In vivo targeting of subventricular zone astrocytes

Progress in Neurobiology

Volumn 92, Issue 1, 2010, Pages 19-32

  Mamber, Carlyn ^a   Verhaagen, Joost ^a   Hol, Elly M ^a  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

AAV; Astrocyte; Cre LoxP; Electroporation; Lentivirus; Neural stem cell; Subventricular zone

Indexed keywords

ADENOVIRUS VECTOR;

ADENO ASSOCIATED VIRUS; ASTROCYTE; BRAIN INJURY; ELECTROPORATION; GENE EXPRESSION; GENE TRANSFER; GENETIC TRANSDUCTION; LOXP SITE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; SUBVENTRICULAR ZONE; TRANSGENE; TRANSIENT EXPRESSION;

EID: 77953923862     PISSN: 03010082     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pneurobio.2010.04.007     Document Type: Review

References (161)

1. Ahmed B.Y., Chakravarthy S., Eggers R., Hermens W.T., Zhang J.Y., Niclou S.P., Levelt C., Sablitzky F., Anderson P.N., Lieberman A.R., Verhaagen J. Efficient delivery of Cre-recombinase to neurons in vivo and stable transduction of neurons using adeno-associated and lentiviral vectors. BMC Neurosci. 2004, 5:4.
2. Aitken M.L., Moss R.B., Waltz D.A., Dovey M.E., Tonelli M.R., McNamara S.C., Gibson R.L., Ramsey B.W., Carter B.J., Reynolds T.C. A phase I study of aerosolized administration of tgAAVCF to cystic fibrosis subjects with mild lung disease. Hum. Gene Ther. 2001, 12:1907-1916.
3. Akache B., Grimm D., Pandey K., Yant S.R., Xu H., Kay M.A. The 37/67-kilodalton laminin receptor is a receptor for adeno-associated virus serotypes 8, 2, 3, and 9. J. Virol. 2006, 80:9831-9836.
4. Allen E. The cessation of mitosis in the central nervous system of the albino rat. J. Comp. Neurol. 1912, 22:547-568.
5. Allocca M., Doria M., Petrillo M., Colella P., Garcia-Hoyos M., Gibbs D., Kim S.R., Maguire A., Rex T.S., Di Vicino U., Cutillo L., Sparrow J.R., Williams D.S., Bennett J., Auricchio A. Serotype-dependent packaging of large genes in adeno-associated viral vectors results in effective gene delivery in mice. J. Clin. Invest. 2008, 118:1955-1964.
6. Alonso M., Ortega-Perez I., Grubb M.S., Bourgeois J.P., Charneau P., Lledo P.M. Turning astrocytes from the rostral migratory stream into neurons: a role for the olfactory sensory organ. J. Neurosci. 2008, 28:11089-11102.
7. Alvarez-Buylla A., Garcia-Verdugo J.M. Neurogenesis in adult subventricular zone. J. Neurosci. 2002, 22:629-634.
8. Alvarez-Buylla A., Garcia-Verdugo J.M., Tramontin A.D. A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2001, 2:287-293.
9. Anthony T.E., Heintz N. The folate metabolic enzyme ALDH1L1 is restricted to the midline of the early CNS, suggesting a role in human neural tube defects. J. Comp. Neurol. 2007, 500:368-383.
10. Atchison R.W., Casto B.C., Hammon W.M. Adenovirus-associated defective virus particles. Science 1965, 149:754-756.
11. Aucoin M.G., Perrier M., Kamen A.A. Critical assessment of current adeno-associated viral vector production and quantification methods. Biotechnol. Adv. 2008, 26:73-88.
12. Azzouz M., Kingsman S.M., Mazarakis N.D. Lentiviral vectors for treating and modeling human CNS disorders. J. Gene. Med. 2004, 6:951-962.
13. Baekelandt V., Claeys A., Eggermont K., Lauwers E., De S.B., Nuttin B., Debyser Z. Characterization of lentiviral vector-mediated gene transfer in adult mouse brain. Hum. Gene Ther. 2002, 13:841-853.
14. Bantel-Schaal U., zur Hausen H. Characterization of the DNA of a defective human parvovirus isolated from a genital site. Virology 1984, 134:52-63.
15. Barnabe-Heider F., Meletis K., Eriksson M., Bergmann O., Sabelstrom H., Harvey M.A., Mikkers H., Frisen J. Genetic manipulation of adult mouse neurogenic niches by in vivo electroporation. Nat. Methods 2008, 5:189-196.
