Viral vectors for therapy of neurologic diseases

Neuropharmacology

Volumn 120, Issue , 2017, Pages 63-80

  Choudhury, Sourav R ^a   Hudry, Eloise ^b   Maguire, Casey A ^c   Sena Esteves, Miguel ^a   Breakefield, Xandra O ^c   Grandi, Paola ^d  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

Brain tumors; Gene therapy; Lysosomal storage diseases; Metabolic diseases; Neurodegeneration; Viral vectors

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; ADENOVIRUS VECTOR; AROMATIC LEVO AMINO ACID DECARBOXYLASE; ASPARTOACYLASE; CEREBROSIDE SULFATASE; CLAUDIN 2; DOPAMINE 2 RECEPTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLUTAMATE DECARBOXYLASE; GUANOSINE TRIPHOSPHATE CYCLOHYDROLASE I; HERPES SIMPLEX VIRUS 1 VECTOR; LENTIVIRUS VECTOR; LEVODOPA; METHYL CPG BINDING PROTEIN 2; MICRORNA; MYELIN BASIC PROTEIN; NERVE GROWTH FACTOR; NEURTURIN; ONCOLYTIC ADENOVIRUS; ONCOLYTIC HERPES VIRUS; ONCOLYTIC POLIOVIRUS; ONCOLYTIC VIRUS; RETROVIRUS VECTOR; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; SURVIVAL MOTOR NEURON PROTEIN 1; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VIRUS VECTOR; WISKOTT ALDRICH SYNDROME PROTEIN;

ABSENCE OF SIDE EFFECTS; ADRENOLEUKODYSTROPHY; AGE; ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; BRAIN BLOOD VESSEL; BRAIN CANCER; BRAIN DEPTH STIMULATION; BRAIN EDEMA; CANAVAN DISEASE; CEREBROSPINAL FLUID; DEGENERATIVE DISEASE; DRUG DOSE ESCALATION; DRUG MEGADOSE; DRUG SAFETY; DRUG TARGETING; DRUG TOLERABILITY; EX VIVO GENE TRANSFER; GENE EXPRESSION; GENE REPLACEMENT THERAPY; GENETIC ENGINEERING; GLIOBLASTOMA; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; HUNTINGTON CHOREA; MACHADO JOSEPH DISEASE; METACHROMATIC LEUKODYSTROPHY; MULTIPLE SCLEROSIS; NEUROFIBROMATOSIS; NEUROLOGIC DISEASE; NEURONAL CEROID LIPOFUSCINOSIS; NONHUMAN; ONCOLYTIC VIROTHERAPY; PARKINSON DISEASE; PRIORITY JOURNAL; RETT SYNDROME; REVIEW; SPINAL MUSCULAR ATROPHY; TUBEROUS SCLEROSIS; TUMOR SUPPRESSOR GENE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; WISKOTT ALDRICH SYNDROME; ANIMAL; BRAIN NEOPLASMS; GENE THERAPY; GENE TRANSFER; GENE VECTOR; NERVOUS SYSTEM DISEASES; PHYSIOLOGY; PROCEDURES; THERAPEUTIC USE;

ANIMALS; BRAIN NEOPLASMS; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; HUMANS; NERVOUS SYSTEM DISEASES;

EID: 84959449697     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2016.02.013     Document Type: Review

References (229)

1. Ahmed, S.S., Li, H., Cao, C., Sikoglu, E.M., Denninger, A.R., Su, Q., Eaton, S., Liso Navarro, A.A., Xie, J., Szucs, S., Zhang, H., Moore, C., Kirschner, D.A., Seyfried, T.N., Flotte, T.R., Matalon, R., Gao, G., A single intravenous rAAV injection as late as P20 achieves efficacious and sustained CNS gene therapy in Canavan mice. Mol. Ther. 21:12 (2013), 2136–2147, 10.1038/mt.2013.138.
2. Aiuti, A., Biasco, L., Scaramuzza, S., Ferrua, F., Cicalese, M.P., Baricordi, C., Dionisio, F., Calabria, A., Giannelli, S., Castiello, M.C., Bosticardo, M., Evangelio, C., Assanelli, A., Casiraghi, M., Di Nunzio, S., Callegaro, L., Benati, C., Rizzardi, P., Pellin, D., Di Serio, C., Schmidt, M., Von Kalle, C., Gardner, J., Mehta, N., Neduva, V., Dow, D.J., Galy, A., Miniero, R., Finocchi, A., Metin, A., Banerjee, P.P., Orange, J.S., Galimberti, S., Valsecchi, M.G., Biffi, A., Montini, E., Villa, A., Ciceri, F., Roncarolo, M.G., Naldini, L., Lentiviral hematopoietic stem cell gene therapy in patients with Wiskott-Aldrich syndrome. Science, 341(6148), 2013, 1233151, 10.1126/science.1233151.
3. Akli, S., Caillaud, C., Vigne, E., Stratford-Perricaudet, L.D., Poenaru, L., Perricaudet, M., Kahn, A., Peschanski, M.R., Transfer of a foreign gene into the brain using adenovirus vectors. Nat. Genet. 3:3 (1993), 224–228.
4. Altman-Hamamdzic, S., Groseclose, C., Ma, J.X., Hamamdzic, D., Vrindavanam, N.S., Middaugh, L.D., Parratto, N.P., Sallee, F.R., Expression of beta-galactosidase in mouse brain: utilization of a novel nonreplicative Sindbis virus vector as a neuronal gene delivery system. Gene Ther. 4:8 (1997), 815–822.
5. Anguela, X.M., Sharma, R., Doyon, Y., Miller, J.C., Li, H., Haurigot, V., Rohde, M.E., Wong, S.Y., Davidson, R.J., Zhou, S., Gregory, P.D., Holmes, M.C., High, K.A., Robust ZFN-mediated genome editing in adult hemophilic mice. Blood 122:19 (2013), 3283–3287, 10.1182/blood-2013-04-497354.
6. Balaj, L., Lessard, R., Dai, L., Cho, Y.-J., Pomeroy, S.L., Breakefield, X.O., Skog, J., Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat. Commun., 2, 2011, 180, 10.1038/ncomms1180.
7. Ballard, C., Gauthier, S., Corbett, A., Brayne, C., Aarsland, D., Jones, E., Alzheimer's disease. Lancet 377:9770 (2011), 1019–1031, 10.1016/S0140-6736(10)61349-9.
8. Bankiewicz, K.S., Eberling, J.L., Kohutnicka, M., Jagust, W., Pivirotto, P., Bringas, J., Cunningham, J., Budinger, T.F., Harvey-White, J., 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. 164:1 (2000), 2–14.
9. Barcia, C., Jimenez-Dalmaroni, M., Kroeger, K.M., Puntel, M., Rapaport, A.J., Larocque, D., King, G.D., Johnson, S.A., Liu, C., Xiong, W., Candolfi, M., Mondkar, S., Ng, P., Palmer, D., Castro, M.G., Lowenstein, P.R., One-year expression from high-capacity adenoviral vectors in the brains of animals with pre-existing anti-adenoviral immunity: clinical implications. Mol. Ther. 15:12 (2007), 2154–2163.
10. Bartus, R.T., Weinberg, M.S., Samulski, R.J., Parkinson's disease gene therapy: success by design meets failure by efficacy. Mol. Ther. 22:3 (2014), 487–497, 10.1038/mt.2013.281.
11. Barzel, A., Paulk, N.K., Shi, Y., Huang, Y., Chu, K., Zhang, F., Valdmanis, P.N., Spector, L.P., Porteus, M.H., Gaensler, K.M., Kay, M.A., Promoterless gene targeting without nucleases ameliorates haemophilia B in mice. Nature 517:7534 (2015), 360–364, 10.1038/nature13864.
12. Bedse, G., Di Domenico, F., Serviddio, G., Cassano, T., Aberrant insulin signaling in Alzheimer's disease: current knowledge. Front. Neurosci., 9, 2015, 204, 10.3389/fnins.2015.00204.
13. Bell, C.L., Vandenberghe, L.H., Bell, P., Limberis, M.P., Gao, G.P., Van Vliet, K., Agbandje-McKenna, M., Wilson, J.M., The AAV9 receptor and its modification to improve in vivo lung gene transfer in mice. J. Clin. Invest. 121:6 (2011), 2427–2435, 10.1172/JCI57367.
14. Bengtsson, N.E., Seto, J.T., Hall, J.K., Chamberlain, J.S., Odom, G.L., Progress and prospects of gene therapy clinical trials for the muscular dystrophies. Hum. Mol. Genet., 2015 Oct 8, pii: ddv420. [Epub ahead of print], PMID: 26450518.
15. Berry, G.E., Asokan, A., Chemical modulation of endocytic sorting augments adeno-associated viral transduction. J. Biol. Chem. 291:2 (2016), 939–947, 10.1074/jbc.M115.687657.
16. Bessis, N., GarciaCozar, F.J., Boissier, M.C., Immune responses to gene therapy vectors: influence on vector function and effector mechanisms. Gene Ther.(Suppl. 1), 2004, S10–S17.
17. Bevan, A.K., Hutchinson, K.R., Foust, K.D., Braun, L., McGovern, V.L., Schmelzer, L., Ward, J.G., Petruska, J.C., Lucchesi, P.A., Burghes, A.H., Kaspar, B.K., Early heart failure in the SMNDelta7 model of spinal muscular atrophy and correction by postnatal scAAV9-SMN delivery. Hum. Mol. Genet. 19:20 (2010), 3895–3905, 10.1093/hmg/ddq300.
