Glycoconjugate Journal

, Volume 23, Issue 1–2, pp 27–37 | Cite as

Role of sialic acids in rotavirus infection

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Abstract

Rotaviruses are the leading cause of childhood diarrhea. The entry of rotaviruses into the host cell is a complex process that includes several interactions of the outer layer proteins of the virus with different cell surface molecules. The fact that neuraminidase treatment of the cells, or preincubation of the virus with sialic acid-containing compounds decrease the infectivity of some rotavirus strains, suggested that these viruses interact with sialic acid on the cell surface. The infectivity of some other rotavirus strains is not affected by neuraminidase treatment of the cells, and therefore they are considered neuraminidase-resistant. However, the current evidence suggests that even these neuraminidase-resistant strains might interact with sialic acids located in context different from that of the sialic acids used by the neuraminidase-sensitive strains. This review summarizes our current knowledge of the rotavirus-sialic acid interaction, its structural basis, the specificity with which distinct rotavirus isolates interact with sialic acid-containing compounds, and also the potential use of these compounds as therapeutic agents.

Keywords

Rotavirus Sialic acid Ganglioside Glycolipid Glycoconjugate 

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References

  1. 1.
    Parashar, U.D., Hummelman, E.G., Bresee, J.S., Miller, M.A., Glass, R.I.: Global illness and deaths caused by rotavirus disease in children. Emerg. Infect. Dis. 9, 565–572 (2003)PubMedGoogle Scholar
  2. 2.
    Cheever, F.S., Mueller, J.H.: Epidemic diarrheal disease of suckling mice. I. Manifestation, epidemiology, and attempts to transmit the disease. J. Exp. Med. 85, 405–416 (1947)CrossRefGoogle Scholar
  3. 3.
    Adams, W.R., Kraft, L.M.: Epizootic diarrhea of infant mice: identification of the etiologic agent. Science 141, 359–360 (1963)PubMedGoogle Scholar
  4. 4.
    Mebus, C.A., Underdahl, N.R., Rhodes, M.B., Twiehaus, M.J.: Further studies on neonatal calf diarrhea virus. Proc. Annu. Meet. U. S. Anim. Health Assoc. 73, 97–99 (1969)PubMedGoogle Scholar
  5. 5.
    Bishop, R.F., Davidson, G.P., Holmes, I.H., Ruck, B.J.: Virus particles in epithelial cells of duodenal mucosa from children with viral gastroenteritis. Lancet. 1281–1283 (1973)Google Scholar
  6. 6.
    Parashar, U.D., Holman, R.C., Cummings, K.C., Staggs, N.W., Curns, A.T., Zimmerman, C.M., Kaufman, S.F., Lewis, J.E., Vugia, D.J., Powell, K.E., Glass, R.I.: Trends in intussusception-associated hospitalizations and deaths among US infants. Pediatrics 106, 1413–1421 (2000)CrossRefPubMedGoogle Scholar
  7. 7.
    Prasad, B.V., Burns, J.W., Marietta, E., Estes, M.K., Chiu, W.: Localization of VP4 neutralization sites in rotavirus by three-dimensional cryo-electron microscopy. Nature 343, 476–479 (1990)CrossRefPubMedGoogle Scholar
  8. 8.
