1887

Abstract

Previously published data suggest that the RGD-recognizing integrin, v3, known as the vitronectin receptor, acts as a cellular receptor for RGD-containing enteroviruses, coxsackievirus A9 (CAV-9) and echovirus 9 (E-9), in several continuous cell lines as well as in primary human Langerhans' islets. As this receptor is also capable of binding the ligands by a non-RGD-dependent mechanism, we investigated whether vitronectin receptors, v integrins, might act as receptors for other echoviruses that do not have the RGD motif. Blocking experiments with polyclonal anti-v3 antibody showed that both primary human islets and a continuous laboratory cell line of green monkey kidney origin (GMK) are protected similarly from the adverse effects of several non-RGD-containing echovirus (E-7, -11, -25, -30, -32) infections. In contrast, corresponding studies on primary human endothelial cells showed that the receptor works only for E-25, E-30, E-32 and CAV-9. The inhibitory effect of the antibody was not restricted to prototype strains of echoviruses, as GMK cells infected with several field isolates of the corresponding serotypes were also protected from virus-induced cytopathic effects. Co-localization of virus particles with the receptor molecules in both GMK and primary human endothelial cells was demonstrated by live-cell stainings and confocal microscopy. Remarkably, in spite of similar virus–receptor co-localization and a comparable protective effect of the v3 antibody, the entry pathways of the studied virus strains seemed to be divergent.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.012450-0
2010-01-01
2019-11-13
Loading full text...

Full text loading...

/deliver/fulltext/jgv/91/1/155.html?itemId=/content/journal/jgv/10.1099/vir.0.012450-0&mimeType=html&fmt=ahah

