Adenovirus Serotype 5 Hexon Mediates Liver Gene Transfer

Cell

Volumn 132, Issue 3, 2008, Pages 397-409

  Waddington, Simon N ^a   McVey, John H ^b   Bhella, David ^c   Parker, Alan L ^d   Barker, Kristeen ^d   Atoda, Hideko ^e   Pink, Rebecca ^c   Buckley, Suzanne M K ^a   Greig, Jenny A ^d   Denby, Laura ^d   Custers, Jerome ^f   Morita, Takashi ^e   Francischetti, Ivo M B ^g   Monteiro, Robson Q ^h   Barouch, Dan H ⁱ   van Rooijen, Nico ^j   Napoli, Claudio ^k,l   Havenga, Menzo J E ^f   Nicklin, Stuart A ^d   Baker, Andrew H ^d  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b MRC CLINICAL SCIENCES CENTRE   (United Kingdom)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e MEIJI PHARMACEUTICAL UNIVERSITY   (Japan)

^f CRUCELL HOLLAND BV   (Netherlands)

^g NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^h FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

ⁱ HARVARD MEDICAL SCHOOL   (United States)

^j VU UNIVERSITY AMSTERDAM   (Netherlands)

^k UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^l Temple University   (United States)

more..

Author keywords

HUMDISEASE; MICROBIO

Indexed keywords

BLOOD CLOTTING FACTOR 9; BLOOD CLOTTING INHIBITOR; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; HEXAMETHONIUM; IXOLARIS; NEMATODE ANTICOAGULANT PEPTIDE 2; UNCLASSIFIED DRUG; WARFARIN;

ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; DRUG INHIBITION; DRUG MECHANISM; GENE TRANSFER; HUMAN; HUMAN CELL; LIVER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; SEROTYPE;

ADENOVIRIDAE; COXSACKIEVIRUS; HUMAN ADENOVIRUS;

EID: 38849134279     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2008.01.016     Document Type: Article

References (55)

