1887

Abstract

Group A rotaviruses are major intestinal pathogens that express potential 41 and 47 integrin ligand sequences Leu–Asp–Val and Leu–Asp–Ile in their outer capsid protein VP7, and Ile–Asp–Ala in their spike protein VP4. Monkey rotavirus SA11 can use recombinant 41 as a cellular receptor. In this study a new potential 41, 47 and 91 integrin ligand sequence, Tyr–Gly–Leu, was identified in VP4. It was shown that several human and monkey rotaviruses bound 41 and 47, but not 91. Binding to 41 mediated the infectivity and growth of monkey rotaviruses, and binding to 47 mediated their infectivity. A porcine rotavirus interacted with 4 integrins at a post-binding stage to facilitate infection. Activation of 41 increased rotavirus infectivity. Cellular treatment with peptides containing the 4 integrin ligand sequences Tyr–Gly–Leu and Ile–Asp–Ala eliminated virus binding to 4 integrins and infectivity. In contrast, rotavirus recognition of 4 integrins was unaffected by a peptide containing the sequence Leu–Asp–Val or by a mutation in the VP7 Leu–Asp–Val sequence. VP4 involvement in rotavirus recognition of 41 was demonstrated with rotavirus reassortants. Swapping and point mutagenesis of 4 surface loops showed that rotaviruses required the same 4 residues and domains for binding as the natural 4 integrin ligands: mucosal addressin cell adhesion molecule-1, fibronectin and vascular cell adhesion molecule-1. Several rotaviruses are able to use 47 and 41 for cell binding or entry, through the recognition of the same 4-subunit domains as natural 4 ligands.

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2005-12-01
2019-11-20
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References

  1. Barry, S. T., Ludbrook, S. B., Murrison, E. & Horgan, C. M. ( 2000; ). Analysis of the α4β1 integrin-osteopontin interaction. Exp Cell Res 258, 342–351.[CrossRef]
    [Google Scholar]
  2. Basora, N., Desloges, N., Chang, Q., Bouatrouss, Y., Gosselin, J., Poisson, J., Sheppard, D. & Beaulieu, J. F. ( 1998; ). Expression of the α9β1 integrin in human colonic epithelial cells: resurgence of the fetal phenotype in a subset of colon cancers and adenocarcinoma cell lines. Int J Cancer 75, 738–743.[CrossRef]
    [Google Scholar]
  3. Blutt, S. E., Kirkwood, C. D., Parreno, V., Warfield, K. L., Ciarlet, M., Estes, M. K., Bok, K., Bishop, R. F. & Conner, M. E. ( 2003; ). Rotavirus antigenaemia and viraemia: a common event? Lancet 362, 1445–1449.[CrossRef]
    [Google Scholar]
  4. Bremont, M., Juste-Lesage, P., Chabanne-Vautherot, D., Charpilienne, A. & Cohen, J. ( 1992; ). Sequences of the four larger proteins of a porcine group C rotavirus and comparison with the equivalent group A rotavirus proteins. Virology 186, 684–692.[CrossRef]
    [Google Scholar]
  5. Brown, K. A., Kriss, J. A., Moser, C. A., Wenner, W. J. & Offit, P. A. ( 2000; ). Circulating rotavirus-specific antibody-secreting cells (ASCs) predict the presence of rotavirus-specific ASCs in the human small intestinal lamina propria. J Infect Dis 182, 1039–1043.[CrossRef]
    [Google Scholar]
  6. Caruso, M., Belloni, L., Sthandier, O., Amati, P. & Garcia, M. I. ( 2003; ). α4β1 integrin acts as a cell receptor for murine polyomavirus at the postattachment level. J Virol 77, 3913–3921.[CrossRef]
    [Google Scholar]
  7. Chan, B. M., Elices, M. J., Murphy, E. & Hemler, M. E. ( 1992; ). Adhesion to vascular cell adhesion molecule 1 and fibronectin. Comparison of α4β1 (VLA-4) and α4β7 on the human B cell line JY. J Biol Chem 267, 8366–8370.