References

  1. Baranowski, E., Ruiz-Jarabo, C. M. & Domingo, E. ( 2001; ). Evolution of cell recognition by viruses. Science 292, 1102–1105.[CrossRef]
    [Google Scholar]
  2. Bergelson, J. M., Chan, M., Solomon, K. R., St John, N. F., Lin, H. & Finberg, R. W. ( 1994; ). Decay-accelerating factor (CD55), a glycosylphosphatidylinositol-anchored complement regulatory protein, is a receptor for several echoviruses. Proc Natl Acad Sci U S A 91, 6245–6249.[CrossRef]
    [Google Scholar]
  3. Bergelson, J. M., Mohanty, J. G., Crowell, R. L., St John, N. F., Lublin, D. M. & Finberg, R. W. ( 1995; ). Coxsackievirus B3 adapted to growth in RD cells binds to decay-accelerating factor (CD55). J Virol 69, 1903–1906.
    [Google Scholar]
  4. Bergelson, J. M., Cunningham, J. A., Droguett, G., Kurt-Jones, E. A., Krithivas, A., Hong, J. S., Horwitz, M. S., Crowell, R. L. & Finberg, R. W. ( 1997a; ). Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275, 1320–1323.[CrossRef]
    [Google Scholar]
  5. Bergelson, J. M., Modlin, J. F., Wieland-Alter, W., Cunningham, J. A., Crowell, R. L. & Finberg, R. W. ( 1997b; ). Clinical coxsackievirus B isolates differ from laboratory strains in their interaction with two cell surface receptors. J Infect Dis 175, 697–700.[CrossRef]
    [Google Scholar]
  6. Coyne, C. B. & Bergelson, J. M. ( 2005; ). CAR: a virus receptor within the tight junction. Adv Drug Deliv Rev 57, 869–882.[CrossRef]
    [Google Scholar]
  7. Coyne, C. B. & Bergelson, J. M. ( 2006; ). Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions. Cell 124, 119–131.[CrossRef]
    [Google Scholar]
  8. Dotta, F., Censini, S., van Halteren, A. G., Marselli, L., Masini, M., Dionisi, S., Mosca, F., Boggi, U., Muda, A. O. & other authors ( 2007; ). Coxsackie B4 virus infection of β cells and natural killer cell insulitis in recent-onset type 1 diabetic patients. Proc Natl Acad Sci U S A 104, 5115–5120.[CrossRef]
    [Google Scholar]
  9. Foulis, A. K., McGill, M., Farquharson, M. A. & Hilton, D. A. ( 1997; ). A search for evidence of viral infection in pancreases of newly diagnosed patients with IDDM. Diabetologia 40, 53–61.[CrossRef]
    [Google Scholar]
  10. Gavrilovskaya, I. N., Shepley, M., Shaw, R., Ginsberg, M. H. & Mackow, E. R. ( 1998; ). β3 integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc Natl Acad Sci U S A 95, 7074–7079.[CrossRef]
    [Google Scholar]
  11. Greve, J. M., Davis, G., Meyer, A. M., Forte, C. P., Yost, S. C., Marlor, C. W., Kamarck, M. E. & McClelland, A. ( 1989; ). The major human rhinovirus receptor is ICAM-1. Cell 56, 839–847.[CrossRef]
    [Google Scholar]
  12. Heikkilä, O., Susi, P., Stanway, G. & Hyypiä, T. ( 2009; ). Integrin αVβ6 is a high-affinity receptor for coxsackievirus A9. J Gen Virol 90, 197–204.[CrossRef]
    [Google Scholar]
  13. Hovi, T. & Roivainen, M. ( 1993; ). Peptide antisera targeted to a conserved sequence in poliovirus capsid VP1 cross-react widely with members of the genus Enterovirus. J Clin Microbiol 31, 1083–1087.
    [Google Scholar]
  14. Hughes, P. J., Horsnell, C., Hyypiä, T. & Stanway, G. ( 1995; ). The coxsackievirus A9 RGD motif is not essential for virus viability. J Virol 69, 8035–8040.
    [Google Scholar]
  15. Johansson, U., Olsson, A., Gabrielsson, S., Nilsson, B. & Korsgren, O. ( 2003; ). Inflammatory mediators expressed in human islets of Langerhans: implications for islet transplantation. Biochem Biophys Res Commun 308, 474–479.[CrossRef]
    [Google Scholar]
  16. Joki-Korpela, P., Marjomäki, V., Krogerus, C., Heino, J. & Hyypiä, T. ( 2001; ). Entry of human parechovirus 1. J Virol 75, 1958–1967.[CrossRef]
    [Google Scholar]
  17. Lange, R., Peng, X., Wimmer, E., Lipp, M. & Bernhardt, G. ( 2001; ). The poliovirus receptor CD155 mediates cell-to-matrix contacts by specifically binding to vitronectin. Virology 285, 218–227.[CrossRef]
    [Google Scholar]
  18. Marsh, M. & Helenius, A. ( 2006; ). Virus entry: open sesame. Cell 124, 729–740.[CrossRef]
    [Google Scholar]
  19. Mendelsohn, C. L., Wimmer, E. & Racaniello, V. R. ( 1989; ). Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 56, 855–865.[CrossRef]
    [Google Scholar]
  20. Mueller, S. & Wimmer, E. ( 2003; ). Recruitment of nectin-3 to cell-cell junctions through trans-heterophilic interaction with CD155, a vitronectin and poliovirus receptor that localizes to α v β 3 integrin-containing membrane microdomains. J Biol Chem 278, 31251–31260.[CrossRef]
    [Google Scholar]
  21. Nobis, P., Zibirre, R., Meyer, G., Kuhne, J., Warnecke, G. & Koch, G. ( 1985; ). Production of a monoclonal antibody against an epitope on HeLa cells that is the functional poliovirus binding site. J Gen Virol 66, 2563–2569.[CrossRef]
    [Google Scholar]
  22. 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.[CrossRef]
    [Google Scholar]
  23. Otonkoski, T., Beattie, G. M., Mally, M. I., Ricordi, C. & Hayek, A. ( 1993; ). Nicotinamide is a potent inducer of endocrine differentiation in cultured human fetal pancreatic cells. J Clin Invest 92, 1459–1466.[CrossRef]
    [Google Scholar]
  24. Paananen, A., Ylipaasto, P., Rieder, E., Hovi, T., Galama, J. & Roivainen, M. ( 2003; ). Molecular and biological analysis of echovirus 9 strain isolated from a diabetic child. J Med Virol 69, 529–537.[CrossRef]
