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BioMed Research International
Volume 2013 (2013), Article ID 974819, 8 pages
http://dx.doi.org/10.1155/2013/974819
Research Article

Systemic Delivery of Tyrosine-Mutant AAV Vectors Results in Robust Transduction of Neurons in Adult Mice

1Division of Neurology, Department of Medicine, Jichi Medical University, 3311-1 Yakushiji, Shimotsuke, Tochigi 329-0498, Japan
2Division of Neurosurgery, Jichi Medical University, 3311-1 Yakushiji, Shimotsuke, Tochigi 329-0498, Japan

Received 6 February 2013; Revised 19 April 2013; Accepted 21 April 2013

Academic Editor: Akhtar Jamal Khan

Copyright © 2013 Asako Iida et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. J. Bowers, X. O. Breakefield, and M. Sena-Esteves, “Genetic therapy for the nervous system,” Human Molecular Genetics, vol. 20, no. R1, pp. R28–R41, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. K. A. High and P. Aubourg, “rAAV human trial experience,” Methods in Molecular Biology, vol. 807, pp. 429–457, 2011.
  3. M. S. Weinberg, R. J. Samulski, and T. J. McCown, “Adeno-associated virus (AAV) gene therapy for neurological disease,” Neuropharmacology, vol. 69, pp. 82-–88, 2013. View at Publisher · View at Google Scholar
  4. P. Hadaczek, J. L. Eberling, P. Pivirotto, J. Bringas, J. Forsayeth, and K. S. Bankiewicz, “Eight years of clinical improvement in MPTP-lesioned primates after gene therapy with AAV2-hAADC,” Molecular Therapy, vol. 18, no. 8, pp. 1458–1461, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Muramatsu, K. Fujimoto, S. Kato et al., “A phase I study of aromatic L-amino acid decarboxylase gene therapy for parkinson's disease,” Molecular Therapy, vol. 18, no. 9, pp. 1731–1735, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. R. T. Bartus, T. L. Baumann, L. Brown, et al., “Advancing neurotrophic factors as treatments for age-related neurodegenerative diseases: developing and demonstrating, “clinical proof-of-concept” for AAV-neurturin (CERE-120) in Parkinson's disease,” Neurobiology of Aging, vol. 34, no. 1, pp. 35–61, 2012.
  7. C. W. Christine, P. A. Starr, P. S. Larson et al., “Safety and tolerability of putaminal AADC gene therapy for Parkinson disease,” Neurology, vol. 73, no. 20, pp. 1662–1669, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. P. A. LeWitt, A. R. Rezai, M. A. Leehey et al., “AAV2-GAD gene therapy for advanced Parkinson's disease: a double-blind, sham-surgery controlled, randomised trial,” The Lancet Neurology, vol. 10, no. 4, pp. 309–319, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. A. K. Bevan, S. Duque, K. D. Foust, et al., “Systemic gene delivery in large species for targeting spinal cord, brain, and peripheral tissues for pediatric disorders,” Molecular Therapy, vol. 19, no. 11, pp. 1971–1980, 2011. View at Publisher · View at Google Scholar
  10. S. Duque, B. Joussemet, C. Riviere et al., “Intravenous administration of self-complementary AAV9 enables transgene delivery to adult motor neurons,” Molecular Therapy, vol. 17, no. 7, pp. 1187–1196, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Federici, J. S. Taub, G. R. Baum, et al., “Robust spinal motor neuron transduction following intrathecal delivery of AAV9 in pigs,” Gene Therapy, vol. 19, no. 8, pp. 852–859, 2012. View at Publisher · View at Google Scholar
  12. K. D. Foust, E. Nurre, C. L. Montgomery, A. Hernandez, C. M. Chan, and B. K. Kaspar, “Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes,” Nature Biotechnology, vol. 27, no. 1, pp. 59–65, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. A. A. Rahim, A. M. Wong, K. Hoefer, et al., “Intravenous administration of AAV2/9 to the fetal and neonatal mouse leads to differential targeting of CNS cell types and extensive transduction of the nervous system,” The FASEB Journal, vol. 25, no. 10, pp. 3505–3518, 2011. View at Publisher · View at Google Scholar
