Skip to main content
PMC home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1987 Jan;79(1):148–154. doi: 10.1172/JCI112775

Sialic acid glycoproteins inhibit in vitro and in vivo replication of rotaviruses.

R H Yolken, R Willoughby, S B Wee, R Miskuff, S Vonderfecht
PMCID: PMC424010  PMID: 3025257

Abstract

We investigated the interactions of rotaviruses with glycoproteins and cells that support rotaviral replication. We found that a wide range of naturally occurring glycoproteins, including ovalbumins and ovomucoids from chicken and turkey eggs, and mucin derived from bovine submaxillary glands, inhibit the replication of rotaviruses in MA-104 cells. Our studies further indicated that the glycoproteins bind directly to rotaviruses and that virus-glycoprotein binding is dependent largely upon interactions with sialic acid oligosaccharides. We found that accessible sialic acid oligosaccharides are required for efficient rotavirus infection of MA-104 cells, thus demonstrating that sialic acid oligosaccharides play an important role in the interactions of rotaviruses with both glycoproteins and cells that support rotaviral replication. Bovine submaxillary mucin and chicken ovoinhibitor can also prevent the shedding of rotavirus antigen and the development of rotavirus gastroenteritis in a mouse model of rotavirus infection. Our findings document that a range of glycoproteins inhibit the in vivo and in vitro replication of rotaviruses and suggest that the alteration in the quantity or chemical composition of intestinal glycoproteins is a potential means for the modulation of enteric infections.

