Replacement of native adenovirus receptor-binding sites with a new attachment moiety diminishes hepatic tropism and enhances bioavailability in mice

Human Gene Therapy

Volumn 19, Issue 8, 2008, Pages 783-794

  Schagen, Frederik H E ^a   Graat, Harm C A ^a   Carette, Jan E ^a,b   Vellinga, Jort ^c   Geer, Michael A Van ^d   Hoeben, Rob C ^c   Dermody, Terence S ^e   Beusechem, Victor W Van ^a,f  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

^e VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f University of Amsterdam   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; ADENOVIRUS VECTOR GL; ADENOVIRUS VECTOR GLP TAIL T(II) MH; INTEGRIN; PENTON BASE PROTEIN; POLYHISTIDINE TAG; UNCLASSIFIED DRUG; VIRUS RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; CHIMERA; CONTROLLED STUDY; DRUG DESIGN; DRUG EFFICACY; ERYTHROCYTE KINETICS; FEMALE; FIBER TAIL DOMAIN; HUMAN; HUMAN CELL; IN VIVO STUDY; INTRACELLULAR TRANSPORT; LIVER BLOOD FLOW; LIVER CELL; LIVER CLEARANCE; LIVER METABOLISM; MOUSE; NONHUMAN; OLIGOMERIZATION; PROTEIN DOMAIN; PROTEIN MOTIF; RECEPTOR BINDING; REOVIRUS SIGMA1 OLIGOMERIZATION DOMAIN; VIRAL GENE DELIVERY SYSTEM; VIRUS CAPSID; VIRUS MORPHOLOGY;

ADENOVIRUSES, HUMAN; ANIMALS; ANTIGENS, VIRAL; BINDING SITES; BIOLOGICAL AVAILABILITY; CAPSID PROTEINS; CELL LINE, TUMOR; ERYTHROCYTES; FEMALE; GENE TARGETING; GENE THERAPY; GENETIC VECTORS; HEPATOCYTES; HUMANS; MICE; MICE, INBRED C57BL; RATS; TRANSDUCTION, GENETIC; VIRAL TAIL PROTEINS;

ADENOVIRIDAE; MIRIDAE; MUS; ORTHOREOVIRUS;

EID: 50649121070     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2007.133     Document Type: Article

References (37)