18. 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.M., Kaspa, B.K., Systemic gene delivery in large species for targeting spinal cord, brain, and peripheral tissues for pediatric disorders. Mol. Ther. 19:11 (2011), 1971–1980, 10.1038/mt.2011.157.
19. Biffi, A., Montini, E., Lorioli, L., Cesani, M., Fumagalli, F., Plati, T., Baldoli, C., Martino, S., Calabria, A., Canale, S., Benedicenti, F., Vallanti, G., Biasco, L., Leo, S., Kabbara, N., Zanetti, G., Rizzo, W.B., Mehta, N.A., Cicalese, M.P., Casiraghi, M., Boelens, J.J., Del Carro, U., Dow, D.J., Schmidt, M., Assanelli, A., Neduva, V., Di Serio, C., Stupka, E., Gardner, J., von Kalle, C., Bordignon, C., Ciceri, F., Rovelli, A., Roncarolo, M.G., Aiuti, A., Sessa, M., Naldini, L., Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science, 341(6148), 2013, 1233158, 10.1126/science.1233158.
20. Bledsoe, A.W., Jackson, C.A., McPherson, S., Morrow, C.D., Cytokine production in motor neurons by poliovirus replicon vector gene delivery. Nat. Biotechnol. 18:9 (2000), 964–969.
21. Blömer, U., Naldini, L., Kafri, T., Trono, D., Verma, I.M., Gage, F.H., Highly efficient and sustained gene transfer in adult neurons with a lentivirus vector. J. Virol. 71:9 (1997), 6641–6649.
22. Bowers, W.J., Breakefield, X.O., Sena-Esteves, M., Genetic therapy for the nervous system. Hum. Mol. Genet. 20:R1 (2011), R28–R41.
23. Breakefield, X.O., Sena-Esteves, M., Healing genes in the nervous system. Neuron 68:2 (2010), 178–181.
24. Breunig, J.J., Guillot-Sestier, M.V., Town, T., Brain injury, neuroinflammation and Alzheimer's disease. Front. Againg Neurosci., 5, 2013, 26, 10.3389/fnagi.2013.00026.
25. Broekman, M.L., Tierney, L.A., Benn, C., Chawla, P., Cha, J.H., Sena-Esteves, M., Mechanisms of distribution of mouse beta-galactosidase in the adult GM1-gangliosidosis brain. Gene Ther. 16:2 (2009), 303–308, 10.1038/gt.2008.149.
26. Brooks, A.I., Stein, C.S., Hughes, S.M., Heth, J., McCray, P.M., Sauter, S.L., Johnston, J.C., Cory-Slechta, D.A., Federoff, H.J., Davidson, B.L., Functional correction of established central nervous system deficits in an animal model of lysosomal storage disease with feline immunodeficiency virus-based vectors. Proc. Natl. Acad. Sci. U. S. A. 99:9 (2002), 6216–6221.
27. Brown, M.C., Gromeier, M., Cytotoxic and immunogenic mechanisms of recombinant oncolytic poliovirus. Curr. Opin. Virol. 13 (2015), 81–85, 10.1016/j.coviro.2015.05.007.
28. Burger, C., Gorbatyuk, O.S., Velardo, M.J., Peden, C.S., Williams, P., Zolotukhin, S., Reier, P.J., Mandel, R.J., Muzyczka, N., 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. 10:2 (2004), 302–317.
29. Burlot, M.A., Braudeau, J., Michaelsen-Preusse, K., Potier, B., Ayciriex, S., Varin, J., Gautier, B., Djelti, F., Audrain, M., Dauphinot, L., Fernandez-Gomez, F.J., Caillierez, R., Laprévote, O., Bièche, I., Auzeil, N., Potier, M.C., Dutar, P., Korte, M., Buée, L., Blum, D., Cartier, N., Cholesterol 24-hydroxylase defect is implicated in memory impairments associated with Alzheimer-like Tau pathology. Hum. Mol. Genet. 24:21 (2015), 5965–5976, 10.1093/hmg/ddv268.
30. Burns, A., Iliffe, S., Alzheimer's disease. BMJ, 338, 2009, b158, 10.1136/bmj.b158.
31. Cachón-González, M.B., Wang, S.Z., Lynch, A., Ziegler, R., Cheng, S.H., Cox, T.M., Effective gene therapy in an authentic model of Tay-Sachs-related diseases. Proc. Natl. Acad. Sci. U. S. A. 103:27 (2006), 10373–10378.
32. Cartier, N., Hacein-Bey-Abina, S., Bartholomae, C.C., Veres, G., Schmidt, M., Kutschera, I., Vidaud, M., Abel, U., Dal-Cortivo, L., Caccavelli, L., Mahlaoui, N., Kiermer, V., Mittelstaedt, D., Bellesme, C., Lahlou, N., Lefrère, F., Blanche, S., Audit, M., Payen, E., Leboulch, P., l'Homme, B., Bougnères, P., Von Kalle, C., Fischer, A., Cavazzana-Calvo, M., Aubourg, P., Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326:5954 (2009), 818–823, 10.1126/science.1171242.
33. Cartier, N., Aubourg, P., Hematopoietic stem cell transplantation and hematopoietic stem cell gene therapy in X-linked adrenoleukodystrophy. Brain Pathol. 20 (2010), 857–862.
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. Mol. Ther. 22:3 (2014), 554–566, 10.1038/mt.2013.237.
35. Castle, M.J., Turunen, H.T., Vandenberghe, L.H., Wolfe, J.H., Controlling AAV tropism in the nervous system with natural and engineered capsids. Methods Mol. Biol. 1382 (2016), 133–149, 10.1007/978-1-4939-3271-9_10.
36. Cattoglio, C., Facchini, G., Sartori, D., Antonelli, A., Miccio, A., Cassani, B., Schmidt, M., von Kalle, C., Howe, S., Thrasher, A.J., Aiuti, A., Ferrari, G., Recchia, A., Mavilio, F., Hot spots of retroviral integration in human CD34+ hematopoietic cells. Blood 110:6 (2007), 1770–1778.
37. Cavazzana-Calvo, M., Hacein-Bey, S., de Saint Basile, G., Gross, F., Yvon, E., Nusbaum, P., Selz, F., Hue, C., Certain, S., Casanova, J.L., Bousso, P., Deist, F.L., Fischer, A., Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 288:5466 (2000), 669–672.
38. 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. Mol. Ther. 13:3 (2006), 528–537.
39. 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. 27:37 (2007), 9928–9940.
40. Cechetto, D.F., Hachinski, V., Whitehead, S.N., Vascular risk factors and Alzheimer's disease. Expert Rev. Neurother. 8:5 (2008), 743–750, 10.1586/14737175.8.5.743.
41. Cesana, D., Ranzani, M., Volpin, M., Bartholomae, C., Duros, C., Artus, A., Merella, S., Benedicenti, F., Sergi Sergi, L., Sanvito, F., Brombin, C., Nonis, A., Serio, C.D., Doglioni, C., von Kalle, C., Schmidt, M., Cohen-Haguenauer, O., Naldini, L., Montini, E., Uncovering and dissecting the genotoxicity of self-inactivating lentiviral vectors in vivo. Mol. Ther. 22:4 (2014), 774–785, 10.1038/mt.2014.3.
42. Cetin, A., Komai, S., Eliava, M., Seeburg, P.H., Osten, P., Stereotaxic gene delivery in the rodent brain. Nat. Protoc. 1:6 (2006), 3166–3173.
43. Chakrabarty, P., Rosario, A., Cruz, P., Siemienski, Z., Ceballos-Diaz, C., Crosby, K., Jansen, K., Borchelt, D.R., Kim, J.Y., Jankowsky, J.L., Golde, T.E., Levites, Y., Capsid serotype and timing of injection determines AAV transduction in the neonatal mice brain. PLoS One, 8(6), 2013, e67680, 10.1371/journal.pone.0067680.
44. Chamberlain, K., Riyad, J.M., Weber, T., Expressing transgenes that exceed the packaging capacity of AAV capsids. Hum. Gene Ther. Methods, 2016 Jan 12, [Epub ahead of print], PMID: 26757051.
45. Chiocca, E.A., Choi, B.B., Cai, W., DeLuca, N.A., Schaffer, P.A., DiFiglia, M., Breakefield, X.O., Martuza, R.L., Transfer and expression of the lacZ gene in rat brain neurons mediated by herpes simplex virus insertion mutants. New Biol. 2 (1990), 739–746.
46. Choudhury, S.R., Harris, A.F., Cabral, D.J., Keeler, A.M., Sapp, E., Ferreira, J.S., Gray-Edwards, H.L., Johnson, J.A., Johnson, A.K., Su, Q., Stoica, L., DiFiglia, M., Aronin, N., Martin, D.R., Gao, G., Sena-Esteves, M., Widespread central nervous system gene transfer and silencing after systemic delivery of novel AAV-AS vector. Dec 28 Mol. Ther., 2015, 10.1038/mt.2015.231 [Epub ahead of print], PMID: 26708003.
47. Christine, C.W., Starr, P.A., Larson, P.S., Eberling, J.L., Jagust, W.J., Hawkins, R.A., VanBrocklin, H.F., Wright, J.F., Bankiewicz, K.S., Aminoff, M.J., Safety and tolerability of putaminal AADC gene therapy for Parkinson disease. Neurology 73:20 (2009), 1662–1669, 10.1212/WNL.0b013e3181c29356.
48. Ciesielska, A., Hadaczek, P., Mittermeyer, G., Zhou, S., Wright, J.F., Bankiewicz, K.S., Forsayeth, J., Cerebral infusion of AAV9 vector-encoding non-self proteins can elicit cell-mediated immune responses. Mol. Ther. 21:1 (2013), 158–166, 10.1038/mt.2012.167.
