Microglia-specific targeting by novel capsid-modified AAV6 vectors

Molecular Therapy Methods and Clinical Development

Volumn 3, Issue , 2016, Pages 16026-

  Rosario, Awilda M ^a   Cruz, Pedro E ^a   Ceballos Diaz, Carolina ^a   Strickland, Michael R ^a   Siemienski, Zoe ^a   Pardo, Meghan ^a   Schob, Keri Lyn ^a   Li, Andrew ^a   Aslanidi, George V ^a   Srivastava, Arun ^a   Golde, Todd E ^a   Chakrabarty, Paramita ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; CD68 ANTIGEN; ENHANCED GREEN FLUORESCENT PROTEIN; INTERLEUKIN 6; BETA ACTIN; CALCIUM ION; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEIN; IONIZED CALCIUM BINDING ADAPTER MOLECULE 1; MICROTUBULE ASSOCIATED PROTEIN 2; PROTEASOME; SERINE; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTOSIS; CONTROLLED STUDY; GENE EXPRESSION; GENE TARGETING; IN VITRO GENE TRANSFER; MICROGLIA; MICROGLIAL CELL CULTURE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; VIRAL GENE DELIVERY SYSTEM; VIRAL TROPISM; VIRUS CAPSID; VIRUS GENOME; VIRUS MUTANT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BRAIN FUNCTION; FEMALE; GENE EXPRESSION PROFILING; GENOME ANALYSIS; IN VITRO STUDY; INNATE IMMUNITY; NERVOUS SYSTEM INFLAMMATION; NEUROMODULATION; PROTEIN EXPRESSION; SEROTYPE; TROPISM;

EID: 85015199667     PISSN: None     EISSN: 23290501     Source Type: Journal    
DOI: 10.1038/mtm.2016.26     Document Type: Article

References (43)