1. Akiyama, M., Thorne, S., Kirn, D., Roelvink, P.W., Einfeld, D.A., King, C.R., and Wickham, T.J. (2004). Ablating CAR and integrin binding in adenovirus vectors reduces nontarget organ transduction and permits sustained bloodstream persistence following intraperitoneal administration. Mol. Ther. 9, 218-230.
2. Alemany, R., and Curiel, D.T. (2001). CAR-binding ablation does not change biodistribution and toxicity of adenoviral vectors. Gene Ther. 8, 1347-1353.
3. Alemany, R., Suzuki, K., and Curiel, D.T. (2000). Blood clearance rates of adenovirus type 5 in mice. J. Gen. Virol. 81, 2605-2609.
4. Barnett, B.G., Crews, C.J., and Douglas, J.T. (2002). Targeted adenoviral vectors. Biochim. Biophys. Acta 1575, 1-14.
5. Bett, A.J., Haddara, W., Prevec, L., and Graham, F.L. (1994). An efficient and flexible system for construction of adenovirus vectors with insertions or deletions in early regions 1 and 3. Proc. Natl. Acad. Sci. U.S.A. 91, 8802-8806.
6. Cichon, G., Boeckh-Herwig, S., Kuemin, D., Hoffmann, C., Schmidt, H.H., Wehnes, E., Haensch, W., Schneider, U., Eckhardt, U., Burger, R., and Pring-Akerblom, P. (2003). Titer determination of Ad5 in blood: A cautionary note. Gene Ther. 10, 1012-1017.
7. Council of the European Community. (1986). Guidelines on the Protection of Experimental Animals (Council of the European Community, Brussels, Belgium).
8. Dechecchi, M.C., Tamanini, A., Bonizzato, A., and Cabrini, G. (2000). Heparan sulfate glycosaminoglycans are involved in adenovirus type 5 and 2-host cell interactions. Virology 268, 382-390.
9. Dechecchi, M.C., Melotti, P., Bonizzato, A., Santacatterina, M., Chilosi, M., and Cabrini, G. (2001). Heparan sulfate glycosaminoglycans are receptors sufficient to mediate the initial binding of adenovirus types 2 and 5. J. Virol. 75, 8772-8780.
10. Douglas, J.T., Rogers, B.E., Rosenfeld, M.E., Michael, S.I., Feng, M., and Curiel, D.T. (1996). Targeted gene delivery by tropism-modified adenoviral vectors. Nat. Biotechnol. 14, 1574-1578.
11. Douglas, J.T., Miller, C.R., Kim, M., Dmitriev, I., Mikheeva, G., Krasnykh, V., and Curiel, D.T. (1999). A system for the propagation of adenoviral vectors with genetically modified receptor specificities. Nat. Biotechnol. 17, 470-475.
12. Einfeld, D.A., Schroeder, R., Roelvink, P.W., Lizonova, A., King, C.R., Kovesdi, I., and Wickham, T.J. (2001). Reducing the native tropism of adenovirus vectors requires removal of both CAR and integrin interactions. J. Virol. 75, 11284-11291.
13. Green, N.K., Herbert, C.W., Hale, S.J., Hale, A.B., Mautner, V., Harkins, R., Hermiston, T., Ulbrich, K., Fisher, K.D., and Seymour, L.W. (2004). Extended plasma circulation time and decreased toxicity of polymer-coated adenovirus. Gene Ther. 11, 1256-1263.
14. Kirby, I., Davison, E., Beavil, A.J., Soh, C.P., Wickham, T.J., Roelvink, P.W., Kovesdi, I., Sutton, B.J., and Santis, G. (2000). Identification of contact residues and definition of the CAR-binding site of adenovirus type 5 fiber protein. J. Virol. 74, 2804-2813.
15. v integrin-binding ablation. J. Virol. 77, 13062-13072.
16. v integrin, and heparan sulfate binding reduce in vivo tissue transduction and toxicity. Hum. Gene Ther. 17, 264-279.
17. Krasnykh, V., Belousova, N., Korokhov, N., Mikheeva, G., and Curiel, D.T. (2001). Genetic targeting of an adenovirus vector via replacement of the fiber protein with the phage T4 fibritin. J. Virol. 75, 4176-4183.
18. 1 is an adenovirus coreceptor. J. Virol. 75, 5405-5409.
19. Lyons, M., Onion, D., Green, N.K., Aslan, K., Rajaratnam, R., Bazan-Peregrino, M., Phipps, S., Hale, S., Mautner, V., Seymour, L.W., and Fisher, K.D. (2006). Adenovirus type 5 interactions with human blood cells may compromise systemic delivery. Mol. Ther. 14, 118-128.
20. Magnusson, M.K., Hong, S.S., Boulanger, P., and Lindholm, L. (2001). Genetic retargeting of adenovirus: Novel strategy employing " deknobbing" of the fiber. J. Virol. 75, 7280-7289.
21. v integrins for infection. J. Virol. 68, 6811-6814.