    [Google Scholar]
  8. Choy, M. Y., Richman, P. I., Horton, M. A. & MacDonald, T. T. ( 1990; ). Expression of the VLA family of integrins in human intestine. J Pathol 160, 35–40.[CrossRef]
    [Google Scholar]
  9. Ciarlet, M., Ludert, J. E., Iturriza-Gomara, M., Liprandi, F., Gray, J. J., Desselberger, U. & Estes, M. K. ( 2002; ). 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]
  10. Coulson, B. S. ( 1997; ). Effects of workshop monoclonal antibodies on rotavirus infection of cells. In Leucocyte Typing VI, pp. 391–393. Edited by T. Kishimoto, H. Kikutani, A. E. G. Kr. von dem Borne, S. M. Goyert, D. Y. Mason, M. Miyasaka, L. Moretta, K. Okumura, S. Shaw, T. A. Springer, K. Sugamura & H. Zola. New York: Garland Publishing, Inc.
  11. Coulson, B. S., Grimwood, K., Hudson, I. L., Barnes, G. L. & Bishop, R. F. ( 1992; ). Role of coproantibody in clinical protection of children during reinfection with rotavirus. J Clin Microbiol 30, 1678–1684.
    [Google Scholar]
  12. 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]
  13. Dormitzer, P. R., Nason, E. B., Prasad, B. V. & Harrison, S. C. ( 2004; ). Structural rearrangements in the membrane penetration protein of a non-enveloped virus. Nature 430, 1053–1058.[CrossRef]
    [Google Scholar]
  14. Eto, K., Puzon-McLaughlin, W., Sheppard, D., Sehara-Fujisawa, A., Zhang, X. P. & Takada, Y. ( 2000; ). RGD-independent binding of integrin α9β1 to the ADAM-12 and -15 disintegrin domains mediates cell–cell interaction. J Biol Chem 275, 34922–34930.[CrossRef]
    [Google Scholar]
  15. Faull, R. J., Wang, J., Leavesley, D. I., Puzon, W., Russ, G. R., Vestweber, D. & Takada, Y. ( 1996; ). A novel activating anti-β1 integrin monoclonal antibody binds to the cysteine-rich repeats in the β1 chain. J Biol Chem 271, 25099–25106.[CrossRef]
    [Google Scholar]
  16. Franco, M. A. & Greenberg, H. B. ( 1999; ). Immunity to rotavirus infection in mice. J Infect Dis 179, S466–S469.[CrossRef]
    [Google Scholar]
  17. Gao, Y. A., Agnihotri, R., Vary, C. P. & Liaw, L. ( 2004; ). Expression and characterization of recombinant osteopontin peptides representing matrix metalloproteinase proteolytic fragments. Matrix Biol 23, 457–466.[CrossRef]
    [Google Scholar]
  18. Gonzalez, A. M., Jaimes, M. C., Cajiao, I. & 8 other authors ( 2003; ). Rotavirus-specific B cells induced by recent infection in adults and children predominantly express the intestinal homing receptor α4β7. Virology 305, 93–105.[CrossRef]
    [Google Scholar]
  19. 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]
  20. 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]
  21. Green, P. M., Ludbrook, S. B., Miller, D. D., Horgan, C. M. & Barry, S. T. ( 2001; ). Structural elements of the osteopontin SVVYGLR motif important for the interaction with α4 integrins. FEBS Lett 503, 75–79.[CrossRef]
    [Google Scholar]
  22. Guerrero, C. A., Mendez, E., Zarate, S., Isa, P., Lopez, S. & Arias, C. F. ( 2000; ). Integrin αvβ3 mediates rotavirus cell entry. Proc Natl Acad Sci U S A 97, 14644–14649.[CrossRef]
    [Google Scholar]
