Flexibility of the adenovirus fiber is required for efficient receptor interaction

Journal of Virology

Volumn 77, Issue 13, 2003, Pages 7225-7235

  Wu, Eugene ^a   Pache, Lars ^a,d   Von Seggern, Dan J ^a   Mullen, Tina Marie ^a   Mikyas, Yeshi ^b   Stewart, Phoebe L ^b,c   Nemerow, Glen R ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; CHIMERIC PROTEIN; GREEN FLUORESCENT PROTEIN; UNCLASSIFIED DRUG; VIRUS FIBER PROTEIN; VIRUS PROTEIN; VIRUS RECEPTOR;

ADENOVIRUS; ARTICLE; CELL SURFACE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; EYE INFECTION; GENE TARGETING; HUMAN; HUMAN CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN STRUCTURE; RECEPTOR BINDING; THREE DIMENSIONAL IMAGING; VIRUS ADSORPTION; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS INFECTIVITY;

ADENOVIRIDAE; AMINO ACID SEQUENCE; BASE SEQUENCE; BLOTTING, WESTERN; CRYOELECTRON MICROSCOPY; DNA PRIMERS; HUMANS; MOLECULAR SEQUENCE DATA; RECEPTORS, VIRUS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 0037663931     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.13.7225-7235.2003     Document Type: Article

References (51)