49. Cordelier, P., Van Bockstaele, E., Calarota, S.A., Strayer, D.S., Inhibiting AIDS in the central nervous system: gene delivery to protect neurons from HIV. Mol. Ther. 7:6 (2003), 801–810.
50. Cortés, M.L., Oehmig, A., Saydam, O., Sanford, J.D., Perry, K.F., Fraefel, C., Breakefield, X.O., Targeted integration of functional human ATM cDNA into genome mediated by HSV/AAV hybrid amplicon vector. Mol. Ther. 16:1 (2008), 81–88.
51. Costantini, L.C., Bakowska, J.C., Breakefield, X.O., Isacson, O., Gene therapy in the CNS. Gene Ther. 7:2 (2000), 93–109.
52. Cox, D.B., Platt, R.J., Zhang, F., Therapeutic genome editing: prospects and challenges. Nat. Med. 21:2 (2015), 121–131, 10.1038/nm.3793.
53. Davidson, B.L., Allen, E.D., Kozarsky, K.F., Wilson, J.M., Roessler, B.J., A model system for in vivo gene transfer into the central nervous system using an adenoviral vector. Nat. Genet. 3:3 (1993), 219–223.
54. 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. 97:7 (2000), 3428–3432.
55. Deverman, B.E., Pravdo, P.L., Simpson, B.P., Kumar, S.R., Chan, K.Y., Banerjee, A., Wu, W.L., Yang, B., Huber, N., Pasca, S.P., Gradinaru, V., Cre-dependent selection yields AAV variants for widespread gene transfer to the adult brain. Feb 1 Nat. Biotechnol., 2016, 10.1038/nbt.3440 [Epub ahead of print], PMID: 26829320.
56. Diefenbach, R.J., Miranda-Saksena, M., Douglas, M.W., Cunningham, A.L., Transport and egress of herpes simplex virus in neurons. Rev. Med. Virol. 18:1 (2008), 35–51.
57. Dobrikova, E.Y., Goetz, C., Walters, R.W., Lawson, S.K., Peggins, J.O., Muszynski, K., Ruppel, S., Poole, K., Giardina, S.L., Vela, E.M., Estep, J.E., Gromeier, M., Attenuation of neurovirulence, biodistribution, and shedding of a poliovirus:rhinovirus chimera after intrathalamic inoculation in Macaca fascicularis. J. Virol. 86:5 (2012), 2750–2759, 10.1128/JVI.06427-11.
58. Dubensky, T.W., (Re-)Engineering tumor cell-selective replicating adenoviruses: a step in the right direction toward systemic therapy for metastatic disease. Cancer Cell. 1:4 (2002), 307–309.
59. 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. Mol. Ther. 22:4 (2014), 797–810, 10.1038/mt.2013.289.
60. Duque, S.I., Arnold, W.D., Odermatt, P., Li, X., Porensky, P.N., Schmelzer, L., Meyer, K., Kolb, S.J., Schümperli, D., Kaspar, B.K., Burghes, A.H., A large animal model of spinal muscular atrophy and correction of phenotype. Ann. Neurol. 77:3 (2015), 399–414, 10.1002/ana.24332.
61. Ehrengruber, M.U., Lundstrom, K., Schweitzer, C., Heuss, C., Schlesinger, S., Gähwiler, B.H., Recombinant Semliki Forest virus and Sindbis virus efficiently infect neurons in hippocampal slice cultures. Proc. Natl. Acad. Sci. U. S. A. 96:12 (1999), 7041–7046.
62. Ehrengruber, M.U., Hennou, S., Büeler, H., Naim, H.Y., Déglon, N., Lundstrom, K., Gene transfer into neurons from hippocampal slices: comparison of recombinant Semliki Forest Virus, adenovirus, adeno-associated virus, lentivirus, and measles virus. Mol. Cell Neurosci. 17:5 (2001), 855–871.
63. 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. Mol. Ther. 21:9 (2013), 1661–1667, 10.1038/mt.2013.
64. 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. 19:8 (2012), 852–859, 10.1038/gt.2011.130.
65. Fields-Berry, S.C., Halliday, A.L., Cepko, C.L., A recombinant retrovirus encoding alkaline phosphatase confirms clonal boundary assignment in lineage analysis of murine retina. Proc. Natl. Acad. Sci. U. S. A. 89:2 (1992), 693–697.
66. Finkelshtein, D., Werman, A., Novick, D., Barak, S., Rubinstein, M., LDL receptor and its family members serve as the cellular receptors for vesicular stomatitis virus. Proc. Natl. Acad. Sci. U. S. A. 110:18 (2013), 7306–7311, 10.1073/pnas.1214441110.
67. 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. 27:1 (2009), 59–65, 10.1038/nbt.1515.
68. 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. 28:3 (2010), 271–274, 10.1038/nbt.1610.
69. 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. Mol. Ther. 21:12 (2013), 2148–2159, 10.1038/mt.2013.211.
70. 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. Mol. Ther. 8:6 (2003), 911–917.
71. 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. Mol. Ther. 19:6 (2011), 1025–1033, 10.1038/mt.2011.34.
72. Gant, J.C., Chen, K.C., Kadish, I., Blalock, E.M., Thibault, O., Porter, N.M., Landfield, P.W., Reversal of aging-related neuronal Ca2+ dysregulation and cognitive impairment by delivery of a transgene encoding FK506-binding protein 12.6/1b to the hippocampus. J. Neurosci. 35:30 (2015), 10878–10887, 10.1523/JNEUROSCI.1248-15.2015.
73. 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. 33:34 (2013), 13612–13620, 10.1523/JNEUROSCI.1854-13.2013.
74. Garriga-Canut, M., Agustín-Pavón, C., Herrmann, F., Sánchez, A., Dierssen, M., Fillat, C., Isalan, M., Synthetic zinc finger repressors reduce mutant huntingtin expression in the brain of R6/2 mice. Proc. Natl. Acad. Sci. U. S. A. 109:45 (2012), E3136–E3145, 10.1073/pnas.1206506109.
75. Gasmi, M., Brandon, E.P., Herzog, C.D., Wilson, A., Bishop, K.M., Hofer, E.K., Cunningham, J.J., Printz, M.A., Kordower, J.H., Bartus, R.T., AAV2-mediated delivery of human neurturin to the rat nigrostriatal system: long-term efficacy and tolerability of CERE-120 for Parkinson's disease. Neurobiol. Dis. 27:1 (2007), 67–76.
76. Gasmi, M., Herzog, C.D., Brandon, E.P., Cunningham, J.J., Ramirez, G.A., Ketchum, E.T., Bartus, R.T., Striatal delivery of neurturin by CERE-120, an AAV2 vector for the treatment of dopaminergic neuron degeneration in Parkinson's disease. Mol. Ther. 15:1 (2007), 62–68.
77. Gaudet, D., Méthot, J., Déry, S., Brisson, D., Essiembre, C., Tremblay, G., Tremblay, K., de Wal, J., Twisk, J., van den Bulk, N., Sier-Ferreira, V., van Deventer, S., Efficacy and long-term safety of alipogene tiparvovec (AAV1-LPLS447X) gene therapy for lipoprotein lipase deficiency: an open-label trial. Gene Ther. 20:4 (2013), 361–369, 10.1038/gt.2012.43.
78. Ginhoux, F., Turbant, S., Gross, D.A., Poupiot, J., Marais, T., Lone, Y., Lemonnier, F.A., Firat, H., Perez, N., Danos, O., Davoust, J., HLA-A*0201-restricted cytolytic responses to the rtTA transactivator dominant and cryptic epitopes compromise transgene expression induced by the tetracycline on system. Mol. Ther. 10:2 (2004), 279–289.
79. Gong, Y., Mu, D., Prabhakar, S., Moser, A., Musolino, P., Ren, J., Breakefield, X.O., Maguire, C.A., Eichler, F.S., Adenoassociated virus seroytpe 9-mediated gene therapy for X-linked adrenoleukodystrophy. Mol. Ther. 23:5 (2015), 824–834, 10.1038/mt.2015.6.
80. Grandi, P., Peruzzi, P., Reinhart, B., Cohen, J.B., Chiocca, E.A., Glorioso, J.C., Design and application of oncolytic HSV vectors for glioblastoma therapy. Expert Rev. Neurother. 9:4 (2009), 505–517, 10.1586/ern.09.9.
81. 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. Mol. Ther. 19:6 (2011), 1058–1069, 10.1038/mt.2011.72.
82. Gray, S.J., Nagabhushan Kalburgi, S., McCown, T.J., Jude Samulski, R., Global CNS gene delivery and evasion of anti-AAV-neutralizing antibodies by intrathecal AAV administration in non-human primates. Gene Ther. 20:4 (2013), 450–459, 10.1038/gt.2012.101.
83. 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 441:7092 (2006), 537–541.
84. Grossman, S.A., Ye, X., Piantadosi, S., Desideri, S., Nabors, L.B., Rosenfeld, M., Fisher, J., NABTT, C.C., Survival of patients with newly diagnosed glioblastoma treated with radiation and temozolomide in research studies in the United States. Clin. Cancer Res. 16:8 (2010), 2443–2449, 10.1158/1078-0432.CCR-09-3106.
85. Grothe, M., Heinsen, H., Teipel, S.J., Atrophy of the cholinergic Basal forebrain over the adult age range and in early stages of Alzheimer's disease. Biol. Psychiatry 71:9 (2012), 805–813, 10.1016/j.biopsych.2011.06.019.
