The epithelial integrin αvβ6 is a receptor for foot-and-mouth disease virus

Journal of Virology

Volumn 74, Issue 11, 2000, Pages 4949-4956

  Jackson, Terry ^a   Sheppard, Dean ^a   Denyer, Michael ^b   Blakemore, Wendy ^a   King, Andrew M Q ^a  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; INTEGRIN; MONOCLONAL ANTIBODY; VIRUS RECEPTOR; ALPHAVBETA6 INTEGRIN; ARGINYL-GLYCYL-ASPARTIC ACID; CAPSID PROTEIN; OLIGOPEPTIDE; TUMOR ANTIGEN; VP1 PROTEIN, FOOT AND MOUTH DISEASE VIRUS; VP1 PROTEIN, FOOT-AND-MOUTH DISEASE VIRUS;

ANIMAL CELL; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ARTICLE; CARCINOMA CELL; CELL STRAIN BHK; CELL SURFACE; COLON CARCINOMA; CONTROLLED STUDY; EPITHELIUM CELL; FOOT AND MOUTH DISEASE VIRUS; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INFECTION SENSITIVITY; NONHUMAN; PRIORITY JOURNAL; VIRUS ADSORPTION; VIRUS CELL INTERACTION; ANIMAL; APHTHOVIRUS; CELL CULTURE; CELL LINE; GENETICS; HAMSTER; METABOLISM; VIRUS CAPSID;

ANIMALS; ANTIGENS, NEOPLASM; APHTHOVIRUS; CAPSID; CAPSID PROTEINS; CELL LINE; CRICETINAE; EPITHELIAL CELLS; HUMANS; INTEGRINS; OLIGOPEPTIDES; RECEPTORS, VIRUS; TUMOR CELLS, CULTURED;

EID: 0033625053     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.11.4949-4956.2000     Document Type: Article

References (49)

