Rapid transgene expression in multiple precursor cell types of adult rat subventricular zone mediated by adeno-associated type 1 vectors

Human Gene Therapy

Volumn 23, Issue 7, 2012, Pages 742-753

  Bockstael, Olivier ^a   Melas, Catherine ^a   Pythoud, Catherine ^b   Levivier, Marc ^a,b   McCarty, Douglas ^c   Jude Samulski, R ^c   De Witte, Olivier ^a,d   Tenenbaum, Liliane ^a,b  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d ERASME HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED TYPE 1 VECTOR; ADENOVIRUS VECTOR; DOUBLECORTIN; ENHANCED GREEN FLUORESCENT PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; TRANSCRIPTION FACTOR MASH1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SPECIFICITY; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HEMISPHERE; NEURAL STEM CELL; NONHUMAN; RAT; SUBVENTRICULAR ZONE; TRANSGENE;

ANIMALS; APOPTOSIS; BRAIN; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CEREBRAL VENTRICLES; DEPENDOVIRUS; FEMALE; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HOMEODOMAIN PROTEINS; HUMANS; NEURAL STEM CELLS; OLFACTORY BULB; RATS; RATS, WISTAR; RECOMBINANT PROTEINS; TRANSCRIPTION FACTORS; TRANSDUCTION, GENETIC; TRANSGENES;

ADENO-ASSOCIATED VIRUS - 2; MIRIDAE; RATTUS;

EID: 84864352807     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2011.216     Document Type: Article

References (58)