    Lopez, S., Arias, C.F.: Multistep entry of rotavirus into cells: a Versaillesque dance. Trends Microbiol. 12, 271–278 (2004)CrossRefPubMedGoogle Scholar
  9. 9.
    Arias, C.F., Romero, P., Alvarez, V., Lopez, S.: Trypsin activation pathway of rotavirus infectivity. Journal Of Virology 70(9), 5832–5839 (1996)PubMedGoogle Scholar
  10. 10.
    Espejo, R.T., Lopez, S., Arias, C.: Structural polypeptides of simian rotavirus SA11 and the effect of trypsin. J. Virol. 37, 156–160 (1981)PubMedGoogle Scholar
  11. 11.
    Estes, M.K., Graham, D.Y., Mason, B.B.: Proteolytic enhancement of rotavirus infectivity: molecular mechanisms. J. Virol. 39, 879–888 (1981)PubMedGoogle Scholar
  12. 12.
    Clark, S.M., Roth, J.R., Clark, M.L., Barnett, B.B., Spendlove, R.S.: Trypsin enhancement of rotavirus infectivity: mechanism of enhancement. J. Virol. 39, 816–822 (1981)PubMedGoogle Scholar
  13. 13.
    Kaljot, K.T., Shaw, R.D., Rubin, D.H., Greenberg, H.B.: Infectious rotavirus enters cells by direct cell membrane penetration, not by endocytosis. J. Virol. 62, 1136–1144 (1988)PubMedGoogle Scholar
  14. 14.
    Mossel, E.C., Ramig, R.F.: A lymphatic mechanism of rotavirus extraintestinal spread in the neonatal mouse. J. Virol. 77, 12352–12356 (2003)CrossRefPubMedGoogle Scholar
  15. 15.
    Ciarlet, M., Crawford, S.E., Cheng, E., Blutt, S.E., Rice, D.A., Bergelson, J.M., Estes, M.K.: VLA-2 (alpha2beta1) integrin promotes rotavirus entry into cells but is not necessary for rotavirus attachment. J. Virol. 76, 1109–1123 (2002)PubMedGoogle Scholar
  16. 16.
    Spence, L., Fauvel, M., Petro, R., Bloch, S.: Haemagglutinin from Rotavirus. Lancet. 2, 1023 (1976)Google Scholar
  17. 17.
    Inaba, Y., Sato, K., Takahashi, E., Kurogi, H., Satoda, K.: Hemagglutination with Nebraska calf diarrhea virus. Microbiol. Immunol. 21, 531–534 (1977)PubMedGoogle Scholar
  18. 18.
    Kalica, A.R., James, J.D.Jr., Kapikian, A.Z.: Hemagglutination by simian rotavirus. J. Clin. Microbiol. 7, 314–315 (1978)PubMedGoogle Scholar
  19. 19.
    Kitaoka, S., Suzuki, H., Numazaki, T., Sato, T., Konno, T., Ebina, T., Ishida, N., Nakagomi, O., Nakagomi, T.: Hemagglutination by human rotavirus strains. J. Med. Virol. 13, 215–222 (1984)PubMedGoogle Scholar
  20. 20.
    Shinozaki, T., Fujii, R., Sato, K., Takahashi, E., Ito, Y., Inaba, Y.: Haemagglutinin from human reovirus-like agent. Lancet. 1, 877–878 (1978)PubMedGoogle Scholar
  21. 21.
    Fukudome, K., Yoshie, O., Konno, T.: Comparison of human, simian, and bovine rotaviruses for requirement of sialic acid in hemagglutination and cell absorption. Virology 172, 196–205 (1989)CrossRefPubMedGoogle Scholar
  22. 22.
    Bastardo, J.W., Holmes, I.H.: Attachment of SA-11 rotavirus to erythrocyte receptors. Infect. Immun. 29, 1134–1140 (1980)PubMedGoogle Scholar
  23. 23.
    Keljo, D.J., Smith, A.K.: Characterization of binding of simian rotavirus SA-11 to cultured epithelial cells. J. Pediatr. Gastroenterol Nutr. 7, 249–256 (1988)PubMedGoogle Scholar
  24. 24.
    Mendez, E., Arias, C.F., Lopez, S.: 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 (1993)PubMedGoogle Scholar
