1887

Abstract

The mechanisms of calicivirus attachment and internalization are not well understood, mainly due to the lack of a reliable cell-culture system for most of its members. In this study, rabbit vesivirus (RaV) virions were shown to bind annexin A2 (ANXA2) in a membrane protein fraction from HEK293T cells, using a virus overlay protein-binding assay and matrix-assisted laser desorption/ionization time-of-flight analysis. A monoclonal anti-ANXA2 antibody and small interfering RNA-mediated knockdown of expression in HEK293T cells reduced virus infection significantly, further supporting the role of ANXA2 in RaV attachment and/or internalization.

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2009-11-01
2019-11-21
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References

  1. Adlish, J. D., Lahijani, R. S. & St Jeor, S. C. ( 1990; ). Identification of a putative cell receptor for human cytomegalovirus. Virology 176, 337–345.[CrossRef]
    [Google Scholar]
  2. Asanaka, M., Atmar, R. L., Ruvolo, V., Crawford, S. E., Neill, F. H. & Estes, M. K. ( 2005; ). Replication and packaging of Norwalk virus RNA in cultured mammalian cells. Proc Natl Acad Sci U S A 102, 10327–10332.[CrossRef]
    [Google Scholar]
  3. Babbin, B. A., Parkos, C. A., Mandell, K. J., Winfree, L. M., Laur, O., Ivanov, A. I. & Nusrat, A. ( 2007; ). Annexin 2 regulates intestinal epithelial cell spreading and wound closure through Rho-related signaling. Am J Pathol 170, 951–966.[CrossRef]
    [Google Scholar]
  4. Bhella, D., Gatherer, D., Chaudhry, Y., Pink, R. & Goodfellow, I. G. ( 2008; ). Structural insights into calicivirus attachment and uncoating. J Virol 82, 8051–8058.[CrossRef]
    [Google Scholar]
  5. Blackstock, W. P. & Weir, M. P. ( 1999; ). Proteomics: quantitative and physical mapping of cellular proteins. Trends Biotechnol 17, 121–127.[CrossRef]
    [Google Scholar]
  6. Borrow, P. & Oldstone, M. B. ( 1992; ). Characterization of lymphocytic choriomeningitis virus-binding protein(s): a candidate cellular receptor for the virus. J Virol 66, 7270–7281.
    [Google Scholar]
  7. Cao, W., Henry, M. D., Borrow, P., Yamada, H., Elder, J. H., Ravkov, E. V., Nichol, S. T., Compans, R. W., Campbell, K. P. & Oldstone, M. B. ( 1998; ). Identification of α-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282, 2079–2081.[CrossRef]
    [Google Scholar]
  8. Casais, R., Molleda, L. G., Machín, A., del Barrio, G., Manso, A. G., Dalton, K. P., Coto, A., Alonso, J. M., Prieto, M. & Parra, F. ( 2008; ). Structural and functional analysis of virus factories purified from Rabbit vesivirus-infected Vero cells. Virus Res 137, 112–121.[CrossRef]
    [Google Scholar]
  9. Choi, A. H., Paul, R. W. & Lee, P. W. ( 1990; ). Reovirus binds to multiple plasma membrane proteins of mouse L fibroblasts. Virology 178, 316–320.[CrossRef]
    [Google Scholar]
  10. Crane, S. E., Kanda, P. & Clements, J. E. ( 1991; ). Identification of the fusion domain in the visna virus transmembrane protein. Virology 185, 488–492.[CrossRef]
    [Google Scholar]
  11. Dolin, R., Blacklow, N. R., DuPont, H., Buscho, R. F., Wyatt, R. G., Kasel, J. A., Hornick, R. & Chanock, R. M. ( 1972; ). Biological properties of Norwalk agent of acute infectious nonbacterial gastroenteritis. Proc Soc Exp Biol Med 140, 578–583.[CrossRef]
    [Google Scholar]
  12. Donato, R. & Russo-Marie, F. ( 1999; ). The annexins: structure and functions. Cell Calcium 26, 85–89.[CrossRef]
    [Google Scholar]
  13. Dveksler, G. S., Pensiero, M. N., Cardellichio, C. B., Williams, R. K., Jiang, G. S., Holmes, K. V. & Dieffenbach, C. W. ( 1991; ). Cloning of the mouse hepatitis virus (MHV) receptor: expression in human and hamster cell lines confers susceptibility to MHV. J Virol 65, 6881–6891.