1. Afione, S.A., Conrad, C.K., Kearns, W.G., et al. (1996). In vivo model of adeno-associated virus vector persistence and rescue. J. Virol. 70, 3235-3241. (Pubitemid 26121942)
2. Alam, S., Sen, E., Brashear, H., and Meyers, C. (2006). Adenoassociated virus type 2 increases proteosome-dependent degradation of p21WAF1 in a human papillomavirus type 31b-positive cervical carcinoma line. J. Virol. 80, 4927-4939.
3. Alam, S., and Meyers, C. (2009). Adeno-associated virus type 2 induces apoptosis in human papillomavirus-infected cell lines but not in normal keratinocytes. J. Virol. 83, 10286-10292.
4. Alvarez-Buylla, A., and Garcia-Verdugo, J.M. (2002). Neurogenesis in adult subventricular zone. J. Neurosci. 22, 629-634. (Pubitemid 34141742)
5. Bantel-Schaal, U., and Stohr, M. (1992). Influence of adenoassociated virus on adherence and growth properties of normal cells. J. Virol. 66, 773-779.
6. Berthet, C., Raj, K., Saudan, P., and Beard, P. (2005). How adenoassociated virus Rep78 protein arrests cells completely in S phase. Proc. Natl. Acad. Sci. U.S.A. 102, 13634-13639. (Pubitemid 41420900)
7. Bockstael, O., Chtarto, A., Wakkinen, J., et al. (2008). Differential transgene expression profiles from rAAV2/1 vectors using the tetON and CMV promoters in the rat brain. Hum. Gene Ther. 19, 1293-1305.
8. Bockstael, O., Foust, K.D., Kaspar, B., and Tenenbaum, L. (2011). Recombinant AAV delivery to the central nervous system. Methods Mol. Biol. 807, 159-177.
9. Cataldi, M.P., and McCarty, D.M. (2010). Differential effects of DNA double-strand break repair pathways on single-strand and self-complementary adeno-associated virus vector genomes. J. Virol. 84, 8673-8682.
10. Chmielnicki, E., Benraiss, A., Economides, A.N., and Goldman, S.A. (2004). Adenovirally expressed noggin and brain-derived neurotrophic factor cooperate to induce new medium spiny neurons from resident progenitor cells in the adult striatal ventricular zone. J. Neurosci. 24, 2133-2142. (Pubitemid 38314545)
11. Cho, S.R., Benraiss, A., Chmielnicki, E., et al. (2007). Induction of neostriatal neurogenesis slows disease progression in a transgenic murine model of Huntington disease. J. Clin. Invest. 117, 2889-2902. (Pubitemid 47529619)
12. Consiglio, A., Gritti, A., Dolcetta, D., et al. (2004). Robust in vivo gene transfer into adult mammalian neural stem cells by lentiviral vectors. Proc. Natl. Acad. Sci. U.S.A. 101, 14835-14840. (Pubitemid 39410761)
13. Craig, C.G., D'sa, R., Morshead, C.M., et al. (1999). Migrational analysis of the constitutively proliferating subependyma population in adult mouse forebrain. Neuroscience 93, 1197-1206. (Pubitemid 29341667)
14. Doetsch, F., Caille, I., Lim, D.A., et al. (1999). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716. (Pubitemid 29278045)
15. Duan, D., Yue, Y., Yan, Z., et al. (2000). Endosomal processing limits gene transfer to polarized airway epithelia by adenoassociated virus. J. Clin. Invest. 105, 1573-1587. (Pubitemid 30390308)
16. Fallon, J., Reid, S., Kinyamu, R., et al. (2000). In vivo induction of massive proliferation, directed migration, and differentiation of neural cells in the adult mammalian brain. Proc. Natl. Acad. Sci. U.S.A. 97, 14686-14691. (Pubitemid 32016636)
17. Ferrari, F.K., Samulski, T., SheNK, T., and Samulski, R.J. (1996). Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors. J. Virol. 70, 3227-3234. (Pubitemid 26121941)
18. Fisher, K.J., Gao, G.P., Weitzman, M.D., et al. (1996). Transduction with recombinant adeno-associated virus for gene therapy is limited by leading-strand synthesis. J. Virol. 70, 520-532. (Pubitemid 126508820)
19. Fragkos, M., Breuleux, M., Clement, N., and Beard, P. (2008). Recombinant adeno-associated viral vectors are deficient in provoking a DNA damage response. J. Virol. 82, 7379-7387. (Pubitemid 352031206)
20. Garcia, A.D., Doan, N.B., Imura, T., et al. (2004). GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat. Neurosci. 7, 1233-1241. (Pubitemid 39426243)
21. Geraerts, M., Eggermont, K., Hernandez-Acosta, P., et al. (2006). Lentiviral vectors mediate efficient and stable gene transfer in adult neural stem cells in vivo. Hum. Gene Ther. 17, 635-650. (Pubitemid 43967867)
22. Goldman, S.A., Lemmon, V., and Chin, S.S. (1993). Migration of newly generated neurons upon ependymally derived radial guide cells in explant cultures of the adult songbird forebrain. Glia 8, 150-160.
23. Grimm, D., Kay, M.A., and Kleinschmidt, J.A. (2003). Helper virus-free, optically controllable, and two-plasmid-based production of adeno-associated virus vectors of serotypes 1 to 6. Mol. Ther. 7, 839-850. (Pubitemid 36790261)
24. Hack, M.A., Saghatelyan, A., de Chevigny, A., et al. (2005). Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat. Neurosci. 8, 865-872.
25. Halbert, C.L., Alexander, I.E., Wolgamot, G.M., and Miller, A.D. (1995). Adeno-associated virus vectors transduce primary cells much less efficiently than immortalized cells. J. Virol. 69, 1473-1479.
26. Henry, R.A., Hughes, S.M., and Connor, B. (2007). AAV-mediated delivery of BDNF augments neurogenesis in the normal and quinolinic acid-lesioned adult rat brain. Eur. J. Neurosci. 25, 3513-3525. (Pubitemid 47020463)
27. Hermanns, J., Schulze, A., Jansen, D., et al. (1997). Infection of primary cells by adeno-associated virus type 2 results in a modulation of cell cycle-regulating proteins. J. Virol. 71, 6020-6027. (Pubitemid 27304940)
28. Hirsch, M.L., Fagan, B.M., Dumitru, R., et al. (2011). Viral singlestrand DNA induces p53-dependent apoptosis in human embryonic stem cells. PLoS One 6, e27520.
29. Hughes, S.M., Moussavi-Harami, F., Sauter, S.L., and Davidson, B.L. (2002). Viral-mediated gene transfer to mouse primary neural progenitor cells. Mol. Ther. 5, 16-24. (Pubitemid 34110476)