  23. Guerrero-Esteo, M., Ruiz-Velasco, N., Munoz, M. & Teixido, J. ( 1998; ). Role of two conserved glycine residues in the β-propeller domain of the integrin α4 subunit in VLA-4 conformation and function. FEBS Lett 429, 123–128.[CrossRef]
    [Google Scholar]
  24. 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]
  25. Higgins, J. M., Cernadas, M., Tan, K., Irie, A., Wang, J., Takada, Y. & Brenner, M. B. ( 2000; ). The role of α and β chains in ligand recognition by β7 integrins. J Biol Chem 275, 25652–25664.[CrossRef]
    [Google Scholar]
  26. Honeyman, M. C., Coulson, B. S., Stone, N. L. & 7 other authors ( 2000; ). Association between rotavirus infection and pancreatic islet autoimmunity in children at risk of developing type 1 diabetes. Diabetes 49, 1319–1324.[CrossRef]
    [Google Scholar]
  27. Hoshino, Y., Jones, R. W. & Kapikian, A. Z. ( 1998; ). Serotypic characterization of outer capsid spike protein VP4 of vervet monkey rotavirus SA11 strain. Arch Virol 143, 1233–1244.[CrossRef]
    [Google Scholar]
  28. Hynes, R. O. ( 2002; ). Integrins: bidirectional, allosteric signaling machines. Cell 110, 673–687.[CrossRef]
    [Google Scholar]
  29. Irie, A., Kamata, T., Puzon-McLaughlin, W. & Takada, Y. ( 1995; ). Critical amino acid residues for ligand binding are clustered in a predicted β-turn of the third N-terminal repeat in the integrin α4 and α5 subunits. EMBO J 14, 5550–5556.
    [Google Scholar]
  30. Irie, A., Kamata, T. & Takada, Y. ( 1997; ). Multiple loop structures critical for ligand binding of the integrin α4 subunit in the upper face of the β-propeller mode 1. Proc Natl Acad Sci U S A 94, 7198–7203.[CrossRef]
    [Google Scholar]
  31. Iturriza-Gomara, M., Auchterlonie, I. A., Zaw, W., Molyneaux, P., Desselberger, U. & Gray, J. ( 2002; ). Rotavirus gastroenteritis and central nervous system (CNS) infection: characterization of the VP7 and VP4 genes of rotavirus strains isolated from paired fecal and cerebrospinal fluid samples from a child with CNS disease. J Clin Microbiol 40, 4797–4799.[CrossRef]
    [Google Scholar]
  32. Jolly, C. L., Beisner, B. M., Ozser, E. & Holmes, I. H. ( 2001; ). Non-lytic extraction and characterisation of receptors for multiple strains of rotavirus. Arch Virol 146, 1307–1323.[CrossRef]
    [Google Scholar]
  33. Kamata, T., Puzon, W. & Takada, Y. ( 1995; ). Identification of putative ligand-binding sites of the integrin α4β1 (VLA-4, CD49d/CD29). Biochem J 305, 945–951.
    [Google Scholar]
  34. Kirkwood, C., Masendycz, P. J. & Coulson, B. S. ( 1993; ). Characteristics and location of cross-reactive and serotype-specific neutralization sites on VP7 of human G type 9 rotaviruses. Virology 196, 79–88.[CrossRef]
    [Google Scholar]
  35. 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]
  36. Komoriya, A., Green, L. J., Mervic, M., Yamada, S. S., Yamada, K. M. & Humphries, M. J. ( 1991; ). The minimal essential sequence for a major cell type-specific adhesion site (CS1) within the alternatively spliced type III connecting segment domain of fibronectin is leucine-aspartic acid-valine. J Biol Chem 266, 15075–15079.
