Enhancing gene delivery of adeno-associated viruses by cell-permeable peptides

Molecular Therapy Methods and Clinical Development

Volumn 1, Issue , 2014, Pages 12-

  Liu, Yarong ^a   Kim, Young Joo ^b   Ji, Man ^b   Fang, Jinxu ^a   Siriwon, Natnaree ^a   Zhang, Li I ^b   Wang, Pin ^a,b  

^a University of Southern California ^*  (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84906671515     PISSN: None     EISSN: 23290501     Source Type: Journal    
DOI: 10.1038/mtm.2013.12     Document Type: Article

References (55)

1. Choi, VW, McCarty, DM and Samulski, RJ (2005). AAV hybrid serotypes: improved vectors for gene delivery. Curr Gene Ther 5: 299-310.
2. Fisher, KJ, Jooss, K, Alston, J, Yang, Y, Haecker, SE, High, K et al. (1997). Recombinant adeno-associated virus for muscle directed gene therapy. Nat Med 3: 306-312.
3. Mueller, C and Flotte, TR (2008). Clinical gene therapy using recombinant adeno-associated virus vectors. Gene Ther 15: 858-863.
4. Wu, Z, Asokan, A and Samulski, RJ (2006). Adeno-associated virus serotypes: vector toolkit for human gene therapy. Mol Ther 14: 316-327.
5. Girod, A, Ried, M, Wobus, C, Lahm, H, Leike, K, Kleinschmidt, J et al. (1999). Genetic capsid modifications allow efficient re-targeting of adeno-associated virus type 2. Nat Med 5: 1052-1056.
6. Bartlett, JS, Kleinschmidt, J, Boucher, RC and Samulski, RJ (1999). Targeted adeno-associated virus vector transduction of nonpermissive cells mediated by a bispecific F(ab'gamma)2 antibody. Nat Biotechnol 17: 181-186.
7. Douar, AM, Poulard, K, Stockholm, D and Danos, O (2001). Intracellular trafficking of adeno-associated virus vectors: routing to the late endosomal compartment and proteasome degradation. J Virol 75: 1824-1833.
8. Hansen, J, Qing, K, Kwon, HJ, Mah, C and Srivastava, A (2000). Impaired intracellular trafficking of adeno-associated virus type 2 vectors limits efficient transduction of murine fibroblasts. J Virol 74: 992-996.
9. Duan, D, Yue, Y, Yan, Z, Yang, J and Engelhardt, JF (2000). Endosomal processing limits gene transfer to polarized airway epithelia by adeno-associated virus. J Clin Invest 105: 1573-1587.
10. Duan, D, Yue, Y, Yan, Z, McCray, PB Jr and Engelhardt, JF (1998). Polarity influences the efficiency of recombinant adenoassociated virus infection in differentiated airway epithelia. Hum Gene Ther 9: 2761-2776.
11. Mizukami, H, Young, NS and Brown, KE (1996). Adeno-associated virus type 2 binds to a 150-kilodalton cell membrane glycoprotein. Virology 217: 124-130.
12. White, SJ, Nicklin, SA, Büning, H, Brosnan, MJ, Leike, K, Papadakis, ED et al. (2004). Targeted gene delivery to vascular tissue in vivo by tropism-modified adeno-associated virus vectors. Circulation 109: 513-519.
13. Yu, CY, Yuan, Z, Cao, Z, Wang, B, Qiao, C, Li, J et al. (2009). A muscle-targeting peptide displayed on AAV2 improves muscle tropism on systemic delivery. Gene Ther 16: 953-962.
14. Shi, W and Bartlett, JS (2003). RGD inclusion in VP3 provides adeno-associated virus type 2 (AAV2)-based vectors with a heparan sulfate-independent cell entry mechanism. Mol Ther 7: 515-525.
15. Douar, AM, Poulard, K and Danos, O (2003). Deleterious effect of peptide insertions in a permissive site of the AAV2 capsid. Virology 309: 203-208.
16. Futaki, S, Suzuki, T, Ohashi, W, Yagami, T, Tanaka, S, Ueda, K et al. (2001). Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. J Biol Chem 276: 5836-5840.
17. Rudolph, C, Plank, C, Lausier, J, Schillinger, U, Müller, RH and Rosenecker, J (2003). Oligomers of the arginine-rich motif of the HIV-1 TAT protein are capable of transferring plasmid DNA into cells. J Biol Chem 278: 11411-11418.