86. György, B., Fitzpatrick, Z., Crommentuijn, M.H., Mu, D., Maguire, C.A., Naturally enveloped AAV vectors for shielding neutralizing antibodies and robust gene delivery in vivo. Biomaterials 35:26 (2014), 7598–7609, 10.1016/j.biomaterials.2014.05.032.
87. Hacein-Bey-Abina, S., Von Kalle, C., Schmidt, M., McCormack, M.P., Wulffraat, N., Leboulch, P., Lim, A., Osborne, C.S., Pawliuk, R., Morillon, E., Sorensen, R., Forster, A., Fraser, P., Cohen, J.I., de Saint Basile, G., Alexander, I., Wintergerst, U., Frebourg, T., Aurias, A., Stoppa-Lyonnet, D., Romana, S., Radford-Weiss, I., Gross, F., Valensi, F., Delabesse, E., Macintyre, E., Sigaux, F., Soulier, J., Leiva, L.E., Wissler, M., Prinz, C., Rabbitts, T.H., Le Deist, F., Fischer, A., Cavazzana-Calvo, M., LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302:5644 (2003), 415–419.
88. Hacein-Bey-Abina, S., Hauer, J., Lim, A., Picard, C., Wang, G.P., Berry, C.C., Martinache, C., Rieux-Laucat, F., Latour, S., Belohradsky, B.H., Leiva, L., Sorensen, R., Debré, M., Casanova, J.L., Blanche, S., Durandy, A., Bushman, F.D., Fischer, A., Cavazzana-Calvo, M., Efficacy of gene therapy for X-linked severe combined immunodeficiency. N. Engl. J. Med. 363:4 (2010), 355–364, 10.1056/NEJMoa1000164.
89. Hall, J., Prabhakar, S., Balaj, L., Lai, C.P., Cerione, R.A., Breakefield, X.O., Review and potential treatments for Parkinson's disease, glioma and schwannoma. J. Cell Mol. Neurobiol., 2015 (in press).
90. Harper, S.Q., Staber, P.D., He, X., Eliason, S.L., Martins, I.H., Mao, Q., Yang, L., Kotin, R.M., Paulson, H.L., Davidson, B.L., RNA interference improves motor and neuropathological abnormalities in a Huntington's disease mouse model. Proc. Natl. Acad. Sci. U. S. A. 102:16 (2005), 5820–5825.
91. Herzog, C.D., Brown, L., Kruegel, B.R., Wilson, A., Tansey, M.G., Gage, F.H., Johnson, E.M.J., Bartus, R.T., Enhanced neurotrophic distribution, cell signaling and neuroprotection following substantia nigral versus striatal delivery of AAV2-NRTN (CERE-120). Neurobiol. Dis. 58 (2013), 38–48, 10.1016/j.nbd.2013.04.011.
92. 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. Mol. Ther. 22:12 (2014), 2018–2027, 10.1038/mt.2014.135.
93. Hordeaux, J., Dubreil, L., Deniaud, J., Iacobelli, F., Moreau, S., Ledevin, M., Le Guiner, C., Blouin, V., Le Duff, J., Mendes-Madeira, A., Rolling, F., Cherel, Y., Moullier, P., Colle, M.A., Efficient central nervous system AAVrh10-mediated intrathecal gene transfer in adult and neonate rats. Gene Ther. 22:4 (2015), 316–324, 10.1038/gt.2014.121.
94. Hsu, P.D., Lander, E.S., Zhang, F., Development and applications of CRISPR-Cas9 for genome engineering. Cell. 157:6 (2014), 1262–1278, 10.1016/j.cell.2014.05.010.
95. Huang, T.T., Hlavaty, J., Ostertag, D., Espinoza, F.L., Martin, B., Petznek, H., Rodriguez-Aguirre, M., Ibanez, C.E., Kasahara, N., Gunzburg, W., Gruber, H.E., Pertschuk, D., Jolly, D.J., Robbins, J.M., Toca 511 gene transfer and 5-fluorocytosine in combination with temozolomide demonstrates synergistic therapeutic efficacy in a temozolomide-sensitive glioblastoma model. Cancer Gene Ther. 20:10 (2013), 544–551, 10.1038/cgt.2013.51.
96. Huang, Y., Skwarek-Maruszewska, A., Horré, K., Vandewyer, E., Wolfs, L., Snellinx, A., Saito, T., Radaelli, E., Corthout, N., Colombelli, J., Lo, A.C., Van Aerschot, L., Callaerts-Vegh, Z., Trabzuni, D., Bossers, K., Verhaagen, J., Ryten, M., Munck, S., D'Hooge, R., Swaab, D.F., Hardy, J., Saido, T.C., De Strooper, B., Thathiah, A., Loss of GPR3 reduces the amyloid plaque burden and improves memory in Alzheimer's disease mouse models. Sci. Transl. Med., 7(309), 2015, 309ra164, 10.1126/scitranslmed.aab3492.
97. Huang, T.T., Parab, S., Burnett, R., Diago, O., Ostertag, D., Hofman, F.M., Espinoza, F.L., Martin, B., Ibañez, C.E., Kasahara, N., Gruber, H.E., Pertschuk, D., Jolly, D.J., Robbins, J.M., Intravenous administration of retroviral replicating vector, Toca 511, demonstrates therapeutic efficacy in orthotopic immune-competent mouse glioma model. Hum. Gene Ther. 26:2 (2015), 82–93, 10.1089/hum.2014.100.
98. Hudry, E., Van Dam, D., Kulik, W., De Deyn, P.P., Stet, F.S., Ahouansou, O., Benraiss, A., Delacourte, A., Bougnères, P., Aubourg, P., Cartier, N., Adeno-associated virus gene therapy with cholesterol 24-hydroxylase reduces the amyloid pathology before or after the onset of amyloid plaques in mouse models of Alzheimer's disease. Mol. Ther. 18:1 (2010), 44–53, 10.1038/mt.2009.175.
99. Hudry, E., Dashkoff, J., Roe, A.D., Takeda, S., Koffie, R.M., Hashimoto, T., Scheel, M., Spires-Jones, T., Arbel-Ornath, M., Betensky, R., Davidson, B.L., Hyman, B.T., Gene transfer of human Apoe isoforms results in differential modulation of amyloid deposition and neurotoxicity in mouse brain. Sci. Transl. Med., 5(212), 2013, 212ra161, 10.1126/scitranslmed.3007000.
100. Hudry, E., Martin, C., Gandhi, S., György, B., Scheffer, D.I., Mu, D., Merkel, S.F., Mingozzi, F., Fitzpatrick, Z., Dimant, H., Masek, M., Ragan, T., Tan, S., Brisson, A.R., Ramirez, S.H., Hyman, B.T., Maguire, C.A., Exosome-associated AAV vector as a robust and convenient neuroscience tool. Feb 2 Gene Ther., 2016, 10.1038/gt.2016.11 [Epub ahead of print], PMID: 26836117.
101. Hutcheson, J., Witkiewicz, A.K., Knudsen, E.S., The RB tumor suppressor at the intersection of proliferation and immunity: relevance to disease immune evasion and immunotherapy. Cell Cycle 14:24 (2015), 3812–3819, 10.1080/15384101.2015.1010922.
102. Hwu, W.L., Muramatsu, S., Tseng, S.H., Tzen, K.Y., Lee, N.C., Chien, Y.H., Snyder, R.O., Byrne, B.J., Tai, C.H., Wu, R.M., Gene therapy for aromatic L-amino acid decarboxylase deficiency. Sci. Transl. Med., 4(134), 2012, 134ra61, 10.1126/scitranslmed.3003640.
103. Jackson, C.A., Cobbs, C., Peduzzi, J.D., Novak, M., Morrow, C.D., Repetitive intrathecal injections of poliovirus replicons result in gene expression in neurons of the central nervous system without pathogenesis. Hum. Gene Ther. 12:15 (2001), 1827–1841.
104. Janson, C., McPhee, S., Bilaniuk, L., Haselgrove, J., Testaiuti, M., Freese, A., Wang, D.J., Shera, D., Hurh, P., Rupin, J., Saslow, E., Goldfarb, O., Goldberg, M., Larijani, G., Sharrar, W., Liouterman, L., Camp, A., Kolodny, E., Samulski, J., Leone, P., Clinical protocol. Gene therapy of Canavan disease: AAV-2 vector for neurosurgical delivery of aspartoacylase gene (ASPA) to the human brain. Hum. Gene Ther. 13:11 (2002), 1391–1412.
105. Jiang, H., Gomez-Manzano, C., Lang, F.F., Alemany, R., Fueyo, J., Oncolytic adenovirus: preclinical and clinical studies in patients with human malignant gliomas. Curr. Gene Ther. 9:5 (2009), 422–427.
106. Jülich, K., Sahin, M., Mechanism-based treatment in tuberous sclerosis complex. Pediatr. Neurol. 50:4 (2014), 290–296, 10.1016/j.pediatrneurol.2013.12.002.
107. Kaludov, N., Brown, K.E., Walters, R.W., Zabner, J., Chiorini, J.A., Adeno-associated virus serotype 4 (AAV4) and AAV5 both require sialic acid binding for hemagglutination and efficient transduction but differ in sialic acid linkage specificity. J. Virol. 75:15 (2001), 6884–6893.
108. Kambara, H., Okano, H., Chiocca, E.A., Saeki, Y., An oncolytic HSV-1 mutant expressing ICP34.5 under control of a nestin promoter increases survival of animals even when symptomatic from a brain tumor. Cancer Res. 65:7 (2005), 2832–2839.
109. Kaplitt, M.G., Feigin, A., Tang, C., Fitzsimons, H.L., Mattis, P., Lawlor, P.A., Bland, R.J., Young, D., Strybing, K., Eidelberg, D., During, M.J., 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 (2007), 2097–2105.