    [Google Scholar]
  37. Lazdins, I., Coulson, B. S., Kirkwood, C., Dyall-Smith, M., Masendycz, P. J., Sonza, S. & Holmes, I. H. ( 1995; ). Rotavirus antigenicity is affected by the genetic context and glycosylation of VP7. Virology 209, 80–89.[CrossRef]
    [Google Scholar]
  38. 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]
  39. 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]
  40. Lopez, S. & Arias, C. F. ( 2004; ). Multistep entry of rotavirus into cells: a Versaillesque dance. Trends Microbiol 12, 271–278.[CrossRef]
    [Google Scholar]
  41. Lopez, S., Lopez, I., Romero, P., Mendez, E., Soberon, X. & Arias, C. F. ( 1991; ). Rotavirus YM gene 4: analysis of its deduced amino acid sequence and prediction of the secondary structure of the VP4 protein. J Virol 65, 3738–3745.
    [Google Scholar]
  42. Mittelbrunn, M., Molina, A., Escribese, M. M., Yanez-Mo, M., Escudero, E., Ursa, A., Tejedor, R., Mampaso, F. & Sanchez-Madrid, F. ( 2004; ). VLA-4 integrin concentrates at the peripheral supramolecular activation complex of the immune synapse and drives T helper 1 responses. Proc Natl Acad Sci U S A 101, 11058–11063.[CrossRef]
    [Google Scholar]
  43. Mossel, E. C. & Ramig, R. F. ( 2003; ). A lymphatic mechanism of rotavirus extraintestinal spread in the neonatal mouse. J Virol 77, 12352–12356.[CrossRef]
    [Google Scholar]
  44. Munoz, M., Serrador, J., Nieto, M., Luque, A., Sanchez-Madrid, F. & Teixido, J. ( 1997; ). A novel region of the α4 integrin subunit with a modulatory role in VLA-4-mediated cell adhesion to fibronectin. Biochem J 327, 727–733.
    [Google Scholar]
  45. Nagesha, H. S. & Holmes, I. H. ( 1991; ). VP4 relationships between porcine and other rotavirus serotypes. Arch Virol 116, 107–118.[CrossRef]
    [Google Scholar]
  46. Nagesha, H. S., Brown, L. E. & Holmes, I. H. ( 1989; ). Neutralizing monoclonal antibodies against three serotypes of porcine rotavirus. J Virol 63, 3545–3549.
    [Google Scholar]
  47. Pender, S. L., Salmela, M. T., Monteleone, G., Schnapp, D., McKenzie, C., Spencer, J., Fong, S., Saarialho-Kere, U. & MacDonald, T. T. ( 2000; ). Ligation of α4β1 integrin on human intestinal mucosal mesenchymal cells selectively up-regulates membrane type-1 matrix metalloproteinase and confers a migratory phenotype. Am J Pathol 157, 1955–1962.[CrossRef]
    [Google Scholar]
  48. Powell, D. W., Mifflin, R. C., Valentich, J. D., Crowe, S. E., Saada, J. I. & West, A. B. ( 1999; ). Myofibroblasts. II. Intestinal subepithelial myofibroblasts. Am J Physiol Cell Physiol 277, C183–C201.
    [Google Scholar]
  49. 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]
  50. Rose, J. R., Williams, M. B., Rott, L. S., Butcher, E. C. & Greenberg, H. B. ( 1998; ). Expression of the mucosal homing receptor α4β7 correlates with the ability of CD8+ memory T cells to clear rotavirus infection. J Virol 72, 726–730.
