This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Jackson, T.
Right arrow Articles by King, A. M. Q.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Jackson, T.
Right arrow Articles by King, A. M. Q.

 Previous Article  |  Next Article 

Journal of Virology, June 2000, p. 4949-4956, Vol. 74, No. 11
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

The Epithelial Integrin alpha vbeta 6 Is a Receptor for Foot-and-Mouth Disease Virus

Terry Jackson,1,* Dean Sheppard,2 Michael Denyer,3 Wendy Blakemore,1 and Andrew M. Q. King1

Department of Molecular Biology1 and Department of Immunology and Pathology,3 Institute for Animal Health, Pirbright, Surrey GU24 ONF, United Kingdom, and Lung Biology Center, Cardiovascular Research Institute, Department of Medicine, University of California, San Francisco, California 94143-08542

Received 3 December 1999/Accepted 1 March 2000

Field isolates of foot-and-mouth disease virus (FMDV) have been shown to use the RGD-dependent integrin alpha vbeta 3 as a cellular receptor on cultured cells. However, several other RGD-dependent integrins may have the potential to act as receptors for FMDV in vivo. Of these, alpha vbeta 6 is a likely candidate for use as a receptor by FMDV as it is expressed on epithelial cells, which correlates with the tissue tropism of the virus. In this report, we show that human colon carcinoma cells (SW480) that are normally nonpermissive for FMDV become susceptible to infection as a result of transfection with the integrin beta 6 subunit and expression of alpha vbeta 6 at the cell surface. Integrin alpha vbeta 6 is the major site for virus attachment on the beta 6-transfected cells, and binding to alpha vbeta 6 serves to increase the rate of virus entry into these cells. In addition, we show that virus binding and infection of the beta 6-transfected cells is mediated through an RGD-dependent interaction that is specifically inhibited by a monoclonal antibody (10D5) that recognizes alpha vbeta 6. These studies establish a role for alpha vbeta 6 as a cellular receptor for FMDV.


* Corresponding author. Mailing address: Pirbright Laboratory, Institute for Animal Health, Ash Rd., Pirbright, Surrey GU24 ONF, United Kingdom. Phone: 44-1483-232441. Fax: 44-1483-237161. E-mail: terry.jackson{at}bbsrc.ac.uk.


