Adenovirus dodecahedron cell attachment and entry are mediated by heparan sulfate and integrins and vary along the cell cycle

Virology

Volumn 371, Issue 1, 2008, Pages 155-164

  Fender, Pascal ^a   Schoehn, Guy ^b   Perron Sierra, Françoise ^c   Tucker, Gordon C ^c   Lortat Jacob, Hugues ^a  

^a CEA GRENOBLE   (France)

^b CNRS   (France)

^c INSTITUT DE RECHERCHES SERVIER   (France)

Author keywords

Adenovirus; Cell cycle; Dodecahedron; Entry; Heparan sulfate proteoglycan; Integrin; Mitosis; Receptor

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; CALCIUM; INTEGRIN; MANGANESE; NANOPARTICLE; PROTEOHEPARAN SULFATE;

ADENOVIRUS; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL CYCLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; INTERNALIZATION; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS ATTACHMENT;

ADENOVIRUSES, HUMAN; ANIMALS; CAPSID PROTEINS; CELL ADHESION; CELL CYCLE; CHO CELLS; CRICETINAE; CRICETULUS; HELA CELLS; HEPARIN; HUMANS; INTEGRINS; PROTEOGLYCANS;

ADENOVIRIDAE; HUMAN ADENOVIRUS;

EID: 37849018277     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.09.026     Document Type: Article

References (48)