16. Belur L.R., Kaemmerer W.F., McIvor R.S., Low W.C. Adeno-associated virus type 2 vectors: transduction and long-term expression in cerebellar Purkinje cells in vivo is mediated by the fibroblast growth factor receptor 1: bFGFR-1 mediates AAV2 transduction of Purkinje cells. Arch. Virol. 2008, 153:2107-2110.
17. Berton O., McClung C.A., Dileone R.J., Krishnan V., Renthal W., Russo S.J., Graham D., Tsankova N.M., Bolanos C.A., Rios M., Monteggia L.M., Self D.W., Nestler E.J. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 2006, 311:864-868.
18. Besnard F., Perraud F., Sensenbrenner M., Labourdette G. Platelet-derived growth factor is a mitogen for glial but not for neuronal rat brain cells in vitro. Neurosci. Lett. 1987, 73:287-292.
19. Bigey P., Bureau M.F., Scherman D. In vivo plasmid DNA electrotransfer. Curr. Opin. Biotechnol. 2002, 13:443-447.
20. Bloquel C., Fabre E., Bureau M.F., Scherman D. Plasmid DNA electrotransfer for intracellular and secreted proteins expression: new methodological developments and applications. J. Gene Med. 2004, 6(Suppl. 1):S11-S23.
21. Bonthius D.J., Mahoney J., Buchmeier M.J., Karacay B., Taggard D. Critical role for glial cells in the propagation and spread of lymphocytic choriomeningitis virus in the developing rat brain. J. Virol. 2002, 76:6618-6635.
22. Brenner M., Kisseberth W.C., Su Y., Besnard F., Messing A. GFAP promoter directs astrocyte-specific expression in transgenic mice. J. Neurosci. 1994, 14:1030-1037.
23. Buffo A., Rite I., Tripathi P., Lepier A., Colak D., Horn A.P., Mori T., Gotz M. Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:3581-3586.
24. Cahoy J.D., Emery B., Kaushal A., Foo L.C., Zamanian J.L., Christopherson K.S., Xing Y., Lubischer J.L., Krieg P.A., Krupenko S.A., Thompson W.J., Barres B.A. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 2008, 28:264-278.
25. Calaora V., Chazal G., Nielsen P.J., Rougon G., Moreau H. mCD24 expression in the developing mouse brain and in zones of secondary neurogenesis in the adult. Neuroscience 1996, 73:581-594.
26. Camp S., Zhang L., Marquez M., de la Torre B., Long J.M., Bucht G., Taylor P. Acetylcholinesterase (AChE) gene modification in transgenic animals: functional consequences of selected exon and regulatory region deletion. Chem. Biol. Interact. 2005, 157-158:79-86.
27. Capela A., Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 2002, 35:865-875.
28. Casper K.B., McCarthy K.D. GFAP-positive progenitor cells produce neurons and oligodendrocytes throughout the CNS. Mol. Cell Neurosci. 2006, 31:676-684.
29. 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. 2006, 13:528-537.
30. Chang L.J., Gay E.E. The molecular genetics of lentiviral vectors-current and future perspectives. Curr. Gene Ther. 2001, 1:237-251.
31. Chow L.M., Zhang J., Baker S.J. Inducible Cre recombinase activity in mouse mature astrocytes and adult neural precursor cells. Transgenic Res. 2008, 17:919-928.
32. Colin A., Faideau M., Dufour N., Auregan G., Hassig R., Andrieu T., Brouillet E., Hantraye P., Bonvento G., Deglon N. Engineered lentiviral vector targeting astrocytes in vivo. Glia 2009, 57:667-679.
33. Conover J.C., Allen R.L. The subventricular zone: new molecular and cellular developments. Cell Mol. Life Sci. 2002, 59:2128-2135.
34. Consiglio A., Gritti A., Dolcetta D., Follenzi A., Bordignon C., Gage F.H., Vescovi A.L., Naldini L. Robust in vivo gene transfer into adult mammalian neural stem cells by lentiviral vectors. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:14835-14840.
35. Curtis M.A., Waldvogel H.J., Synek B., Faull R.L. A histochemical and immunohistochemical analysis of the subependymal layer in the normal and Huntington's disease brain. J. Chem. Neuroanat. 2005, 30:55-66.
36. 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. 2000, 97:3428-3432.
