A Rationally Engineered Capsid Variant of AAV9 for Systemic CNS-Directed and Peripheral Tissue-Detargeted Gene Delivery in Neonates

Molecular Therapy Methods and Clinical Development

Volumn 9, Issue , 2018, Pages 234-246

  Wang, Dan ^a   Li, Shaoyong ^a   Gessler, Dominic J ^a   Xie, Jun ^a   Zhong, Li ^a   Li, Jia ^a   Tran, Karen ^a   Van Vliet, Kim ^b   Ren, Lingzhi ^a   Su, Qin ^a   He, Ran ^a   Goetzmann, Jason E ^c   Flotte, Terence R ^a   Agbandje McKenna, Mavis ^b   Gao, Guangping ^a,d  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF LOUISIANA AT LAFAYETTE   (United States)

^d SICHUAN UNIVERSITY   (China)

Author keywords

AAV capsid; adeno associated virus; CNS disease; gene therapy; tissue detargeting

Indexed keywords

VIRUS VECTOR;

ADENO ASSOCIATED VIRUS 9; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOENGINEERING; BLOOD BRAIN BARRIER; CANAVAN DISEASE; CENTRAL NERVOUS SYSTEM DISEASE; GENE REPLACEMENT THERAPY; GENE TARGETING; GENE THERAPY; GENETIC TRANSDUCTION; LEUKODYSTROPHY; MOUSE; NATURAL SCIENCE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ANALYSIS; VIRUS CAPSID;

EID: 85056375996     PISSN: None     EISSN: 23290501     Source Type: Journal    
DOI: 10.1016/j.omtm.2018.03.004     Document Type: Article

References (39)