Journal of Virology, June 2000, p. 4949-4956, Vol. 74, No. 11
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Goodwin, S., Tuthill, T. J., Arias, A., Killington, R. A., Rowlands, D. J. (2009). Foot-and-Mouth Disease Virus Assembly: Processing of Recombinant Capsid Precursor by Exogenous Protease Induces Self-Assembly of Pentamers In Vitro in a Myristoylation-Dependent Manner. J. Virol. 83: 11275-11282 [Abstract] [Full Text]  
  • Brehm, K. E., Ferris, N. P., Lenk, M., Riebe, R., Haas, B. (2009). Highly Sensitive Fetal Goat Tongue Cell Line for Detection and Isolation of Foot-and-Mouth Disease Virus. J. Clin. Microbiol. 47: 3156-3160 [Abstract] [Full Text]  
  • Coughlan, L., Vallath, S., Saha, A., Flak, M., McNeish, I. A., Vassaux, G., Marshall, J. F., Hart, I. R., Thomas, G. J. (2009). In Vivo Retargeting of Adenovirus Type 5 to {alpha}v{beta}6 Integrin Results in Reduced Hepatotoxicity and Improved Tumor Uptake following Systemic Delivery. J. Virol. 83: 6416-6428 [Abstract] [Full Text]  
  • Johns, H. L., Berryman, S., Monaghan, P., Belsham, G. J., Jackson, T. (2009). A Dominant-Negative Mutant of rab5 Inhibits Infection of Cells by Foot-and-Mouth Disease Virus: Implications for Virus Entry. J. Virol. 83: 6247-6256 [Abstract] [Full Text]  
  • Li, S., McGuire, M. J., Lin, M., Liu, Y.-H., Oyama, T., Sun, X., Brown, K. C. (2009). Synthesis and characterization of a high-affinity {alpha}v{beta}6-specific ligand for in vitro and in vivo applications. Molecular Cancer Therapeutics 8: 1239-1249 [Abstract] [Full Text]  
  • Cseke, G., Maginnis, M. S., Cox, R. G., Tollefson, S. J., Podsiad, A. B., Wright, D. W., Dermody, T. S., Williams, J. V. (2009). Integrin {alpha}v{beta}1 promotes infection by human metapneumovirus. Proc. Natl. Acad. Sci. USA 106: 1566-1571 [Abstract] [Full Text]  
  • Veettil, M. V., Sadagopan, S., Sharma-Walia, N., Wang, F.-Z., Raghu, H., Varga, L., Chandran, B. (2008). Kaposi's Sarcoma-Associated Herpesvirus Forms a Multimolecular Complex of Integrins ({alpha}V{beta}5, {alpha}V{beta}3, and {alpha}3{beta}1) and CD98-xCT during Infection of Human Dermal Microvascular Endothelial Cells, and CD98-xCT Is Essential for the Postentry Stage of Infection. J. Virol. 82: 12126-12144 [Abstract] [Full Text]  
  • Gutierrez-Rivas, M., Pulido, M. R., Baranowski, E., Sobrino, F., Saiz, M. (2008). Tolerance to mutations in the foot-and-mouth disease virus integrin-binding RGD region is different in cultured cells and in vivo and depends on the capsid sequence context. J. Gen. Virol. 89: 2531-2539 [Abstract] [Full Text]  
  • O'Donnell, V., LaRocco, M., Baxt, B. (2008). Heparan Sulfate-Binding Foot-and-Mouth Disease Virus Enters Cells via Caveola-Mediated Endocytosis. J. Virol. 82: 9075-9085 [Abstract] [Full Text]  
  • Harwood, L. J., Gerber, H., Sobrino, F., Summerfield, A., McCullough, K. C. (2008). Dendritic Cell Internalization of Foot-and-Mouth Disease Virus: Influence of Heparan Sulfate Binding on Virus Uptake and Induction of the Immune Response. J. Virol. 82: 6379-6394 [Abstract] [Full Text]  
  • DiCara, D., Burman, A., Clark, S., Berryman, S., Howard, M. J., Hart, I. R., Marshall, J. F., Jackson, T. (2008). Foot-and-Mouth Disease Virus Forms a Highly Stable, EDTA-Resistant Complex with Its Principal Receptor, Integrin {alpha}v 6: Implications for Infectiousness. J. Virol. 82: 1537-1546 [Abstract] [Full Text]  
  • Gulbahar, M. Y., Davis, W. C., Guvenc, T., Yarim, M., Parlak, U., Kabak, Y. B. (2007). Myocarditis Associated with Foot-and-Mouth Disease Virus Type O in Lambs. Vet Pathol 44: 589-599 [Abstract] [Full Text]  