37. de Leeuw B., Su M., ter Horst M., Iwata S., Rodijk M., Hoeben R.C., Messing A., Smitt P.S., Brenner M. Increased glia-specific transgene expression with glial fibrillary acidic protein promoters containing multiple enhancer elements. J. Neurosci. Res. 2006, 83:744-753.
38. Desilva T.M., Kinney H.C., Borenstein N.S., Trachtenberg F.L., Irwin N., Volpe J.J., Rosenberg P.A. The glutamate transporter EAAT2 is transiently expressed in developing human cerebral white matter. J. Comp. Neurol. 2007, 501:879-890.
39. Di Pasquale G., Davidson B.L., Stein C.S., Martins I., Scudiero D., Monks A., Chiorini J.A. Identification of PDGFR as a receptor for AAV-5 transduction. Nat. Med. 2003, 9:1306-1312.
40. Doetsch F., Alvarez-Buylla A. Network of tangential pathways for neuronal migration in adult mammalian brain. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:14895-14900.
41. Doetsch F., Caille I., Lim D.A., Garcia-Verdugo J.M., Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999, 97:703-716.
42. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 1997, 17:5046-5061.
43. Doetsch F., Petreanu L., Caille I., Garcia-Verdugo J.M., Alvarez-Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 2002, 36:1021-1034.
44. 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. Mol. Ther. 2009, 17:1187-1196.
45. Feng X., Eide F.F., Jiang H., Reder A.T. Adeno-associated viral vector-mediated ApoE expression in Alzheimer's disease mice: low CNS immune response, long-term expression, and astrocyte specificity. Front. Biosci. 2004, 9:1540-1546.
46. Follenzi A., Santambrogio L., Annoni A. Immune responses to lentiviral vectors. Curr. Gene Ther. 2007, 7:306-315.
47. 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. 2009, 27:59-65.
48. Gal J.S., Morozov Y.M., Ayoub A.E., Chatterjee M., Rakic P., Haydar T.F. Molecular and morphological heterogeneity of neural precursors in the mouse neocortical proliferative zones. J. Neurosci. 2006, 26:1045-1056.
49. Ganat Y.M., Silbereis J., Cave C., Ngu H., Anderson G.M., Ohkubo Y., Ment L.R., Vaccarino F.M. Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J. Neurosci. 2006, 26:8609-8621.
50. 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. 2004, 78:6381-6388.
51. Garcia-Verdugo J.M., Doetsch F., Wichterle H., Lim D.A., Alvarez-Buylla A. Architecture and cell types of the adult subventricular zone: in search of the stem cells. J. Neurobiol. 1998, 36:234-248.
52. Garcia A.D., Doan N.B., Imura T., Bush T.G., Sofroniew M.V. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat. Neurosci. 2004, 7:1233-1241.
53. Geraerts M., Eggermont K., Hernandez-Acosta P., Garcia-Verdugo J.M., Baekelandt V., Debyser Z. Lentiviral vectors mediate efficient and stable gene transfer in adult neural stem cells in vivo. Hum. Gene Ther. 2006, 17:635-650.
54. Gilyarov A.V. Nestin in central nervous system cells. Neurosci. Behav. Physiol. 2008, 38:165-169.
55. Gray S.J., Samulski R.J. Optimizing gene delivery vectors for the treatment of heart disease. Expert Opin. Biol. Ther. 2008, 8:911-922.
56. Grieger J.C., Samulski R.J. Packaging capacity of adeno-associated virus serotypes: impact of larger genomes on infectivity and postentry steps. J. Virol. 2005, 79:9933-9944.
57. Haas K., Sin W.C., Javaherian A., Li Z., Cline H.T. Single-cell electroporation for gene transfer in vivo. Neuron 2001, 29:583-591.
58. Haberman R.P., McCown T.J., Samulski R.J. Inducible long-term gene expression in brain with adeno-associated virus gene transfer. Gene Ther. 1998, 5:1604-1611.
59. Hagiwara T., Tanaka K., Takai S., Maeno-Hikichi Y., Mukainaka Y., Wada K. Genomic organization, promoter analysis, and chromosomal localization of the gene for the mouse glial high-affinity glutamate transporter Slc1a3. Genomics 1996, 33:508-515.
60. Hajjar R.J., Zsebo K., Deckelbaum L., Thompson C., Rudy J., Yaroshinsky A., Ly H., Kawase Y., Wagner K., Borow K., Jaski B., London B., Greenberg B., Pauly D.F., Patten R., Starling R., Mancini D., Jessup M. Design of a phase 1/2 trial of intracoronary administration of AAV1/SERCA2a in patients with heart failure. J. Card. Fail. 2008, 14:355-367.