110. Kaul, R., Gao, G.P., Balamurugan, K., Matalon, R., Cloning of the human aspartoacylase cDNA and a common missense mutation in Canavan disease. Nat. Genet. 5:2 (1993), 118–123.
111. Kay, M.A., Rothenberg, S., Landen, C.N., Bellinger, D.A., Leland, F., Toman, C., Finegold, M., Thompson, A.R., Read, M.S., Brinkhous, K.M., Woo, S.C., In vivo gene therapy of hemophilia B: sustained partial correction in factor IX-deficient dogs. Science 262:5130 (1993), 117–119.
112. 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. 106:7 (2009), 2407–2411, 10.1073/pnas.0810682106.
113. Kemppainen, S., Lindholm, P., Galli, E., Lahtinen, H.M., Koivisto, H., Hämäläinen, E., Saarma, M., Tanila, H., Cerebral dopamine neurotrophic factor improves long-term memory in APP/PS1 transgenic mice modeling Alzheimer's disease as well as in wild-type mice. Behav. Brain Res. 291 (2015), 1–11, 10.1016/j.bbr.2015.05.002.
114. Kim, J.Y., Grunke, S.D., Levites, Y., Golde, T.E., Jankowsky, J.L., Intracerebroventricular viral injection of the neonatal mouse brain for persistent and widespread neuronal transduction. J. Vis. Exp., 91, 2014, 51863, 10.3791/51863.
115. Kiyota, T., Zhang, G., Morrison, C.M., Bosch, M.E., Weir, R.A., Lu, Y., Dong, W., Gendelman, H.E., AAV2/1 CD74 gene transfer reduces β-amyloidosis and improves learning and memory in a mouse model of Alzheimer's disease. Mol. Ther. 23:11 (2015), 1712–1721, 10.1038/mt.2015.142.
116. Klein, R.L., Dayton, R.D., Leidenheimer, N.J., Jansen, K., Golde, T.E., Zweig, R.M., Efficient neuronal gene transfer with AAV8 leads to neurotoxic levels of tau or green fluorescent proteins. Mol. Ther. 13:3 (2006), 517–527.
117. Kohli, M., Rago, C., Lengauer, C., Kinzler, K.W., Vogelstein, B., Facile methods for generating human somatic cell gene knockouts using recombinant adeno-associated viruses. Nucleic Acids Res., 32(1), 2004, e3.
118. Kordower, J.H., Herzog, C.D., Dass, B., Bakay, R.A., Stansell, J., Gasmi, M., Bartus, R., Delivery of neurturin by AAV2 (CERE-120)-mediated gene transfer provides structural and functional neuroprotection and neurorestoration in MPTP-treated monkeys. Ann. Neurol. 60:6 (2006), 706–715.
119. Lang, F.F., Conrad, C., Gomez-Manzano, C., Tufaro, F., Yung, W., Sawaya, R., Weinberg, J., Prabhu, S., Fuller, G., Aldape, K., Fueyo, J., First-in-human phase I clinical trial of oncolytic delta-24-RGD (DNX-2401) with biological endpoints: implications for viro-immunotherapy. Neuro Oncol., 16(Suppl. 3), 2014, iii39, 10.1093/neuonc/nou208.61.
120. Lebson, L., Nash, K., Kamath, S., Herber, D., Carty, N., Lee, D.C., Li, Q., Szekeres, K., Jinwal, U., Koren, J., Dickey, C.A., Gottschall, P.E., Morgan, D., Gordon, M.N., Trafficking CD11b-positive blood cells deliver therapeutic genes to the brain of amyloid-depositing transgenic mice. J. Neurosci. 30 (2010), 9651–9658.
121. Leone, P., Janson, C.G., Bilaniuk, L., Wang, Z., Sorgi, F., Huang, L., Matalon, R., Kaul, R., Zeng, Z., Freese, A., McPhee, S.W., Mee, E., During, M.J., Aspartoacylase gene transfer to the mammalian central nervous system with therapeutic implications for Canavan disease. Ann. Neurol. 48:1 (2000), 27–38.
122. 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(165), 2012, 165ra163, 10.1126/scitranslmed.3003454.
123. Levites, Y., O'Nuallain, B., Puligedda, R.D., Ondrejcak, T., Adekar, S.P., Chen, C., Cruz, P.E., Rosario, A.M., Macy, S., Mably, A.J., Walsh, D.M., Vidal, R., Solomon, A., Brown, D., Rowan, M.J., Golde, T.E., Dessain, S.K., A human monoclonal IgG that binds aβ assemblies and diverse amyloids exhibits anti-amyloid activities in vitro and in vivo. J. Neurosci. 35:16 (2015), 6265–6276, 10.1523/JNEUROSCI.5109-14.2015.
124. LeWitt, P.A., Rezai, A.R., Leehey, M.A., Ojemann, S.G., Flaherty, A.W., Eskandar, E.N., Kostyk, S.K., Thomas, K., Sarkar, A., Siddiqui, M.S., Tatter, S.B., Schwalb, J.M., Poston, K.L., Henderson, J.M., Kurlan, R.M., Richard, I.H., Van Meter, L., Sapan, C.V., During, M.J., Kaplitt, M.G., Feigin, A., AAV2-GAD gene therapy for advanced Parkinson's disease: a double-blind, sham-surgery controlled, randomised trial. Lancet Neurol. 10:4 (2011), 309–319, 10.1016/S1474-4422(11)70039-4.
125. Li, C., Xiao, P., Gray, S.J., Weinberg, M.S., Samulski, R.J., Combination therapy utilizing shRNA knockdown and an optimized resistant transgene for rescue of diseases caused by misfolded proteins. Proc. Natl. Acad. Sci. U. S. A. 108:34 (2011), 14258–14263, 10.1073/pnas.1109522108 475(7355), 217-221. doi: 10.1038/nature10177.
126. Li, H., Haurigot, V., Doyon, Y., Li, T., Wong, S.Y., Bhagwat, A.S., Malani, N., Anguela, X.M., Sharma, R., Ivanciu, L., Murphy, S.L., Finn, J.D., Khazi, F.R., Zhou, S., Paschon, D.E., Rebar, E.J., Bushman, F.D., Gregory, P.D., Holmes, M.C., High, K.A., In vivo genome editing restores haemostasis in a mouse model of haemophilia. Nature 475:7355 (2011), 217–221, 10.1038/nature10177.
127. Li, Y., Wang, J., Zhang, S., Liu, Z., Neprilysin gene transfer: a promising therapeutic approach for Alzheimer's disease. J. Neurosci. Res. 93:9 (2015), 1325–1329, 10.1002/jnr.23564.
128. Liao, F., Hori, Y., Hudry, E., Bauer, A.Q., Jiang, H., Mahan, T.E., Lefton, K.B., Zhang, T.J., Dearborn, J.T., Kim, J., Culver, J.P., Betensky, R., Wozniak, D.F., Hyman, B.T., Holtzman, D.M., Anti-ApoE antibody given after plaque onset decreases Aβ accumulation and improves brain function in a mouse model of Aβ amyloidosis. J. Neurosci. 34:21 (2014), 7281–7292, 10.1523/JNEUROSCI.0646-14.2014.
129. Liu, G., Martins, I.H., Chiorini, J.A., Davidson, B.L., Adeno-associated virus type 4 (AAV4) targets ependyma and astrocytes in the subventricular zone and RMS. Gene Ther. 12:20 (2005), 1503–1508.
130. Louboutin, J.P., Chekmasova, A.A., Marusich, E., Chowdhury, J.R., Strayer, D.S., Efficient CNS gene delivery by intravenous injection. Nat. Methods 7:11 (2010), 905–907, 10.1038/nmeth.1518.
131. Lu-Emerson, C., Plotkin, S.R., The neurofibromatoses. Part 1: NF1. Rev. Neurol. Dis. 6:2 (2009), E47–E53.
132. Mager, D.L., Stoye, J.P., Mammalian endogenous retroviruses. Microbiol. Spectr., 3(1), 2015, 10.1128/microbiolspec.MDNA3-0009-2014 MDNA3-0009-2014.
133. Maguire, C.A., Balaj, L., Sivaraman, S., Crommentuijn, M., Ericsson, M., Mincheva-Nilsson, L., Baranov, V., Gianni, D., Tannous, B.A., Sena-Esteves, M., Breakefield, X.O., Skog, J., Microvesicle-associated AAV vector as a novel gene delivery system. Mol. Ther. 20:5 (2012), 960–971.
134. Maguire, C., Ramirex, S.H., Merkel, S.F., Sena-Esteves, M., Breakefield, X.O., Gene therapy for the nervous system: challenges and new strategies. Neurotherapeutics 11:4 (2014), 817–839, 10.1007/s13311-014-0299-5.
135. Mao, H., Gorbatyuk, M.S., Rossmiller, B., Hauswirth, W.W., Lewin, A.S., Long-term rescue of retinal structure and function by rhodopsin RNA replacement with a single adeno-associated viral vector in P23H RHO transgenic mice. Hum. Gene Ther. 23:4 (2012), 356–366, 10.1089/hum.2011.213.
136. Markert, J.M., Medlock, M.D., Rabkin, S.D., Gillespie, G.Y., Todo, T., Hunter, W.D., Palmer, C.A., Feigenbaum, F., Tornatore, C., Tufaro, F., Martuza, R.L., Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: results of a phase I trial. Gene Ther. 7:10 (2000), 867–874.