1. Abbink P., Lemckert A.A.C., Ewald B.A., Lynch D.M., Denholtz M., Smits S., Holterman L., Damen I., Vogels R., Thorner A.R., et al. Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from Subgroups B and D. J. Virol. 81 (2007) 4654-4663
2. Adrian M., Dubochet J., Lepault J., and McDowall A. Cryo-electron microscopy of viruses. Nature 308 (1984) 32-36
3. Alemany R., and Curiel D.T. CAR-binding ablation does not change biodistribution and toxicity of adenoviral vectors. Gene Ther. 8 (2001) 1347-1353
4. Athappilly F., Murali R., Rux J., Cai Z., and Burnett R. The refined crystal structure of hexon, the major coat protein of adenovirus type 2, at 29 A resolution. J. Mol. Biol. 242 (1995) 430-455
5. Atoda H., Ishikawa M., Mizuno H., and Morita T. Coagulation factor X-binding protein from Deinagkistrodon acutus venom is a gla domain-binding protein. Biochemistry 37 (1998) 17361-17370
6. Baker T.S., and Cheng R. A model-based approach for determining orientations of biological macromolecules imaged by cryoelectron microscopy. J. Struct. Biol. 116 (1996) 120-130
7. Bayo-Puxan N., Cascallo M., Gros A., Huch M., Fillat C., and Alemany R. Role of the putative heparan sulfate glycosaminoglycan-binding site of the adenovirus type 5 fiber shaft on liver detargeting and knob-mediated retargeting. J. Gen. Virol. 87 (2006) 2487-2495
8. Bergelson J.M., Cunningham J.A., Droguett G., Kurt-Jones E.A., Krithivas A., Hong J.S., Horwitz M.S., Crowell R.L., and Finberg R.W. Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275 (1997) 1320-1323
9. Bubeck D., Filman D., Cheng N., Steven A., Hogle J., and Belnap D. The structure of the poliovirus 135S cell entry intermediate at 10-angstrom resolution reveals the location of an externalized polypeptide that binds to membranes. J. Virol. 79 (2005) 7745-7755
10. Conway J., and Steven A. Methods for reconstructing density maps of "single" particles from cryoelectron micrographs to subnanometer resolution. J. Struct. Biol. 128 (1999) 106-118
11. Crowther R., Amos L., Finch J., De Rosier D., and Klug A. Three dimensional reconstructions of spherical viruses by fourier synthesis from electron micrographs. Nature 226 (1970) 421-425
12. Fuller S., Butcher S., Cheng R., and Baker T.S. Three-dimensional reconstruction of icosahedral particles-the uncommon line. J. Struct. Biol. 116 (1996) 48-55
13. Gaggar A., Shayakhmetov D.M., and Lieber A. CD46 is a cellular receptor for group B adenoviruses. Nat. Med. 9 (2003) 1408-1412
14. Heymann J. Bsoft: image and molecular processing in electron microscopy. J. Struct. Biol. 133 (2001) 156-169
15. Hiltunen M.O., Turunen M.P., Turunen A.-M., Rissanen T.T., Laitinen M., Kosma V.-M., and Yla-Herttuala S. Biodistribution of adenoviral vector to nontarget tissues after local in vivo gene transfer to arterial wall using intravascular and periadventitial gene delivery methods. FASEB J. 14 (2000) 2230-2236
16. Huard J., Lochmuller H., Ascadi G., Jani A., Massie B., and Karpati G. The route of administration is a major determinant of the transduction efficiency of rat tissues by adenoviral recombinants. Gene Ther. 107 (1995) 107-115
17. Kawabata K., Sakurai F., Koizumi N., Hayakawa T., and Mizuguchi H. Adenovirus vector-mediated gene transfer into stem cells. Mol. Pharm. 3 (2006) 95-103
18. v integrin, and heparan sulphate binding reduce in vivo tissue transduction and toxicity. Hum. Gene Ther. 17 (2006) 264-279
19. Kritz A., Nicol C., Dishart K., Nelson R., Holbeck S., Von Seggern D., Work L., McVey J., Nicklin S., and Baker A. Adenovirus 5 fibers mutated at the KKTK putative HSPG binding site show restricted retargeting capacity when engineered with targeting peptides in the HI loop. Mol. Ther. 15 (2007) 741-749
20. Lecollinet S., Gavard F., Havenga M.J.E., Spiller O.B., Lemckert A., Goudsmit J., Eloit M., and Richardson J. Improved gene delivery to intestinal mucosa by adenoviral vectors bearing subgroup B and D fibers. J. Virol. 80 (2006) 2747-2759
21. Li J., Lad S., Yang G., Luo Y., Iacobelli-Martinez M., Primus F.J., Reisfeld R.A., and Li E. Adenovirus fiber shaft contains a trimerization element that supports peptide fusion for targeted gene delivery. J. Virol. 80 (2006) 12324-12331
22. Madisch I., Harste G., Pommer H., and Heim A. Phylogenetic analysis of the main neutralization and hemagglutination determinants of all human adenovirus prototypes as a basis for molecular classification and taxonomy. J. Virol. 79 (2005) 15265-15276
23. v integrin-binding ablation fails to reduce Ad5 liver tropism. Mol. Ther. 8 (2003) 485-494
24. Monteiro R., Rezaie A., Ribeiro J., and Francishetti I. Ixolaris: a factor Xa heparin-binding exosite inhibitor. Biochem. J. 387 (2005) 871-877
25. Murakami M.T., Rios-Steiner J., Weaver S.E., Tulinsky A., Geiger J.H., and Arni R.K. Intermolecular interactions and characterization of the novel factor Xa exosite involved in macromolecular recognition and inhibition: Crystal structure of human Gla-domainless factor Xa complexed with the anticoagulant protein NAPc2 from the hematophagous nematode Ancylostoma caninum. J. Mol. Biol. 366 (2007) 602-610
26. Nicklin S., Wu E., Nemerow G., and Baker A. The influence of adenovirus fiber structure and function on vector development for gene therapy. Mol. Ther. 12 (2005) 384-393
27. Nicol C.G., Graham D., Miller W.H., White S.J., Smith T.A., Nicklin S.A., Stevenson S.C., and Baker A.H. Effect of adenovirus serotype 5 fiber and penton modifications on in vivo tropism in rats. Mol. Ther. 10 (2004) 344-354
28. Oldstone M., Lewicki H., Thomas D., Tishon A., Dales S., Patterson J., Manchester M., Homann D., Naniche D., and Holz A. Measles virus infection in a trasgenic model: virus-induced immunosuppression and central nervous system disease. Cell 98 (1999) 629-640