22. v integrin-binding ablated adenovirus vectors, but not fiber-modified vectors containing RGD peptide, do not change the systemic gene transfer properties in mice. Gene Ther. 9, 769-776.
23. Nakamura, T., Sato, K., and Hamada, H. (2003). Reduction of natural adenovirus tropism to the liver by both ablation of fiber-coxsackievirus and adenovirus receptor interaction and use of replaceable short fiber. J. Virol. 77, 2512-2521.
24. Nicol, C.G., Graham, D., Miller, W.H., White, S.J., Smith, T.A., Nicklin, S.A., Stevenson, S.C., and Baker, A.H. (2004). Effect of adenovirus serotype 5 fiber and penton modifications on in vivo tropism in rats. Mol. Ther. 10, 344-354.
25. Obara, M., Kang, M.S., and Yamada, K.M. (1988). Site-directed mutagenesis of the cell-binding domain of human fibronectin: Separable, synergistic sites mediate adhesive function. Cell 53, 649-657.
26. Ogawara, K., Rots, M.G., Kok, R.J., Moorlag, H.E., Van Loenen, A.M., Meijer, D.K., Haisma, H.J., and Molema, G. (2004). A novel strategy to modify adenovirus tropism and enhance transgene delivery to activated vascular endothelial cells in vitro and in vivo. Hum. Gene Ther. 15, 433-443.
27. Parker, A.L., Waddington, S.N., Nicol, C.G., Shayakhmetov, D.M., Buckley, S.M., Denby, L., Kemball-Cook, G., Ni, S., Lieber, A., McVey, J.H., Nicklin, S.A., and Baker, A.H. (2006). Multiple vitamin K-dependent coagulation zymogens promote adenovirus-mediated gene delivery to hepatocytes. Blood 108, 2554-2561.
28. Reynolds, P., Dmitriev, I., and Curiel, D. (1999). Insertion of an RGD motif into the HI loop of adenovirus fiber protein alters the distribution of transgene expression of the systemically administered vector. Gene Ther. 6, 1336-1339.
29. Roelvink, P.W., Mi Lee, G., Einfeld, D.A., Kovesdi, I., and Wickham, T.J. (1999). Identification of a conserved receptor-binding site on the fiber proteins of CAR-recognizing Adenoviridae. Science 286, 1568-1571.
30. Schagen, F.H., Wensveen, F.M., Carette, J.E., Dermody, T.S., Gerritsen, W.R., and van Beusechem, V.W. (2006). Genetic targeting of adenovirus vectors using a reovirus sigma1-based attachment protein. Mol. Ther. 13, 997-1005.
31. Seki, T., Dmitriev, I., Suzuki, K., Kashentseva, E., Takayama, K., Rots, M., Uil, T., Wu, H., Wang, M., and Curiel, D.T. (2002). Fiber shaft extension in combination with HI loop ligands augments infectivity for CAR-negative tumor targets but does not enhance hepatotropism in vivo. Gene Ther. 9, 1101-1108.
32. Shayakhmetov, D.M., Gaggar, A., Ni, S., Li, Z.Y., and Lieber, A. (2005). Adenovirus binding to blood factors results in liver cell infection and hepatotoxicity. J. Virol. 79, 7478-7491.
33. Smith, T.A., Idamakanti, N., Marshall-Neff, J., Rollence, M.L., Wright, P., Kaloss, M., King, L., Mech, C., Dinges, L., Iverson, W.O., Sherer, A.D., Markovits, J.E., Lyons, R.M., Kaleko, M., and Stevenson, S.C. (2003a). Receptor interactions involved in adenoviral-mediated gene delivery after systemic administration in non-human primates. Hum. Gene Ther. 14, 1595-1604.
34. Smith, T.A., Idamakanti, N., Rollence, M.L., Marshall-Neff, J., Kim, J., Mulgrew, K., Nemerow, G.R., Kaleko, M., and Stevenson, S.C. (2003b). Adenovirus serotype 5 fiber shaft influences in vivo gene transfer in mice. Hum. Gene Ther. 14, 777-787.
35. Tao, N., Gao, G.-P., Parr, M., Johnston, J., Baradet, T., Wilson, J.M., Barsoum, J., and Fawell, S.E. (2001). Sequestration of adenoviral vector by Kupffer cells leads to a nonlinear dose response of transduction in liver. Mol. Ther. 3, 28-35.
36. van Beusechem, V.W., van Rijswijk, A.L., van Es, H.H., Haisma, H.J., Pinedo, H.M., and Gerritsen, W.R. (2000). Recombinant adenovirus vectors with knobless fibers for targeted gene transfer. Gene Ther. 7, 1940-1946.
37. Vellinga, J., Rabelink, M.J., Cramer, S.J., van den Wollenberg, D.J., van der Meulen, H., Leppard, K.N., Fallaux, F.J., and Hoeben, R.C. (2004). Spacers increase the accessibility of peptide ligands linked to the carboxyl terminus of adenovirus minor capsid protein IX. J. Virol. 78, 3470-3479.