    [Google Scholar]
  51. Rott, L. S., Rose, J. R., Bass, D., Williams, M. B., Greenberg, H. B. & Butcher, E. C. ( 1997; ). Expression of mucosal homing receptor α4β7 by circulating CD4+ cells with memory for intestinal rotavirus. J Clin Invest 100, 1204–1208.[CrossRef]
    [Google Scholar]
  52. Ruegg, C., Postigo, A. A., Sikorski, E. E., Butcher, E. C., Pytela, R. & Erle, D. J. ( 1992; ). Role of integrin α4β7/α4βP in lymphocyte adherence to fibronectin and VCAM-1 and in homotypic cell clustering. J Cell Biol 117, 179–189.[CrossRef]
    [Google Scholar]
  53. Ruiz-Velasco, N., Guerrero-Esteo, M., Briskin, M. J. & Teixido, J. ( 2000; ). The α4 integrin subunit Tyr187 has a key role in α4β7-dependent cell adhesion. J Biol Chem 275, 7052–7059.[CrossRef]
    [Google Scholar]
  54. Schreiner, C. L., Bauer, J. S., Danilov, Y. N., Hussein, S., Sczekan, M. M. & Juliano, R. L. ( 1989; ). Isolation and characterization of Chinese hamster ovary cell variants deficient in the expression of fibronectin receptor. J Cell Biol 109, 3157–3167.[CrossRef]
    [Google Scholar]
  55. Sharma, A., Askari, J. A., Humphries, M. J., Jones, E. Y. & Stuart, D. I. ( 1999; ). Crystal structure of a heparin- and integrin-binding segment of human fibronectin. EMBO J 18, 1468–1479.[CrossRef]
    [Google Scholar]
  56. Springer, T. A. ( 1997; ). Folding of the N-terminal, ligand-binding region of integrin α-subunits into a β-propeller domain. Proc Natl Acad Sci U S A 94, 65–72.[CrossRef]
    [Google Scholar]
  57. Sriramarao, P., DiScipio, R. G., Cobb, R. R., Cybulsky, M., Stachnick, G., Castaneda, D., Elices, M. & Broide, D. H. ( 2000; ). VCAM-1 is more effective than MAdCAM-1 in supporting eosinophil rolling under conditions of shear flow. Blood 95, 592–601.
    [Google Scholar]
  58. Tidswell, M., Pachynski, R., Wu, S. W. & 10 other authors ( 1997; ). Structure-function analysis of the integrin β7 subunit: identification of domains involved in adhesion to MAdCAM-1. J Immunol 159, 1497–1505.
    [Google Scholar]
  59. Triantafilou, K., Takada, Y. & Triantafilou, M. ( 2001; ). Mechanisms of integrin-mediated virus attachment and internalization process. Crit Rev Immunol 21, 311–322.
    [Google Scholar]
  60. Wayner, E. A. & Kovach, N. L. ( 1992; ). Activation-dependent recognition by hematopoietic cells of the LDV sequence in the V region of fibronectin. J Cell Biol 116, 489–497.[CrossRef]
    [Google Scholar]
  61. Williams, M. B., Rose, J. R., Rott, L. S., Franco, M. A., Greenberg, H. B. & Butcher, E. C. ( 1998; ). The memory B cell subset responsible for the secretory IgA response and protective humoral immunity to rotavirus expresses the intestinal homing receptor, α4β7. J Immunol 161, 4227–4235.
    [Google Scholar]
  62. Xiao, T., Takagi, J., Coller, B. S., Wang, J. H. & Springer, T. A. ( 2004; ). Structural basis for allostery in integrins and binding to fibrinogen-mimetic therapeutics. Nature 432, 59–67.[CrossRef]
    [Google Scholar]
  63. Yokosaki, Y., Matsuura, N., Sasaki, T. & 7 other authors ( 1999; ). The integrin α9β1 binds to a novel recognition sequence (SVVYGLR) in the thrombin-cleaved amino-terminal fragment of osteopontin. J Biol Chem 274, 36328–36334.[CrossRef]
    [Google Scholar]
  64. Youngman, K. R., Franco, M. A., Kuklin, N. A., Rott, L. S., Butcher, E. C. & Greenberg, H. B. ( 2002; ). Correlation of tissue distribution, developmental phenotype, and intestinal homing receptor expression of antigen-specific B cells during the murine anti-rotavirus immune response. J Immunol 168, 2173–2181.[CrossRef]
    [Google Scholar]
  65. Yuan, L., Ward, L. A., Rosen, B. I., To, T. L. & Saif, L. J. ( 1996; ). Systematic and intestinal antibody-secreting cell responses and correlates of protective immunity to human rotavirus in a gnotobiotic pig model of disease. J Virol 70, 3075–3083.
    [Google Scholar]
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