1. Adrian, M., J. Dubochet, J. Lepault, and A. W. McDowall. 1984. Cryoelectron microscopy of viruses. Nature 308:32-36.
2. Arnberg, N., K. Edlund, A. H. Kidd, and G. Wadell. 2000. Adenovirus type 37 uses sialic acid as a cellular receptor. J. Virol. 74:42-48.
3. Bai, M., B. Harfe, and P. Freimuth. 1993. Mutations that alter an Arg-Gly-Asp (RGD) sequence in the adenovirus type 2 penton base protein abolish its cell-rounding activity and delay virus reproduction in flat cells. J. Virol. 67:5198-5205.
4. Barton, E. S., J. C. Forrest, J. L. Connolly, J. D. Chappell, Y. Liu, F. J. Schnell, A. Nusrat, C. A. Parkos, and S. Dermody. 2001. Junction adhesion molecule is a receptor for reovirus. Cell 104:441-451.
5. Bergelson, J. M., J. A. Cunningham, G. Droguett, E. A. Kurt-Jones, A. Krithivas, J. S. Hong, M. S. Horwitz, R. L. Crowell, and R. W. Finberg. 1997. Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320-1323.
6. Bewley, M. C., K. Springer, and Y.-B. Zhang. 1999. Structural analysis of the mechanism of adenovirus binding to its human cellular receptor, CAR. Science 286:1579-1583.
7. Chappell, J. D., A. E. Prota, T. S. Dermody, and T. Stehle. 2002. Crystal structure of reovirus attachment protein σ1 reveals evolutionary relationship to adenovirus fiber. EMBO J. 21:1-11.
8. Chiu, C. Y., P. Mathias, N. R. Nemerow, and P. L. Stewart. 1999. Structure of adenovirus complexed with its internalization receptor. J. Virol. 73:6759-6768.
9. Chiu, C. Y., E. Wu, S. L. Brown, D. J. Von Seggern, G. R. Nemerow, and P. L. Stewart. 2001. Structural analysis of a fiber-pseudotyped adenovirus with ocular tropism suggests differential modes of cell receptor interactions. J. Virol. 75:5375-5380.
10. Chodosh, J., D. Miller, W. G. Stroop, and S. C. Pflugfelder. 1995. Adeno-virus epithelial keratitis. Cornea 14:167-174.
11. Chroboczek, J., R. W. H. Ruigrok, and S. Cusack. 1995. Adenovirus fiber. Curr. Top. Microbiol. Immunol. 199:163-200.
12. Cohen, C. J., J. T. Shieh, R. J. Pickles, T. Okegawa, J. T. Hsieh, and J. M. Bergelson. 2001. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc. Natl. Acad. Sci. USA 98:15191-15196.
13. DuBridge, R. B., P. Tang, H. C. Hsia, P.-M. Leong, J. H. Miller, and M. P. Calos. 1987. Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol. Cell. Biol. 7:379-387.
14. Einfeld, D. A., R. Schroeder, P. W. Roelvink, A. Lizonova, C. R. King, I. Kovesdi, and T. J. Wickham. 2001. Reducing the native tropism of adenovirus vectors requires removal of both CAR and integrin interactions. J. Virol. 75:11284-11291.
15. Gorziglia, M. I., M. J. Kadan, S. Yei, J. Lim, G. M. Lee, R. Luthra, and B. C. Trapnell. 1996. Elimination of both E1 and E2a from adenovirus vectors further improves prospects for in vivo human gene therapy. J. Virol. 70:4173-4178.
16. Greber, U. F., M. Willetts, P. Webster, and A. Helenius. 1993. Stepwise dismantling of adenovirus 2 during entry into cells. Cell 75:477-486.
17. He, Y., P. R. Chipman, J. Howitt, C. M. Bator, M. A. Whitt, T. S. Baker, R. J. Kuhn, C. W. Anderson, P. Freimuth, and M. G. Rossmann. 2001. Interaction of coxsackievirus B3 with the full length coxsackievirus-adenovirus receptor. Nature Struct. Biol. 8:874-878.
18. Horton, R. M., Z. L. Cai, S. N. Ho, and L. R. Pease. 1990. Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8:528-535.
19. Huang, S., V. Reddy, N. Dasgupta, and G. R. Nemerow. 1999. A single amino acid in the adenovirus type 37 fiber confers binding to human conjunctival cells. J. Virol. 73:2798-2802.
20. Jakubczak, J. L., M. L. Rollence, D. A. Stewart, J. D. Jafari, D. J. Von Seggern, G. R. Nemerow, S. C. Stevenson, and P. L. Hallenbeck. 2001. Adenovirus type 5 viral particles pseudotyped with mutagenized fiber proteins show diminished infectivity of coxsackie B-adenovirus receptor-bearing cells. J. Virol. 75:2972-2981.
21. Klein, D., B. Bugl, W. H. Gunzburg, and B. Salmons. 2000. Accurate estimation of transduction efficiency necessitates a multiplex real-time PCR. Gene Ther. 7:458-463.
22. Kostrewa, D., M. Brockhaus, A. D'Arcy, G. E. Dale, P. Nelboeck, G. Schmid, F. Mueller, G. Bazzoni, E. Dejana, T. Bartfai, F. K. Winkler, and M. Hennig. 2001. X-ray structure of junctional adhesion molecule: structural basis for homophilic adhesion via a novel dimerization motif. EMBO J. 20:4391-4398.
23. Kraulis, P. J. 1991. A program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24:946-950.
24. Liddington, R. C., and M. H. Ginsberg. 2002. Integrin activation takes shape. J. Cell Biol. 158:833-839.
25. Lu, G. 2000. TOP: a new method for protein structure comparisons and similarity searches. J. Appl. Cryst. 33:176-183.