61. Han Z., Zhong L., Maina N., Hu Z., Li X., Chouthai N.S., Bischof D., Weigel-Van Aken K.A., Slayton W.B., Yoder M.C., Srivastava A. Stable integration of recombinant adeno-associated virus vector genomes after transduction of murine hematopoietic stem cells. Hum. Gene Ther. 2008, 19:267-278.
62. Hermens W.T., Verhaagen J. Viral vectors, tools for gene transfer in the nervous system. Prog. Neurobiol. 1998, 55:399-432.
63. Hommel J.D., Sears R.M., Georgescu D., Simmons D.L., Dileone R.J. Local gene knockdown in the brain using viral-mediated RNA interference. Nat. Med. 2003, 9:1539-1544.
64. Ishii Y., Matsumoto Y., Watanabe R., Elmi M., Fujimori T., Nissen J., Cao Y., Nabeshima Y., Sasahara M., Funa K. Characterization of neuroprogenitor cells expressing the PDGF beta-receptor within the subventricular zone of postnatal mice. Mol. Cell Neurosci. 2008, 37:507-518.
65. Jackson E.L., Garcia-Verdugo J.M., Gil-Perotin S., Roy M., Quinones-Hinojosa A., VandenBerg S., Alvarez-Buylla A. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 2006, 51:187-199.
66. Jakobsson J., Lundberg C. Lentiviral vectors for use in the central nervous system. Mol. Ther. 2006, 13:484-493.
67. Jin K., Sun Y., Xie L., Peel A., Mao X.O., Batteur S., Greenberg D.A. Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum. Mol. Cell Neurosci. 2003, 24:171-189.
68. Johnson M.A., Ables J.L., Eisch A.J. Cell-intrinsic signals that regulate adult neurogenesis in vivo: insights from inducible approaches. BMB Rep. 2009, 42:245-259.
69. Jucker M., Bialobok P., Kleinman H.K., Walker L.C., Hagg T., Ingram D.K. Laminin-like and laminin-binding protein-like immunoreactive astrocytes in rat hippocampus after transient ischemia. Antibody to laminin-binding protein is a sensitive marker of neural injury and degeneration. Ann. N.Y. Acad. Sci. 1993, 679:245-252.
70. 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. 2001, 75:6884-6893.
71. Kang Y., Stein C.S., Heth J.A., Sinn P.L., Penisten A.K., Staber P.D., Ratliff K.L., Shen H., Barker C.K., Martins I., Sharkey C.M., Sanders D.A., McCray P.B., Davidson B.L. In vivo gene transfer using a nonprimate lentiviral vector pseudotyped with Ross River Virus glycoproteins. J. Virol. 2002, 76:9378-9388.
72. 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 2007, 369:2097-2105.
73. Kim V.N., Mitrophanous K., Kingsman S.M., Kingsman A.J. Minimal requirement for a lentivirus vector based on human immunodeficiency virus type 1. J. Virol. 1998, 72:811-816.
74. Klein R.L., Dayton R.D., Tatom J.B., Henderson K.M., Henning P.P. AAV8, 9, Rh10, Rh43 vector gene transfer in the rat brain: effects of serotype, promoter and purification method. Mol. Ther. 2008, 16:89-96.
75. Koerber J.T., Klimczak R., Jang J.H., Dalkara D., Flannery J.G., Schaffer D.V. Molecular evolution of adeno-associated virus for enhanced glial gene delivery. Mol. Ther. 2009, 17:2088-2095.
76. Komitova M., Eriksson P.S. Sox-2 is expressed by neural progenitors and astroglia in the adult rat brain. Neurosci. Lett. 2004, 369:24-27.
77. Kornack D.R., Rakic P. The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:4752-4757.
78. Kreiss P., Cameron B., Rangara R., Mailhe P., Aguerre-Charriol O., Airiau M., Scherman D., Crouzet J., Pitard B. Plasmid DNA size does not affect the physicochemical properties of lipoplexes but modulates gene transfer efficiency. Nucleic Acids Res. 1999, 27:3792-3798.
79. Kuo C.T., Mirzadeh Z., Soriano-Navarro M., Rasin M., Wang D., Shen J., Sestan N., Garcia-Verdugo J., Alvarez-Buylla A., Jan L.Y., Jan Y.N. Postnatal deletion of Numb/Numblike reveals repair and remodeling capacity in the subventricular neurogenic niche. Cell 2006, 127:1253-1264.