1. 1 Lentz, TB, Gray, SJ, Samulski, RJ, Viral vectors for gene delivery to the central nervous system. Neurobiol Dis 48 (2012), 179–188.
2. 2 Murlidharan, G, Samulski, RJ, Asokan, A, Biology of adeno-associated viral vectors in the central nervous system. Front Mol Neurosci, 7, 2014, 76.
3. 3 Grimm, D, Zolotukhin, S, E pluribus unum: 50 years of research, millions of viruses, and one goal-tailored acceleration of AAV evolution. Mol Ther 23 (2015), 1819–1831.
4. 4 Chakrabarty, P, Rosario, A, Cruz, P, Siemienski, Z, Ceballos-Diaz, C, Crosby, K, et al. Capsid serotype and timing of injection determines AAV transduction in the neonatal mice brain. PLoS One, 8, 2013, e67680.
5. 5 Ayers, JI, Fromholt, S, Sinyavskaya, O, Siemienski, Z, Rosario, AM, Li, A, et al. Widespread and efficient transduction of spinal cord and brain following neonatal AAV injection and potential disease modifying effect in ALS mice. Mol Ther 23 (2015), 53–62.
6. 6 Kantor, B, McCown, T, Leone, P, Gray, SJ, Clinical applications involving CNS gene transfer. Adv Genet 87 (2014), 71–124.
7. 7 Weinberg, MS, Samulski, RJ, McCown, TJ, Adeno-associated virus (AAV) gene therapy for neurological disease. Neuropharmacology 69 (2013), 82–88.
8. 8 Prinz, M, Priller, J, Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat Rev Neurosci 15 (2014), 300–312.
9. 9 Pandya, J, Ortiz, L, Ling, C, Rivers, AE, Aslanidi, G, Rationally designed capsid and transgene cassette of AAV6 vectors for dendritic cell-based cancer immunotherapy. Immunol Cell Biol 92 (2014), 116–123.
10. 10 Aslanidi, GV, Rivers, AE, Ortiz, L, Govindasamy, L, Ling, C, Jayandharan, GR, et al. High-efficiency transduction of human monocyte-derived dendritic cells by capsid-modified recombinant AAV2 vectors. Vaccine 30 (2012), 3908–3917.
11. 11 Zhong, L, Li, B, Jayandharan, G, Mah, CS, Govindasamy, L, Agbandje-McKenna, M, et al. Tyrosine-phosphorylation of AAV2 vectors and its consequences on viral intracellular trafficking and transgene expression. Virology 381 (2008), 194–202.
12. 12 Zhong, L, Zhou, X, Li, Y, Qing, K, Xiao, X, Samulski, RJ, et al. Single-polarity recombinant adeno-associated virus 2 vector-mediated transgene expression in vitro and in vivo: mechanism of transduction. Mol Ther 16 (2008), 290–295.
13. 13 McCarty, DM, Self-complementary AAV vectors; advances and applications. Mol Ther 16 (2008), 1648–1656.
14. 14 Chan, WY, Kohsaka, S, Rezaie, P, The origin and cell lineage of microglia: new concepts. Brain Res Rev 53 (2007), 344–354.
15. 15 Kettenmann, H, Hanisch, UK, Noda, M, Verkhratsky, A, Physiology of microglia. Physiol Rev 91 (2011), 461–553.
16. 16 Kishimoto, T, IL-6: from its discovery to clinical applications. Int Immunol 22 (2010), 347–352.
17. 17 Clarke, S, Gordon, S, Myeloid-specific gene expression. J Leukoc Biol 63 (1998), 153–168.
18. 18 Chakrabarty, P, Jansen-West, K, Beccard, A, Ceballos-Diaz, C, Levites, Y, Verbeeck, C, et al. Massive gliosis induced by interleukin-6 suppresses Abeta deposition in vivo: evidence against inflammation as a driving force for amyloid deposition. FASEB J 24 (2010), 548–559.
19. 19 Asokan, A, Schaffer, DV, Samulski, RJ, The AAV vector toolkit: poised at the clinical crossroads. Mol Ther 20 (2012), 699–708.
20. 20 Cucchiarini, M, Ren, XL, Perides, G, Terwilliger, EF, Selective gene expression in brain microglia mediated via adeno-associated virus type 2 and type 5 vectors. Gene Ther 10 (2003), 657–667.
21. 21 Bartlett, JS, Samulski, RJ, McCown, TJ, Selective and rapid uptake of adeno-associated virus type 2 in brain. Hum Gene Ther 9 (1998), 1181–1186.
22. 22 Pfrieger, FW, Slezak, M, Genetic approaches to study glial cells in the rodent brain. Glia 60 (2012), 681–701.
23. 23 Balcaitis, S, Weinstein, JR, Li, S, Chamberlain, JS, Möller, T, Lentiviral transduction of microglial cells. Glia 50 (2005), 48–55.
24. 24 Hacein-Bey-Abina, S, Garrigue, A, Wang, GP, Soulier, J, Lim, A, Morillon, E, et al. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J Clin Invest 118 (2008), 3132–3142.
