Engineering liver-detargeted AAV9 vectors for cardiac and musculoskeletal gene transfer

Molecular Therapy

Volumn 19, Issue 6, 2011, Pages 1070-1078

  Pulicherla, Nagesh ^a   Shen, Shen ^a,b   Yadav, Swati ^a   Debbink, Kari ^a   Govindasamy, Lakshmanan ^c   Agbandje Mckenna, Mavis ^c   Asokan, Aravind ^a,b  

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

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; PARVOVIRUS VECTOR;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS 9; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOENGINEERING; CONTROLLED STUDY; FEASIBILITY STUDY; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; GENE TRANSFER; HEART MUSCLE; HUMAN; HUMAN CELL; LIVER; MOUSE; MUSCLE TISSUE; MUSCULOSKELETAL SYSTEM; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; VIRAL GENE DELIVERY SYSTEM; VIRAL TROPISM; VIRUS CAPSID; VIRUS GENOME;

ADENO-ASSOCIATED VIRUS; ANIMALIA; MIRIDAE;

EID: 79957890386     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2011.22     Document Type: Article

References (46)

1. Herzog, RW, Cao, O and Srivastava, A (2010). Two decades of clinical gene therapy-success is fnally mounting. Discov Med 9: 105-111.
2. Mitchell, AM, Nicolson, SC, Warischalk, JK and Samulski, RJ (2010). AAV's anatomy: roadmap for optimizing vectors for translational success. Curr Gene Ther 10: 319-340.
3. Zincarelli, C, Soltys, S, Rengo, G and Rabinowitz, JE (2008). Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 16: 1073-1080. (Pubitemid 351737072)
4. Inagaki, K, Fuess, S, Storm, TA, Gibson, GA, Mctiernan, CF, Kay, MA et al. (2006). Robust systemic transduction with AAV9 vectors in mice: effcient global cardiac gene transfer superior to that of AAV8. Mol Ther 14: 45-53. (Pubitemid 43899488)
5. Pacak, CA, Mah, CS, Thattaliyath, BD, Conlon, TJ, Lewis, MA, Cloutier, DE et al. (2006). Recombinant adeno-associated virus serotype 9 leads to preferential cardiac transduction in vivo. Circ Res 99: e3-e9. (Pubitemid 44255502)
6. Yang, L, Jiang, J, Drouin, LM, Agbandje-McKenna, M, Chen, C, Qiao, C et al. (2009). A myocardium tropic adeno-associated virus (AAV) evolved by DNA shuffing and in vivo selection. Proc Natl Acad Sci USA 106: 3946-3951.
7. Foust, KD, Nurre, E, Montgomery, CL, Hernandez, A, Chan, CM and Kaspar, BK (2009). Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 27: 59-65.
8. Kornegay, JN, Li, J, Bogan, JR, Bogan, DJ, Chen, C, Zheng, H et al. (2010). Widespread muscle expression of an AAV9 human mini-dystrophin vector after intravenous injection in neonatal dystrophin-defcient dogs. Mol Ther 18: 1501-1508.
9. Lipskaia, L, Chemaly, ER, Hadri, L, Lompre, AM and Hajjar, RJ (2010). Sarcoplasmic reticulum Ca(2+) ATPase as a therapeutic target for heart failure. Expert Opin Biol Ther 10: 29-41.
10. Hasbrouck, NC and High, KA (2008). AAV-mediated gene transfer for the treatment of hemophilia B: problems and prospects. Gene Ther 15: 870-875. (Pubitemid 351712621)
11. Brantly, ML, Chulay, JD, Wang, L, Mueller, C, Humphries, M, Spencer, LT et al. (2009). Sustained transgene expression despite T lymphocyte responses in a clinical trial of rAAV1-AAT gene therapy. Proc Natl Acad Sci USA 106: 16363-16368.
12. Halbert, CL, Madtes, DK, Vaughan, AE, Wang, Z, Storb, R, Tapscott, SJ et al. (2010). Expression of human alpha1-antitrypsin in mice and dogs following AAV6 vector-mediated gene transfer to the lungs. Mol Ther 18: 1165-1172.
13. Salva, MZ, Himeda, CL, Tai, PW, Nishiuchi, E, Gregorevic, P, Allen, JM et al. (2007). Design of tissue-specifc regulatory cassettes for high-level rAAV-mediated expression in skeletal and cardiac muscle. Mol Ther 15: 320-329. (Pubitemid 46111882)
