Enhanced selective gene delivery to neural stem cells in vivo by an adeno-associated viral variant

Development (Cambridge)

Volumn 142, Issue 10, 2015, Pages 1885-1892

  Kotterman, Melissa A ^a,b,c,d   Vazin, Tandis ^a,b,d   Schaffer, David V ^a,b,c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California at Berkeley   (United States)

^c 4D Molecular Therapeutics   (United States)

^d Berkeley   (United States)

Author keywords

Adeno associated virus; Gene delivery; Neural stem cell

Indexed keywords

ADENO ASSOCIATED VIRUS R3.45 VECTOR; BETA CATENIN; PARVOVIRUS VECTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; EMBRYO; FEMALE; GENETIC REGULATION; HIPPOCAMPUS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO GENE TRANSFER; IN VIVO STUDY; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SEROTYPE; VIRAL GENE DELIVERY SYSTEM; ANIMAL; CELL LINE; CYTOLOGY; DEPENDOPARVOVIRUS; GENE TRANSFER; GENETICS; METABOLISM; MOUSE;

ADENO-ASSOCIATED VIRUS; RATTUS;

ANIMALS; BETA CATENIN; CELL LINE; DEPENDOVIRUS; GENE TRANSFER TECHNIQUES; HUMANS; MICE; NEURAL STEM CELLS; RATS;

EID: 84929152734     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.115253     Document Type: Article

References (60)

