Richards, A.M., Treleaven, C.M., Sullivan, J.A., O'Riordan, C.R., Scaria, A., Kells, A.P., Samaranch, L., San Sebastian, W., Federici, T., Fiandaca, M.S., Boulis, N.M., Bankiewicz, K.S., Shihabuddin, L.S., Cheng, S.H., Translational fidelity of intrathecal delivery of self-complementary AAV9-survival motor neuron 1 for spinal muscular atrophy. Hum. Gene Ther. 25 (2014), 619–630.
108. [108] Little, D., Valori, C.F., Mutsaers, C.A., Bennett, E.J., Wyles, M., Sharrack, B., Shaw, P.J., Gillingwater, T.H., Azzouz, M., Ning, K., PTEN depletion decreases disease severity and modestly prolongs survival in a mouse model of spinal muscular atrophy. Molecular therapy: the journal of the American Society of Gene Therapy 23 (2015), 270–277.
109. [109] Nizzardo, M., Simone, C., Rizzo, F., Salani, S., Dametti, S., Rinchetti, P., Del Bo, R., Foust, K., Kaspar, B.K., Bresolin, N., Comi, G.P., Corti, S., Gene therapy rescues disease phenotype in a spinal muscular atrophy with respiratory distress type 1 (SMARD1) mouse model. Science advances, 1, 2015, e1500078.
110. [110] Foust, K.D., Salazar, D.L., Likhite, S., Ferraiuolo, L., Ditsworth, D., Ilieva, H., Meyer, K., Schmelzer, L., Braun, L., Cleveland, D.W., Kaspar, B.K., Therapeutic AAV9-mediated suppression of mutant SOD1 slows disease progression and extends survival in models of inherited ALS. Molecular therapy: the journal of the American Society of Gene Therapy 21 (2013), 2148–2159.
111. [111] Thomsen, G.M., Gowing, G., Latter, J., Chen, M., Vit, J.P., Staggenborg, K., Avalos, P., Alkaslasi, M., Ferraiuolo, L., Likhite, S., Kaspar, B.K., Svendsen, C.N., Delayed disease onset and extended survival in the SOD1G93A rat model of amyotrophic lateral sclerosis after suppression of mutant SOD1 in the motor cortex. J. Neurosci. 34 (2014), 15587–15600.
112. [112] Yamashita, T., Chai, H.L., Teramoto, S., Tsuji, S., Shimazaki, K., Muramatsu, S., Kwak, S., Rescue of amyotrophic lateral sclerosis phenotype in a mouse model by intravenous AAV9-ADAR2 delivery to motor neurons. EMBO molecular medicine 5 (2013), 1710–1719.
113. [113] Gadalla, K.K., Bailey, M.E., Spike, R.C., Ross, P.D., Woodard, K.T., Kalburgi, S.N., Bachaboina, L., Deng, J.V., West, A.E., Samulski, R.J., Gray, S.J., Cobb, S.R., Improved survival and reduced phenotypic severity following AAV9/MECP2 gene transfer to neonatal and juvenile male Mecp2 knockout mice. Molecular therapy: the journal of the American Society of Gene Therapy 21 (2013), 18–30.
114. [114] Hinderer, C., Bell, P., Gurda, B.L., Wang, Q., Louboutin, J.P., Zhu, Y., Bagel, J., O'Donnell, P., Sikora, T., Ruane, T., Wang, P., Haskins, M.E., Wilson, J.M., Intrathecal gene therapy corrects CNS pathology in a feline model of mucopolysaccharidosis I. Molecular therapy: the journal of the American Society of Gene Therapy 22 (2014), 2018–2027.
115. [115] Ruzo, A., Marco, S., Garcia, M., Villacampa, P., Ribera, A., Ayuso, E., Maggioni, L., Mingozzi, F., Haurigot, V., Bosch, F., Correction of pathological accumulation of glycosaminoglycans in central nervous system and peripheral tissues of MPSIIIA mice through systemic AAV9 gene transfer. Hum. Gene Ther. 23 (2012), 1237–1246.
116. [116] Haurigot, V., Marco, S., Ribera, A., Garcia, M., Ruzo, A., Villacampa, P., Ayuso, E., Anor, S., Andaluz, A., Pineda, M., Garcia-Fructuoso, G., Molas, M., Maggioni, L., Munoz, S., Motas, S., Ruberte, J., Mingozzi, F., Pumarola, M., Bosch, F., Whole body correction of mucopolysaccharidosis IIIA by intracerebrospinal fluid gene therapy. J. Clin. Invest., 2013.
117. [117] Ribera, A., Haurigot, V., Garcia, M., Marco, S., Motas, S., Villacampa, P., Maggioni, L., Leon, X., Molas, M., Sanchez, V., Munoz, S., Leborgne, C., Moll, X., Pumarola, M., Mingozzi, F., Ruberte, J., Anor, S., Bosch, F., Biochemical, histological and functional correction of mucopolysaccharidosis type IIIB by intra-cerebrospinal fluid gene therapy. Hum. Mol. Genet. 24 (2015), 2078–2095.
118. [118] Cearley, C.N., Wolfe, J.H., A single injection of an adeno-associated virus vector into nuclei with divergent connections results in widespread vector distribution in the brain and global correction of a neurogenetic disease. J. Neurosci. 27 (2007), 9928–9940.