    [Google Scholar]
  14. Farkas, T., Sestak, K., Wei, C. & Jiang, X. ( 2008; ). Characterization of a rhesus monkey calicivirus representing a new genus of Caliciviridae. J Virol 82, 5408–5416.[CrossRef]
    [Google Scholar]
  15. Gerke, V. & Moss, S. E. ( 2002; ). Annexins: from structure to function. Physiol Rev 82, 331–371.
    [Google Scholar]
  16. Gershoni, J. M., Lapidot, M., Zakai, N. & Loyter, A. ( 1986; ). Protein blot analysis of virus receptors: identification and characterization of the Sendai virus receptor. Biochim Biophys Acta 856, 19–26.[CrossRef]
    [Google Scholar]
  17. Green, K. Y., Ando, T., Balayan, M. S., Berke, T., Clarke, I. N., Estes, M. K., Matson, D. O., Nakata, S., Neill, J. D. & other authors ( 2000; ). Taxonomy of the caliciviruses. J Infect Dis 181 (Suppl. 2), S322–S330.[CrossRef]
    [Google Scholar]
  18. Guix, S., Asanaka, M., Katayama, K., Crawford, S. E., Neill, F. H., Atmar, R. L. & Estes, M. K. ( 2007; ). Norwalk virus RNA is infectious in mammalian cells. J Virol 81, 12238–12248.[CrossRef]
    [Google Scholar]
  19. Harrington, P. R., Lindesmith, L., Yount, B., Moe, C. L. & Baric, R. S. ( 2002; ). Binding of Norwalk virus-like particles to ABH histo-blood group antigens is blocked by antisera from infected human volunteers or experimentally vaccinated mice. J Virol 76, 12335–12343.[CrossRef]
    [Google Scholar]
  20. Hayes, M. J., Longbottom, R. E., Evans, M. A. & Moss, S. E. ( 2007; ). Annexinopathies. Subcell Biochem 45, 1–28.
    [Google Scholar]
  21. Hoover, E. A. & Kahn, D. E. ( 1975; ). Experimentally induced feline calicivirus infection: clinical signs and lesions. J Am Vet Med Assoc 166, 463–468.
    [Google Scholar]
  22. Hutson, A. M., Atmar, R. L., Graham, D. Y. & Estes, M. K. ( 2002; ). Norwalk virus infection and disease is associated with ABO histo-blood group type. J Infect Dis 185, 1335–1337.[CrossRef]
    [Google Scholar]
  23. Kapikian, A. Z., Wyatt, R. G., Dolin, R., Thornhill, T. S., Kalica, A. R. & Chanock, R. M. ( 1972; ). Visualization by immune electron microscopy of a 27-nm particle associated with acute infectious nonbacterial gastroenteritis. J Virol 10, 1075–1081.
    [Google Scholar]
  24. Kapikian, A. Z., Estes, M. K. & Chanock, R. M. ( 1996; ). Norwalk group of viruses. In Fields Virology, 3rd edn, pp. 783–810. Edited by B. N. Fields, D. M. Knipe, P. M. Howley, R. M. Chanock, J. L. Melnick, T. P. Monath, B. Roizman & S. E. Straus. Philadelphia: Lippincott-Raven.
  25. Kilpatrick, D. R. & Lipton, H. L. ( 1991; ). Predominant binding of Theiler's viruses to a 34-kilodalton receptor protein on susceptible cell lines. J Virol 65, 5244–5249.
    [Google Scholar]
  26. Makino, A., Shimojima, M., Miyazawa, T., Kato, K., Tohya, Y. & Akashi, H. ( 2006; ). Junctional adhesion molecule 1 is a functional receptor for feline calicivirus. J Virol 80, 4482–4490.[CrossRef]
    [Google Scholar]
  27. Malhotra, R., Ward, M., Bright, H., Priest, R., Foster, M. R., Hurle, M., Blair, E. & Bird, M. ( 2003; ). Isolation and characterisation of potential respiratory syncytial virus receptor(s) on epithelial cells. Microbes Infect 5, 123–133.[CrossRef]
    [Google Scholar]
  28. Marionneau, S., Ruvoen, N., Le Moullac-Vaidye, B., Clement, M., Cailleau-Thomas, A., Ruiz-Palacois, G., Huang, P., Jiang, X. & Le Pendu, J. ( 2002; ). Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals. Gastroenterology 122, 1967–1977.[CrossRef]
    [Google Scholar]
  29. Martín-Alonso, J. M., Skilling, D. E., González-Molleda, L., del Barrio, G., Machín, A., Keefer, N. K., Matson, D. O., Iversen, P. L., Smith, A. W. & Parra, F. ( 2005; ). Isolation and characterization of a new Vesivirus from rabbits. Virology 337, 373–383.[CrossRef]
    [Google Scholar]
  30. Morens, D. M., Zweighaft, R. M., Vernon, T. M., Gary, G. W., Eslien, J. J., Wood, B. T., Holman, R. C. & Dolin, R. ( 1979; ). A waterborne outbreak of gastroenteritis with secondary person-to-person spread. Association with a viral agent. Lancet 1, 964–966.
    [Google Scholar]
  31. Oh, J. S., Song, D. S. & Park, B. K. ( 2003; ). Identification of a putative cellular receptor 150 kDa polypeptide for porcine epidemic diarrhea virus in porcine enterocytes. J Vet Sci 4, 269–275.
