1887

Abstract

Rotaviruses recognize several cell-surface molecules, including the 21 integrin, and the processes of rotavirus cell attachment and entry appear to be multifactorial. The VP5* subunit of the rotavirus spike protein VP4 contains the 21 ligand sequence Asp–Gly–Glu at residues 308–310. Binding to 21 and infectivity of monkey rotavirus strain RRV and human rotavirus strain Wa, but not porcine rotavirus strain CRW-8, are inhibited by peptides containing Asp–Gly–Glu. Asp308 and Gly309 are necessary for the binding of RRV VP5* (aa 248–474) to expressed I domain of the 2 integrin subunit. Here, the ability of RRV VP5* to bind cells and affect rotavirus–integrin interactions was determined. Interestingly, VP5* bound to cells at 4 and 37 °C, both via 21 and independently of this integrin. Prior VP5* binding at 37 °C eliminated RRV binding to cellular 21 and reduced RRV and Wa infectivity in MA104 cells by 38–46 %. VP5* binding did not affect the infectivity of CRW-8. VP5* binding at 4 °C did not affect permissive-cell infection by RRV, indicating an energy requirement for VP5* competition with virus for infectivity. Mutagenesis of VP5* Asp308 and Gly309 eliminated VP5* binding to 21 and the VP5* inhibition of rotavirus cell binding and infection, but not 21-independent cell binding by VP5*. These studies show for the first time that expressed VP5* binds cell-surface 21 using Asp308 and Gly309 and inhibits the infection of homologous and heterologous rotaviruses that use 21 as a receptor.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.81580-0
2006-05-01
2020-01-24
Loading full text...

Full text loading...

/deliver/fulltext/jgv/87/5/1275.html?itemId=/content/journal/jgv/10.1099/vir.0.81580-0&mimeType=html&fmt=ahah