29. 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., et al. Multiple vitamin K-dependent coagulation zymogens promote adenovirus-mediated gene delivery to hepatocytes. Blood 108 (2006) 2554-2561
30. Parker A.L., McVey J.H., Doctor J.H., Lopez-Franco O., Waddington S.N., Havenga M.J.E., Nicklin S.A., and Baker A.H. Influence of coagulation factor zymogens on the infectivity of adenoviruses pseudotyped with fibers from subgroup D. J. Virol. 81 (2007) 3627-3631
31. Pettersen E., Goddard T., Huang C., Couch G., Greenblatt D., Meng E., and Ferrin T. UCSF chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612
32. Pichla-Gollon S.L., Drinker M., Zhou X., Xue F., Rux J.J., Gao G.-P., Wilson J.M., Ertl H.C., Burnett R.M., and Bergelson J.M. Structure-based identification of a major neutralizing site in an adenovirus hexon. J. Virol. 81 (2007) 1680-1689
33. Raper S.E., Chirmule N., Lee F.S., Wivel N.A., Bagg A., Gao G.-P., Wilson J.M., and Batshaw M.L. Fatal systemic inflammatory response syndrome in a ornithine transcarbamylase deficient patient following adenoviral gene transfer. Mol. Genet. Metab. 80 (2003) 148-158
34. Rezaie A.R. Identification of basic residues in the heparin-binding exosite of factor Xa critical for heparin and factor Va binding. J. Biol. Chem. 275 (2000) 3320-3327
35. Roberts D., Nanda A., Havenga M., Abbink P., Lynch D., Ewald B., Liu J., Thorner A., Swanson P., Gorgone D., et al. Hexon-chimaeric adenovirus serotype 5 vectors circumvent pre-existing anti-vector immunity. Nature 441 (2006) 239-243
36. Roberts M., White J., Grutter M., and Burnett R. Three-dimensional structure of the adenovirus major coat protein hexon. Science 232 (1986) 1148-1151
37. Rux J., and Burnett R. Type-specific epitope locations revealed by X-ray crystallographic study of adenovirus type 5 hexon. Mol. Ther. 1 (2000) 18-30
38. Rux J.J., Pascolini D., and Burnett R.M. Large-scale purification and crystallization of adenovirus hexon. In: Wold W.S.M. (Ed). Methods in Molecular Medicine, Vol 21: Adenovirus Methods and Protocols (1999), Humana Press Inc., Totowa NJ 259-275
39. Sakurai F., Kawabata K., Koizumi N., Inoue N., Okabe M., Yamaguchi T., Hayakawa T., and Mizuguchi H. Adenovirus serotype 35 vector-mediated transduction into human CD46-transgenic mice. Gene Ther. 13 (2006) 1118-1126
40. San Martin C., and Burnett R. Structural studies on adenoviruses. Curr. Top. Microbiol. Immunol. 272 (2003) 57-94
41. Segerman A., Atkinson J.P., Marttila M., Dennerquist V., Wadell G., and Arnberg N. Adenovirus type 11 uses CD46 as a cellular receptor. J. Virol. 77 (2003) 9183-9191
42. Shayakhmetov D.M., Papayannopoulou T., Stamatoyannopoulos G., and Lieber A. Efficient gene transfer into human CD34+ cells by a retargeted adenovirus vector. J. Virol. 74 (2000) 2567-2583
43. Shayakhmetov D., Li Z., Ni S., and Lieber A. Targeting of adenovirus vectors to tumor cells does not enable efficient transduction of breast cancer metastases. Cancer Res. 62 (2002) 1063-1068
44. Shayakhmetov D., Gaggar A., Ni S., Li Z.-Y., and Lieber A. Adenovirus binding to blood factors results in liver cell infection and hepatotoxicity. J. Virol. 79 (2005) 7478-7491
45. Schenk-Braat E.A.M., van Mierlo M.M.K.B., Wagemaker G., Bangma C.H., and Kaptein L.C.M. An inventory of shedding data from clinical gene therapy trials. J. Gene Med. 9 (2007) 910-921
46. Smith T.A.G., Idamakanti N., Marshall-Neff J., Rollence M.L., Wright P., Kaloss M., King L., Mech C., Dinges L., Iverson W.O., et al. Receptor interactions involved in adenoviral-mediated gene delivery after systemic administration in non-human primates. Hum. Gene Ther. 14 (2003) 1595-1604
47. Sumida S.M., Truitt D.M., Lemckert A.A.C., Vogels R., Custers J.H.H.V., Addo M.M., Lockman S., Peter T., Peyerl F.W., Kishko M.G., et al. Neutralizing antibodies to adenovirus serotype 5 vaccine vectors are directed primarily against the adenovirus hexon protein. J. Immunol. 174 (2005) 7179-7185
48. Tomko R.P., Xu R., and Philipson L. HCAR and MCAR: The human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc. Natl. Acad. Sci. USA 94 (1997) 3352-3356
49. Tuve S., Wang H., Ware C., Liu Y., Gaggar A., Bernt K., Shayakhmetov D., Li Z., Strauss R., Stone D., and Lieber A. A new group B adenovirus receptor is expressed at high levels on human stem and tumor cells. J. Virol. 80 (2006) 12109-12120
50. Van Rooijen N., and Sanders A. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J. Immunol. Methods 174 (1994) 83-93
51. Venkateswarlu D., Perera L., Darden T., and Pedersen L. Structure and dynamics of zymogen human blood coagulation factor X. Biophys. J. 82 (2002) 1190-1206
52. Vogels R., Zuijeest D., Rijnsoever R.V., Hartkoorn E., Damen I., Bethune M.-P.D., Kostense S., Penders G., Helmus N., Koudstaal W., et al. Replication-deficient human adenovirus type 35 vectors for gene transfer and vaccination: efficient human cell infection and bypass of preexisting adenovirus immunity. J. Virol. 77 (2003) 8263-8271
53. Von Seggern D.J., Chiu C.Y., Fleck S.K., Stewart P.L., and Nemerow G.R. A helper-independent adenovirus vector with E1, E3 and fiber deleted: Structure and infectivity of fiberless particles. J. Virol. 73 (1999) 1601-1608
54. Waddington S., Parker A., Havenga M., Nicklin S., Buckley S., McVey J., and Baker A. Targeting of adenovirus serotype 5 (Ad5) and 5/47 pseudotyped vectors in vivo: A fundamental involvement of coagulation factors and redundancy of CAR binding by Ad5. J. Virol. 81 (2007) 9568-9571
55. 5 promote adenovirus internalization but not virus attachment. Cell 73 (1993) 309-319