  • Hausner, S. H., DiCara, D., Marik, J., Marshall, J. F., Sutcliffe, J. L. (2007). Use of a Peptide Derived from Foot-and-Mouth Disease Virus for the Noninvasive Imaging of Human Cancer: Generation and Evaluation of 4-[18F]Fluorobenzoyl A20FMDV2 for In vivo Imaging of Integrin {alpha}v{beta}6 Expression with Positron Emission Tomography. Cancer Res. 67: 7833-7840 [Abstract] [Full Text]  
  • Nunez, J. I., Molina, N., Baranowski, E., Domingo, E., Clark, S., Burman, A., Berryman, S., Jackson, T., Sobrino, F. (2007). Guinea Pig-Adapted Foot-and-Mouth Disease Virus with Altered Receptor Recognition Can Productively Infect a Natural Host. J. Virol. 81: 8497-8506 [Abstract] [Full Text]  
  • Elayadi, A. N., Samli, K. N., Prudkin, L., Liu, Y.-H., Bian, A., Xie, X.-J., Wistuba, I. I., Roth, J. A., McGuire, M. J., Brown, K. C. (2007). A Peptide Selected by Biopanning Identifies the Integrin {alpha}v{beta}6 as a Prognostic Biomarker for Nonsmall Cell Lung Cancer. Cancer Res. 67: 5889-5895 [Abstract] [Full Text]  
  • Maidji, E., Genbacev, O., Chang, H.-T., Pereira, L. (2007). Developmental Regulation of Human Cytomegalovirus Receptors in Cytotrophoblasts Correlates with Distinct Replication Sites in the Placenta. J. Virol. 81: 4701-4712 [Abstract] [Full Text]  
  • DiCara, D., Rapisarda, C., Sutcliffe, J. L., Violette, S. M., Weinreb, P. H., Hart, I. R., Howard, M. J., Marshall, J. F. (2007). Structure-Function Analysis of Arg-Gly-Asp Helix Motifs in {alpha}vbeta6 Integrin Ligands. J. Biol. Chem. 282: 9657-9665 [Abstract] [Full Text]  
  • Al-Sunaidi, M., Williams, C. H., Hughes, P. J., Schnurr, D. P., Stanway, G. (2007). Analysis of a New Human Parechovirus Allows the Definition of Parechovirus Types and the Identification of RNA Structural Domains. J. Virol. 81: 1013-1021 [Abstract] [Full Text]  
  • Burman, A., Clark, S., Abrescia, N. G. A., Fry, E. E., Stuart, D. I., Jackson, T. (2006). Specificity of the VP1 GH Loop of Foot-and-Mouth Disease Virus for {alpha}v Integrins. J. Virol. 80: 9798-9810 [Abstract] [Full Text]  
  • Pellinen, T., Ivaska, J. (2006). Integrin traffic.. J. Cell Sci. 119: 3723-3731 [Abstract] [Full Text]  
  • Brown, J. K., McAleese, S. M., Thornton, E. M., Pate, J. A., Schock, A., Macrae, A. I., Scott, P. R., Miller, H. R.P., Collie, D. D.S. (2006). Integrin-{alpha}v{beta}6, a Putative Receptor for Foot-and-Mouth Disease Virus, Is Constitutively Expressed in Ruminant Airways. J. Histochem. Cytochem. 54: 807-816 [Abstract] [Full Text]  
  • Maginnis, M. S., Forrest, J. C., Kopecky-Bromberg, S. A., Dickeson, S. K., Santoro, S. A., Zutter, M. M., Nemerow, G. R., Bergelson, J. M., Dermody, T. S. (2006). {beta}1 Integrin Mediates Internalization of Mammalian Reovirus. J. Virol. 80: 2760-2770 [Abstract] [Full Text]  
  • Rieder, E., Henry, T., Duque, H., Baxt, B. (2005). Analysis of a Foot-and-Mouth Disease Virus Type A24 Isolate Containing an SGD Receptor Recognition Site In Vitro and Its Pathogenesis in Cattle. J. Virol. 79: 12989-12998 [Abstract] [Full Text]  
  • Monaghan, P., Gold, S., Simpson, J., Zhang, Z., Weinreb, P. H., Violette, S. M., Alexandersen, S., Jackson, T. (2005). The {alpha}v{beta}6 integrin receptor for Foot-and-mouth disease virus is expressed constitutively on the epithelial cells targeted in cattle. J. Gen. Virol. 86: 2769-2780 [Abstract] [Full Text]  
  • Ostrowski, M., Vermeulen, M., Zabal, O., Geffner, J. R., Sadir, A. M., Lopez, O. J. (2005). Impairment of Thymus-Dependent Responses by Murine Dendritic Cells Infected with Foot-and-Mouth Disease Virus. J. Immunol. 175: 3971-3979 [Abstract] [Full Text]  
  • Fry, E. E., Newman, J. W. I., Curry, S., Najjam, S., Jackson, T., Blakemore, W., Lea, S. M., Miller, L., Burman, A., King, A. M. Q., Stuart, D. I. (2005). Structure of Foot-and-mouth disease virus serotype A1061 alone and complexed with oligosaccharide receptor: receptor conservation in the face of antigenic variation. J. Gen. Virol. 86: 1909-1920 [Abstract] [Full Text]  