14. Wang, B, Li, J, Fu, FH, Chen, C, Zhu, X, Zhou, L et al. (2008). Construction and analysis of compact muscle-specifc promoters for AAV vectors. Gene Ther 15: 1489-1499.
15. Brown, BD and Naldini, L (2009). Exploiting and antagonizing microRNA regulation for therapeutic and experimental applications. Nat Rev Genet 10: 578-585.
16. Michelfelder, S, Kohlschütter, J, Skorupa, A, Pfennings, S, Müller, O, Kleinschmidt, JA et al. (2009). Successful expansion but not complete restriction of tropism of adeno-associated virus by in vivo biopanning of random virus display peptide libraries. PLoS ONE 4: e5122.
17. Ying, Y, Müller, OJ, Goehringer, C, Leuchs, B, Trepel, M, Katus, HA et al. (2010). Heart-targeted adeno-associated viral vectors selected by in vivo biopanning of a random viral display peptide library. Gene Ther 17: 980-990.
18. Excoffon, KJ, Koerber, JT, Dickey, DD, Murtha, M, Keshavjee, S, Kaspar, BK et al. (2009). Directed evolution of adeno-associated virus to an infectious respiratory virus. Proc Natl Acad Sci USA 106: 3865-3870.
19. Koerber, JT, Klimczak, R, Jang, JH, Dalkara, D, Flannery, JG and Schaffer, DV (2009). Molecular evolution of adeno-associated virus for enhanced glial gene delivery. Mol Ther 17: 2088-2095.
20. Opie, SR, Warrington, KH Jr, Agbandje-McKenna, M, Zolotukhin, S and Muzyczka, N (2003). Identifcation of amino acid residues in the capsid proteins of adeno-associated virus type 2 that contribute to heparan sulfate proteoglycan binding. J Virol 77: 6995-7006. (Pubitemid 36666892)
21. Kern, A, Schmidt, K, Leder, C, Müller, OJ, Wobus, CE, Bettinger, K et al. (2003). Identifcation of a heparin-binding motif on adeno-associated virus type 2 capsids. J Virol 77: 11072-11081. (Pubitemid 37204297)
22. Asokan, A, Hamra, JB, Govindasamy, L, Agbandje-McKenna, M and Samulski, RJ (2006). Adeno-associated virus type 2 contains an integrin alpha5beta1 binding domain essential for viral cell entry. J Virol 80: 8961-8969. (Pubitemid 44359970)
23. Xie, Q, Bu, W, Bhatia, S, Hare, J, Somasundaram, T, Azzi, A et al. (2002). The atomic structure of adeno-associated virus (AAV-2), a vector for human gene therapy. Proc Natl Acad Sci USA 99: 10405-10410.
24. Govindasamy, L, Padron, E, McKenna, R, Muzyczka, N, Kaludov, N, Chiorini, JA et al. (2006). Structurally mapping the diverse phenotype of adeno-associated virus serotype 4. J Virol 80: 11556-11570. (Pubitemid 44788870)
25. Wu, Z, Asokan, A, Grieger, JC, Govindasamy, L, Agbandje-McKenna, M and Samulski, RJ (2006). Single amino acid changes can infuence titer, heparin binding, and tissue tropism in different adeno-associated virus serotypes. J Virol 80: 11393-11397. (Pubitemid 44706580)
26. Nam, HJ, Lane, MD, Padron, E, Gurda, B, McKenna, R, Kohlbrenner, E et al. (2007). Structure of adeno-associated virus serotype 8, a gene therapy vector. J Virol 81: 12260-12271. (Pubitemid 350085841)
27. Asokan, A, Conway, JC, Phillips, JL, Li, C, Hegge, J, Sinnott, R et al. (2010). Reengineering a receptor footprint of adeno-associated virus enables selective and systemic gene transfer to muscle. Nat Biotechnol 28: 79-82.
28. Bish, LT, Morine, K, Sleeper, MM, Sanmiguel, J, Wu, D, Gao, G et al. (2008). Adeno-associated virus (AAV) serotype 9 provides global cardiac gene transfer superior to AAV1, AAV6, AAV7, and AAV8 in the mouse and rat. Hum Gene Ther 19: 1359-1368.
29. Levy, HC, Bowman, VD, Govindasamy, L, McKenna, R, Nash, K, Warrington, K et al. (2009). Heparin binding induces conformational changes in Adeno-associated virus serotype 2. J Struct Biol 165: 146-156.