  14. L. Samaranch, E. A. Salegio, W. San Sebastian, et al., “Adeno-associated virus serotype 9 transduction in the central nervous system of nonhuman primates,” Human Gene Therapy, vol. 23, no. 4, pp. 382–389, 2012. View at Publisher · View at Google Scholar
  15. J. J. Glascock, E. Y. Osman, M. J. Wetz, et al., “Decreasing disease severity in symptomatic, Smn(−/−);SMN2(+/+), spinal muscular atrophy mice following scAAV9-SMN delivery,” Human Gene Therapy, vol. 23, no. 3, pp. 330–335, 2012. View at Publisher · View at Google Scholar
  16. K. D. Foust, X. Wang, V. L. McGovern et al., “Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN,” Nature Biotechnology, vol. 28, no. 3, pp. 271–274, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. D. M. McCarty, “Self-complementary AAV vectors; advances and applications,” Molecular Therapy, vol. 16, no. 10, pp. 1648–1656, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. S. J. Gray, V. Matagne, L. Bachaboina, S. Yadav, S. R. Ojeda, and R. J. Samulski, “Preclinical differences of intravascular AAV9 delivery to neurons and glia: a comparative study of adult mice and nonhuman primates,” Molecular Therapy, vol. 19, no. 6, pp. 1058–1069, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Ciesielska, P. Hadaczek, G. Mittermeyer, et al., “Cerebral infusion of AAV9 vector-encoding non-self proteins can elicit cell-mediated immune responses,” Molecular Therapy, vol. 21, no. 1, pp. 158–166, 2012.
  20. A. Delzor, N. Dufour, F. Petit, et al., “Restricted transgene expression in the brain with cell-type specific neuronal promoters,” Human Gene Therapy Methods, vol. 23, no. 4, pp. 242–254, 2012.
  21. C. A. Ku, V. A. Chiodo, S. L. Boye, et al., “Gene therapy using self-complementary Y733F capsid mutant AAV2/8 restores vision in a model of early onset Leber congenital amaurosis,” Human Molecular Genetics, vol. 20, no. 23, pp. 4569–4581, 2011. View at Publisher · View at Google Scholar
  22. M. Li, G. R. Jayandharan, B. Li et al., “High-efficiency transduction of fibroblasts and mesenchymal stem cells by tyrosine-mutant AAV2 vectors for their potential use in cellular therapy,” Human Gene Therapy, vol. 21, no. 11, pp. 1527–1543, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Petrs-Silva, A. Dinculescu, Q. Li et al., “Novel properties of tyrosine-mutant AAV2 vectors in the mouse retina,” Molecular Therapy, vol. 19, no. 2, pp. 293–301, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Qiao, W. Zhang, Z. Yuan et al., “Adeno-associated virus serotype 6 capsid tyrosine-to-phenylalanine mutations improve gene transfer to skeletal muscle,” Human Gene Therapy, vol. 21, no. 10, pp. 1343–1348, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. B. Cheng, C. Ling, Y. Dai et al., “Development of optimized AAV3 serotype vectors: mechanism of high-efficiency transduction of human liver cancer cells,” Gene Therapy, vol. 19, no. 4, pp. 375–384, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. D. Dalkara, L. C. Byrne, T. Lee, et al., “Enhanced gene delivery to the neonatal retina through systemic administration of tyrosine-mutated AAV9,” Gene Therapy, vol. 19, no. 2, pp. 176–181, 2012. View at Publisher · View at Google Scholar
  27. Y. Zhang and D. Duan, “Novel mini-dystrophin gene dual adeno-associated virus vectors restore neuronal nitric oxide synthase expression at the sarcolemma,” Human Gene Therapy, vol. 23, no. 1, pp. 98–103, 2012. View at Publisher · View at Google Scholar