  • O'Donnell, V., LaRocco, M., Duque, H., Baxt, B. (2005). Analysis of Foot-and-Mouth Disease Virus Internalization Events in Cultured Cells. J. Virol. 79: 8506-8518 [Abstract] [Full Text]  
  • Berryman, S., Clark, S., Monaghan, P., Jackson, T. (2005). Early Events in Integrin {alpha}v{beta}6-Mediated Cell Entry of Foot-and-Mouth Disease Virus. J. Virol. 79: 8519-8534 [Abstract] [Full Text]  
  • Monaghan, P., Simpson, J., Murphy, C., Durand, S., Quan, M., Alexandersen, S. (2005). Use of Confocal Immunofluorescence Microscopy To Localize Viral Nonstructural Proteins and Potential Sites of Replication in Pigs Experimentally Infected with Foot-and-Mouth Disease Virus. J. Virol. 79: 6410-6418 [Abstract] [Full Text]  
  • Peng, J.-M., Liang, S.-M., Liang, C.-M. (2004). VP1 of Foot-and-Mouth Disease Virus Induces Apoptosis via the Akt Signaling Pathway. J. Biol. Chem. 279: 52168-52174 [Abstract] [Full Text]  
  • Duque, H., LaRocco, M., Golde, W. T., Baxt, B. (2004). Interactions of Foot-and-Mouth Disease Virus with Soluble Bovine {alpha}V{beta}3 and {alpha}V{beta}6 Integrins. J. Virol. 78: 9773-9781 [Abstract] [Full Text]  
  • Stevenson, R. A., Huang, J.-a., Studdert, M. J., Hartley, C. A. (2004). Identification of a neutralizing epitope in the {beta}E-{beta}F loop of VP1 of equine rhinitis A virus, defined by a neutralization-resistant variant. J. Gen. Virol. 85: 2545-2553 [Abstract] [Full Text]  
  • Bose, S., Basu, M., Banerjee, A. K. (2004). Role of Nucleolin in Human Parainfluenza Virus Type 3 Infection of Human Lung Epithelial Cells. J. Virol. 78: 8146-8158 [Abstract] [Full Text]  
  • Williams, C. H., Kajander, T., Hyypia, T., Jackson, T., Sheppard, D., Stanway, G. (2004). Integrin {alpha}v{beta}6 Is an RGD-Dependent Receptor for Coxsackievirus A9. J. Virol. 78: 6967-6973 [Abstract] [Full Text]  
  • Jackson, T., Clark, S., Berryman, S., Burman, A., Cambier, S., Mu, D., Nishimura, S., King, A. M. Q. (2004). Integrin {alpha}v{beta}8 Functions as a Receptor for Foot-and-Mouth Disease Virus: Role of the {beta}-Chain Cytodomain in Integrin-Mediated Infection. J. Virol. 78: 4533-4540 [Abstract] [Full Text]  
  • Grubman, M. J., Baxt, B. (2004). Foot-and-Mouth Disease. Clin. Microbiol. Rev. 17: 465-493 [Abstract] [Full Text]  
  • Salone, B., Martina, Y., Piersanti, S., Cundari, E., Cherubini, G., Franqueville, L., Failla, C. M., Boulanger, P., Saggio, I. (2003). Integrin {alpha}3{beta}1 Is an Alternative Cellular Receptor for Adenovirus Serotype 5. J. Virol. 77: 13448-13454 [Abstract] [Full Text]  
  • Baranowski, E., Molina, N., Nunez, J. I., Sobrino, F., Saiz, M. (2003). Recovery of Infectious Foot-and-Mouth Disease Virus from Suckling Mice after Direct Inoculation with In Vitro-Transcribed RNA. J. Virol. 77: 11290-11295 [Abstract] [Full Text]  
  • Harvala, H., Kalimo, H., Stanway, G., Hyypia, T. (2003). Pathogenesis of coxsackievirus A9 in mice: role of the viral arginine-glycine-aspartic acid motif. J. Gen. Virol. 84: 2375-2379 [Abstract] [Full Text]  
  • SHEPPARD, D. (2003). Functions of Pulmonary Epithelial Integrins: From Development to Disease. Physiol. Rev. 83: 673-686 [Abstract] [Full Text]  
  • Stevenson, R. A., Hartley, C. A., Huang, J.-a., Studdert, M. J., Crabb, B. S., Warner, S. (2003). Mapping epitopes in equine rhinitis A virus VP1 recognized by antibodies elicited in response to infection of the natural host. J. Gen. Virol. 84: 1607-1612 [Abstract] [Full Text]  