18. Torchilin, VP, Rammohan, R, Weissig, V and Levchenko, TS (2001). TAT peptide on the surface of liposomes affords their efficient intracellular delivery even at low temperature and in the presence of metabolic inhibitors. Proc Natl Acad Sci USA 98: 8786-8791.
19. Gratton, J P, Yu, J, Griffith, JW, Babbitt, RW, Scotland, RS, Hickey, R et al. (2003). Cell-permeable peptides improve cellular uptake and therapeutic gene delivery of replication-deficient viruses in cells and in vivo. Nat Med 9: 357-362.
20. Matsushita, M, Noguchi, H, Lu, YF, Tomizawa, K, Michiue, H, Li, ST et al. (2004). Photo-acceleration of protein release from endosome in the protein transduction system. FEBS Lett 572: 221-226.
21. Wadia, JS, Stan, RV and Dowdy, SF (2004). Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med 10: 310-315.
22. El-Sayed, A, Futaki, S and Harashima, H (2009). Delivery of macromolecules using arginine-rich cell-penetrating peptides: ways to overcome endosomal entrapment. AAPS J 11: 13-22.
23. Lin, C and Engbersen, JF (2008). Effect of chemical functionalities in poly(amido amine)s for non-viral gene transfection. J Control Release 132: 267-272.
24. Moreira, C, Oliveira, H, Pires, LR, Simões, S, Barbosa, MA and Pêgo, AP (2009). Improving chitosan-mediated gene transfer by the introduction of intracellular buffering moieties into the chitosan backbone. Acta Biomater 5: 2995-3006.
25. Pack, DW, Putnam, D and Langer, R (2000). Design of imidazole-containing endosomolytic biopolymers for gene delivery. Biotechnol Bioeng 67: 217-223.
26. Duan, D, Li, Q, Kao, AW, Yue, Y, Pessin, JE and Engelhardt, JF (1999). Dynamin is required for recombinant adeno-associated virus type 2 infection. J Virol 73: 10371-10376.
27. Seisenberger, G, Ried, MU, Endress, T, Büning, H, Hallek, M and Bräuchle, C (2001). Realtime single-molecule imaging of the infection pathway of an adeno-associated virus. Science 294: 1929-1932.
28. Suikkanen, S, Antila, M, Jaatinen, A, Vihinen-Ranta, M and Vuento, M (2003). Release of canine parvovirus from endocytic vesicles. Virology 316: 267-280.
29. Wang, LH, Rothberg, KG and Anderson, RG (1993). Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol 123: 1107-1117.
30. Orlandi, PA and Fishman, PH (1998). Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J Cell Biol 141: 905-915.
31. West, MA, Bretscher, MS and Watts, C (1989). Distinct endocytotic pathways in epidermal growth fac tor-stimulated human carcinoma A431 cells. J Cell Biol 109(6 Pt 1): 2731-2739.
32. Summerford, C and Samulski, RJ (1998). Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J Virol 72: 1438-1445.
33. Sanlioglu, S, Benson, PK, Yang, J, Atkinson, EM, Reynolds, T and Engelhardt, JF (2000). Endocytosis and nuclear trafficking of adeno-associated virus type 2 are controlled by rac1 and phosphatidylinositol-3 kinase activation. J Virol 74: 9184-9196.
34. Ding, W, Zhang, LN, Yeaman, C and Engelhardt, JF (2006). rAAV2 traffics through both the late and the recycling endosomes in a dose-dependent fashion. Mol Ther 13: 671-682.
35. Joo, KI, Fang, Y, Liu, Y, Xiao, L, Gu, Z, Tai, A et al. (2011). Enhanced real-time monitoring of adeno-associated virus trafficking by virus-quantum dot conjugates. ACS Nano 5: 3523-3535.
36. Sonntag, F, Bleker, S, Leuchs, B, Fischer, R and Kleinschmidt, JA (2006). Adeno-associated virus type 2 capsids with externalized VP1/VP2 trafficking domains are generated prior to passage through the cytoplasm and are maintained until uncoating occurs in the nucleus. J Virol 80: 11040-11054.
37. Bowman, EJ, Siebers, A and Altendorf, K (1988). Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci USA 85: 7972-7976.