30. International Society for BioProcess Technology. (2011). Protocols and test records for AAV2 Reference Material: AAV2-RSS genome copy titration QPCR. Available at www.isbiotech .org/ReferenceMaterials/pdfs/AAV2-RSS genome copy titration QPCR.pdf (accessed April 12, 2012).
31. Jones, K.S., and Connor, B. (2011). Proneural transcription factors Dlx2 and Pax6 are altered in adult SVZ neural precursor cells following striatal cell loss. Mol. Cell. Neurosci. 47, 53-60.
32. Jurvansuu, J., Raj, K., Stasiak, A., and Beard, P. (2005). Viral transport of DNA damage that mimics a stalled replication fork. J. Virol. 79, 569-580. (Pubitemid 39648409)
33. Kim, E.J., Leung, C.T., Reed, R.R., and Johnson, J.E. (2007). In vivo analysis of Ascl1 defined progenitors reveals distinct developmental dynamics during adult neurogenesis and gliogenesis. J. Neurosci. 27, 12764-12774. (Pubitemid 350159578)
34. Kim, E.J., Ables, J.L., Dickel, L.K., et al. (2011). Ascl1 (Mash1) defines cells with long-term neurogenic potential in subgranular and subventricular zones in adult mouse brain. PLoS One 6, e18472.
35. Kosaka, K., Aika, Y., Toida, K., et al. (1995). Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb. Neurosci. Res. 23, 73-88.
36. Kube, D.M., Ponnazhagan, S., and Srivastava, A. (1997). Encapsidation of adeno-associated virus type 2 Rep proteins in wild-type and recombinant progeny virions: Rep-mediated growth inhibition of primary human cells. J. Virol. 71, 7361-7371. (Pubitemid 27391675)
37. Lock, M., McGorray, S., Auricchio, A., et al. (2010). Characterization of a recombinant adeno-associated virus type 2 Reference Standard Material. Hum. Gene Ther. 21, 1273-1285.
38. Malik, A.K., Monahan, P.E., Allen, D.L., et al. (2000). Kinetics of recombinant adeno-associated virus-mediated gene transfer. J. Virol. 74, 3555-3565. (Pubitemid 30180298)
39. McCarty, D.M. (2008). Self-complementary AAV vectors: Advances and applications. Mol. Ther. 16, 1648-1656.
40. McCarty, D.M., Monhan, P.E., and Samulski, R.J. (2001). Selfcomplementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther. 8, 1248-1254. (Pubitemid 32780813)
41. McCarty, D.M., Fu, H., Monahan, P.E., et al. (2003). Adenoassociated virus terminal repeat (TR) mutant generates selfcomplementary vectors to overcome the rate-limiting step to transduction in vivo. Gene Ther. 10, 2112-2118. (Pubitemid 37536760)
42. McCown, T.J. (2005). Adeno-associated virus (AAV) vectors in the CNS. Curr. Gene Ther. 5, 333-338. (Pubitemid 40895017)
43. Ng, R., Govindasamy, L., Gurda, B.L., et al. (2010). Structural characterization of the dual glycan binding adeno-associated virus serotype 6. J. Virol. 84, 12945-12957.
44. Parrish-Aungst, S., Shipley, M.T., Erdelyi, F., et al. (2007). Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J. Comp. Neurol. 501, 825-836. (Pubitemid 46797133)
45. Passini, M.A., Watson, D.J., Vite, C.H., et al. (2003). Intraventricular brain injection of adeno-associated virus type 1 (AAV1) in neonatal mice results in complementary patterns of neuronal transduction to AAV2 and total long-term correction of storage lesions in the brains of b-glucuronidase-deficient mice. J. Virol. 77, 7034-7040. (Pubitemid 36666896)
46. Paxinos G., and Watson C. (1986). The Rat Brain in Stereotaxic Coordinates (San Diego, CA, Academic Press).
47. Reimsnider, S., Manfredsson, F.P., Muzyczka, N., and Mandel, R.J. (2007). Time course of transgene expression after intrastriatal pseudotyped rAAV2/1, rAAV2/2, rAAV2/5, and rAAV2/8 transduction in the rat. Mol. Ther. 15, 1504-1511. (Pubitemid 47103062)
48. Ricard, J., Salinas, J., Garcia, L., and Liebl, D.J. (2006). EphrinB3 regulates cell proliferation and survival in adult neurogenesis. Mol. Cell. Neurosci. 31, 713-722.
49. Schnepp, B.C., Clark, K.R., Klemanski, D.L., et al. (2003). Genetic fate of recombinant adeno-associated virus vector genomes in muscle. J. Virol. 77, 3495-3504. (Pubitemid 36297269)
50. Schnepp, B.C., Jensen, R.L., Chen, C.L., et al. (2005). Characterization of adeno-associated virus genomes isolated from human tissues. J. Virol. 79, 14793-14803. (Pubitemid 41636277)
51. Smith, C.M., and Luskin, M.B. (1998). Cell cycle length of olfactory bulb neuronal progenitors in the rostral migratory stream. Dev. Dyn. 213, 220-227. (Pubitemid 28457773)
52. Tenenbaum, L., Hamdane, M., Pouzet, M., et al. (1999). Cellular contaminants of adeno-associated virus vector stocks can enhance transduction. Gene Ther. 6, 1045-1053. (Pubitemid 29295210)
53. Thomas, C.E., Storm, T.A., Huang, Z., and Kay, M.A. (2004). Rapid uncoating of vector genomes is the key to efficient liver transduction with pseudotyped adeno-associated virus vectors. J. Virol. 78, 3110-3122. (Pubitemid 38314369)
54. Wang, C., Wang, C.M., Clark, K.R., and Sferra, T.J. (2003). Recombinant AAV serotype 1 transduction efficiency and tropism in the murine brain. Gene Ther. 10, 1528-1534. (Pubitemid 36987147)
55. Winocour, E., Callaham, M.F., and Huberman, E. (1988). Perturbation of the cell cycle by adeno-associated virus. Virology 167, 393-399. (Pubitemid 19037133)
56. Wu, P., Ye, Y., and Svendsen, C.N. (2002). Transduction of human neural progenitor cells using recombinant adenoassociated viral vectors. Gene Ther. 9, 245-255. (Pubitemid 34256899)
57. Yanez-Munoz, R.J., Balaggan, K.S., MacNeil, A., et al. (2006). Effective gene therapy with nonintegrating lentiviral vectors. Nat. Med. 12, 348-353. (Pubitemid 43355085)
58. Zolotukhin, S., Byrne, B.J., Mason, E., et al. (1999). Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene Ther. 6, 973-985. (Pubitemid 29295202)