References

  1. Bass, D. M., Mackow, E. R. & Greenberg, H. B. ( 1991; ). Identification and partial characterization of a rhesus rotavirus binding glycoprotein on murine enterocytes. Virology 183, 602–610.[CrossRef]
    [Google Scholar]
  2. Ciarlet, M., Crawford, S. E., Cheng, E., Blutt, S. E., Rice, D. A., Bergelson, J. M. & Estes, M. K. ( 2002a; ). VLA-2 (α2β1) integrin promotes rotavirus entry into cells but is not necessary for rotavirus attachment. J Virol 76, 1109–1123.[CrossRef]
    [Google Scholar]
  3. Ciarlet, M., Ludert, J. E., Iturriza-Gómara, M., Liprandi, F., Gray, J. J., Desselberger, U. & Estes, M. K. ( 2002b; ). Initial interaction of rotavirus strains with N-acetylneuraminic (sialic) acid residues on the cell surface correlates with VP4 genotype, not species of origin. J Virol 76, 4087–4095.[CrossRef]
    [Google Scholar]
  4. Clark, S. M., Roth, J. R., Clark, M. L., Barnett, B. B. & Spendlove, R. S. ( 1981; ). Trypsin enhancement of rotavirus infectivity: mechanism of enhancement. J Virol 39, 816–822.
    [Google Scholar]
  5. Coulson, B. S. & Kirkwood, C. ( 1991; ). Relation of VP7 amino acid sequence to monoclonal antibody neutralization of rotavirus and rotavirus monotype. J Virol 65, 5968–5974.
    [Google Scholar]
  6. Coulson, B. S., Fowler, K. J., Bishop, R. F. & Cotton, R. G. ( 1985; ). Neutralizing monoclonal antibodies to human rotavirus and indications of antigenic drift among strains from neonates. J Virol 54, 14–20.
    [Google Scholar]
  7. Coulson, B. S., Tursi, J. M., McAdam, W. J. & Bishop, R. F. ( 1986; ). Derivation of neutralizing monoclonal antibodies to human rotaviruses and evidence that an immunodominant neutralization site is shared between serotypes 1 and 3. Virology 154, 302–312.[CrossRef]
    [Google Scholar]
  8. Coulson, B. S., Londrigan, S. L. & Lee, D. J. ( 1997; ). Rotavirus contains integrin ligand sequences and a disintegrin-like domain that are implicated in virus entry into cells. Proc Natl Acad Sci U S A 94, 5389–5394.[CrossRef]
    [Google Scholar]
  9. Crawford, S. E., Labbe, M., Cohen, J., Burroughs, M. H., Zhou, Y. J. & Estes, M. K. ( 1994; ). Characterization of virus-like particles produced by the expression of rotavirus capsid proteins in insect cells. J Virol 68, 5945–5952.
    [Google Scholar]
  10. Crawford, S. E., Mukherjee, S. K., Estes, M. K., Lawton, J. A., Shaw, A. L., Ramig, R. F. & Prasad, B. V. V. ( 2001; ). Trypsin cleavage stabilizes the rotavirus VP4 spike. J Virol 75, 6052–6061.[CrossRef]
    [Google Scholar]
  11. Delorme, C., Brüssow, H., Sidoti, J., Roche, N., Karlsson, K.-A., Neeser, J.-R. & Teneberg, S. ( 2001; ). Glycosphingolipid binding specificities of rotavirus: identification of a sialic acid-binding epitope. J Virol 75, 2276–2287.[CrossRef]
    [Google Scholar]
  12. Denisova, E., Dowling, W., LaMonica, R., Shaw, R., Scarlata, S., Ruggeri, F. & Mackow, E. R. ( 1999; ). Rotavirus capsid protein VP5* permeabilizes membranes. J Virol 73, 3147–3153.
    [Google Scholar]
  13. Dormitzer, P. R., Sun, Z. Y., Wagner, G. & Harrison, S. C. ( 2002; ). The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J 21, 885–897.[CrossRef]
    [Google Scholar]
  14. Dormitzer, P. R., Nason, E. B., Prasad, B. V. V. & Harrison, S. C. ( 2004; ). Structural rearrangements in the membrane penetration protein of a non-enveloped virus. Nature 430, 1053–1058.[CrossRef]
    [Google Scholar]
  15. Dowling, W., Denisova, E., LaMonica, R. & Mackow, E. R. ( 2000; ). Selective membrane permeabilization by the rotavirus VP5* protein is abrogated by mutations in an internal hydrophobic domain. J Virol 74, 6368–6376.[CrossRef]
    [Google Scholar]
  16. Espejo, R. T., López, S. & Arias, C. ( 1981; ). Structural polypeptides of simian rotavirus SA11 and the effect of trypsin. J Virol 37, 156–160.
    [Google Scholar]
  17. Estes, M. K., Graham, D. Y. & Mason, B. B. ( 1981; ). Proteolytic enhancement of rotavirus infectivity: molecular mechanisms. J Virol 39, 879–888.
    [Google Scholar]