1. Muzyczka, N., Berns, K., Parvoviridae: the viruses and their replication. Knipe, D., et al. (eds.) Fields Virology, Volume 2, 2001, Lippincott, Williams and Wilkins, Philadelphia, PA, 2327–2359.
2. Gao, G., Zhong, L., Danos, O., Exploiting natural diversity of AAV for the design of vectors with novel properties. Methods Mol. Biol. 807 (2011), 93–118.
3. Münch, R.C., Muth, A., Muik, A., Friedel, T., Schmatz, J., Dreier, B., Trkola, A., Plückthun, A., Büning, H., Buchholz, C.J., Off-target-free gene delivery by affinity-purified receptor-targeted viral vectors. Nat. Commun., 6, 2015, 6246.
4. Asokan, A., Conway, J.C., Phillips, J.L., Li, C., Hegge, J., Sinnott, R., Yadav, S., DiPrimio, N., Nam, H.J., Agbandje-McKenna, M., et al. Reengineering a receptor footprint of adeno-associated virus enables selective and systemic gene transfer to muscle. Nat. Biotechnol. 28 (2010), 79–82.
5. Grimm, D., Lee, J.S., Wang, L., Desai, T., Akache, B., Storm, T.A., Kay, M.A., In vitro and in vivo gene therapy vector evolution via multispecies interbreeding and retargeting of adeno-associated viruses. J. Virol. 82 (2008), 5887–5911.
6. 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. 16 (2008), 1073–1080.
7. 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. 27 (2009), 59–65.
8. 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. 17 (2009), 1187–1196.
9. Ahmed, S.S., Li, H., Cao, C., Sikoglu, E.M., Denninger, A.R., Su, Q., Eaton, S., Liso Navarro, A.A., Xie, J., Szucs, S., et al. A single intravenous rAAV injection as late as P20 achieves efficacious and sustained CNS Gene therapy in Canavan mice. Mol. Ther. 21 (2013), 2136–2147.
10. Gessler, D.J., Li, D., Xu, H., Su, Q., Sanmiguel, J., Tuncer, S., Moore, C., King, J., Matalon, R., Gao, G., RedirectingN-acetylaspartate metabolism in the central nervous system normalizes myelination and rescues Canavan disease. JCI Insight, 2, 2017, e90807.
11. Mendell, J.R., Al-Zaidy, S., Shell, R., Arnold, W.D., Rodino-Klapac, L., Kissel, J.T., Prior, T.W., Miranda, C., Lowes, L., Alfano, L., et al. Gene therapy for spinal muscular atrophy type 1 shows potential to improve survival and motor functional outcomes. Mol. Ther., 24, 2016, S190.
12. Hinderer, C., Katz, N., Buza, E.L., Dyer, C., Goode, T., Bell, P., Richman, L.K., Wilson, J.M., Severe toxicity in nonhuman primates and piglets following high-dose intravenous administration of an adeno-associated virus vector expressing human SMN. Hum. Gene Ther., 2018, 10.1089/hum.2018.015 Published online February 12, 2018.
13. Salva, M.Z., Himeda, C.L., Tai, P.W., Nishiuchi, E., Gregorevic, P., Allen, J.M., Finn, E.E., Nguyen, Q.G., Blankinship, M.J., Meuse, L., et al. Design of tissue-specific regulatory cassettes for high-level rAAV-mediated expression in skeletal and cardiac muscle. Mol. Ther. 15 (2007), 320–329.
14. Xie, J., Xie, Q., Zhang, H., Ameres, S.L., Hung, J.H., Su, Q., He, R., Mu, X., Seher Ahmed, S., Park, S., et al. MicroRNA-regulated, systemically delivered rAAV9: a step closer to CNS-restricted transgene expression. Mol. Ther. 19 (2011), 526–535.
15. Pulicherla, N., Shen, S., Yadav, S., Debbink, K., Govindasamy, L., Agbandje-McKenna, M., Asokan, A., Engineering liver-detargeted AAV9 vectors for cardiac and musculoskeletal gene transfer. Mol. Ther. 19 (2011), 1070–1078.
16. Manno, C.S., Pierce, G.F., Arruda, V.R., Glader, B., Ragni, M., Rasko, J.J., Ozelo, M.C., Hoots, K., Blatt, P., Konkle, B., et al. Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat. Med. 12 (2006), 342–347.
17. Drouin, L.M., Agbandje-McKenna, M., Adeno-associated virus structural biology as a tool in vector development. Future Virol. 8 (2013), 1183–1199.
18. Bell, C.L., Vandenberghe, L.H., Bell, P., Limberis, M.P., Gao, G.P., Van Vliet, K., Agbandje-McKenna, M., Wilson, J.M., The AAV9 receptor and its modification to improve in vivo lung gene transfer in mice. J. Clin. Invest. 121 (2011), 2427–2435.
19. Shen, S., Bryant, K.D., Brown, S.M., Randell, S.H., Asokan, A., Terminal N-linked galactose is the primary receptor for adeno-associated virus 9. J. Biol. Chem. 286 (2011), 13532–13540.