119. [119] Gurda, B.L., De Guilhem De Lataillade, A., Bell, P., Zhu, Y., Yu, H., Wang, P., Bagel, J., Vite, C.H., Sikora, T., Hinderer, C., Calcedo, R., Yox, A.D., Steet, R.A., Ruane, T., O'Donnell, P., Gao, G., Wilson, J.M., Casal, M., Ponder, K.P., Haskins, M.E., Evaluation of AAV-mediated gene therapy for central nervous system disease in canine mucopolysaccharidosis VII. Molecular therapy: the journal of the American Society of Gene Therapy 24 (2016), 206–216.
120. [120] Weismann, C.M., Ferreira, J., Keeler, A.M., Su, Q., Qui, L., Shaffer, S.A., Xu, Z., Gao, G., Sena-Esteves, M., Systemic AAV9 gene transfer in adult GM1 gangliosidosis mice reduces lysosomal storage in CNS and extends lifespan. Hum. Mol. Genet. 24 (2015), 4353–4364.
121. [121] Walia, J.S., Altaleb, N., Bello, A., Kruck, C., LaFave, M.C., Varshney, G.K., Burgess, S.M., Chowdhury, B., Hurlbut, D., Hemming, R., Kobinger, G.P., Triggs-Raine, B., Long-term correction of Sandhoff disease following intravenous delivery of rAAV9 to mouse neonates. Molecular therapy: the journal of the American Society of Gene Therapy 23 (2015), 414–422.
122. [122] Spampanato, C., De Leonibus, E., Dama, P., Gargiulo, A., Fraldi, A., Sorrentino, N.C., Russo, F., Nusco, E., Auricchio, A., Surace, E.M., Ballabio, A., Efficacy of a combined intracerebral and systemic gene delivery approach for the treatment of a severe lysosomal storage disorder. Molecular therapy: the journal of the American Society of Gene Therapy 19 (2011), 860–869.
123. [123] Miyake, N., Miyake, K., Asakawa, N., Yamamoto, M., Shimada, T., Long-term correction of biochemical and neurological abnormalities in MLD mice model by neonatal systemic injection of an AAV serotype 9 vector. Gene Ther. 21 (2014), 427–433.
124. [124] Elmallah, M.K., Falk, D.J., Nayak, S., Federico, R.A., Sandhu, M.S., Poirier, A., Byrne, B.J., Fuller, D.D., Sustained correction of motoneuron histopathology following intramuscular delivery of AAV in pompe mice. Molecular therapy: the journal of the American Society of Gene Therapy 22 (2014), 702–712.
125. [125] Todd, A.G., McElroy, J.A., Grange, R.W., Fuller, D.D., Walter, G.A., Byrne, B.J., Falk, D.J., Correcting neuromuscular deficits with gene therapy in Pompe disease. Ann. Neurol. 78 (2015), 222–234.
126. [126] Gong, Y., Mu, D., Prabhakar, S., Moser, A., Musolino, P., Ren, J., Breakefield, X.O., Maguire, C.A., Eichler, F.S., Adenoassociated virus serotype 9-mediated gene therapy for x-linked adrenoleukodystrophy. Molecular therapy: the journal of the American Society of Gene Therapy 23 (2015), 824–834.
127. [127] Xue, Y.Q., Ma, B.F., Zhao, L.R., Tatom, J.B., Li, B., Jiang, L.X., Klein, R.L., Duan, W.M., AAV9-mediated erythropoietin gene delivery into the brain protects nigral dopaminergic neurons in a rat model of Parkinson's disease. Gene Ther. 17 (2010), 83–94.
128. [128] Sanftner, L.M., Suzuki, B.M., Doroudchi, M.M., Feng, L., McClelland, A., Forsayeth, J.R., Cunningham, J., Striatal delivery of rAAV-hAADC to rats with preexisting immunity to AAV. Molecular therapy: the journal of the American Society of Gene Therapy 9 (2004), 403–409.
129. [129] Peden, C.S., Burger, C., Muzyczka, N., Mandel, R.J., Circulating anti-wild-type adeno-associated virus type 2 (AAV2) antibodies inhibit recombinant AAV2 (rAAV2)-mediated, but not rAAV5-mediated, gene transfer in the brain. J. Virol. 78 (2004), 6344–6359.
130. [130] Snyder, B.R., Gray, S.J., Quach, E.T., Huang, J.W., Leung, C.H., Samulski, R.J., Boulis, N.M., Federici, T., Comparison of adeno-associated viral vector serotypes for spinal cord and motor neuron gene delivery. Hum. Gene Ther. 22 (2011), 1129–1135.
131. [131] Federici, T., Taub, J.S., Baum, G.R., Gray, S.J., Grieger, J.C., Matthews, K.A., Handy, C.R., Passini, M.A., Samulski, R.J., Boulis, N.M., Robust spinal motor neuron transduction following intrathecal delivery of AAV9 in pigs. Gene Ther. 19 (2012), 852–859.
132. [132] Bucher, T., Dubreil, L., Colle, M.A., Maquigneau, M., Deniaud, J., Ledevin, M., Moullier, P., Joussemet, B., Intracisternal delivery of AAV9 results in oligodendrocyte and motor neuron transduction in the whole central nervous system of cats. Gene Ther. 21 (2014), 522–528.
133. [133] Schuster, D.J., Dykstra, J.A., Riedl, M.S., Kitto, K.F., Belur, L.R., McIvor, R.S., Elde, R.P., Fairbanks, C.A., Vulchanova, L., Biodistribution of adeno-associated virus serotype 9 (AAV9) vector after intrathecal and intravenous delivery in mouse. Front. Neuroanat., 8, 2014, 42.