  28. T. Dittgen, A. Nimmerjahn, S. Komai et al., “Lentivirus-based genetic manipulations of cortical neurons and their optical and electrophysiological monitoring in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 52, pp. 18206–18211, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. O. Meyuhas and A. Klein, “The mouse ribosomal protein L7 gene. Its primary structure and functional analysis of the promoter region,” Journal of Biological Chemistry, vol. 265, no. 20, pp. 11465–11473, 1990. View at Scopus
  30. G. Gao, L. H. Vandenberghe, M. R. Alvira et al., “Clades of adeno-associated viruses are widely disseminated in human tissues,” Journal of Virology, vol. 78, no. 12, pp. 6381–6388, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. X. G. Li, T. Okada, M. Kodera et al., “Viral-mediated temporally controlled dopamine production in a rat model of Parkinson disease,” Molecular Therapy, vol. 13, no. 1, pp. 160–166, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. W. Wagner, S. McCroskery, and J. A. Hammer III, “An efficient method for the long-term and specific expression of exogenous cDNAs in cultured Purkinje neurons,” Journal of Neuroscience Methods, vol. 200, no. 2, pp. 95–105, 2011.
  33. H. Nakai, S. Fuess, T. A. Storm, S. I. Muramatsu, Y. Nara, and M. A. Kay, “Unrestricted hepatocyte transduction with adeno-associated virus serotype 8 vectors in mice,” Journal of Virology, vol. 79, no. 1, pp. 214–224, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Wang, C. Ling, L. Song, et al., “Limitations of encapsidation of recombinant self-complementary adeno-associated viral genomes in different serotype capsids and their quantitation,” Human Gene Therapy Methods, vol. 23, no. 4, pp. 225–233, 2012.
  35. H. Zhang, B. Yang, X. Mu et al., “Several rAAV vectors efficiently cross the blood-brain barrier and transduce neurons and astrocytes in the neonatal mouse central nervous system,” Molecular Therapy, vol. 19, no. 8, pp. 1440–1448, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Philips and W. Robberecht, “Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease,” The Lancet Neurology, vol. 10, no. 3, pp. 253–263, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. P. M. Rappold and K. Tieu, “Astrocytes and therapeutics for Parkinson's disease,” Neurotherapeutics, vol. 7, no. 4, pp. 413–423, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. E. D. Horowitz, M. G. Finn, and A. Asokan, “Tyrosine cross-linking reveals interfacial dynamics in adeno-associated viral capsids during infection,” ACS Chemical Biology, vol. 7, no. 6, pp. 1059–1066, 2012. View at Publisher · View at Google Scholar
  39. L. Zhong, B. Li, C. S. Mah et al., “Next generation of adeno-associated virus 2 vectors: point mutations in tyrosines lead to high-efficiency transduction at lower doses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 22, pp. 7827–7832, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Petrs-Silva, A. Dinculescu, Q. Li et al., “High-efficiency transduction of the mouse retina by tyrosine-mutant AAV serotype vectors,” Molecular Therapy, vol. 17, no. 3, pp. 463–471, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Miyazaki, H. Adachi, M. Katsuno, et al., “Viral delivery of miR-196a ameliorates the SBMA phenotype via the silencing of CELF2,” Nature Medicine, vol. 18, no. 7, pp. 1136–1141, 2012. View at Publisher · View at Google Scholar
  42. D. M. Markusic, R. W. Herzog, G. V. Aslanidi et al., “High-efficiency transduction and correction of murine hemophilia B using AAV2 vectors devoid of multiple surface-exposed tyrosines,” Molecular Therapy, vol. 18, no. 12, pp. 2048–2056, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Naumer, F. Sonntag, K. Schmidt, et al., “Properties of the adeno-associated virus assembly activating protein,” Journal of Virology, vol. 86, no. 23, pp. 13038–13048, 2012. View at Publisher · View at Google Scholar