  25. 25.
    Yolken, R.H., Willoughby, R., Wee, S.B., Miskuff, R., Vonderfecht, S.: Sialic acid glycoproteins inhibit in vitro and in vivo replication of rotaviruses. J. Clin. Invest. 79, 148–154 (1987)PubMedGoogle Scholar
  26. 26.
    Guo, C.T., Nakagomi, O., Mochizuki, M., Ishida, H., Kiso, M., Ohta, Y., Suzuki, T., Miyamoto, D., Hidari, K.I., Suzuki, Y, Ganglioside GM(1a) on the cell surface is involved in the infection by human rotavirus KUN and MO strains. J. Biochem. (Tokyo) 126, 683–688 (1999)Google Scholar
  27. 27.
    Ciarlet, M., Estes, M.K.: Human and most animal rotavirus strains do not require the presence of sialic acid on the cell surface for efficient infectivity. J. Gen. Virol. 80, 943–948 (1999)PubMedGoogle Scholar
  28. 28.
    Ciarlet, M., Ludert, J.E., Iturriza-Gomara, M., Liprandi, F., Gray, J.J., Desselberger, U., Estes, M.K.: 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 (2002)PubMedGoogle Scholar
  29. 29.
    Fauvel, M., Spence, L., Babiuk, L.A., Petro, R., Bloch, S.: Hemagglutination and hemagglutination-inhibition studies with a strain of Nebraska calf diarrhea virus (bovine rotavirus). Intervirology 9, 95–105 (1978)PubMedGoogle Scholar
  30. 30.
    Lee, J., Yoo, D., Redmond, M.J., Attah-Poku, S.K., van den Hurk, J.V., Babiuk, L.A.: Characterization of the interaction between VP8 of bovine rotavirus C486 and cellular components on MA-104 cells and erythrocytes. Can. J. Vet. Res. 62, 56–62 (1998)PubMedGoogle Scholar
  31. 31.
    Spence, L., Fauvel, M., Petro, R., Babiuk, L.A.: Comparison of rotavirus strains by hemagglutination inhibition. Can. J. Microbiol. 24, 353–362 (1978)PubMedGoogle Scholar
  32. 32.
    Nakagomi, O., Mochizuki, M., Aboudy, Y., Shif, I., Silberstein, I., Nakagomi, T.: Hemagglutination by a human rotavirus isolate as evidence for transmission of animal rotaviruses to humans. J. Clin. Microbiol. 30, 1011–1013 (1992)PubMedGoogle Scholar
  33. 33.
    Hoshino, Y., Wyatt, R.G., Greenberg, H.B., Kalica, A.R., Flores, J., Kapikian, A.Z.: Serological comparison of canine rotavirus with various simian and human rotaviruses by plaque reduction neutralization and hemagglutination inhibition tests. Infect. Immun. 41, 169–173 (1983)PubMedGoogle Scholar
  34. 34.
    Mochizuki, M., Nakagomi, O.: Haemagglutination by rotaviruses in relation to VP4 genotypes. Res. Virol. 146, 371–374 (1995)PubMedGoogle Scholar
  35. 35.
    Lee, J.B., Youn, S.J., Nakagomi, T., Park, S.Y., Kim, T.J., Song, C.S., Jang, H.K., Kim, B.S., Nakagomi, O.: Isolation, serologic and molecular characterization of the first G3 caprine rotavirus. Arch. Virol. 148, 643–657 (2003)PubMedGoogle Scholar
  36. 36.
    Ludert, J.E., Feng, N., Yu, J.H., Broome, R.L., Hoshino, Y., Greenberg, H.B.: Genetic mapping indicates that VP4 is the rotavirus cell attachment protein in vitro and in vivo. J. Virol. 70, 487–493 (1996)PubMedGoogle Scholar
  37. 37.