30. Lerch, TF, Xie, Q and Chapman, MS (2010). The structure of adeno-associated virus serotype 3B (AAV-3B): insights into receptor binding and immune evasion. Virology 403: 26-36.
31. Molenaar, TJ, Michon, I, de Haas, SA, van Berkel, TJ, Kuiper, J and Biessen, EA (2002). Uptake and processing of modifed bacteriophage M13 in mice: implications for phage display. Virology 293: 182-191.
32. Prasuhn, DE Jr, Singh, P, Strable, E, Brown, S, Manchester, M and Finn, MG (2008). Plasma clearance of bacteriophage Qbeta particles as a function of surface charge. J Am Chem Soc 130: 1328-1334. (Pubitemid 351171012)
33. Michelfelder, S and Trepel, M (2009). Adeno-associated viral vectors and their redirection to cell-type specifc receptors. Adv Genet 67: 29-60.
34. Lochrie, MA, Tatsuno, GP, Christie, B, McDonnell, JW, Zhou, S, Surosky, R et al. (2006). Mutations on the external surfaces of adeno-associated virus type 2 capsids that affect transduction and neutralization. J Virol 80: 821-834. (Pubitemid 43062894)
35. Akache, B, Grimm, D, Pandey, K, Yant, SR, Xu, H and Kay, MA (2006). The 37/67-kilodalton laminin receptor is a receptor for adeno-associated virus serotypes 8, 2, 3, and 9. J Virol 80: 9831-9836. (Pubitemid 44435657)
36. Rubio, MP, López-Bueno, A and Almendral, JM (2005). Virulent variants emerging in mice infected with the apathogenic prototype strain of the parvovirus minute virus of mice exhibit a capsid with low avidity for a primary receptor. J Virol 79: 11280-11290. (Pubitemid 41170670)
37. Nam, HJ, Gurda-Whitaker, B, Gan, WY, Ilaria, S, McKenna, R, Mehta, P et al. (2006). Identifcation of the sialic acid structures recognized by minute virus of mice and the role of binding affnity in virulence adaptation. J Biol Chem 281: 25670-25677. (Pubitemid 44401956)
38. Kalyuzhniy, O, Di Paolo, NC, Silvestry, M, Hofherr, SE, Barry, MA, Stewart, PL et al. (2008). Adenovirus serotype 5 hexon is critical for virus infection of hepatocytes in vivo. Proc Natl Acad Sci USA 105: 5483-5488. (Pubitemid 351753889)
39. Boecker, W, Bernecker, OY, Wu, JC, Zhu, X, Sawa, T, Grazette, L et al. (2004). Cardiac-specifc gene expression facilitated by an enhanced myosin light chain promoter. Mol Imaging 3: 69-75.
40. Qiao, C, Yuan, Z, Li, J, He, B, Zheng, H, Mayer, C,et al. (2010). Liver-specifc microRNA-122 target sequences incorporated in AAV vectors effciently inhibits transgene expression in the liver. Gene Ther (epub ahead of print).
41. Geisler, A, Jungmann, A, Kurreck, J, Poller, W, Katus, HA, Vetter, R et al. (2011). microRNA122-regulated transgene expression increases specifcity of cardiac gene transfer upon intravenous delivery of AAV9 vectors. Gene Ther 18: 199-209.
42. Gao, G, Vandenberghe, LH, Alvira, MR, Lu, Y, Calcedo, R, Zhou, X et al. (2004). Clades of Adeno-associated viruses are widely disseminated in human tissues. J Virol 78: 6381-6388. (Pubitemid 38715936)
43. Arnold, K, Bordoli, L, Kopp, J and Schwede, T (2006). The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201. (Pubitemid 43205406)
44. Carrillo-Tripp, M, Shepherd, CM, Borelli, IA, Venkataraman, S, Lander, G, Natarajan, P et al. (2009). VIPERdb2: an enhanced and web API enabled relational database for structural virology. Nucleic Acids Res 37(Database issue): D436-D442.
45. Xiao, C and Rossmann, MG (2007). Interpretation of electron density with stereographic roadmap projections. J Struct Biol 158: 182-187. (Pubitemid 46719989)
46. Grieger, JC, Choi, VW and Samulski, RJ (2006). Production and characterization of adeno-associated viral vectors. Nat Protoc 1: 1412-1428