1. Ashton, R. S., Conway, A., Pangarkar, C., Bergen, J., Lim, K.-I., Shah, P., Bissell, M. and Schaffer, D. V. (2012). Astrocytes regulate adult hippocampal neurogenesis through ephrin-B signaling. Nat. Neurosci. 15, 1399-1406
2. Asuri, P., Bartel, M. A., Vazin, T., Jang, J.-H., Wong, T. B. and Schaffer, D. V. (2012). Directed evolution of adeno-associated virus for enhanced gene delivery and gene targeting in human pluripotent stem cells. Mol. Ther. 20, 329-338
3. Bainbridge, J. W. B., Smith, A. J., Barker, S. S., Robbie, S., Henderson, R., Balaggan, K., Viswanathan, A., Holder, G. E., Stockman, A., Tyler, N. et al. (2008). Effect of gene therapy on visual function in Leber’s congenital amaurosis. N. Engl. J. Med. 358, 2231-2239
4. Bartlett, J. S., Samulski, R. J. and McCown, T. J. (1998). Selective and rapid uptake of adeno-associated virus type 2 in brain. Hum. Gene Ther. 9, 1181-1186
5. Blesch, A., Lu, P. and Tuszynski, M. H. (2002). Neurotrophic factors, gene therapy, and neural stem cells for spinal cord repair. Brain Res. Bull. 57, 833-838
6. Bonaguidi, M. A., Wheeler, M. A., Shapiro, J. S., Stadel, R. P., Sun, G. J., Ming, G.-l. and Song, H. (2011). In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 145, 1142-1155
7. Bowman, A. N., van Amerongen, R., Palmer, T. D. and Nusse, R. (2013). Lineage tracing with Axin2 reveals distinct developmental and adult populations of Wnt/β-catenin-responsive neural stem cells. Proc. Natl. Acad. Sci. USA 110, 7324-7329
8. Brown, B. D. and Naldini, L. (2009). Exploiting and antagonizing microRNA regulation for therapeutic and experimental applications. Nat. Rev. Genet. 10, 578-585
9. Chen, B.-Y., Wang, X., Wang, Z.-Y., Wang, Y.-Z., Chen, L.-W. and Luo, Z.-J. (2013). Brain-derived neurotrophic factor stimulates proliferation and differentiation of neural stem cells, possibly by triggering the Wnt/β-catenin signaling pathway. J. Neurosci. Res. 91, 30-41
10. Deng,W., Aimone, J. B. and Gage, F. H. (2010). New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat. Rev. Neurosci. 11, 339-350
11. Duan, X., Kang, E., Liu, C. Y., Ming, G.-l. and Song, H. (2008). Development of neural stem cell in the adult brain. Curr. Opin. Neurobiol. 18, 108-115
12. Ernst, A., Alkass, K., Bernard, S., Salehpour, M., Perl, S., Tisdale, J., Possnert, G., Druid, H. and Frisén, J. (2014). Neurogenesis in the striatum of the adult human brain. Cell 156, 1072-1083
13. Excoffon, K. J. D. A., Koerber, J. T., Dickey, D. D., Murtha, M., Keshavjee, S., Kaspar, B. K., Zabner, J. and Schaffer, D. V. (2009). Directed evolution of adeno-associated virus to an infectious respiratory virus. Proc. Natl. Acad. Sci. USA 106, 3865-3870
14. Faigle, R. and Song, H. (2013). Signaling mechanisms regulating adult neural stem cells and neurogenesis. Biochim. Biophys. Acta 1830, 2435-2448
15. Falk, A., Holmström, N., Carlén, M., Cassidy, R., Lundberg, C. and Frisén, J. (2002). Gene delivery to adult neural stem cells. Exp. Cell Res. 279, 34-39
16. Flotte, T. R. (2004). Gene therapy progress and prospects: recombinant adenoassociated virus (rAAV) vectors. Gene Ther. 11, 805-810
17. Gage, F. H. (2000). Mammalian neural stem cells. Science 287, 1433-1438
18. Guo, W., Allan, A. M., Zong, R., Zhang, L., Johnson, E. B., Schaller, E. G., Murthy, A. C., Goggin, S. L., Eisch, A. J., Oostra, B. A. et al. (2011). Ablation of Fmrp in adult neural stem cells disrupts hippocampus-dependent learning. Nat. Med. 17, 559-565
19. Haruyama, N., Cho, A. and Kulkarni, A. B. (2009). Overview: engineering transgenic constructs and mice. Curr. Protoc. Cell Biol. Chapter 19, Unit 19.10
20. Hashimoto, M. and Mikoshiba, K. (2004). Neuronal birthdate-specific gene transfer with adenoviral vectors. J. Neurosci. 24, 286-296
21. Israsena, N., Hu, M., Fu, W., Kan, L. and Kessler, J. A. (2004). The presence of FGF2 signaling determines whether beta-catenin exerts effects on proliferation or neuronal differentiation of neural stem cells. Dev. Biol. 268, 220-231
22. Jang, J.-H., Koerber, J. T., Kim, J.-S., Asuri, P., Vazin, T., Bartel, M., Keung, A., Kwon, I., Park, K. I. and Schaffer, D. V. (2011). An evolved adeno-associated viral variant enhances gene delivery and gene targeting in neural stem cells. Mol. Ther. 19, 667-675