80. Kwon I., Schaffer D.V. Designer gene delivery vectors: molecular engineering and evolution of adeno-associated viral vectors for enhanced gene transfer. Pharm. Res. 2008, 25:489-499.
81. Lai Z., Brady R.O. Gene transfer into the central nervous system in vivo using a recombinanat lentivirus vector. J. Neurosci. Res. 2002, 67:363-371.
82. Laywell E.D., Rakic P., Kukekov V.G., Holland E.C., Steindler D.A. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:13883-13888.
83. Lee Y., Messing A., Su M., Brenner M. GFAP promoter elements required for region-specific and astrocyte-specific expression. Glia 2008, 56:481-493.
84. Lepekhin E.A., Eliasson C., Berthold C.H., Berezin V., Bock E., Pekny M. Intermediate filaments regulate astrocyte motility. J. Neurochem. 2001, 79:617-625.
85. Lewandoski M. Conditional control of gene expression in the mouse. Nat. Rev. Genet. 2001, 2:743-755.
86. Lichty B.D., Power A.T., Stojdl D.F., Bell J.C. Vesicular stomatitis virus: re-inventing the bullet. Trends Mol. Med. 2004, 10:210-216.
87. Lim D.A., Tramontin A.D., Trevejo J.M., Herrera D.G., Garcia-Verdugo J.M., Alvarez-Buylla A. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 2000, 28:713-726.
88. 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. 2005, 12:1503-1508.
89. Liu X., Bolteus A.J., Balkin D.M., Henschel O., Bordey A. GFAP-expressing cells in the postnatal subventricular zone display a unique glial phenotype intermediate between radial glia and astrocytes. Glia 2006, 54:394-410.
90. Lledo P.M., Alonso M., Grubb M.S. Adult neurogenesis and functional plasticity in neuronal circuits. Nat. Rev. Neurosci. 2006, 7:179-193.
91. Lledo P.M., Merkle F.T., Alvarez-Buylla A. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci. 2008, 31:392-400.
92. Lois C., Garcia-Verdugo J.M., Alvarez-Buylla A. Chain migration of neuronal precursors. Science 1996, 271:978-981.
93. Loonstra A., Vooijs M., Beverloo H.B., Allak B.A., van Drunen E., Kanaar R., Berns A., Jonkers J. Growth inhibition and DNA damage induced by Cre recombinase in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:9209-9214.
94. Luskin M.B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 1993, 11:173-189.
95. Marks W.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. 2008, 7:400-408.
96. Martinian L., Boer K., Middeldorp J., Hol E.M., Sisodiya S.M., Squier W., Aronica E., Thom M. Expression patterns of glial fibrillary acidic protein (GFAP)-delta in epilepsy-associated lesional pathologies. Neuropathol. Appl. Neurobiol. 2009, 35:394-405.
97. Mazarakis N.D., Azzouz M., Rohll J.B., Ellard F.M., Wilkes F.J., Olsen A.L., Carter E.E., Barber R.D., Baban D.F., Kingsman S.M., Kingsman A.J., O'Malley K., Mitrophanous K.A. Rabies virus glycoprotein pseudotyping of lentiviral vectors enables retrograde axonal transport and access to the nervous system after peripheral delivery. Hum. Mol. Genet. 2001, 10:2109-2121.
98. McCarty D.M., Young S.M., Samulski R.J. Integration of adeno-associated virus (AAV) and recombinant AAV vectors. Annu. Rev. Genet. 2004, 38:819-845.
99. McCown T.J., Xiao X., Li J., Breese G.R., Samulski R.J. Differential and persistent expression patterns of CNS gene transfer by an adeno-associated virus (AAV) vector. Brain Res. 1996, 713:99-107.
100. Meunier A., Pohl M. Lentiviral vectors for gene transfer into the spinal cord glial cells. Gene Ther. 2009, 16:476-482.
101. Middeldorp J., Boer K., Sluijs J.A., De Filippis L., Encha-Razavi F., Vescovi A.L., Swaab D.F., Aronica E., Hol E.M. GFAPdelta in radial glia and subventricular zone progenitors in the developing human cortex. Development 2010, 137:313-321.