20. Bell, C.L., Gurda, B.L., Van Vliet, K., Agbandje-McKenna, M., Wilson, J.M., Identification of the galactose binding domain of the adeno-associated virus serotype 9 capsid. J. Virol. 86 (2012), 7326–7333.
21. Shen, S., Berry, G.E., Castellanos Rivera, R.M., Cheung, R.Y., Troupes, A.N., Brown, S.M., Kafri, T., Asokan, A., Functional analysis of the putative integrin recognition motif on adeno-associated virus 9. J. Biol. Chem. 290 (2015), 1496–1504.
22. 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. 80 (2006), 9831–9836.
23. Kotchey, N.M., Adachi, K., Zahid, M., Inagaki, K., Charan, R., Parker, R.S., Nakai, H., A potential role of distinctively delayed blood clearance of recombinant adeno-associated virus serotype 9 in robust cardiac transduction. Mol. Ther. 19 (2011), 1079–1089.
24. DiMattia, M.A., Nam, H.J., Van Vliet, K., Mitchell, M., Bennett, A., Gurda, B.L., McKenna, R., Olson, N.H., Sinkovits, R.S., Potter, M., et al. Structural insight into the unique properties of adeno-associated virus serotype 9. J. Virol. 86 (2012), 6947–6958.
25. Shen, S., Bryant, K.D., Sun, J., Brown, S.M., Troupes, A., Pulicherla, N., Asokan, A., Glycan binding avidity determines the systemic fate of adeno-associated virus type 9. J. Virol. 86 (2012), 10408–10417.
26. Wang, L., Wang, H., Bell, P., McMenamin, D., Wilson, J.M., Hepatic gene transfer in neonatal mice by adeno-associated virus serotype 8 vector. Hum. Gene Ther. 23 (2012), 533–539.
27. Ahmed, S.S., Schattgen, S.A., Frakes, A.E., Sikoglu, E.M., Su, Q., Li, J., Hampton, T.G., Denninger, A.R., Kirschner, D.A., Kaspar, B., et al. rAAV gene therapy in a Canavan's disease mouse model reveals immune impairments and an extended pathology beyond the central nervous system. Mol. Ther. 24 (2016), 1030–1041.
28. Di Pasquale, G., Chiorini, J.A., AAV transcytosis through barrier epithelia and endothelium. Mol. Ther. 13 (2006), 506–516.
29. Merkel, S.F., Andrews, A.M., Lutton, E.M., Mu, D., Hudry, E., Hyman, B.T., Maguire, C.A., Ramirez, S.H., Trafficking of adeno-associated virus vectors across a model of the blood-brain barrier; a comparative study of transcytosis and transduction using primary human brain endothelial cells. J. Neurochem. 140 (2017), 216–230.
30. Xu, G., Luo, L., Tai, P.W.L., Qin, W., Xiao, Y., Wang, C., Su, Q., Ma, H., He, R., Wei, Y., et al. High-throughput sequencing of AAV proviral libraries from the human population reveals novel variants with unprecedented intra- and inter-tissue diversity. Mol. Ther., 24, 2016, S4.
31. Gao, G., Alvira, M.R., Somanathan, S., Lu, Y., Vandenberghe, L.H., Rux, J.J., Calcedo, R., Sanmiguel, J., Abbas, Z., Wilson, J.M., Adeno-associated viruses undergo substantial evolution in primates during natural infections. Proc. Natl. Acad. Sci. USA 100 (2003), 6081–6086.
32. Davidoff, A.M., Ng, C.Y., Zhou, J., Spence, Y., Nathwani, A.C., Sex significantly influences transduction of murine liver by recombinant adeno-associated viral vectors through an androgen-dependent pathway. Blood 102 (2003), 480–488.
33. Matalon, R., Rady, P.L., Platt, K.A., Skinner, H.B., Quast, M.J., Campbell, G.A., Matalon, K., Ceci, J.D., Tyring, S.K., Nehls, M., et al. Knock-out mouse for Canavan disease: a model for gene transfer to the central nervous system. J. Gene Med. 2 (2000), 165–175.
34. Gao, G., Sena-Esteves, M., Introducing genes into mammalian cells: viral vectors. Green, M.R., Sambrook, J.R., (eds.) Molecular Cloning, Fourth Edition, 2012, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, 1209–1330.
35. Emsley, P., Cowtan, K., Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004), 2126–2132.
36. Carrillo-Tripp, M., Shepherd, C.M., Borelli, I.A., Venkataraman, S., Lander, G., Natarajan, P., Johnson, J.E., Brooks, C.L. 3rd, Reddy, V.S., VIPERdb2: an enhanced and web API enabled relational database for structural virology. Nucleic Acids Res. 37 (2009), D436–D442.
37. DeLano, W.L., The PyMOL Molecular Graphics System. 2008, DeLano Scientific, New York, NY.
38. Lu, J., Jiang, C., Detergents inhibit chloramphenicol acetyl transferase. Biotechniques 12 (1992), 643–644.
39. Provencher, S.W., Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed. 14 (2001), 260–264.