137. Markert, J.M., Liechty, P.G., Wang, W., Gaston, S., Braz, E., Karrasch, M., Nabors, L.B., Markiewicz, M., Lakeman, A.D., Palmer, C.A., Parker, J.N., Whitley, R.J., Gillespie, G.Y., Phase Ib trial of mutant herpes simplex virus G207 inoculated pre-and post-tumor resection for recurrent GBM. Mol. Ther. 17:1 (2009), 199–207, 10.1038/mt.2008.228.
138. Markert, J.M., Razdan, S.N., Kuo, H.C., Cantor, A., Knoll, A., Karrasch, M., Nabors, L.B., Markiewicz, M., Agee, B.S., Coleman, J.M., Lakeman, A.D., Palmer, C.A., Parker, J.N., Whitley, R.J., Weichselbaum, R.R., Fiveash, J.B., Gillespie, G.Y., A phase 1 trial of oncolytic HSV-1, G207, given in combination with radiation for recurrent GBM demonstrates safety and radiographic responses. Mol. Ther. 22:5 (2014), 1048–1055, 10.1038/mt.2014.22.
139. Marks, W.J.J., Ostrem, J.L., Verhagen, L., Starr, P.A., Larson, P.S., Bakay, R.A., Taylor, R., Cahn-Weiner, D.A., Stoessl, A.J., Olanow, C.W., Bartus, R.T., 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. 7:5 (2008), 400–408, 10.1016/S1474-4422(08)70065-6.
140. Marks, W.J.J., Bartus, R.T., Siffert, J., Davis, C.S., Lozano, A., Boulis, N., Vitek, J., Stacy, M., Turner, D., Verhagen, L., Bakay, R., Watts, R., Guthrie, B., Jankovic, J., Simpson, R., Tagliati, M., Alterman, R., Stern, M., Baltuch, G., Starr, P.A., Larson, P.S., Ostrem, J.L., Nutt, J., Kieburtz, K., Kordower, J.H., Olanow, C.W., Gene delivery of AAV2-neurturin for Parkinson's disease: a double-blind, randomised, controlled trial. Lancet Neurol. 9 (2010), 1164–1172.
141. 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.
142. McCarty, D.M., Young, S.M., Samulski, R.J., Integration of adeno-associated virus (AAV) and recombinant AAV vectors. Annu. Rev. Genet. 38 (2004), 819–845.
143. 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. 16:11 (2009), 1340–1352, 10.1038/gt.2009.85.
144. McIntosh, J.H., Cochrane, M., Cobbold, S., Waldmann, H., Nathwani, S.A., Davidoff, A.M., Nathwani, A.C., Successful attenuation of humoral immunity to viral capsid and transgenic protein following AAV-mediated gene transfer with a non-depleting CD4 antibody and cyclosporine. Gene Ther. 19:1 (2012), 78–85, 10.1038/gt.2011.64.
145. McKelvey, T., Tang, A., Bett, A.J., Casimiro, D.R., Chastain, M., T-cell response to adenovirus hexon and DNA-binding protein in mice. Gene Ther. 11:9 (2004), 791–796.
146. McLean, J.R., Smith, G.A., Rocha, E.M., Hayes, M.A., Beagan, J.A., Hallett, P.J., Isacson, O., Widespread neuron-specific transgene expression in brain and spinal cord following synapsin promoter-driven AAV9 neonatal intracerebroventricular injection. Neurosci. Lett. 576 (2014), 73–78, 10.1016/j.neulet.2014.05.044.
147. McPhee, S.W., Janson, C.G., Li, C., Samulski, R.J., Camp, A.S., Francis, J., Shera, D., Lioutermann, L., Feely, M., Freese, A., Leone, P., Immune responses to AAV in a phase I study for Canavan disease. J. Gene Med. 8:5 (2006), 577–588.
148. Meikle, L., Talos, D.M., Onda, H., Pollizzi, K., Rotenberg, A., Sahin, M., Jensen, F.E., Kwiatkowski, D.J., A mouse model of tuberous sclerosis: neuronal loss of Tsc1 causes dysplastic and ectopic neurons, reduced myelination, seizure activity, and limited survival. J. Neurosci. 27:21 (2007), 5546–5558.
149. 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. Mol. Ther. 23:3 (2015), 477–487, 10.1038/mt.2014.210.
150. Miller, D.G., Trobridge, G.D., Petek, L.M., Jacobs, M.A., Kaul, R., Russell, D.W., Large-scale analysis of adeno-associated virus vector integration sites in normal human cells. J. Virol. 79:17 (2005), 11434–11442.
151. Miller, D.G., Wang, P.R., Petek, L.M., Hirata, R.K., Sands, M.S., Russell, D.W., Gene targeting in vivo by adeno-associated virus vectors. Nat. Biotechnol. 24:8 (2006), 1022–1026.
152. Mittermeyer, G., Christine, C.W., Rosenbluth, K.H., Baker, S.L., Starr, P., Larson, P., Kaplan, P.L., Forsayeth, J., Aminoff, M.J., Bankiewicz, K.S., Long-term evaluation of a phase 1 study of AADC gene therapy for Parkinson's disease. Hum. Gene Ther. 23:4 (2012), 377–381, 10.1089/hum.2011.220.
153. 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. 21:4 (2014), 427–433, 10.1038/gt.2014.1.
154. Montini, E., Cesana, D., Schmidt, M., Sanvito, F., Ponzoni, M., Bartholomae, C., Sergi Sergi, L., Benedicenti, F., Ambrosi, A., Di Serio, C., Doglioni, C., von Kalle, C., Naldini, L., Hematopoietic stem cell gene transfer in a tumor-prone mouse model uncovers low genotoxicity of lentiviralvector integration. Nat. Biotechnol. 24:6 (2006), 687–696.
155. Mueller, C., Tang, Q., Gruntman, A., Blomenkamp, K., Teckman, J., Song, L., Zamore, P.D., Flotte, T.R., Sustained miRNA-mediated knockdown of mutant AAT with simultaneous augmentation of wild-type AAT has minimal effect on global liver miRNA profiles. Mol. Ther. 20:3 (2012), 590–600, 10.1038/mt.2011.292.
156. Muramatsu, S., Fujimoto, K., Kato, S., Mizukami, H., Asari, S., Ikeguchi, K., Kawakami, T., Urabe, M., Kume, A., Sato, T., Watanabe, E., Ozawa, K., Nakano, I., A phase I study of aromatic L-amino acid decarboxylase gene therapy for Parkinson's disease. Mol. Ther. 18:9 (2010), 1731–1735, 10.1038/mt.2010.135.
157. Murphy, S.R., Chang, C.C., Dogbevia, G., Bryleva, E.Y., Bowen, Z., Hasan, M.T., Chang, T.Y., Acat1 knockdown gene therapy decreases amyloid-β in a mouse model of Alzheimer's disease. Mol. Ther. 21:8 (2013), 1497–1506, 10.1038/mt.2013.118.
158. Mussolino, C., Cathomen, T., TALE nucleases: tailored genome engineering made easy. Curr. Opin. Biotechnol. 23:5 (2012), 644–650, 10.1016/j.copbio.2012.01.013.
159. Nagahara, A.H., Mateling, M., Kovacs, I., Wang, L., Eggert, S., Rockenstein, E., Koo, E.H., Masliah, E., Tuszynski, M.H., Early BDNF treatment ameliorates cell loss in the entorhinal cortex of APP transgenic mice. J. Neurosci. 33:39 (2013), 15596–15602, 10.1523/JNEUROSCI.5195-12.2013.
160. Nakai, H., Montini, E., Fuess, S., Storm, T.A., Grompe, M., Kay, M.A., AAV serotype 2 vectors preferentially integrate into active genes in mice. Nat. Genet. 34:3 (2003), 297–302.
161. Nakai, H., Wu, X., Fuess, S., Storm, T.A., Munroe, D., Montini, E., Burgess, S.M., Grompe, M., Kay, M.A., Large-scale molecular characterization of adeno-associated virus vector integration in mouse liver. J. Virol. 79:6 (2005), 3606–3614.
162. Naldini, L., Gene therapy returns to centre stage. Nature 526:7573 (2015), 351–360, 10.1038/nature15818.
163. Nathwani, A.C., Reiss, U.M., Tuddenham, E.G., Rosales, C., Chowdary, P., McIntosh, J., Della Peruta, M., Lheriteau, E., Patel, N., Raj, D., Riddell, A., Pie, J., Rangarajan, S., Bevan, D., Recht, M., Shen, Y.M., Halka, K.G., Basner-Tschakarjan, E., Mingozzi, F., High, K.A., Allay, J., Kay, M.A., Ng, C.Y., Zhou, J., Cancio, M., Morton, C.L., Gray, J.T., Srivastava, D., Nienhuis, A.W., Davidoff, A.M., Long-term safety and efficacy of factor IX gene therapy in hemophilia B. N. Engl. J. Med. 371:21 (2014), 1994–2004, 10.1056/NEJMoa1407309.
164. Nawrot, B., Targeting BACE with small inhibitory nucleic acids – a future for Alzheimer's disease therapy?. Acta Biochim. Pol. 51:2 (2004), 431–444.
165. Nelson, C.E., Hakim, C.H., Ousterout, D.G., Thakore, P.I., Moreb, E.A., Castellanos Rivera, R.M., Madhavan, S., Pan, X., Ran, F.A., Yan, W.X., Asokan, A., Zhang, F., Duan, D., Gersbach, C.A., In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science 351:6271 (2016), 403–407, 10.1126/science.aad5143.
166. Nicolson, S.C., Samulski, R.J., Recombinant adeno-associated virus utilizes host cell nuclear import machinery to enter the nucleus. J. Virol. 88:8 (2014), 4132–4144, 10.1128/JVI.02660-13.