1. Acharya, R., E. Fry, D. Stuart, G. Fox, D. Rowlands, and F. Brown. 1989. The three-dimensional structure of foot-and-mouth disease virus at 2.9Å resolution. Nature 337:709-716.
2. Agrez, M., A. Chen, R. I. Cone, R. Pytela, and D. Sheppard. 1994. The αvβ6 integrin promotes proliferation of colon carcinoma cells through a unique region of the β6 cytoplasmic domain. J. Cell. Biol. 127:545-556.
3. Agrez, M., D. R. Shafren, X. Gu, K. Cox, D. Sheppard, and R. D. Barry. 1997. Integrin αvβ6 enhances coxsackievirus Bl lytic infection of human colon carcinoma cells. Virology 239:71-77.
4. Baranowski, E., N. Sevilla, N. Verdaguer, C. M. Ruiz-Jarabo, E. Beck, and E. Domingo. 1998 Multiple virulence determinants of foot-and-mouth disease virus in cell culture. J. Virol. 72:6362-6372.
5. Belsham, G. J. 1993. Distinctive features of foot-and-mouth disease virus, a member of the picornavirus family: aspects of virus protein synthesis, protein processing and structure. Prog. Biophys. Mol. Biol. 69:241-260.
6. Berinstein, A., M. Roivainen, T. Hovi, P. W. Mason, and B. Baxt. 1995. Antibodies to the vitronectin receptor (integrin αvβ3) inhibit binding and infection of foot-and-mouth disease virus to cultured cells. J. Virol. 69:2664-2666.
7. Blystone, S. D., S. E. Slater, M. P. Williams, M. T. Crow, and E. Brown. 1999. A molecular mechanism of integrin crosstalk: αvβ3 suppression of calcium/ calmodulin-dependent protein kinase II regulates α5β1 function. J. Cell. Biol. 145:889-897.
8. Bretscher, M. S. 1992. Circulating integrins: α5β1, α6β4 and Mac-1, but not α3β1, α4β1 or LFA-1. EMBO J. 11:405-410.
9. Breuss, J. M., J. Gallo, H. M. DeLisser, I. V. Kilmanskaya, H. G. Folkesson, J. F. Pittet, S. L. Nishimura, K. Aldape, D. V. Landers, W. Carpenter, N. Gillett, D. Sheppard, M. A. Matthay, S. M. Albelda, R. H. Krammer, and R. Pytela. 1995. Expression of the β6 integrin subunit in development, neoplasia and tissue repair suggests a role in epithelial remodelling. J. Cell Sci. 108:2241-2251.
10. Breuss, J. M., N. Gillett, L. Lu, D. Sheppard, and R. Pytela. 1993. Restricted distribution of integrin β6 messenger RNA in primate epithelial tissues. J. Histochem. Cytochem. 41:1521-1527.
11. Brown, C. C., R. F. Meyer, H. J. Olander, C. House, and C. A. Mebus. 1992. A pathogenesis study of foot-and-mouth disease virus in cattle, using in situ hybridisation. Can. J. Vet. Res. 56:189-193.
12. Brown, C. C., H. J. Olander, and R. F. Meyer. 1991. A preliminary study of the pathogenesis of foot-and-mouth disease virus, using in situ hybridisation. Vet. Pathol. 28:216-222.
13. Burrows, R., J. A. Mann, A. J. M. Garland, A. Greig, and D. Goodridge. 1981. The pathogenesis of natural and stimulated natural foot-and-mouth disease virus infection in cattle. J. Comp. Pathol. 91:599-609.
14. Curry, S., E. Fry, W. E. Blakemore, R. Abu-Ghazaleh, T. Jackson, A. King, S. Lea, J. Newman, D. Rowlands, and D. Stuart. 1996. Perturbations in the surface structure of A22 Iraq foot-and-mouth disease virus accompanying coupled changes in host cell specificity and antigenicity. Structure 4:135-145.
15. Damjanovich, L., S. M. Albelda, S. A. Mette, and C. A. Buck. 1992 Distribution of integrin cell adhesion receptors in normal and malignant lung tissue. Am. J. Respir. Cell Mol. Biol. 6:197-206.
16. Dedhar, S., and G. E. Hannigan. 1996. Integrin cytoplasmic interactions and bidirectional transmembrane signalling. Curr. Opin. Cell Biol. 8:657-669.
17. Finnemann, S., and E. Rodriguez-Boulan. 1999. Macrophage and retinal pigment epithelium phagocytosis: apoptolic and photoreceptor compete for αvβ3 and αvβ5 integrins, protein kinase C regulates αvβ5 binding and cytoskeletal linkage. J. Exp. Med. 190:861-874.