38. Stenmark, H, Parton, RG, Steele-Mortimer, O, Lütcke, A, Gruenberg, J and Zerial, M (1994). Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J 13: 1287-1296.
39. Press, B, Feng, Y, Hoflack, B and Wandinger-Ness, A (1998). Mutant Rab7 causes the accumulation of cathepsin D and cation-independent mannose 6-phosphate receptor in an early endocytic compartment. J Cell Biol 140: 1075-1089.
40. Liu, Y, Joo, KI and Wang, P (2013). Endocytic processing of adeno-associated virus type 8 vectors for transduction of target cells. Gene Ther 20: 308-317.
41. Hansen, J, Qing, K and Srivastava, A (2001). Infection of purified nuclei by adeno-associated virus 2. Mol Ther 4: 289-296.
42. Van de Water, TR, Staecker, H, Halterman, MW and Federoff, HJ (1999). Genetherapy in the inner ear: mechanisms and clinical implications. ANN N Y Acad Sci 884: 345-360.
43. Luebke, AE, Foster, PK, Muller, CD and Peel, AL (2001). Cochlear function and transgene expression in the guinea pig cochlea, using adenovirus-and adeno-associated virus-directed gene transfer. Hum Gene Ther 12: 773-781.
44. Konishi, M, Kawamoto, K, Izumikawa, M, Kuriyama, H and Yamashita, T (2008). Gene transfer into guinea pig cochlea using adeno-associated virus vectors. J Gene Med 10: 610-618.
45. Kay, MA, Manno, CS, Ragni, MV, Larson, PJ, Couto, LB, McClelland, A et al. (2000). Evidence for gene transfer and expression of factor IX in haemophilia B patients treated with an AAV vector. Nat Genet 24: 257-261.
46. Nakai, H, Fuess, S, Storm, TA, Muramatsu, S, Nara, Y and Kay, MA (2005). Unrestricted hepatocyte transduction with adeno-associated virus serotype 8 vectors in mice. J Virol 79: 214-224.
47. Wang, Z, Zhu, T, Qiao, C, Zhou, L, Wang, B, Zhang, J et al. (2005). Adeno-associated virus serotype 8 efficiently delivers genes to muscle and heart. Nat Biotechnol 23: 321-328.
48. Zhong, L, Zhao, W, Wu, J, Li, B, Zolotukhin, S, Govindasamy, L et al. (2007). A dual role of EGFR protein tyrosine kinase signaling in ubiquitination of AAV2 capsids and viral second-strand DNA synthesis. Mol Ther 15: 1323-1330.
49. Zhong, L, Li, B, Jayandharan, G, Mah, CS, Govindasamy, L, Agbandje-McKenna, M et al. (2008). Tyrosine-phosphorylation of AAV2 vectors and its consequences on viral intracellular trafficking and transgene expression. Virology 381: 194-202.
50. Li, M, Jayandharan, GR, Li, B, Ling, C, Ma, W, Srivastava, A et al. (2010). 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: 1527-1543.
51. Yuasa, K, Yoshimura, M, Urasawa, N, Ohshima, S, Howell, JM, Nakamura, A et al. (2007). Injection of a recombinant AAV serotype 2 into canine skeletal muscles evokes strong immune responses against transgene products. Gene Ther 14: 1249-1260.
52. Manno, CS, Chew, AJ, Hutchison, S, Larson, PJ, Herzog, RW, Arruda, VR et al. (2003). AAV-mediated factor IX gene transfer to skeletal muscle in patients with severe hemophilia B. Blood 101: 2963-2972.
53. Conway, JE, Rhys, CM, Zolotukhin, I, Zolotukhin, S, Muzyczka, N, Hayward, GS et al. (1999). High-titer recombinant adeno-associated virus production utilizing a recombinant herpes simplex virus type I vector expressing AAV-2 Rep and Cap. Gene Ther 6: 986-993.
54. Joo, KI, Tai, A, Lee, CL, Wong, C and Wang, P (2010). Imaging multiple intermediates of single-virus membrane fusion mediated by distinct fusion proteins. Microsc Res Tech 73: 886-900.
55. Sommer, JM, Smith PH, Parthasarathy S, Isaacs J, Vijay S, Kiera J et al. (2003). Quantification of adeno-associated virus particles and empty capsids by optical density measurement. Mol Ther 7: 122-128.