1. Anilkumar N., Bhattacharya A.K., Manogaran P.S., and Pande G. Modulation of alpha 5 beta 1 and alpha V beta 3 integrins on the cell surface during mitosis. J. Cell. Biochem. 61 3 (1996) 338-349
2. Asokan A., Hamra J.B., Govindasamy L., Agbandje-McKenna M., and Samulski R.J. Adeno-associated virus type 2 contains an integrin alpha5beta1 binding domain essential for viral cell entry. J. Virol. 80 18 (2006) 8961-8969
3. Belin M.T., and Boulanger P. Involvement of cellular adhesion sequences in the attachment of adenovirus to the HeLa cell surface. J. Gen. Virol. 74 Pt 8 (1993) 1485-1497
4. 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 5304 (1997) 1320-1323
5. Berinstein A., Roivainen M., Hovi T., Mason P.W., and Baxt B. Antibodies to the vitronectin receptor (integrin alpha V beta 3) inhibit binding and infection of foot-and-mouth disease virus to cultured cells. J. Virol. 69 4 (1995) 2664-2666
6. Byrnes A.P., and Griffin D.E. Binding of Sindbis virus to cell surface heparan sulfate. J. Virol. 72 9 (1998) 7349-7356
7. Cardin A.D., and Weintraub H.J. Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis 9 1 (1989) 21-32
8. Chen Y., Maguire T., Hileman R.E., Fromm J.R., Esko J.D., Linhardt R.J., and Marks R.M. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 3 8 (1997) 866-871
9. Dechecchi M.C., Tamanini A., Bonizzato A., and Cabrini G. Heparan sulfate glycosaminoglycans are involved in adenovirus type 5 and 2-host cell interactions. Virology 268 2 (2000) 382-390
10. Dechecchi M.C., Melotti P., Bonizzato A., Santacatterina M., Chilosi M., and Cabrini G. Heparan sulfate glycosaminoglycans are receptors sufficient to mediate the initial binding of adenovirus types 2 and 5. J. Virol. 75 18 (2001) 8772-8780
11. Dransfield I., Cabanas C., Craig A., and Hogg N. Divalent cation regulation of the function of the leukocyte integrin LFA-1. J. Cell Biol. 116 1 (1992) 219-226
12. Fender P., Ruigrok R.W., Gout E., Buffet S., and Chroboczek J. Adenovirus dodecahedron, a new vector for human gene transfer. Nat. Biotechnol. 15 1 (1997) 52-56
13. Fender P., Schoehn G., Foucaud-Gamen J., Gout E., Garcel A., Drouet E., and Chroboczek J. Adenovirus dodecahedron allows large multimeric protein transduction in human cells. J. Virol. 77 8 (2003) 4960-4964
14. Fender P., Boussaid A., Mezin P., and Chroboczek J. Synthesis, cellular localization, and quantification of penton-dodecahedron in serotype 3 adenovirus-infected cells. Virology 340 2 (2005) 167-173
15. Fry E.E., Lea S.M., Jackson T., Newman J.W., Ellard F.M., Blakemore W.E., Abu-Ghazaleh R., Samuel A., King A.M., and Stuart D.I. The structure and function of a foot-and-mouth disease virus-oligosaccharide receptor complex. EMBO J. 18 3 (1999) 543-554
16. Fuschiotti P., Fender P., Schoehn G., and Conway J.F. Development of the dodecahedral penton particle from adenovirus 3 for therapeutic application. J. Gen. Virol. 87 Pt 10 (2006) 2901-2905
17. Fuschiotti P., Schoehn G., Fender P., Fabry C.M., Hewat E.A., Chroboczek J., Ruigrok R.W., and Conway J.F. Structure of the dodecahedral penton particle from human adenovirus type 3. J. Mol. Biol. 356 2 (2006) 510-520
18. Garcel A., Gout E., Timmins J., Chroboczek J., and Fender P. Protein transduction into human cells by adenovirus dodecahedron using WW domains as universal adaptors. J. Gene Med. 8 4 (2006) 524-531
19. Germi R., Crance J.M., Garin D., Guimet J., Lortat-Jacob H., Ruigrok R.W., Zarski J.P., and Drouet E. Cellular glycosaminoglycans and low density lipoprotein receptor are involved in hepatitis C virus adsorption. J. Med. Virol. 68 2 (2002) 206-215
20. Glotzer M. Animal cell cytokinesis. Annu. Rev. Cell Dev. Biol. 17 (2001) 351-386
21. Hynes R.O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69 1 (1992) 11-25
22. Jackson T., Ellard F.M., Ghazaleh R.A., Brookes S.M., Blakemore W.E., Corteyn A.H., Stuart D.I., Newman J.W., and King A.M. Efficient infection of cells in culture by type O foot-and-mouth disease virus requires binding to cell surface heparan sulfate. J. Virol. 70 8 (1996) 5282-5287
23. Kern A., Schmidt K., Leder C., Muller O.J., Wobus C.E., Bettinger K., Von der Lieth C.W., King J.A., and Kleinschmidt J.A. Identification of a heparin-binding motif on adeno-associated virus type 2 capsids. J. Virol. 77 20 (2003) 11072-11081