  18. Falconer, M. M., Gilbert, J. M., Roper, A. M., Greenberg, H. B. & Gavora, J. S. ( 1995; ). Rotavirus-induced fusion from without in tissue culture cells. J Virol 69, 5582–5591.
    [Google Scholar]
  19. Fiore, L., Greenberg, H. B. & Mackow, E. R. ( 1991; ). The VP8 fragment of VP4 is the rhesus rotavirus hemagglutinin. Virology 181, 553–563.[CrossRef]
    [Google Scholar]
  20. Fukudome, K., Yoshie, O. & Konno, T. ( 1989; ). Comparison of human, simian, and bovine rotaviruses for requirement of sialic acid in hemagglutination and cell adsorption. Virology 172, 196–205.[CrossRef]
    [Google Scholar]
  21. Gilbert, J. M. & Greenberg, H. B. ( 1998; ). Cleavage of rhesus rotavirus VP4 after arginine 247 is essential for rotavirus-like particle-induced fusion from without. J Virol 72, 5323–5327.
    [Google Scholar]
  22. Golantsova, N. E., Gorbunova, E. E. & Mackow, E. R. ( 2004; ). Discrete domains within the rotavirus VP5* direct peripheral membrane association and membrane permeability. J Virol 78, 2037–2044.[CrossRef]
    [Google Scholar]
  23. Graham, K. L., Halasz, P., Tan, Y., Hewish, M. J., Takada, Y., Mackow, E. R., Robinson, M. K. & Coulson, B. S. ( 2003; ). Integrin-using rotaviruses bind α2β1 integrin α2 I domain via VP4 DGE sequence and recognize αXβ2 and αVβ3 by using VP7 during cell entry. J Virol 77, 9969–9978.[CrossRef]
    [Google Scholar]
  24. Graham, K. L., Zeng, W., Takada, Y., Jackson, D. C. & Coulson, B. S. ( 2004; ). Effects on rotavirus cell binding and infection of monomeric and polymeric peptides containing α2β1 and αxβ2 integrin ligand sequences. J Virol 78, 11786–11797.[CrossRef]
    [Google Scholar]
  25. Graham, K. L., Fleming, F. E., Halasz, P., Hewish, M. J., Nagesha, H. S., Holmes, I. H., Takada, Y. & Coulson, B. S. ( 2005; ). Rotaviruses interact with α4β7 and α4β1 integrins by binding the same integrin domains as natural ligands. J Gen Virol 86, 3397–3408.[CrossRef]
    [Google Scholar]
  26. Guerrero, C. A., Méndez, E., Zárate, S., Isa, P., López, S. & Arias, C. F. ( 2000; ). Integrin α v β 3 mediates rotavirus cell entry. Proc Natl Acad Sci U S A 97, 14644–14649.[CrossRef]
    [Google Scholar]
  27. Guo, C. T., Nakagomi, O., Mochizuki, M. & 7 other authors ( 1999; ). Ganglioside GM(1a) on the cell surface is involved in the infection by human rotavirus KUN and MO strains. J Biochem 126, 683–688.[CrossRef]
    [Google Scholar]
  28. Halasz, P., Fleming, F. E. & Coulson, B. S. ( 2005; ). Evaluation of specificity and effects of monoclonal antibodies submitted to the Eighth Human Leucocyte Differentiation Antigen Workshop on rotavirus-cell attachment and entry. Cell Immunol 236, 179–187.[CrossRef]
    [Google Scholar]
  29. Hewish, M. J., Takada, Y. & Coulson, B. S. ( 2000; ). Integrins α2β1 and α4β1 can mediate SA11 rotavirus attachment and entry into cells. J Virol 74, 228–236.[CrossRef]
    [Google Scholar]
  30. Jolly, C. L., Beisner, B. M. & Holmes, I. H. ( 2000; ). Rotavirus infection of MA104 cells is inhibited by Ricinus lectin and separately expressed single binding domains. Virology 275, 89–97.[CrossRef]
    [Google Scholar]
  31. Jolly, C. L., Beisner, B. M., Ozser, E. & Holmes, I. H. ( 2001a; ). Non-lytic extraction and characterisation of receptors for multiple strains of rotavirus. Arch Virol 146, 1307–1323.[CrossRef]
    [Google Scholar]
  32. Jolly, C. L., Huang, J.-A. & Holmes, I. H. ( 2001b; ). Selection of rotavirus VP4 cell receptor binding domains for MA104 cells using a phage display library. J Virol Methods 98, 41–51.[CrossRef]
    [Google Scholar]
  33. Kaljot, K. T., Shaw, R. D., Rubin, D. H. & Greenberg, H. B. ( 1988; ). Infectious rotavirus enters cells by direct cell membrane penetration, not by endocytosis. J Virol 62, 1136–1144.
    [Google Scholar]
  34. Kirkwood, C. D., Bishop, R. F. & Coulson, B. S. ( 1998; ). Attachment and growth of human rotaviruses RV-3 and S12/85 in Caco-2 cells depend on VP4. J Virol 72, 9348–9352.
    [Google Scholar]