    Hoshino, Y., Sereno, M.M., Midthun, K., Flores, J., Chanock, R.M., Kapikian, A.Z.: Analysis by plaque reduction neutralization assay of intertypic rotaviruses suggests that gene reassortment occurs in vivo. J. Clin. Microbiol. 25, 290–294 (1987)PubMedGoogle Scholar
  38. 38.
    Hoshino, Y., Wyatt, R.G., Greenberg, H.B., Kalica, A.R., Flores, J., Kapikian, A.Z.: Isolation and characterization of an equine rotavirus. J. Clin. Microbiol. 18, 585–591 (1983)PubMedGoogle Scholar
  39. 39.
    Fuentes Panana, E.M., Lopez, S., Gorziglia, M., Arias, C.F.: Mapping the hemagglutination domain of rotaviruses. J. Virol. 69, 2629–2632 (1995)PubMedGoogle Scholar
  40. 40.
    Hoshino, Y., Wyatt, R.G., Greenberg, H.B., Kalica, A.R., Flores, J., Kapikian, A.Z.: Isolation, propagation, and characterization of a second equine rotavirus serotype. Infect. Immun. 41, 1031–1037 (1983)PubMedGoogle Scholar
  41. 41.
    Sugiyama, M., Goto, K., Uemukai, H., Mori, Y., Ito, N., Minamoto, N.: Attachment and infection to MA104 cells of avian rotaviruses require the presence of sialic acid on the cell surface. J. Vet. Med. Sci. 66, 461–463 (2004)PubMedGoogle Scholar
  42. 42.
    Greenberg, H.B., Valdesuso, J., van, W.K., Midthun, K., Walsh, M., McAuliffe, V., Wyatt, R.G., Kalica, A.R., Flores, J., Hoshino, Y.: Production and preliminary characterization of monoclonal antibodies directed at two surface proteins of rhesus rotavirus. J. Virol. 47, 267–275 (1983)PubMedGoogle Scholar
  43. 43.
    Kalica, A.R., Flores, J., Greenberg, H.B.: Identification of the rotaviral gene that codes for hemagglutination and protease-enhanced plaque formation. Virology 125, 194–205 (1983)CrossRefPubMedGoogle Scholar
  44. 44.
    Mackow, E.R., Barnett, J.W., Chan, H., Greenberg, H.B.: The rhesus rotavirus outer capsid protein VP4 functions as a hemagglutinin and is antigenically conserved when expressed by a baculovirus recombinant. J. Virol. 63, 1661–1668 (1989)PubMedGoogle Scholar
  45. 45.
    Lizano, M., Lopez, S., Arias, C.F.: The amino-terminal half of rotavirus SA114fM VP4 protein contains a hemagglutination domain and primes for neutralizing antibodies to the virus. J. Virol. 65, 1383–1391 (1991)PubMedGoogle Scholar
  46. 46.
    Fiore, L., Greenberg, H.B., Mackow, E.R.: The VP8 fragment of VP4 is the rhesus rotavirus hemagglutinin. Virology 181, 553–563 (1991)CrossRefPubMedGoogle Scholar
  47. 47.
    Isa, P., Lopez, S., Segovia, L., Arias, C.F.: Functional and structural analysis of the sialic acid-binding domain of rotaviruses. J. Virol. 71(9), 6749–6756 (1997)PubMedGoogle Scholar
  48. 48.
    Dormitzer, P.R., Sun, Z.Y., Blixt, O., Paulson, J.C., Wagner, G., Harrison, S.C.: Specificity and affinity of sialic acid binding by the rhesus rotavirus VP8 core. J. Virol. 76, 10512–10517 (2002)CrossRefPubMedGoogle Scholar
  49. 49.
    Dormitzer, P.R., Sun, Z.Y., Wagner, G., Harrison, S.C.: The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. Embo. J. 21, 885–897 (2002)CrossRefPubMedGoogle Scholar
  50. 50.
    Delorme, C., Brussow, H., Sidoti, J., Roche, N., Karlsson, K.A., Neeser, J.R., Teneberg, S.: Glycosphingolipid binding specificities of rotavirus: identification of a sialic acid-binding epitope. J. Virol. 75, 2276–2287 (2001)CrossRefPubMedGoogle Scholar