26. Martin-Padura, I., S. Lostaglio, M. Schneemann, L. Williams, M. Romano, P. Fruscella, C. Panzeri, A. Stoppacciaro, L. Ruco, A. Villa, D. Simmons, and E. Dejana. 1998. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J. Cell Biol. 142:117-127.
27. Mathias, P., M. Galleno, and G. R. Nemerow. 1998. Interactions of soluble recombinant integrin αvβ5 with human adenoviruses. J. Virol. 72:8669-8675.
28. Roelvink, P. W., G. M. Lee, D. A. Einfeld, I. Kovesdi, and T. J. Wickham. 1999. Identification of a conserved receptor-binding site on the fiber proteins of CAR-recognizing adenoviridae. Science 286:1568-1571.
29. Roelvink, P. W., A. Lizonova, J. G. M. Lee, Y. Li, J. M. Bergelson, R. W. Finberg, D. E. Brough, I. Kovesdi, and T. J. Wickham. 1998. The coxsackievirus-adenovirus receptor protein can function as a cellular attachment protein for adenovirus serotypes from subgroups A, C, D, E, and F. J. Virol. 72:7909-7915.
30. Ruigrok, R. W. H., A. Barge, C. Albiges-Rizo, and S. Dayan. 1990. Structure of adenovirus fibre: II morphology of single fibres. J. Mol. Biol. 215:589-596.
31. Shah, A. K., and P. L. Stewart. 1998. Qview: software for rapid selection of particles from digital electron micrographs. J. Struct. Biol. 123:17-21.
32. Shayakhmetov, D. M., and A. Lieber. 2000. Dependence of adenovirus infectivity on length of the fiber shaft domain. J. Virol. 74:10274-10286.
33. Shimaoka, M., J. Takagi, and T. A. Springer. 2002. Conformational regulation of integrin structure and function. Annu. Rev. Biophys. Biomol. Struct. 31:485-516.
34. Smith, T., N. Idamakanti, H. Kylefjord, M. Rollence, L. King, M. Kaloss, M. Kaleko, and S. C. Stevenson. 2002. In vivo hepatic adenoviral gene delivery occurs independently of the coxsackievirus-adenovirus receptor. Mol. Ther. 5:770-775.
35. Stewart, P. L., R. M. Burnett, M. Cyrklaff, and S. D. Fuller. 1991. Image reconstruction reveals the complex molecular organization of adenovirus. Cell 67:145-154.
36. Stewart, P. L., R. B. Cary, S. R. Peterson, and C. Y. Chiu. 2000. Digitally collected cryo-electron micrographs for single particle reconstruction. Microsc. Res. Tech. 49:224-232.
37. Stewart, P. L., C. Y. Chiu, S. Huang, T. Muir, Y. Zhao, B. Chait, P. Mathias, and G. R. Nemerow. 1997. Cryo-EM visualization of an exposed RGD epitope on adenovirus that escapes antibody neutralization. EMBO J. 16:1189-1198.
38. Takagi, J., B. Petre, T. Walz, and T. Springer. 2002. Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell 110:599-611.
39. Tomko, R. P., R. Xu, and L. Philipson. 1997. HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc. Natl. Acad. Sci. USA 94:3352-3356.
40. van Heel, M., G. Harauz, E. V. Orlova, R. Schmidt, and M. Schatz. 1996. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116:17-24.
41. van Raaij, M. J., E. Chouin, H. van der Zandt, J. M. Bergelson, and S. Cusack. 2000. Dimeric structure of the coxsackievirus and adenovirus receptor D1 domain at 1.7 Å resolution. Structure 8:1147-1155.
42. van Raaij, M. J., A. Mitraki, G. Lavigne, and S. Cusack. 1999. A triple β-spiral in the adenovirus fibre shaft reveals a new structural motif for a fibrous protein. Nature 401:935-938.
43. Von Seggern, D. J., C. Y. Chiu, S. K. Fleck, P. L. Stewart, and G. R. Nemerow. 1999. A helper-independent adenovirus vector with E1, E3, and fiber deleted: structure and infectivity of fiberless particles. J. Virol. 73:1601-1608.
44. Von Seggern, D. J., S. Huang, S. K. Fleck, S. C. Stevenson, and G. R. Nemerow. 2000. Adenovirus vector pseudotyping in fiber-expressing cell lines: improved transduction of Epstein-Barr virus-transformed B cells. J. Virol. 74:354-362.
45. Walters, R. W., P. Freimuth, T. O. Moninger, I. Ganske, J. Zabner, and M. J. Welsh. 2002. Adenovirus fiber disrupts CAR-mediated intercellular adhesion allowing virus escape. Cell 110:789-799.
46. Wickham, T. J., E. J. Filardo, D. A. Cheresh, and G. R. Nemerow. 1994. Integrin αvβ5 selectively promotes adenovirus mediated cell membrane permeabilization. J. Cell Biol. 127:257-264.
47. 5 promote adenovirus internalization but not virus attachment. Cell 73:309-319.
48. Williams, L. A., I. Martin-Padura, E. Dejana, N. Hogg, and D. L. Simmons. 1999. Identification and characterisation of human junctional adhesion molecule (JAM). Mol. Immunol. 36:1175-1188.
49. Wu, E., J. Fernandez, S. K. Fleck, D. J. Von Seggern, S. Huang, and G. R. Nemerow. 2001. A 50 kDa membrane protein mediates sialic acid-independent binding and infection of conjunctival cells by adenovirus type 37. Virology 279:78-89.
50. Xia, D., L. J. Henry, R. D. Gerard, and J. Deisenhofer. 1994. Crystal structure of the receptor-binding domain of adenovirus type 5 fiber protein at 1.7 Å resolution. Structure 2:1259-1270.
51. vβ3. Science 294:339-345.