23. Jaski, B. E., Jessup, M. L., Mancini, D. M., Cappola, T. P., Pauly, D. F., Greenberg, B., Borow, K., Dittrich, H., Zsebo, K. M. and Hajjar, R. J. (2009). Calcium upregulation by percutaneous administration of gene therapy in cardiac disease (CUPID Trial), a first-in-human phase 1/2 clinical trial. J. Card. Fail. 15, 171-181
24. Jessberger, S., Toni, N., Clemenson, G. D., Jr, Ray, J. and Gage, F. H. (2008). Directed differentiation of hippocampal stem/progenitor cells in the adult brain. Nat. Neurosci. 11, 888-893
25. Kaspar, B. K., Vissel, B., Bengoechea, T., Crone, S., Randolph-Moore, L., Muller, R., Brandon, E. P., Schaffer, D., Verma, I. M., Lee, K.-F. et al. (2002). Adeno-associated virus effectively mediates conditional gene modification in the brain. Proc. Natl. Acad. Sci. USA 99, 2320-2325
26. Kim, W. R., Christian, K., Ming, G.-L. and Song, H. (2012a). Time-dependent involvement of adult-born dentate granule cells in behavior. Behav. Brain Res. 227, 470-479
27. Kim, J.-S., Chu, H. S., Park, K. I., Won, J.-I. and Jang, J.-H. (2012b). Elastin-like polypeptide matrices for enhancing adeno-associated virus-mediated gene delivery to human neural stem cells. Gene Ther. 19, 329-337
28. Klimczak, R. R., Koerber, J. T., Dalkara, D., Flannery, J. G. and Schaffer, D. V. (2009). A novel adeno-associated viral variant for efficient and selective intravitreal transduction of rat Müller cells. PLoS ONE 4, e7467
29. Knipe, D. M. and Howley, P.M. (2007). Fields’ Virology. Philadelphia, PA, USA: Lippincott Williams & Wilkins.
30. Koerber, J. T., Jang, J.-H. and Schaffer, D. V. (2008). DNA shuffling of adenoassociated virus yields functionally diverse viral progeny. Mol. Ther. 16, 1703-1709
31. Koerber, J. T., Klimczak, R., Jang, J.-H., Dalkara, D., Flannery, J. G. and Schaffer, D. V. (2009). Molecular evolution of adeno-associated virus for enhanced glial gene delivery. Mol. Ther. 17, 2088-2095
32. Kotterman, M. A. and Schaffer, D. V. (2014). Engineering adeno-associated viruses for clinical gene therapy. Nat. Rev. Genet. 15, 445-451
33. Lagace, D. C., Whitman, M. C., Noonan, M. A., Ables, J. L., DeCarolis, N. A., Arguello, A. A., Donovan, M. H., Fischer, S. J., Farnbauch, L. A., Beech, R. D. et al. (2007). Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J. Neurosci. 27, 12623-12629
34. Lai, K., Kaspar, B. K., Gage, F. H. and Schaffer, D. V. (2002). Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat. Neurosci. 6, 21-27
35. Lemkine, G. F., Mantero, S., Migné, C., Raji, A., Goula, D., Normandie, P., Levi, G. and Demeneix, B. A. (2002). Preferential transfection of adult mouse neural stem cells and their immediate progeny in vivo with polyethylenimine. Mol. Cell. Neurosci. 19, 165-174
36. Lie, D.-C., Colamarino, S. A., Song, H.-J., Désiré, L., Mira, H., Consiglio, A., Lein, E. S., Jessberger, S., Lansford, H., Dearie, A. R. et al. (2005). Wnt signalling regulates adult hippocampal neurogenesis. Nature 437, 1370-1375
37. Logan, C. Y. and Nusse, R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810
38. Lugert, S., Basak, O., Knuckles, P., Haussler, U., Fabel, K., Götz, M., Haas, C. A., Kempermann, G., Taylor, V. and Giachino, C. (2010). Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell 6, 445-456
39. MacLaren, R. E., Groppe, M., Barnard, A. R., Cottriall, C. L., Tolmachova, T., Seymour, L., Clark, K. R., During, M. J., Cremers, F. P. M., Black, G. C. M. et al. (2014). Retinal gene therapy in patients with choroideremia: initial findings from a phase 1/2 clinical trial. Lancet 6736, 2117-2120
40. Maguire, A. M., Simonelli, F., Pierce, E. A., Pugh, E. N., Jr, Mingozzi, F., Bennicelli, J., Banfi, S., Marshall, K. A., Testa, F., Surace, E. M. et al. (2008). Safety and efficacy of gene transfer for Leber’s congenital amaurosis. N. Engl. J. Med. 358, 2240-2248
41. Maguire, A. M., High, K. A., Auricchio, A., Wright, J. F., Pierce, E. A., Testa, F., Mingozzi, F., Bennicelli, J. L., Ying, G.-S., Rossi, S. et al. (2009). Agedependent effects of RPE65 gene therapy for Leber’s congenital amaurosis: a phase 1 dose-escalation trial. Lancet 374, 1597-1605