  51. 51.
    Mendez, E., Arias, C.F., Lopez, S.: Interactions between the two surface proteins of rotavirus may alter the receptor-binding specificity of the virus. J. Virol. 70, 1218–1222 (1996)PubMedGoogle Scholar
  52. 52.
    Monnier, N.K., Dormitzer, P.R.: High resolution structural and functional studies of sialic acid binding variants of rotavirus VP8. 8th Interl Symp Double-Stranded Viruses, P2.8 (2003)Google Scholar
  53. 53.
    Willoughby, R.E., Yolken, R.H., Schnaar, R.L.: Rotaviruses specifically bind to the neutral glycosphingolipid asialo-GM1. J. Virol. 64, 4830–4835 (1990)PubMedGoogle Scholar
  54. 54.
    Willoughby, R.E.: Rotaviruses preferentially bind O-linked sialylglycoconjugates and sialomucins. Glycobiology 3, 437–445 (1993)PubMedGoogle Scholar
  55. 55.
    Srnka, C.A., Tiemeyer, M., Gilbert, J.H., Moreland, M., Schweingruber, H., de, L.B., James, P.G., Gant, T., Willoughby, R.E., Yolken, RH, et al.: Cell surface ligands for rotavirus: mouse intestinal glycolipids and synthetic carbohydrate analogs. Virology 190, 794–805 (1992)CrossRefPubMedGoogle Scholar
  56. 56.
    Rolsma, M.D., Kuhlenschmidt, T.B., Gelberg, H.B., Kuhlenschmidt, M.S.: Structure and function of a ganglioside receptor for porcine rotavirus. J. Virol. 72, 9079–9091 (1998)PubMedGoogle Scholar
  57. 57.
    Superti, F., Donelli, G.: Gangliosides as binding sites in SA-11 rotavirus infection of LLC-MK2 cells. J. Gen. Virol. (1991)Google Scholar
  58. 58.
    Rolsma, M.D., Gelberg, HB., Kuhlenschmidt, M.S.: Assay for evaluation of rotavirus-cell interactions: identification of an enterocyte ganglioside fraction that mediates group A porcine rotavirus recognition. J. Virol. 68, 258–268 (1994)PubMedGoogle Scholar
  59. 59.
    Colarow, L., Turini, M., Teneberg, S., Berger, A.: Characterization and biological activity of gangliosides in buffalo milk. Biochim. Biophys. Acta. 1631, 94–106 (2003)PubMedGoogle Scholar
  60. 60.
    Guerrero, C.A., Zarate, S., Corkidi, G., Lopez, S., Arias, C.F.: Biochemical characterization of rotavirus receptors in MA104 cells. J. Virol. 74, 9362–9371 (2000)CrossRefPubMedGoogle Scholar
  61. 61.
    Jolly, C.L., Beisner, B.M., Ozser, E., Holmes, I.H.: Non-lytic extraction and characterisation of receptors for multiple strains of rotavirus. Arch. Virol. 146, 1307–1323 (2001)CrossRefPubMedGoogle Scholar
  62. 62.
    Elbein, A.D.: Inhibitors of glycoprotein synthesis. Methods Enzymol. 98, 135–154 (1983)PubMedGoogle Scholar
  63. 63.
    Pan, Y.T., Elbein, A.D.: How can N-linked glycosylation and processing inhibitors be used to study carbohydrate synthesis and function. In: Glycoproteins edited by Montreuil J, Vliegenthart JFG, Schachter H (Elsevier, Amsterdam, 1995), pp. 415–454.Google Scholar
  64. 64.
    Roberts, L.: Vaccines. Rotavirus vaccines' second chance. Science 305, 1890–1893 (2004)PubMedGoogle Scholar
  65. 65.