167. O'Connor, D.M., Boulis, N.M., Gene therapy for neurodegenerative diseases. Trends Mol. Med. 21:8 (2015), 504–512, 10.1016/j.molmed.2015.06.001.
168. Osten, P., Dittgen, T., Licznerski, P., Lentivirus-based genetic manipulations in neurons in vivo. Moss, S., Kittler, J., (eds.) The Dynamic Synapse: Molecular Methods in Ionotropic Receptor Biology, 2006, CRC Press/Taylor & Francis, Boca Raton, FL, 249–259 (Chapter 13).
169. Palfi, S., Gurruchaga, J.M., Ralph, G.S., Lepetit, H., Lavisse, S., Buttery, P.C., Watts, C., Miskin, J., Kelleher, M., Deeley, S., Iwamuro, H., Lefaucheur, J.P., Thiriez, C., Fenelon, G., Lucas, C., Brugières, P., Gabriel, I., Abhay, K., Drouot, X., Tani, N., Kas, A., Ghaleh, B., Le Corvoisier, P., Dolphin, P., Breen, D.P., Mason, S., Guzman, N.V., Mazarakis, N.D., Radcliffe, P.A., Harrop, R., Kingsman, S.M., Rascol, O., Naylor, S., Barker, R.A., Hantraye, P., Remy, P., Cesaro, P., Mitrophanous, K.A., Long-term safety and tolerability of ProSavin, a lentiviral vector-based gene therapy for Parkinson's disease: a dose escalation, open-label, phase 1/2 trial. Lancet 383:9923 (2014), 1138–1146, 10.1016/S0140-6736(13)61939-X.
170. Papapetrou, E.P., Lee, G., Malani, N., Setty, M., Riviere, I., Tirunagari, L.M., Kadota, K., Roth, S.L., Giardina, P., Viale, A., Leslie, C., Bushman, F.D., Studer, L., Sadelain, M., Genomic safe harbors permit high β-globin transgene expression in thalassemia induced pluripotent stem cells. Nat. Biotechnol. 29:1 (2011), 73–78, 10.1038/nbt.1717.
171. Pascual-Lucas, M., Viana da Silva, S., Di Scala, M., Garcia-Barroso, C., González-Aseguinolaza, G., Mulle, C., Alberini, C.M., Cuadrado-Tejedor, M., Garcia-Osta, A., Insulin-like growth factor 2 reverses memory and synaptic deficits in APP transgenic mice. EMBO Mol. Med. 6:10 (2014), 1246–1262, 10.15252/emmm.201404228.
172. Passini, M.A., Macauley, S.L., Huff, M.R., Taksir, T.V., Bu, J., Wu, I.H., Piepenhagen, P.A., Dodge, J.C., Shihabuddin, L.S., O'Riordan, C.R., Schuchman, E.H., Stewart, G.R., AAV vector-mediated correction of brain pathology in a mouse model of Niemann-Pick A disease. Mol. Ther. 11:5 (2005), 754–762.
173. 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.
174. Patel, P., Kriz, J., Gravel, M., Soucy, G., Bareil, C., Gravel, C., Julien, J.P., Adeno-associated virus-mediated delivery of a recombinant single-chain antibody against misfolded superoxide dismutase for treatment of amyotrophic lateral sclerosis. Mol. Ther. 22:3 (2014), 498–510, 10.1038/mt.2013.239.
175. Paulk, N.K., Wursthorn, K., Wang, Z., Finegold, M.J., Kay, M.A., Grompe, M., Adeno-associated virus gene repair corrects a mouse model of hereditary tyrosinemia in vivo. Hepatology 51:4 (2010), 1200–1208, 10.1002/hep.23481.
176. Piccioni, D.E., Kesari, S., Clinical trials of viral therapy for malignant gliomas. Expert Rev. Anticancer Ther. 13:11 (2013), 1297–1305, 10.1586/14737140.2013.851160.
177. Pierce, E.A., Bennett, J., The status of RPE65 gene therapy trials: safety and efficacy. Cold Spring Harb. Perspect. Med., 5(9), 2015, 10.1101/cshperspect.a017285 pii: a017285.
178. Prabhakar, S., Goto, J., Zhang, X., Sena-Esteves, M., Bronson, R., Brockmann, J., Gianni, D., Wojtkiewicz, G.R., Chen, J.W., Stemmer-Rachamimov, A., Kwiatkowski, D.J., Breakefield, X.O., Stochastic model of Tsc1 lesions in mouse brain. PLoS One, 8(5), 2013, e64224, 10.1371/journal.pone.0064224.
179. Prabhakar, S., Zhang, X., Goto, J., Han, S., Lai, C., Bronson, R., Sena-Esteves, M., Ramesh, V., Stemmer-Rachamimov, A., Kwiatkowski, D.J., Breakefield, X.O., Survival benefit and phenotypic improvement by hamartin gene therapy in a tuberous sclerosis mouse brain model. Neurobiol. Dis. 82 (2015), 22–31, 10.1016/j.nbd.2015.04.018.
180. Ran, F.A., Cong, L., Yan, W.X., Scott, D.A., Gootenberg, J.S., Kriz, A.J., Zetsche, B., Shalem, O., Wu, X., Makarova, K.S., Koonin, E.V., Sharp, P.A., Zhang, F., In vivo genome editing using Staphylococcus aureus Cas9. Nature 520:7546 (2015), 186–191, 10.1038/nature14299.
181. Rodríguez-Lebrón, E., Costa Mdo, C., Luna-Cancalon, K., Peron, T.M., Fischer, S., Boudreau, R.L., Davidson, B.L., Paulson, H.L., Silencing mutant ATXN3 expression resolves molecular phenotypes in SCA3 transgenic mice. Mol. Ther. 21:10 (2013), 1909–1918, 10.1038/mt.2013.152.
182. Rogers, G.L., Martino, A.T., Zolotukhin, I., Ertl, H.C., Herzog, R.W., Role of the vector genome and underlying factor IX mutation in immune responses to AAV gene therapy for hemophilia B. J. Transl. Med., 12, 2014, 25, 10.1186/1479-5876-12-25.
183. Russell, D.W., Hirata, R.K., Human gene targeting by viral vectors. Nat. Genet. 18:4 (1998), 325–330.
184. Ruzo, A., Marcó, S., García, 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. 23:12 (2012), 1237–1246, 10.1089/hum.2012.029.
185. Sack, B.K., Herzog, R.W., Evading the immune response upon in vivo gene therapy with viral vectors. Curr. Opin. Mol. Ther. 11:5 (2009), 493–503.
186. 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. 23:4 (2012), 382–389, 10.1089/hum.2011.200.
187. Samaranch, L., San Sebastian, W., Kells, A.P., Salegio, E.A., Heller, G., Bringas, J.R., Pivirotto, P., DeArmond, S., Forsayeth, J., Bankiewicz, K.S., 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. 22:2 (2014), 329–337, 10.1038/mt.2013.26.
188. Samii, A., Nutt, J.G., Ransom, B.R., Parkinson's disease. Lancet 363:9423 (2004), 1783–1793.
189. Sands, M.S., Davidson, B.L., Gene therapy for lysosomal storage diseases. Mol. Ther. 13:5 (2006), 839–849.
190. Sargeant, T.J., Wang, S., Bradley, J., Smith, N.J., Raha, A.A., McNair, R., Ziegler, R.J., Cheng, S.H., Cox, T.M., Cachón-González, M.B., Adeno-associated virus-mediated expression of β-hexosaminidase prevents neuronal loss in the Sandhoff mouse brain. Hum. Mol. Genet. 20:22 (2011), 4371–4380, 10.1093/hmg/ddr364.
191. 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, 10.3389/fnana.2014.00042.
192. Sena-Esteves, M., Saeki, Y., Fraefel, C., Breakefield, X.O., HSV-1 amplicon vectors–simplicity and versatility. Mol. Ther. 2:1 (2000), 9–15.
193. Sevin, C., Benraiss, A., Van Dam, D., Bonnin, D., Nagels, G., Verot, L., Laurendeau, I., Vidaud, M., Gieselmann, V., Vanier, M., De Deyn, P.P., Aubourg, P., Cartier, N., Intracerebral adeno-associated virus-mediated gene transfer in rapidly progressive forms of metachromatic leukodystrophy. Hum. Mol. Genet. 15:1 (2006), 53–64.
194. Shen, S., Bryant, K.D., Brown, S.M., Randell, S.H., Asokan, A., Terminal N-linked galactose is the primary receptor for adeno-associated virus 9. J. Biol. Chem. 286:15 (2011), 13532–13540, 10.1074/jbc.M110.210922.
195. Sheridan, C., Gene therapy finds its niche. Nat. Biotechnol. 29:2 (2011), 121–128, 10.1038/nbt.1769.
196. 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. 22:9 (2011), 1129–1135, 10.1089/hum.2011.008.
197. Spaete, R.R., Frenkel, N., The herpes simplex virus amplicon: a new eucaryotic defective-virus cloning-amplifying vector. Cell. 30:1 (1982), 295–304.
198. 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. Mol. Ther. 19:5 (2011), 860–869, 10.1038/mt.2010.299.
199. Stahnke, S., Lux, K., Uhrig, S., Kreppel, F., Hösel, M., Coutelle, O., Ogris, M., Hallek, M., Büning, H., Intrinsic phospholipase A2 activity of adeno-associated virus is involved in endosomal escape of incoming particles. Virology 409:1 (2011), 77–83, 10.1016/j.virol.2010.09.025.
200. Swiech, L., Heidenreich, M., Banerjee, A., Habib, N., Li, Y., Trombetta, J., Sur, M., Zhang, F., In vivo interrogation of gene function in the mammalian brain using CRISPR-Cas9. Nat. Biotechnol. 33:1 (2015), 102–106, 10.1038/nbt.3055.