42. Maheshri, N., Koerber, J. T., Kaspar, B. K. and Schaffer, D. V. (2006). Directed evolution of adeno-associated virus yields enhanced gene delivery vectors. Nat. Biotechnol. 24, 198-204
43. Manno, C. S., Chew, A. J., Hutchison, S., Larson, P. J., Herzog, R. W., Arruda, V. R., Tai, S. J., Ragni, M. V., Thompson, A., Ozelo, M. et al. (2003). AAVmediated factor IX gene transfer to skeletal muscle in patients with severe hemophilia B. Blood 101, 2963-2972
44. Manno, C. S., Pierce, G. F., Arruda, V. R., Glader, B., Ragni, M., Rasko, J. J. E., Ozelo, M. C., Hoots, K., Blatt, P., Konkle, B. et al. (2006). Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat. Med. 12, 342-347
45. Ming, G.-l. and Song, H. (2011). Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70, 687-702
46. Mira, H., Andreu, Z., Suh, H., Lie, D. C., Jessberger, S., Consiglio, A., San Emeterio, J., Hortigüela, R., Marqués-Torrejón, M. Á., Nakashima, K. et al. (2010). Signaling through BMPR-IA regulates quiescence and long-term activity of neural stem cells in the adult hippocampus. Cell Stem Cell 7, 78-89
47. Moss, R. B., Milla, C., Colombo, J., Accurso, F., Zeitlin, P. L., Clancy, J. P., Spencer, L. T., Pilewski, J., Waltz, D. A., Dorkin, H. L. et al. (2007). Repeated aerosolized AAV-CFTR for treatment of cystic fibrosis: a randomized placebocontrolled phase 2B trial. Hum. Gene Ther. 18, 726-732
48. Nathwani, A. C., Tuddenham, E. G. D., Rangarajan, S., Rosales, C., McIntosh, J., Linch, D. C., Chowdary, P., Riddell, A., Pie, A. J., Harrington, C. et al. (2011). Adenovirus-associated virus vector–mediated gene transfer in Hemophilia B. N. Engl. J. Med. 365, 2357-2365
49. Oh, S.W., Harris, J. A., Ng, L., Winslow, B., Cain, N., Mihalas, S., Wang, Q., Lau, C., Kuan, L., Henry, A. M. et al. (2014). A mesoscale connectome of the mouse brain. Nature 508, 207-214
50. Ojala, D. S., Amara, D. P. and Schaffer, D. V. (2015). Adeno-associated virus vectors and neurological gene therapy. Neuroscientist 21, 84-98
51. Ortinski, P. I., Dong, J., Mungenast, A., Yue, C., Takano, H., Watson, D. J., Haydon, P. G. and Coulter, D. A. (2010). Selective induction of astrocytic gliosis generates deficits in neuronal inhibition. Nat. Neurosci. 13, 584-591
52. Otero, J. J., Fu, W., Kan, L., Cuadra, A. E. and Kessler, J. A. (2004). Beta-catenin signaling is required for neural differentiation of embryonic stem cells. Development 131, 3545-3557
53. Qu, Q., Sun, G., Li, W., Yang, S., Ye, P., Zhao, C., Yu, R. T., Gage, F. H., Evans, R. M. and Shi, Y. (2010). Orphan nuclear receptor TLX activates Wnt/betacatenin signalling to stimulate neural stem cell proliferation and self-renewal. Nat. Cell Biol. 12, 31-40
54. Schaffer, D. V., Koerber, J. T. and Lim, K.-l. (2008). Molecular engineering of viral gene delivery vehicles. Annu. Rev. Biomed. Eng. 10, 169-194
55. Suh, H., Deng, W. and Gage, F. H. (2009). Signaling in adult neurogenesis. Annu. Rev. Cell Dev. Biol. 25, 253-275
56. Temple, S. (2001). The development of neural stem cells. Nature 414, 112-117.
57. van Hooijdonk, L.W. A., Ichwan, M., Dijkmans, T. F., Schouten, T. G., de Backer, M.W. A., Adan, R. A. H., Verbeek, F. J., Vreugdenhil, E. and Fitzsimons, C. P. (2009). Lentivirus-mediated transgene delivery to the hippocampus reveals subfield specific differences in expression. BMC Neurosci. 10, 2
58. Wagner, J. A., Nepomuceno, I. B., Messner, A. H., Moran, M. L., Batson, E. P., Dimiceli, S., Brown, B. W., Desch, J. K., Norbash, A. M., Conrad, C. K. et al. (2002). A phase II, double-blind, randomized, placebo-controlled clinical trial of tgAAVCF using maxillary sinus delivery in patients with cystic fibrosis with antrostomies. Hum. Gene Ther. 13, 1349-1359
59. Wu, Z., Asokan, A. and Samulski, R. J. (2006). Adeno-associated virus serotypes: vector toolkit for human gene therapy. Mol. Ther. 14, 316-327
60. Zincarelli, C., Soltys, S., Rengo, G. and Rabinowitz, J. E. (2008). Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol. Ther. 16, 1073-1080.