25. 25 Martino, AT, Basner-Tschakarjan, E, Markusic, DM, Finn, JD, Hinderer, C, Zhou, S, et al. Engineered AAV vector minimizes in vivo targeting of transduced hepatocytes by capsid-specific CD8+ T cells. Blood 121 (2013), 2224–2233.
26. 26 Jayandharan, GR, Aslanidi, G, Martino, AT, Jahn, SC, Perrin, GQ, Herzog, RW, et al. Activation of the NF-kappaB pathway by adeno-associated virus (AAV) vectors and its implications in immune response and gene therapy. Proc Natl Acad Sci USA 108 (2011), 3743–3748.
27. 27 Aslanidi, GV, Rivers, AE, Ortiz, L, Song, L, Ling, C, Govindasamy, L, et al. Optimization of the capsid of recombinant adeno-associated virus 2 (AAV2) vectors: the final threshold?. PLoS One, 8, 2013, e59142.
28. 28 Markusic, DM, Hoffman, BE, Perrin, GQ, Nayak, S, Wang, X, LoDuca, PA, et al. Effective gene therapy for haemophilic mice with pathogenic factor IX antibodies. EMBO Mol Med 5 (2013), 1698–1709.
29. 29 Martino, AT, Nayak, S, Hoffman, BE, Cooper, M, Liao, G, Markusic, DM, et al. Tolerance induction to cytoplasmic beta-galactosidase by hepatic AAV gene transfer: implications for antigen presentation and immunotoxicity. PLoS One, 4, 2009, e6376.
30. 30 LoDuca, PA, Hoffman, BE, Herzog, RW, Hepatic gene transfer as a means of tolerance induction to transgene products. Curr Gene Ther 9 (2009), 104–114.
31. 31 Zhong, L, Li, B, Mah, CS, Govindasamy, L, Agbandje-McKenna, M, Cooper, M, et al. Next generation of adeno-associated virus 2 vectors: point mutations in tyrosines lead to high-efficiency transduction at lower doses. Proc Natl Acad Sci USA 105 (2008), 7827–7832.
32. 32 Horowitz, ED, Finn, MG, Asokan, A, Tyrosine cross-linking reveals interfacial dynamics in adeno-associated viral capsids during infection. ACS Chem Biol 7 (2012), 1059–1066.
33. 33 Markusic, DM, Herzog, RW, Aslanidi, GV, Hoffman, BE, Li, B, Li, M, et al. High-efficiency transduction and correction of murine hemophilia B using AAV2 vectors devoid of multiple surface-exposed tyrosines. Mol Ther 18 (2010), 2048–2056.
34. 34 Li, M, Jayandharan, GR, Li, B, Ling, C, Ma, W, Srivastava, A, et al. High-efficiency transduction of fibroblasts and mesenchymal stem cells by tyrosine-mutant AAV2 vectors for their potential use in cellular therapy. Hum Gene Ther 21 (2010), 1527–1543.
35. 35 Tydlacka, S, Wang, CE, Wang, X, Li, S, Li, XJ, Differential activities of the ubiquitin-proteasome system in neurons versus glia may account for the preferential accumulation of misfolded proteins in neurons. J Neurosci 28 (2008), 13285–13295.
36. 36 Gray, SJ, Matagne, V, Bachaboina, L, Yadav, S, Ojeda, SR, Samulski, RJ, Preclinical differences of intravascular AAV9 delivery to neurons and glia: a comparative study of adult mice and nonhuman primates. Mol Ther 19 (2011), 1058–1069.
37. 37 Lawson, LJ, Perry, VH, Gordon, S, Turnover of resident microglia in the normal adult mouse brain. Neuroscience 48 (1992), 405–415.
38. 38 Zhang, Y, Chen, K, Sloan, SA, Bennett, ML, Scholze, AR, O'Keeffe, S, et al. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J Neurosci 34 (2014), 11929–11947.
39. 39 Niwa, H, Yamamura, K, Miyazaki, J, Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108 (1991), 193–199.
40. 40 Zhong, L, Chen, L, Li, Y, Qing, K, Weigel-Kelley, KA, Chan, RJ, et al. Self-complementary adeno-associated virus 2 (AAV)-T cell protein tyrosine phosphatase vectors as helper viruses to improve transduction efficiency of conventional single-stranded AAV vectors in vitro and in vivo. Mol Ther 10 (2004), 950–957.
41. 41 Chen, KA, Cruz, PE, Lanuto, DJ, Flotte, TR, Borchelt, DR, Srivastava, A, et al. Cellular fusion for gene delivery to SCA1 affected Purkinje neurons. Mol Cell Neurosci 47 (2011), 61–70.
42. 42 Zolotukhin, S, Byrne, BJ, Mason, E, Zolotukhin, I, Potter, M, Chesnut, K, et al. Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene Ther 6 (1999), 973–985.
43. 43 Wang, Y, Ling, C, Song, L, Wang, L, Aslanidi, GV, Tan, M, et al. Limitations of encapsidation of recombinant self-complementary adeno-associated viral genomes in different serotype capsids and their quantitation. Hum Gene Ther Methods 23 (2012), 225–233.