  35. Liakatos, A., Kiefel, M. J., Fleming, F., Coulson, B. & von Itzstein, M. ( 2006; ). The synthesis and biological evaluation of lactose-based sialylmimetics as inhibitors of rotaviral infection. Bioorg Med Chem 14, 739–757.[CrossRef]
    [Google Scholar]
  36. Londrigan, S. L., Hewish, M. J., Thomson, M. J., Sanders, G. M., Mustafa, H. & Coulson, B. S. ( 2000; ). Growth of rotaviruses in continuous human and monkey cell lines that vary in their expression of integrins. J Gen Virol 81, 2203–2213.
    [Google Scholar]
  37. Londrigan, S. L., Graham, K. L., Takada, Y., Halasz, P. & Coulson, B. S. ( 2003; ). Monkey rotavirus binding to α2β1 integrin requires the α2 I domain and is facilitated by the homologous β1 subunit. J Virol 77, 9486–9501.[CrossRef]
    [Google Scholar]
  38. Ludert, J. E., Feng, N., Yu, J. H., Broome, R. L., Hoshino, Y. & Greenberg, H. B. ( 1996; ). Genetic mapping indicates that VP4 is the rotavirus cell attachment protein in vitro and in vivo. J Virol 70, 487–493.
    [Google Scholar]
  39. Ludert, J. E., Ruiz, M. C., Hidalgo, C. & Liprandi, F. ( 2002; ). Antibodies to rotavirus outer capsid glycoprotein VP7 neutralize infectivity by inhibiting virion decapsidation. J Virol 76, 6643–6651.[CrossRef]
    [Google Scholar]
  40. Luque, A., Gómez, M., Puzon, W., Takada, Y., Sánchez-Madrid, F. & Cabañas, C. ( 1996; ). Activated conformations of very late activation integrins detected by a group of antibodies (HUTS) specific for a novel regulatory region (355–425) of the common β1 chain. J Biol Chem 271, 11067–11075.[CrossRef]
    [Google Scholar]
  41. Méndez, E., Arias, C. F. & López, S. ( 1993; ). Binding to sialic acids is not an essential step for the entry of animal rotaviruses to epithelial cells in culture. J Virol 67, 5253–5259.
    [Google Scholar]
  42. Méndez, E., López, S., Cuadras, M. A., Romero, P. & Arias, C. F. ( 1999; ). Entry of rotaviruses is a multistep process. Virology 263, 450–459.[CrossRef]
    [Google Scholar]
  43. Nagesha, H. S. & Holmes, I. H. ( 1991; ). VP4 relationships between porcine and other rotavirus serotypes. Arch Virol 116, 107–118.[CrossRef]
    [Google Scholar]
  44. Pesavento, J. B., Crawford, S. E., Roberts, E., Estes, M. K. & Prasad, B. V. V. ( 2005; ). pH-induced conformational change of the rotavirus VP4 spike: implications for cell entry and antibody neutralization. J Virol 79, 8572–8580.[CrossRef]
    [Google Scholar]
  45. Rolsma, M. D., Kuhlenschmidt, T. B., Gelberg, H. B. & Kuhlenschmidt, M. S. ( 1998; ). Structure and function of a ganglioside receptor for porcine rotavirus. J Virol 72, 9079–9091.
    [Google Scholar]
  46. 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.[CrossRef]
    [Google Scholar]
  47. Yeager, M., Dryden, K. A., Olson, N. H., Greenberg, H. B. & Baker, T. S. ( 1990; ). Three-dimensional structure of rhesus rotavirus by cryoelectron microscopy and image reconstruction. J Cell Biol 110, 2133–2144.[CrossRef]
    [Google Scholar]
  48. Zárate, S., Espinosa, R., Romero, P., Guerrero, C. A., Arias, C. F. & López, S. ( 2000a; ). Integrin α2β1 mediates the cell attachment of the rotavirus neuraminidase-resistant variant nar3. Virology 278, 50–54.[CrossRef]
    [Google Scholar]
  49. Zárate, S., Espinosa, R., Romero, P., Méndez, E., Arias, C. F. & López, S. ( 2000b; ). The VP5 domain of VP4 can mediate attachment of rotaviruses to cells. J Virol 74, 593–599.[CrossRef]
    [Google Scholar]
  50. Zárate, S., Cuadras, M. A., Espinosa, R., Romero, P., Juárez, K. O., Camacho-Nuez, M., Arias, C. F. & López, S. ( 2003; ). Interaction of rotaviruses with Hsc70 during cell entry is mediated by VP5. J Virol 77, 7254–7260.[CrossRef]
    [Google Scholar]
  51. Zárate, S., Romero, P., Espinosa, R., Arias, C. F. & López, S. ( 2004; ). VP7 mediates the interaction of rotaviruses with integrin αvβ3 through a novel integrin-binding site. J Virol 78, 10839–10847.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.81580-0
Loading
/content/journal/jgv/10.1099/vir.0.81580-0
Loading

Data & Media loading...

Most cited articles

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