102. Miletic H., Fischer Y.H., Neumann H., Hans V., Stenzel W., Giroglou T., Hermann M., Deckert M., Von L.D. Selective transduction of malignant glioma by lentiviral vectors pseudotyped with lymphocytic choriomeningitis virus glycoproteins. Hum. Gene Ther. 2004, 15:1091-1100.
103. Mitchell R.S., Beitzel B.F., Schroder A.R., Shinn P., Chen H., Berry C.C., Ecker J.R., Bushman F.D. Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol. 2004, 2:E234.
104. Mori T., Tanaka K., Buffo A., Wurst W., Kuhn R., Gotz M. Inducible gene deletion in astroglia and radial glia-a valuable tool for functional and lineage analysis. Glia 2006, 54:21-34.
105. Nagy A. Cre recombinase: the universal reagent for genome tailoring. Genesis 2000, 26:99-109.
106. Naldini L., Blomer U., Gage F.H., Trono D., Verma I.M. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:11382-11388.
107. Nam H.S., Benezra R. High levels of Id1 expression define B1 type adult neural stem cells. Cell Stem Cell 2009, 5:515-526.
108. Neumann E., Schaefer-Ridder M., Wang Y., Hofschneider P.H. Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J. 1982, 1:841-845.
109. Neymeyer V., Tephly T.R., Miller M.W. Folate and 10-formyltetrahydrofolate dehydrogenase (FDH) expression in the central nervous system of the mature rat. Brain Res. 1997, 766:195-204.
110. Oehmig A., Fraefel C., Breakefield X.O., Ackermann M. Herpes simplex virus type 1 amplicons and their hybrid virus partners, EBV, AAV, and retrovirus. Curr. Gene Ther. 2004, 4:385-408.
111. Ogunkoya A.B., Beran G.W., Umoh J.U., Gomwalk N.E., Abdulkadir I.A. Serological evidence of infection of dogs and man in Nigeria by lyssaviruses (family Rhabdoviridae). Trans. R. Soc. Trop. Med. Hyg. 1990, 84:842-845.
112. Oumesmar B.N., Vignais L., Baron-Van E.A. Developmental expression of platelet-derived growth factor alpha-receptor in neurons and glial cells of the mouse CNS. J. Neurosci. 1997, 17:125-139.
113. Pallari H.M., Eriksson J.E. Intermediate filaments as signaling platforms. Sci. STKE 2006, 2006:pe53.
114. Parks W.P., Melnick J.L., Rongey R., Mayor H.D. Physical assay and growth cycle studies of a defective adeno-satellite virus. J. Virol. 1967, 1:171-180.
115. Pastrana E., Cheng L.C., Doetsch F. Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:6387-6392.
116. Paz H., Wong C.A., Li W., Santat L., Wong K.K., Chatterjee S. Quiescent subpopulations of human CD34-positive hematopoietic stem cells are preferred targets for stable recombinant adeno-associated virus type 2 transduction. Hum. Gene Ther. 2007, 18:614-626.
117. Peel A.L., Klein R.L. Adeno-associated virus vectors: activity and applications in the CNS. J. Neurosci. Methods 2000, 98:95-104.
118. Philippe S., Sarkis C., Barkats M., Mammeri H., Ladroue C., Petit C., Mallet J., Serguera C. Lentiviral vectors with a defective integrase allow efficient and sustained transgene expression in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:17684-17689.
119. Pilpel N., Landeck N., Klugmann M., Seeburg P.H., Schwarz M.K. Rapid, reproducible transduction of select forebrain regions by targeted recombinant virus injection into the neonatal mouse brain. J. Neurosci. Methods 2009, 182:55-63.
120. Platel J.C., Gordon V., Heintz T., Bordey A. GFAP-GFP neural progenitors are antigenically homogeneous and anchored in their enclosed mosaic niche. Glia 2009, 57:66-78.
121. Quinones-Hinojosa A., Sanai N., Soriano-Navarro M., Gonzalez-Perez O., Mirzadeh Z., Gil-Perotin S., Romero-Rodriguez R., Berger M.S., Garcia-Verdugo J.M., Alvarez-Buylla A. Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J. Comp. Neurol. 2006, 494:415-434.
122. Raponi E., Agenes F., Delphin C., Assard N., Baudier J., Legraverend C., Deloulme J.C. S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 2007, 55:165-177.
123. Regan M.R., Huang Y.H., Kim Y.S., Dykes-Hoberg M.I., Jin L., Watkins A.M., Bergles D.E., Rothstein J.D. Variations in promoter activity reveal a differential expression and physiology of glutamate transporters by glia in the developing and mature CNS. J. Neurosci. 2007, 27:6607-6619.