201. Tabebordbar, M., Zhu, K., Cheng, J.K., Chew, W.L., Widrick, J.J., Yan, W.X., Maesner, C., Wu, E.Y., Xiao, R., Ran, F.A., Cong, L., Zhang, F., Vandenberghe, L.H., Church, G.M., Wagers, A.J., In vivo gene editing in dystrophic mouse muscle and muscle stem cells. Science 351:6271 (2016), 407–411, 10.1126/science.aad5177.
202. Tardieu, M., Zérah, M., Husson, B., de Bournonville, S., Deiva, K., Adamsbaum, C., Vincent, F., Hocquemiller, M., Broissand, C., Furlan, V., Ballabio, A., Fraldi, A., Crystal, R.G., Baugnon, T., Roujeau, T., Heard, J.M., Danos, O., Intracerebral administration of adeno-associated viral vector serotype rh.10 carrying human SGSH and SUMF1 cDNAs in children with mucopolysaccharidosis type IIIA disease: results of a phase I/II trial. Hum. Gene Ther. 25:6 (2014), 506–516, 10.1089/hum.2013.238.
203. Tebas, P., Stein, D., Tang, W.W., Frank, I., Wang, S.Q., Lee, G., Spratt, S.K., Surosky, R.T., Giedlin, M.A., Nichol, G., Holmes, M.C., Gregory, P.D., Ando, D.G., Kalos, M., Collman, R.G., Binder-Scholl, G., Plesa, G., Hwang, W.T., Levine, B.L., June, C.H., Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. N. Engl. J. Med. 370:10 (2014), 901–910, 10.1056/NEJMoa1300662.
204. Tenney, R.M., Bell, C.L., Wilson, J.M., AAV8 capsid variable regions at the two-fold symmetry axis contribute to high liver transduction by mediating nuclear entry and capsid uncoating. Virology 454–455:454–455 (2014), 227–236, 10.1016/j.virol.2014.02.017.
205. Topaloglu, O., Hurley, P.J., Yildirim, O., Civin, C.I., Bunz, F., Improved methods for the generation of human gene knockout and knockin cell lines. Nucleic Acids Res., 33(18), 2005, e158.
206. Trapani, I., Colella, P., Sommella, A., Iodice, C., Cesi, G., de Simone, S., Marrocco, E., Rossi, S., Giunti, M., Palfi, A., Farrar, G.J., Polishchuk, R., Auricchio, A., Effective delivery of large genes to the retina by dual AAV vectors. EMBO Mol. Med. 6:2 (2014), 194–211, 10.1002/emmm.201302948.
207. Turner, D.L., Snyder, E.Y., Cepko, C.L., Lineage-independent determination of cell type in the embryonic mouse retina. Neuron 4:6 (1990), 833–845.
208. Tuszynski, M.H., Yang, J.H., Barba, D., H.S., U., Bakay, R.A., Pay, M.M., Masliah, E., Conner, J.M., Kobalka, P., Roy, S., Nagahara, A.H., Nerve growth factor gene therapy: activation of neuronal responses in Alzheimer disease. JAMA Neurol. 72:10 (2015), 1139–1147, 10.1001/jamaneurol.2015.1807.
209. Uchida, H., Marzulli, M., Nakano, K., Goins, W.F., Chan, J., Hong, C.S., Mazzacurati, L., Yoo, J.Y., Haseley, A., Nakashima, H., Baek, H., Kwon, H., Kumagai, I., Kuroki, M., Kaur, B., Chiocca, E.A., Grandi, P., Cohen, J.B., Glorioso, J.C., Effective treatment of an orthotopic xenograft model of human glioblastoma using an EGFR-retargeted oncolytic herpes simplex virus. Mol. Ther. 21:3 (2013), 561–569, 10.1038/mt.2012.211.
210. Urabe, M., Ding, C., Kotin, R.M., Insect cells as a factory to produce adeno-associated virus type 2 vectors. Hum. Gene Ther. 13:16 (2002), 1935–1943.
211. Vite, C.H., Passini, M.A., Haskins, M.E., Wolfe, J.H., Adeno-associated virus vector-mediated transduction in the cat brain. Gene Ther. 10:22 (2003), 1874–1881.
212. Wang, R.Y., Bodamer, O.A., Watson, M.S., Wilcox, W.R., ACMG, W., Group, on Diagnostic Confirmation of Lysosomal Storage Diseases. Lysosomal storage diseases: diagnostic confirmation and management of presymptomatic individuals. Genet. Med. 13:5 (2011), 457–484, 10.1097/GIM.0b013e318211a7e1.
213. Wang, N., Gray, M., Lu, X.H., Cantle, J.P., Holley, S.M., Greiner, E., Gu, X., Shirasaki, D., Cepeda, C., Li, Y., Dong, H., Levine, M.S., Yang, X.W., Neuronal targets for reducing mutant huntingtin expression to ameliorate disease in a mouse model of Huntington's disease. Nat. Med. 20:5 (2014), 536–541, 10.1038/nm.3514.
214. Wang, S., Olumolade, O.O., Sun, T., Samiotaki, G., Konofagou, E.E., Noninvasive, neuron-specific gene therapy can be facilitated by focused ultrasound and recombinant adeno-associated virus. Gene Ther. 22:1 (2015), 104–110, 10.1038/gt.2014.91.
215. 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. 24:15 (2015), 4353–4364, 10.1093/hmg/ddv168.
216. Wilson, J.M., Lessons learned from the gene therapy trial for ornithine transcarbamylase deficiency. Mol. Genet. Metab. 96:4 (2009), 151–157.
217. Wong, A.D., Ye, M., Levy, A.F., Rothstein, J.D., Bergles, D.E., Searson, P.C., The blood-brain barrier: an engineering perspective. Front. Neuroeng., 6, 2013, 7, 10.3389/fneng.2013.00007.
218. Worgall, S., Sondhi, D., Hackett, N.R., Kosofsky, B., Kekatpure, M.V., Neyzi, N., Dyke, J.P., Ballon, D., Heier, L., Greenwald, B.M., Christos, P., Mazumdar, M., Souweidane, M.M., Kaplitt, M.G., Crystal, R.G., Treatment of late infantile neuronal ceroid lipofuscinosis by CNS administration of a serotype 2 adeno-associated virus expressing CLN2 cDNA. Hum. Gene Ther. 19:5 (2008), 463–474, 10.1089/hum.2008.022.
219. Xiao, W., Chirmule, N., Berta, S.C., McCullough, B., Gao, G., Wilson, J.M., Gene therapy vectors based on adeno-associated virus type 1. J. Virol. 73:5 (1999), 3994–4003.
220. Xiao, P.J., Samulski, R.J., Cytoplasmic trafficking, endosomal escape, and perinuclear accumulation of adeno-associated virus type 2 particles are facilitated by microtubule network. J. Virol., 86(19), 2012, 10.1128/JVI.00935-12 10462–10471-473.
221. 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 Mol. Med. 5:11 (2013), 1710–1719, 10.1002/emmm.201302935.
222. Yan, Z., Zhang, Y., Duan, D., Engelhardt, J.F., Trans-splicing vectors expand the utility of adeno-associated virus for gene therapy. Proc. Natl. Acad. Sci. U. S. A. 97:12 (2000), 6716–6721.
223. 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. Mol. Ther. 22:7 (2014), 1299–1309, 10.1038/mt.2014.68.
224. Yang, Y., Wang, L., Bell, P., McMenamin, D., He, Z., White, J., Yu, H., Xu, C., Morizono, H., Musunuru, K., Batshaw, M.L., Wilson, J.M., A dual AAV system enables the Cas9-mediated correction of a metabolic liver disease in newborn mice. Feb 1 Nat. Biotechnol., 2016, 10.1038/nbt. 3469 [Epub ahead of print], PMID: 26829317.
225. Yuasa, K., Sakamoto, M., Miyagoe-Suzuki, Y., Tanouchi, A., Yamamoto, H., Li, J., Chamberlain, J.S., Xiao, X., Takeda, S., Adeno-associated virus vector-mediated gene transfer into dystrophin-deficient skeletal muscles evokes enhanced immune response against the transgene product. Gene Ther. 9:23 (2002), 1576–1588.
226. Zetsche, B., Gootenberg, J.S., Abudayyeh, O.O., Slaymaker, I.M., Makarova, K.S., Essletzbichler, P., Volz, S.E., Joung, J., van der Oost, J., Regev, A., Koonin, E.V., Zhang, F., Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell. 163:3 (2015), 759–771, 10.1016/j.cell.2015.09.038.
227. 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. Mol. Ther. 19:8 (2011), 1440–1448, 10.1038/mt.2011.98.
228. Zharikov, A.D., Cannon, J.R., Tapias, V., Bai, Q., Horowitz, M.P., Shah, V., El Ayadi, A., Hastings, T.G., Greenamyre, J.T., Burton, E.A., shRNA targeting α-synuclein prevents neurodegeneration in a Parkinson's disease model. J. Clin. Invest. 125:7 (2015), 2721–2735, 10.1172/JCI64502.
229. Zirger, J.M., Puntel, M., Bergeron, J., Wibowo, M., Moridzadeh, R., Bondale, N., Barcia, C., Kroeger, K.M., Liu, C., Castro, M.G., Lowenstein, P.R., Immune-mediated loss of transgene expression from virally transduced brain cells is irreversible, mediated by IFNγ, perforin, and TNFα, and due to the elimination of transduced cells. Mol. Ther. 20:4 (2012), 808–819, 10.1038/mt.2011.243.