18. Fry, E., S. M. Lea, T. Jackson, J. W. I. Newman, F. M. Ellard, W. E. Blakemore, R. Abu-Ghazaleh, A. Samuel, A. M. Q. King, and D. I. Stuart. 1999. The structure and function of a foot-and-mouth disease virus-oligo-saccharide receptor complex. EMBO J. 18:543-554.
19. Haapasalmi, K., K. Zhang, M. Tonnesen, J. Olerud, D. Sheppard, T. Salo, R. Krammer, R. Clark, V. Uitto, and H. Larjava. 1996. Keratinocytes in human wounds express alpha v beta 6 integrin. J. Investig. Dermatol. 106: 42-48.
20. Healy, J. M., O. Murayama, T. Maeda, K. Yoshino, K. Sekiguchi, and M. Kikuchi. 1995. Peptide ligands for integrin αvβ3 selected from random phage display libraries. Biochemistry 34:3948-3955.
21. Huang, X., J. F. Wu, D. Cass, D. J. Erle, D. Corey, S. G. Young, R. V. Farese, Jr., and D. Sheppard. 1996. Inactivation of the integrin β6 subunit gene reveals a role of epithelial integrins in regulating inflammation in the lungs and skin. J. Cell Biol. 133:921-928.
22. Huang, X., J. F. Wu, S. Spong, and D. Sheppard. 1998. The integrin αvβ6 is critical for keratinocyte migration on both its known ligand, fibronectin, and on vitronectin. J. Cell Sci. 111:2189-2195.
23. Hynes, R. O. 1992. Integrins: versatility, modulation, and signalling in cell adhesion. Cell 69:11-25.
24. Jackson, T., A. Sharma, R. Abu-Ghazaleh, W. E. Blakemore, F. M. Ellard, D. L. Simmons, J. W. I. Newman, D. I. Stuart, and A. M. Q. King. 1997. Arginine-glycine-aspartic acid-specific binding by foot-and-mouth disease virus to the purified integrin αvβ3 in vitro. J. Virol. 71:8357-8361.
25. Jackson, T., F. M. Ellard, R. Abu-Ghazaleh, S. M. Brookes, W. E. Blakemore, A. H. Corteyn, D. I. Stuart, J. W. I. Newman, and A. M. Q. King. 1996. Efficient infection of cells in culture by type O foot-and mouth disease virus requires binding to cell surface heparan sulfate. J. Virol. 70:5282-5287.
26. Kraft, S., B. Diefenbach, R. Mehta, A. Jonczyk, A. Luckenbach, and S. L. Goodman. 1999. Definition of an unexpected ligand recognition motif for αvβ6 integrin. J. Biol. Chem. 274:1979-1985.
27. Lea, S., R. Abu-Ghazaleh, W. E. Blakemore, S. Curry, E. Fry, T. Jackson, A. King, D. Logan, J. Newman, and D. Stuart. 1995. Structural comparison of two strains of foot-and-mouth disease virus subtype O1 and a laboratory antigenic variant, G67. Structure 3:571-580.
28. Lea, S., J. Hernández, W. E. Blakemore, E. Brocchi, S. Curry, E. Domingo, E. Fry, R. Abu-Ghazaleh, A. King, J. Newman, D. Stuart, and M. G. Mateu. 1994. The structure and antigenicity of a type C foot-and-mouth disease virus. Structure 2:123-139.
29. Logan, D., R. Abu-Ghazaleh, W. E. Blakemore, S. Curry, T. Jackson, A. King, S. Lea, R. Lewis, J. W. I. Newman, N. Parry, D. Rowlands, D. Stuart, and E. Fry. 1993. Structure of a major immunogenic site on foot-and-mouth disease virus. Nature 362:566-568.
30. Mason, P. W., E. Reider, and B. Baxt. 1994. RGD sequence of foot-and-mouth disease virus is essential for infecting cells via the natural receptor but can he bypassed by an antibody-dependent enhancement pathway. Proc. Natl. Acad. Sci. USA 91:1932-1936.
31. Mateu, M. G., M. Luz Valero, D. Andreu, and E. Domingo. 1996. Systematic replacement of amino acid residues within an Arg-Gly-Asp-containing loop of foot-and-mouth disease virus and effects on cell recognition. J. Biol. Chem. 271:12814-12819.