    Chen, C.C., Baylor, M., Bass, D.M.: Murine intestinal mucins inhibit rotavirus infection. Gastroenterology 105, 84–92 (1993)PubMedGoogle Scholar
  66. 66.
    Willoughby, R.E., Yolken, R.H.: SA11 rotavirus is specifically inhibited by an acetylated sialic acid. J. Infect. Dis. 161, 116–119 (1990)PubMedGoogle Scholar
  67. 67.
    Yolken, R.H., Ojeh, C., Khatri, I.A., Sajjan U, Forstner, J.F.: Intestinal mucins inhibit rotavirus replication in an oligosaccharide-dependent manner. J. Infect. Dis. 169, 1002–1006 (1994)PubMedGoogle Scholar
  68. 68.
    Yolken, R.H., Peterson, J.A., Vonderfecht, S.L., Fouts, E.T., Midthun, K., Newburg, D.S.: Human milk mucin inhibits rotavirus replication and prevents experimental gastroenteritis. J. Clin. Invest. 90, 1984–1991 (1992)PubMedGoogle Scholar
  69. 69.
    Reading, P.C., Holmskov, U., Anders, E.M.: Antiviral activity of bovine collectins against rotaviruses. Journal Of General Virology 79(9), 2255–2263 (1998)PubMedGoogle Scholar
  70. 70.
    Superti, F., Siciliano, R., Rega, B., Giansanti, F., Valenti, P., Antonini, G.: Involvement of bovine lactoferrin metal saturation, sialic acid and protein fragments in the inhibition of rotavirus infection. Biochim. Biophys. Acta. 1528, 107–115 (2001)PubMedGoogle Scholar
  71. 71.
    Kvistgaard, A.S., Pallesen, L.T., Arias, C.F., Lopez, S., Petersen, T.E.: Heegaard CW, and Rasmussen JT, Inhibitory effects of human and bovine milk constituents on rotavirus infections. J. Dairy. Sci. 87, 4088–96 (2004)PubMedGoogle Scholar
  72. 72.
    Kiefel, M.J., Beisner, B., Bennett, S., Holmes, I.D., vonItzstein, M.: Synthesis and biological evaluation of N-acetylneuraminic acid-based rotavirus inhibitors. J. Med. Chem. 39 (6), 1314–1320 (1996)CrossRefPubMedGoogle Scholar
  73. 73.
    Fazli, A., Bradley, S.J., Kiefel, M.J., Jolly, C., Holmes, I.H., von Itzstein, M.: Synthesis and biological evaluation of sialylmimetics as rotavirus inhibitors. J. Med. Chem. 44, 3292–3301 (2001)CrossRefPubMedGoogle Scholar
  74. 74.
    Koketsu, M., Nitoda, T., Sugino, H., Juneja, L.R., Kim, M., Yamamoto, T., Abe, N., Kajimoto, T., Wong, C.H.: Synthesis of a novel sialic acid derivative (sialylphospholipid) as an antirotaviral agent. J. Med. Chem. 40(21), 3332–3335 (1997)CrossRefPubMedGoogle Scholar
  75. 75.
    Takahashi, K., Ohashi, K., Abe, Y., Mori, S., Taniguchi, K., Ebina, T., Nakagomi, O., Terada, M., Shigeta, S.: Protective efficacy of a sulfated sialyl lipid (NMSO3) against human rotavirus-induced diarrhea in a mouse model. Antimicrob. Agents Chemother 46, 420–424 (2002)PubMedGoogle Scholar
  76. 76.
    Urashima. T., Saito, T., Nakamura, T., Messer, M.: Oligosaccharides of milk and colostrum in non-human mammals. Glycoconj J. 18, 357–371 (2001)CrossRefPubMedGoogle Scholar

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© Springer Science + Business Media, LLC 2006

Authors and Affiliations

  1. 1.Departamento de Genética del Desarrollo y Fisiología Molecular, Instituto de BiotecnologíaUniversidad Nacional Autónoma de MéxicoCuernavacaMexico

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