    [Google Scholar]
  32. Oliferenko, S., Paiha, K., Harder, T., Gerke, V., Schwarzler, C., Schwarz, H., Beug, H., Gunthert, U. & Huber, L. A. ( 1999; ). Analysis of CD44-containing lipid rafts: recruitment of annexin II and stabilization by the actin cytoskeleton. J Cell Biol 146, 843–854.[CrossRef]
    [Google Scholar]
  33. Oliver, S. L., Asobayire, E., Dastjerdi, A. M. & Bridger, J. C. ( 2006; ). Genomic characterization of the unclassified bovine enteric virus Newbury agent-1 (Newbury1) endorses a new genus in the family Caliciviridae. Virology 350, 240–250.[CrossRef]
    [Google Scholar]
  34. Otto, M., Gunther, A., Fan, H., Rick, O. & Huang, R. T. ( 1994; ). Identification of annexin 33 kDa in cultured cells as a binding protein of influenza viruses. FEBS Lett 356, 125–129.[CrossRef]
    [Google Scholar]
  35. Parwani, A. V., Flynn, W. T., Gadfield, K. L. & Saif, L. J. ( 1991; ). Serial propagation of porcine enteric calicivirus in a continuous cell line. Effect of medium supplementation with intestinal contents or enzymes. Arch Virol 120, 115–122.[CrossRef]
    [Google Scholar]
  36. Perkins, D. N., Pappin, D. J., Creasy, D. M. & Cottrell, J. S. ( 1999; ). Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551–3567.[CrossRef]
    [Google Scholar]
  37. Raynor, C. M., Wright, J. F., Waisman, D. M. & Pryzdial, E. L. ( 1999; ). Annexin II enhances cytomegalovirus binding and fusion to phospholipid membranes. Biochemistry 38, 5089–5095.[CrossRef]
    [Google Scholar]
  38. Reed, L. J. & Muench, H. ( 1938; ). A simple method of estimating fifty percent endpoints. . Am J Hyg 27, 493
    [Google Scholar]
  39. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V. & Mann, M. ( 2006; ). In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1, 2856–2860.
    [Google Scholar]
  40. Straub, T. M., Höner zu Bentrup, K., Orosz-Coghlan, P., Dohnalkova, A., Mayer, B. K., Bartholomew, R. A., Valdez, C. O., Bruckner-Lea, C. J., Gerba, C. P. & other authors ( 2007; ). In vitro cell culture infectivity assay for human noroviruses. Emerg Infect Dis 13, 396–403.[CrossRef]
    [Google Scholar]
  41. Stuart, A. D. & Brown, T. D. ( 2007; ). α2,6-linked sialic acid acts as a receptor for Feline calicivirus. J Gen Virol 88, 177–186.[CrossRef]
    [Google Scholar]
  42. Suckau, D., Resemann, A., Schuerenberg, M., Hufnagel, P., Franzen, J. & Holle, A. ( 2003; ). A novel MALDI LIFT-TOF/TOF mass spectrometer for proteomics. Anal Bioanal Chem 376, 952–965.[CrossRef]
    [Google Scholar]
  43. Taylor, H. P. & Cooper, N. R. ( 1990; ). The human cytomegalovirus receptor on fibroblasts is a 30-kilodalton membrane protein. J Virol 64, 2484–2490.
    [Google Scholar]
  44. Thiel, H. J. & Konig, M. ( 1999; ). Caliciviruses: an overview. Vet Microbiol 69, 55–62.[CrossRef]
    [Google Scholar]
  45. Trauger, S. A., Wu, E., Bark, S. J., Nemerow, G. R. & Siuzdak, G. ( 2004; ). The identification of an adenovirus receptor by using affinity capture and mass spectrometry. ChemBioChem 5, 1095–1099.[CrossRef]
    [Google Scholar]
  46. Verdin, E. M., King, G. L. & Maratos-Flier, E. ( 1989; ). Characterization of a common high-affinity receptor for reovirus serotypes 1 and 3 on endothelial cells. J Virol 63, 1318–1325.
    [Google Scholar]
  47. Wobus, C. E., Karst, S. M., Thackray, L. B., Chang, K. O., Sosnovtsev, S. V., Belliot, G., Krug, A., Mackenzie, J. M., Green, K. Y. & Virgin, H. W. ( 2004; ). Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol 2, e432 [CrossRef]
    [Google Scholar]
  48. Wu, E., Fernandez, J., Fleck, S. K., Von Seggern, D. J., Huang, S. & Nemerow, G. R. ( 2001; ). A 50-kDa membrane protein mediates sialic acid-independent binding and infection of conjunctival cells by adenovirus type 37. Virology 279, 78–89.[CrossRef]
    [Google Scholar]
  49. Yates, J. R., III ( 2000; ). Mass spectrometry. From genomics to proteomics. Trends Genet 16, 5–8.
    [Google Scholar]
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