32. McCahon, D., J. R. Crowther, G. J. Belsham, J. D. A. Kitson, M. Duchesne, P. Have, R. H. Meloen, D. O. Morga, and F. de Simone. 1989. Evidence for at least 4 antigenic sites on type O foot-and-mouth disease virus involved in neutralization; identification by single and multiple monoclonal antibody-resistant mutants. J. Gen. Virol. 70:639-645.
33. Mette, S. A., J. Pilewski, C. A. Buck, and S. M. Albelda. 1993. Distribution of integrin cell adhesion receptors in normal bronchial epithelial cells and lung cancer cells in vitro and in vivo. Am. J. Respir. Cell Mol. Biol. 8:562-572.
34. Montgomery, A. M. P., R. A. Reisfeld, and D. A. Cheresh. 1994. Integrin αvβ3 rescues melanoma cells from apoptosis in three dimensional dermal collagen. Proc. Natl. Acad. Sci. USA 91:8856-8860.
35. Mould, A. P., S. K. Akiyama, and M. J. Humphries. 1995. Regulation of integrin α5β1-fibronectin interactions by divalent cations. J. Biol. Chem. 270:26270-26277.
36. Munger, J. S., X. Huang, H. Kawakatsu, M. D. J. Griffiths, S. L. Dalton, J. Wu, J. F. Pittet, N. Kaminski, C. Garat, M. A. Matthay, D. B. Rifkin, and D. Sheppard. 1999. The integrin αvβ6 binds and activates latent TGFβ1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96:319-328.
37. Neff, S., D. Sa-Carvalho, E. Rieder, P. W. Mason, S. D. Blystone, E. J. Brown, and B. Baxt. 1998. Foot-and-mouth disease virus virulent tor cattle utilizes the integrin αvβ3 as its receptor. J. Virol. 72:3587-3594.
38. Nishimura, S. L., D. Sheppard, and R. Pytela. 1994. Integrin αvβ8. Interaction with vitronectin and functional divergence of the β8 cytoplasmic domain. J. Biol. Chem. 269:28708-28715.
39. O'Toole, T. E., Y. Katagiri, R. J. Fault, R. K. Peter, R. Tamura, R. Quaranta, J. C. Loftus, S. J. Shattil, and M. H. Ginsnerg. 1994. Integrin cytoplasmic domains mediate inside-out signal-transduction. J. Cell Biol. 124:1047-1059.
40. Pacifici, R., J. Roman, R. Kimble, R. Civitelli, C. M. Brownfield, and C. Bizzarri. 1994. Ligand binding to monocyte α5β1 integrin activates the α2β1 receptor via the α5 subunit cytoplasmic domain and protein kinase C. J. Immunol. 153:2222-2233.
41. Pampori, N., T. Halo, D. G. Stupack, S. Aidoudi, D. A. Cheresh, G. R. Nemerow, and S. J. Shattil. 1999. Mechanisms and consequences of affinity modulation of integrin αvβ3 detected with a novel patch-engineered monovalent ligand. J. Biol. Chem. 274:21609-21616.
42. Pijuan-Thompson, V., and C. L. Gladson. 1997. Ligation of integrin α5β1 is required for internalization of vitronectin by integrin αvβ3. J. Biol. Chem. 272:2736-2743.
43. Prieto, A. L., G. M. Edelman, and K. L. Crossin. 1993. Multiple integrins mediate cell attachment to cytotactin/tenascin. Proc. Natl. Acad. Sci. USA 90:10154-10158.
44. Sa-Carvalho, D., E. Rieder, B. Baxt, R. Rodarte, A. Tanuri, and P. W. Mason. 1997. Tissue culture adaptation of foot-and-mouth disease virus selects viruses that bind to heparin and are attenuated in cattle. J. Virol. 71:5115-5123.
45. Salt, J. S. 1998. Persistent infection with foot-and-mouth disease virus. Top. Trop. Virol. 1:77-129.
46. Schnapp, L. M., N. Hatch, D. M. Ramos, I. V. Kilmanskaya, D. Sheppard, and R. Pytela. 1995. The human integrin α8β1 functions as a receptor for tenascin, fibronectin and vitronectin. J. Biol. Chem. 270:23196-23202.
47. Springer, T. A. 1990. Adhesion receptors of the immune system. Nature 346:425-434.
48. Weinacker, A., A. Chen, M. Agrez, R. I. Cone, S. Nishimura, E. Wayner, R. Pytela, and D. Sheppard. 1994. Role of the integrin αvβ6 in cell attachment to fibronectin. J. Biol. Chem. 269:6940-6948.
49. Yokosaki, Y., H. Monis, J. Chen, and D. Sheppard. 1996. Differential effects of the integrins α9β1, αvβ3 and αvβ6 on cell proliferative responses to tenascin. J. Biol. Chem. 271:24144-24150.