24. Lee J.O., Bankston L.A., Arnaout M.A., and Liddington R.C. Two conformations of the integrin A-domain (I-domain): a pathway for activation?. Structure 3 12 (1995) 1333-1340
25. Lindahl U., Kusche-Gullberg M., and Kjellen L. Regulated diversity of heparan sulfate. J. Biol. Chem. 273 39 (1998) 24979-24982
26. Maddox A.S., and Burridge K. RhoA is required for cortical retraction and rigidity during mitotic cell rounding. J. Cell Biol. 160 2 (2003) 255-265
27. Mathias P., Galleno M., and Nemerow G.R. Interactions of soluble recombinant integrin alphav beta5 with human adenoviruses. J. Virol. 72 11 (1998) 8669-8675
28. Mould A.P. Getting integrins into shape: recent insights into how integrin activity is regulated by conformational changes. J. Cell Sci. 109 Pt 11 (1996) 2613-2618
29. 2+. J. Biol. Chem. 270 44 (1995) 26270-26277
30. Nemerow G.R., and Stewart P.L. Role of alpha(v) integrins in adenovirus cell entry and gene delivery. Microbiol. Mol. Biol. Rev. 63 3 (1999) 725-734
31. Perron-Sierra F., Saint Dizier D., Bertrand M., Genton A., Tucker G.C., and Casara P. Substituted benzocyloheptenes as potent and selective alpha(v) integrin antagonists. Bioorg. Med. Chem. Lett. 12 22 (2002) 3291-3296
32. Rentsendorj A., Xie J., MacVeigh M., Agadjanian H., Bass S., Kim D.H., Rossi J., Hamm-Alvarez S.F., and Medina-Kauwe L.K. Typical and atypical trafficking pathways of Ad5 penton base recombinant protein: implications for gene transfer. Gene Ther. 13 10 (2006) 821-836
33. Schoehn G., Fender P., Chroboczek J., and Hewat E.A. Adenovirus 3 penton dodecahedron exhibits structural changes of the base on fibre binding. EMBO J. 15 24 (1996) 6841-6846
34. Seidman M.A., Hogan S.M., Wendland R.L., Worgall S., Crystal R.G., and Leopold P.L. Variation in adenovirus receptor expression and adenovirus vector-mediated transgene expression at defined stages of the cell cycle. Mol. Ther. 4 1 (2001) 13-21
35. Shukla D., and Spear P.G. Herpesviruses and heparan sulfate: an intimate relationship in aid of viral entry. J. Clin. Invest. 108 4 (2001) 503-510
36. Smith J.W., Piotrowicz R.S., and Mathis D. A mechanism for divalent cation regulation of beta 3-integrins. J. Biol. Chem. 269 2 (1994) 960-967
37. Stewart P.L., Chiu C.Y., Huang S., Muir T., Zhao Y., Chait B., Mathias P., and Nemerow G.R. Cryo-EM visualization of an exposed RGD epitope on adenovirus that escapes antibody neutralization. EMBO J. 16 6 (1997) 1189-1198
38. Summerford C., and Samulski R.J. Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J. Virol. 72 2 (1998) 1438-1445
39. Summerford C., Bartlett J.S., and Samulski R.J. AlphaVbeta5 integrin: a co-receptor for adeno-associated virus type 2 infection. Nat. Med. 5 1 (1999) 78-82
40. Suomalainen M., Nakano M.Y., Keller S., Boucke K., Stidwill R.P., and Greber U.F. Microtubule-dependent plus- and minus end-directed motilities are competing processes for nuclear targeting of adenovirus. J. Cell Biol. 144 4 (1999) 657-672
41. Veiga S.S., Elias M., Gremski W., Porcionatto M.A., da Silva R., Nader H.B., and Brentani R.R. Post-translational modifications of alpha5beta1 integrin by glycosaminoglycan chains. The alpha5beta1 integrin is a facultative proteoglycan. J. Biol. Chem. 272 19 (1997) 12529-12535
42. Vives R.R., Lortat-Jacob H., Chroboczek J., and Fender P. Heparan sulfate proteoglycan mediates the selective attachment and internalization of serotype 3 human adenovirus dodecahedron. Virology 321 2 (2004) 332-340
43. Vives R.R., Lortat-Jacob H., and Fender P. Heparan sulphate proteoglycans and viral vectors: ally or foe?. Curr. Gene Ther. 6 1 (2006) 35-44
44. Wang K., Huang S., Kapoor-Munshi A., and Nemerow G. Adenovirus internalization and infection require dynamin. J. Virol. 72 4 (1998) 3455-3458
45. White J.M. Integrins as virus receptors. Curr. Biol. 3 9 (1993) 596-599
46. Wickham T.J., Mathias P., Cheresh D.A., and Nemerow G.R. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 73 2 (1993) 309-319
47. Xiong J.P., Stehle T., Zhang R., Joachimiak A., Frech M., Goodman S.L., and Arnaout M.A. Crystal structure of the extracellular segment of integrin alpha Vbeta3 in complex with an Arg-Gly-Asp ligand. Science 296 5565 (2002) 151-155
48. Yanagishita M., and Hascall V.C. Cell surface heparan sulfate proteoglycans. J. Biol. Chem. 267 14 (1992) 9451-9454