  • Caruso, M., Belloni, L., Sthandier, O., Amati, P., Garcia, M.-I. (2003). {alpha}4{beta}1 Integrin Acts as a Cell Receptor for Murine Polyomavirus at the Postattachment Level. J. Virol. 77: 3913-3921 [Abstract] [Full Text]  
  • Zhao, Q., Pacheco, J. M., Mason, P. W. (2003). Evaluation of Genetically Engineered Derivatives of a Chinese Strain of Foot-and-Mouth Disease Virus Reveals a Novel Cell-Binding Site Which Functions in Cell Culture and in Animals. J. Virol. 77: 3269-3280 [Abstract] [Full Text]  
  • Duque, H., Baxt, B. (2003). Foot-and-Mouth Disease Virus Receptors: Comparison of Bovine {alpha}V Integrin Utilization by Type A and O Viruses. J. Virol. 77: 2500-2511 [Abstract] [Full Text]  
  • Tami, C., Taboga, O., Berinstein, A., Nunez, J. I., Palma, E. L., Domingo, E., Sobrino, F., Carrillo, E. (2002). Evidence of the Coevolution of Antigenicity and Host Cell Tropism of Foot-and-Mouth Disease Virus In Vivo. J. Virol. 77: 1219-1226 [Abstract] [Full Text]  
  • Boulanger, D., Green, P., Jones, B., Henriquet, G., Hunt, L. G., Laidlaw, S. M., Monaghan, P., Skinner, M. A. (2002). Identification and Characterization of Three Immunodominant Structural Proteins of Fowlpox Virus. J. Virol. 76: 9844-9855 [Abstract] [Full Text]  
  • Jackson, T., Mould, A. P., Sheppard, D., King, A. M. Q. (2002). Integrin {alpha}v{beta}1 Is a Receptor for Foot-and-Mouth Disease Virus. J. Virol. 76: 935-941 [Abstract] [Full Text]  
  • Ciarlet, M., Crawford, S. E., Cheng, E., Blutt, S. E., Rice, D. A., Bergelson, J. M., Estes, M. K. (2002). VLA-2 ({alpha}2{beta}1) Integrin Promotes Rotavirus Entry into Cells but Is Not Necessary for Rotavirus Attachment. J. Virol. 76: 1109-1123 [Abstract] [Full Text]  
  • Lu, M., Munger, J. S., Steadele, M., Busald, C., Tellier, M., Schnapp, L. M. (2002). Integrin {alpha}8{beta}1 mediates adhesion to LAP-TGF{beta}1. J. Cell Sci. 115: 4641-4648 [Abstract] [Full Text]  
  • Boonyakiat, Y., Hughes, P. J., Ghazi, F., Stanway, G. (2001). Arginine-Glycine-Aspartic Acid Motif Is Critical for Human Parechovirus 1 Entry. J. Virol. 75: 10000-10004 [Abstract] [Full Text]  
  • Warner, S., Hartley, C. A., Stevenson, R. A., Ficorilli, N., Varrasso, A., Studdert, M. J., Crabb, B. S. (2001). Evidence that Equine Rhinitis A Virus VP1 Is a Target of Neutralizing Antibodies and Participates Directly in Receptor Binding. J. Virol. 75: 9274-9281 [Abstract] [Full Text]  
  • Baranowski, E., Ruiz-Jarabo, C. M., Domingo, E. (2001). Evolution of Cell Recognition by Viruses. Science 292: 1102-1105 [Abstract] [Full Text]  
  • Miller, L. C., Blakemore, W., Sheppard, D., Atakilit, A., King, A. M. Q., Jackson, T. (2001). Role of the Cytoplasmic Domain of the {beta}-Subunit of Integrin {alpha}v{beta}6 in Infection by Foot-and-Mouth Disease Virus. J. Virol. 75: 4158-4164 [Abstract] [Full Text]  
  • Núñez, J. I., Baranowski, E., Molina, N., Ruiz-Jarabo, C. M., Sánchez, C., Domingo, E., Sobrino, F. (2001). A Single Amino Acid Substitution in Nonstructural Protein 3A Can Mediate Adaptation of Foot-and-Mouth Disease Virus to the Guinea Pig. J. Virol. 75: 3977-3983 [Abstract] [Full Text]  
  • Neff, S., Baxt, B. (2001). The Ability of Integrin {alpha}v{beta}3 To Function as a Receptor for Foot-and-Mouth Disease Virus Is Not Dependent on the Presence of Complete Subunit Cytoplasmic Domains. J. Virol. 75: 527-532 [Abstract] [Full Text]  
  • Guerrero, C. A., Méndez, E., Zárate, S., Isa, P., López, S., Arias, C. F. (2000). Integrin alpha vbeta 3 mediates rotavirus cell entry. Proc. Natl. Acad. Sci. USA 10.1073/pnas.250299897v1 [Abstract] [Full Text]  
  • Guerrero, C. A., Mendez, E., Zarate, S., Isa, P., Lopez, S., Arias, C. F. (2000). Integrin alpha vbeta 3 mediates rotavirus cell entry. Proc. Natl. Acad. Sci. USA 97: 14644-14649 [Abstract] [Full Text]