124. Reich S.J., Auricchio A., Hildinger M., Glover E., Maguire A.M., Wilson J.M., Bennett J. Efficient trans-splicing in the retina expands the utility of adeno-associated virus as a vector for gene therapy. Hum. Gene Ther. 2003, 14:37-44.
125. Roelofs R.F., Fischer D.F., Houtman S.H., Sluijs J.A., Van H.W., Van Leeuwen F.W., Hol E.M. Adult human subventricular, subgranular, and subpial zones contain astrocytes with a specialized intermediate filament cytoskeleton. Glia 2005, 52:289-300.
126. Rols M.P., Delteil C., Golzio M., Dumond P., Cros S., Teissie J. In vivo electrically mediated protein and gene transfer in murine melanoma. Nat. Biotechnol. 1998, 16:168-171.
127. Romera C., Hurtado O., Mallolas J., Pereira M.P., Morales J.R., Romera A., Serena J., Vivancos J., Nombela F., Lorenzo P., Lizasoain I., Moro M.A. Ischemic preconditioning reveals that GLT1/EAAT2 glutamate transporter is a novel PPARgamma target gene involved in neuroprotection. J. Cereb. Blood Flow Metab. 2007, 27:1327-1338.
128. Rothstein J.D., Martin L., Levey A.I., Dykes-Hoberg M., Jin L., Wu D., Nash N., Kuncl R.W. Localization of neuronal and glial glutamate transporters. Neuron 1994, 13:713-725.
129. Sanai N., Tramontin A.D., Quinones-Hinojosa A., Barbaro N.M., Gupta N., Kunwar S., Lawton M.T., McDermott M.W., Parsa A.T., Manuel-Garcia V.J., Berger M.S., Alvarez-Buylla A. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004, 427:740-744.
130. Schipani E. Conditional gene inactivation using cre recombinase. Calcif. Tissue Int. 2002, 71:100-102.
131. Sevin C., Benraiss A., Van D.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. 2006, 15:53-64.
132. Shevtsova Z., Malik J.M., Michel U., Bahr M., Kugler S. Promoters and serotypes: targeting of adeno-associated virus vectors for gene transfer in the rat central nervous system in vitro and in vivo. Exp. Physiol. 2005, 90:53-59.
133. Slezak M., Goritz C., Niemiec A., Frisen J., Chambon P., Metzger D., Pfrieger F.W. Transgenic mice for conditional gene manipulation in astroglial cells. Glia 2007, 55:1565-1576.
134. Slotkin J.R., Chakrabarti L., Dai H.N., Carney R.S., Hirata T., Bregman B.S., Gallicano G.I., Corbin J.G., Haydar T.F. In vivo quantum dot labeling of mammalian stem and progenitor cells. Dev. Dyn. 2007, 236:3393-3401.
135. Stein C.S., Martins I., Davidson B.L. The lymphocytic choriomeningitis virus envelope glycoprotein targets lentiviral gene transfer vector to neural progenitors in the murine brain. Mol. Ther. 2005, 11:382-389.
136. Stieger K., Schroeder J., Provost N., Mendes-Madeira A., Belbellaa B., Le Meur G., Weber M., Deschamps J.Y., Lorenz B., Moullier P., Rolling F. Detection of intact rAAV particles up to 6 years after successful gene transfer in the retina of dogs and primates. Mol. Ther. 2009, 17:516-523.
137. Storck T., Schulte S., Hofmann K., Stoffel W. Structure, expression, and functional analysis of a Na(+)-dependent glutamate/aspartate transporter from rat brain. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:10955-10959.
138. Su M., Hu H., Lee Y., d'Azzo A., Messing A., Brenner M. Expression specificity of GFAP transgenes. Neurochem. Res. 2004, 29:2075-2093.
139. Su Z.Z., Leszczyniecka M., Kang D.C., Sarkar D., Chao W., Volsky D.J., Fisher P.B. Insights into glutamate transport regulation in human astrocytes: cloning of the promoter for excitatory amino acid transporter 2 (EAAT2). Proc. Natl. Acad. Sci. U.S.A. 2003, 100:1955-1960.
140. Swartz M., Eberhart J., Mastick G.S., Krull C.E. Sparking new frontiers: using in vivo electroporation for genetic manipulations. Dev. Biol. 2001, 233:13-21.