    [Google Scholar]
  25. Pietiäinen, V. M., Marjomäki, V., Heino, J. & Hyypiä, T. ( 2005; ). Viral entry, lipid rafts and caveosomes. Ann Med 37, 394–403.[CrossRef]
    [Google Scholar]
  26. Powell, R. M., Schmitt, V., Ward, T., Goodfellow, I., Evans, D. J. & Almond, J. W. ( 1998; ). Characterization of echoviruses that bind decay accelerating factor (CD55): evidence that some haemagglutinating strains use more than one cellular receptor. J Gen Virol 79, 1707–1713.
    [Google Scholar]
  27. Roivainen, M. ( 1999; ). Enteroviruses and myocardial infarction. Am Heart J 138, S479–S483.[CrossRef]
    [Google Scholar]
  28. Roivainen, M., Hyypiä, T., Piirainen, L., Kalkkinen, N., Stanway, G. & Hovi, T. ( 1991; ). RGD-dependent entry of coxsackievirus A9 into host cells and its bypass after cleavage of VP1 protein by intestinal proteases. J Virol 65, 4735–4740.
    [Google Scholar]
  29. Roivainen, M., Piirainen, L., Hovi, T., Virtanen, I., Riikonen, T., Heino, J. & Hyypiä, T. ( 1994; ). Entry of coxsackievirus A9 into host cells: specific interactions with α v β 3 integrin, the vitronectin receptor. Virology 203, 357–365.[CrossRef]
    [Google Scholar]
  30. Roivainen, M., Piirainen, L. & Hovi, T. ( 1996; ). Efficient RGD-independent entry process of coxsackievirus A9. Arch Virol 141, 1909–1919.[CrossRef]
    [Google Scholar]
  31. Roivainen, M., Rasilainen, S., Ylipaasto, P., Nissinen, R., Ustinov, J., Bouwens, L., Eizirik, D. L., Hovi, T. & Otonkoski, T. ( 2000; ). Mechanisms of coxsackievirus-induced damage to human pancreatic β-cells. J Clin Endocrinol Metab 85, 432–440.
    [Google Scholar]
  32. Saijets, S., Ylipaasto, P., Vaarala, O., Hovi, T. & Roivainen, M. ( 2003; ). Enterovirus infection and activation of human umbilical vein endothelial cells. J Med Virol 70, 430–439.[CrossRef]
    [Google Scholar]
  33. Schmidtke, M., Selinka, H. C., Heim, A., Jahn, B., Tonew, M., Kandolf, R., Stelzner, A. & Zell, R. ( 2000; ). Attachment of coxsackievirus B3 variants to various cell lines: mapping of phenotypic differences to capsid protein VP1. Virology 275, 77–88.[CrossRef]
    [Google Scholar]
  34. Shafren, D. R., Bates, R. C., Agrez, M. V., Herd, R. L., Burns, G. F. & Barry, R. D. ( 1995; ). Coxsackieviruses B1, B3, and B5 use decay accelerating factor as a receptor for cell attachment. J Virol 69, 3873–3877.
    [Google Scholar]
  35. Shafren, D. R., Dorahy, D. J., Ingham, R. A., Burns, G. F. & Barry, R. D. ( 1997; ). Coxsackievirus A21 binds to decay-accelerating factor but requires intercellular adhesion molecule 1 for cell entry. J Virol 71, 4736–4743.
    [Google Scholar]
  36. Stanway, G., Kalkkinen, N., Roivainen, M., Ghazi, F., Khan, M., Smyth, M., Meurman, O. & Hyypiä, T. ( 1994; ). Molecular and biological characteristics of echovirus 22, a representative of a new picornavirus group. J Virol 68, 8232–8238.
    [Google Scholar]
  37. Staunton, D. E., Merluzzi, V. J., Rothlein, R., Barton, R., Marlin, S. D. & Springer, T. A. ( 1989; ). A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 56, 849–853.[CrossRef]
    [Google Scholar]
  38. Tomassini, J. E., Graham, D., DeWitt, C. M., Lineberger, D. W., Rodkey, J. A. & Colonno, R. J. ( 1989; ). cDNA cloning reveals that the major group rhinovirus receptor on HeLa cells is intercellular adhesion molecule 1. Proc Natl Acad Sci U S A 86, 4907–4911.[CrossRef]
    [Google Scholar]
  39. Tomko, R. P., Xu, R. & Philipson, L. ( 1997; ). HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc Natl Acad Sci U S A 94, 3352–3356.[CrossRef]
    [Google Scholar]
  40. Triantafilou, K., Triantafilou, M., Takada, Y. & Fernandez, N. ( 2000a; ). Human parechovirus 1 utilizes integrins αvβ3 and αvβ1 as receptors. J Virol 74, 5856–5862.[CrossRef]
    [Google Scholar]
  41. Triantafilou, M., Triantafilou, K., Wilson, K. M., Takada, Y. & Fernandez, N. ( 2000b; ). High affinity interactions of Coxsackievirus A9 with integrin αvβ3 (CD51/61) require the CYDMKTTC sequence of β3, but do not require the RGD sequence of the CAV-9 VP1 protein. Hum Immunol 61, 453–459.[CrossRef]
    [Google Scholar]
  42. Triantafilou, K., Fradelizi, D., Wilson, K. & Triantafilou, M. ( 2002; ). GRP78, a coreceptor for coxsackievirus A9, interacts with major histocompatibility complex class I molecules which mediate virus internalization. J Virol 76, 633–643.[CrossRef]
    [Google Scholar]
  43. Williams, C. H., Kajander, T., Hyypiä, T., Jackson, T., Sheppard, D. & Stanway, G. ( 2004; ). Integrin α v β 6 is an RGD-dependent receptor for coxsackievirus A9. J Virol 78, 6967–6973.[CrossRef]
    [Google Scholar]
  44. Ylipaasto, P., Klingel, K., Lindberg, A. M., Otonkoski, T., Kandolf, R., Hovi, T. & Roivainen, M. ( 2004; ). Enterovirus infection in human pancreatic islet cells, islet tropism in vivo and receptor involvement in cultured islet beta cells. Diabetologia 47, 225–239.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.012450-0
Loading
/content/journal/jgv/10.1099/vir.0.012450-0
Loading

Data & Media loading...

Supplements

vol. , part 1, pp. 155–165

Kinetics of echovirus infections (E-7, E-11, E-25, E-30, E-32) in GMK cells.

Expression of αv integrins in GMK cells.

[ Single PDF of figures] (1.5 MB)



PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error