141. Tenenbaum L., Chtarto A., Lehtonen E., Velu T., Brotchi J., Levivier M. Recombinant AAV-mediated gene delivery to the central nervous system. J. Gene Med. 2004, 6(Suppl. 1):S212-S222.
142. Terzi D., Zachariou V. Adeno-associated virus-mediated gene delivery approaches for the treatment of CNS disorders. Biotechnol. J. 2008, 3:1555-1563.
143. Teschemacher A.G., Paton J.F., Kasparov S. Imaging living central neurones using viral gene transfer. Adv. Drug Deliv. Rev. 2005, 57:79-93.
144. van den Berge S.A., Middeldorp J., Zhang C.E., Curtis M.A., Leonard B.W., Mastroeni D., Voorn P., Berg W.D.J.v.d., Huitinga I., Hol E.M. Longterm quiescent cells in the aged human subventricular neurogenic system specifically express GFAP-delta. Aging Cell 2010, 9:313-326.
145. VandenDriessche T. Muscling through AAV immunity. Blood 2009, 114:2009-2010.
146. Wang C.Y., Wang S. Astrocytic expression of transgene in the rat brain mediated by baculovirus vectors containing an astrocyte-specific promoter. Gene Ther. 2006, 13:1447-1456.
147. Wang D.D., Bordey A. The astrocyte odyssey. Prog. Neurobiol. 2008, 86:342-367.
148. Wang W.C., Mihlbachler K.A., Brunnett A.C., Liggett S.B. Targeted transgenesis reveals discrete attenuator functions of GRK and PKA in airway beta2-adrenergic receptor physiologic signaling. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:15007-15012.
149. Watson D.J., Kobinger G.P., Passini M.A., Wilson J.M., Wolfe J.H. Targeted transduction patterns in the mouse brain by lentivirus vectors pseudotyped with VSV, Ebola, Mokola, LCMV, or MuLV envelope proteins. Mol. Ther. 2002, 5:528-537.
150. Watson D.J., Passini M.A., Wolfe J.H. Transduction of the choroid plexus and ependyma in neonatal mouse brain by vesicular stomatitis virus glycoprotein-pseudotyped lentivirus and adeno-associated virus type 5 vectors. Hum. Gene Ther. 2005, 16:49-56.
151. Wegner M. A matter of identity: transcriptional control in oligodendrocytes. J. Mol. Neurosci. 2008, 35:3-12.
152. Whitman M.C., Greer C.A. Adult neurogenesis and the olfactory system. Prog. Neurobiol. 2009, 89:162-175.
153. Wichterle H., Garcia-Verdugo J.M., Alvarez-Buylla A. Direct evidence for homotypic, glia-independent neuronal migration. Neuron 1997, 18:779-791.
154. Wu Z., Yang H., Colosi P. Effect of genome size on AAV vector packaging. Mol. Ther. 2009.
155. Yamashita T., Ninomiya M., Hernandez A.P., Garcia-Verdugo J.M., Sunabori T., Sakaguchi M., Adachi K., Kojima T., Hirota Y., Kawase T., Araki N., Abe K., Okano H., Sawamoto K. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J. Neurosci. 2006, 26:6627-6636.
156. Yanez-Munoz R.J., Balaggan K.S., MacNeil A., Howe S.J., Schmidt M., Smith A.J., Buch P., MacLaren R.E., Anderson P.N., Barker S.E., Duran Y., Bartholomae C., von Kalle C., Heckenlively J.R., Kinnon C., Ali R.R., Thrasher A.J. Effective gene therapy with nonintegrating lentiviral vectors. Nat. Med. 2006, 12:348-353.
157. Young S.M., McCarty D.M., Degtyareva N., Samulski R.J. Roles of adeno-associated virus Rep protein and human chromosome 19 in site-specific recombination. J. Virol. 2000, 74:3953-3966.
158. Zhu H., Dahlstrom A. Glial fibrillary acidic protein-expressing cells in the neurogenic regions in normal and injured adult brains. J. Neurosci. Res. 2007, 85:2783-2792.
159. Zhuo L., Theis M., Alvarez-Maya I., Brenner M., Willecke K., Messing A. hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis 2001, 31:85-94.
160. 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. Mol. Ther. 2008, 16:1073-1080.
161. Zufferey R., Dull T., Mandel R.J., Bukovsky A., Quiroz D., Naldini L., Trono D. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J. Virol. 1998, 72:9873-9880.