Full text

PDF
150

Images in this article

151Image
on p.151

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Armstrong G. D., Paul R. W., Lee P. W. Studies on reovirus receptors of L cells: virus binding characteristics and comparison with reovirus receptors of erythrocytes. Virology. 1984 Oct 15;138(1):37–48. doi: 10.1016/0042-6822(84)90145-4. [DOI] [PubMed] [Google Scholar]
  2. Bastardo J. W., Holmes I. H. Attachment of SA-11 rotavirus to erythrocyte receptors. Infect Immun. 1980 Sep;29(3):1134–1140. doi: 10.1128/iai.29.3.1134-1140.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Carlson S. E. N-acetylneuraminic acid concentrations in human milk oligosaccharides and glycoproteins during lactation. Am J Clin Nutr. 1985 Apr;41(4):720–726. doi: 10.1093/ajcn/41.4.720. [DOI] [PubMed] [Google Scholar]
  4. Co M. S., Gaulton G. N., Fields B. N., Greene M. I. Isolation and biochemical characterization of the mammalian reovirus type 3 cell-surface receptor. Proc Natl Acad Sci U S A. 1985 Mar;82(5):1494–1498. doi: 10.1073/pnas.82.5.1494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cukor G., Blacklow N. R. Human viral gastroenteritis. Microbiol Rev. 1984 Jun;48(2):157–179. doi: 10.1128/mr.48.2.157-179.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Eiden J., Lederman H. M., Vonderfecht S., Yolken R. T-cell-deficient mice display normal recovery from experimental rotavirus infection. J Virol. 1986 Feb;57(2):706–708. doi: 10.1128/jvi.57.2.706-708.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Estes M. K., Palmer E. L., Obijeski J. F. Rotaviruses: a review. Curr Top Microbiol Immunol. 1983;105:123–184. doi: 10.1007/978-3-642-69159-1_3. [DOI] [PubMed] [Google Scholar]
  8. Eydelloth R. S., Vonderfecht S. L., Sheridan J. F., Enders L. D., Yolken R. H. Kinetics of viral replication and local and systemic immune responses in experimental rotavirus infection. J Virol. 1984 Jun;50(3):947–950. doi: 10.1128/jvi.50.3.947-950.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Flores J., Nakagomi O., Nakagomi T., Glass R., Gorziglia M., Askaa J., Hoshino Y., Perez-Schael I., Kapikian A. Z. The role of rotaviruses in pediatric diarrhea. Pediatr Infect Dis. 1986 Jan-Feb;5(1 Suppl):S53–S62. doi: 10.1097/00006454-198601001-00011. [DOI] [PubMed] [Google Scholar]
  10. Gentsch J. R., Pacitti A. F. Effect of neuraminidase treatment of cells and effect of soluble glycoproteins on type 3 reovirus attachment to murine L cells. J Virol. 1985 Nov;56(2):356–364. doi: 10.1128/jvi.56.2.356-364.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Greenberg H. B., Valdesuso J., van Wyke 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. 1983 Aug;47(2):267–275. doi: 10.1128/jvi.47.2.267-275.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Greenberg H., McAuliffe V., Valdesuso J., Wyatt R., Flores J., Kalica A., Hoshino Y., Singh N. Serological analysis of the subgroup protein of rotavirus, using monoclonal antibodies. Infect Immun. 1983 Jan;39(1):91–99. doi: 10.1128/iai.39.1.91-99.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hauttecoeur B., Sonnino S., Ghidoni R. Characterization of two molecular species GD3 ganglioside from bovine buttermilk. Biochim Biophys Acta. 1985 Feb 8;833(2):303–307. doi: 10.1016/0005-2760(85)90202-4. [DOI] [PubMed] [Google Scholar]
  14. Hoshino Y., Sereno M. M., Midthun K., Flores J., Kapikian A. Z., Chanock R. M. Independent segregation of two antigenic specificities (VP3 and VP7) involved in neutralization of rotavirus infectivity. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8701–8704. doi: 10.1073/pnas.82.24.8701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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. 1983 Jul;41(1):169–173. doi: 10.1128/iai.41.1.169-173.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hoskins L. C., Agustines M., McKee W. B., Boulding E. T., Kriaris M., Niedermeyer G. Mucin degradation in human colon ecosystems. Isolation and properties of fecal strains that degrade ABH blood group antigens and oligosaccharides from mucin glycoproteins. J Clin Invest. 1985 Mar;75(3):944–953. doi: 10.1172/JCI111795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kalica A. R., Flores J., Greenberg H. B. Identification of the rotaviral gene that codes for hemagglutination and protease-enhanced plaque formation. Virology. 1983 Feb;125(1):194–205. doi: 10.1016/0042-6822(83)90073-9. [DOI] [PubMed] [Google Scholar]
  18. Krah D. L., Crowell R. L. A solid-phase assay of solubilized HeLa cell membrane receptors for binding group B coxsackieviruses and polioviruses. Virology. 1982 Apr 15;118(1):148–156. doi: 10.1016/0042-6822(82)90328-2. [DOI] [PubMed] [Google Scholar]
  19. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  20. Losonsky G. A., Johnson J. P., Winkelstein J. A., Yolken R. H. Oral administration of human serum immunoglobulin in immunodeficient patients with viral gastroenteritis. A pharmacokinetic and functional analysis. J Clin Invest. 1985 Dec;76(6):2362–2367. doi: 10.1172/JCI112248. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Markwell M. A. A new solid-state reagent to iodinate proteins. I. Conditions for the efficient labeling of antiserum. Anal Biochem. 1982 Sep 15;125(2):427–432. doi: 10.1016/0003-2697(82)90025-2. [DOI] [PubMed] [Google Scholar]
  22. Muresan V., Iwanij V., Smith Z. D., Jamieson J. D. Purification and use of limulin: a sialic acid-specific lectin. J Histochem Cytochem. 1982 Sep;30(9):938–946. doi: 10.1177/30.9.6897073. [DOI] [PubMed] [Google Scholar]
  23. Norin K. E., Gustafsson B. E., Lindblad B. S., Midtvedt T. The establishment of some microflora associated biochemical characteristics in feces from children during the first years of life. Acta Paediatr Scand. 1985 Mar;74(2):207–212. doi: 10.1111/j.1651-2227.1985.tb10951.x. [DOI] [PubMed] [Google Scholar]
  24. Riepenhoff-Talty M., Lee P. C., Carmody P. J., Barrett H. J., Ogra P. L. Age-dependent rotavirus-enterocyte interactions. Proc Soc Exp Biol Med. 1982 Jun;170(2):146–154. doi: 10.3181/00379727-170-41410. [DOI] [PubMed] [Google Scholar]
  25. Rotbart H. A., Yolken R. H., Nelson W. L., Davis D., Roe M. H., Levin M. J. Confirmatory testing of Rotazyme results in neonates. J Pediatr. 1985 Aug;107(2):289–292. doi: 10.1016/s0022-3476(85)80153-0. [DOI] [PubMed] [Google Scholar]
  26. Slomiany A., Zdebska E., Slomiany B. L. Structures of the neutral oligosaccharides isolated from A-active human gastric mucin. J Biol Chem. 1984 Dec 10;259(23):14743–14749. [PubMed] [Google Scholar]
  27. Stanley R. A., Lee S. P., Roberton A. M. Heterogeneity in gastrointestinal mucins. Biochim Biophys Acta. 1983 Oct 18;760(2):262–269. doi: 10.1016/0304-4165(83)90172-1. [DOI] [PubMed] [Google Scholar]
  28. Suzuki Y., Matsunaga M., Matsumoto M. N-Acetylneuraminyllactosylceramide, GM3-NeuAc, a new influenza A virus receptor which mediates the adsorption-fusion process of viral infection. Binding specificity of influenza virus A/Aichi/2/68 (H3N2) to membrane-associated GM3 with different molecular species of sialic acid. J Biol Chem. 1985 Feb 10;260(3):1362–1365. [PubMed] [Google Scholar]
  29. Suzuki Y., Suzuki T., Matsumoto M. Isolation and characterization of receptor sialoglycoprotein for hemagglutinating virus of Japan (Sendai virus) from bovine erythrocyte membrane. J Biochem. 1983 Jun;93(6):1621–1633. doi: 10.1093/oxfordjournals.jbchem.a134301. [DOI] [PubMed] [Google Scholar]
  30. Tidwell R. R., Geratz J. D., Dubovi E. J. Aromatic amidines: comparison of their ability to block respiratory syncytial virus induced cell fusion and to inhibit plasmin, urokinase, thrombin, and trypsin. J Med Chem. 1983 Feb;26(2):294–298. doi: 10.1021/jm00356a036. [DOI] [PubMed] [Google Scholar]
  31. Utagawa E. T., Miyamura K., Mukoyama A., Kono R. Neuraminidase-sensitive erythrocyte receptor for enterovirus type 70. J Gen Virol. 1982 Nov;63(Pt 1):141–148. doi: 10.1099/0022-1317-63-1-141. [DOI] [PubMed] [Google Scholar]
  32. Vonderfecht S. L., Huber A. C., Eiden J., Mader L. C., Yolken R. H. Infectious diarrhea of infant rats produced by a rotavirus-like agent. J Virol. 1984 Oct;52(1):94–98. doi: 10.1128/jvi.52.1.94-98.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Wyatt R. G., Mebus C. A., Yolken R. H., Kalica A. R., James H. D., Jr, Kapikian A. Z., Chanock R. M. Rotaviral immunity in gnotobiotic calves: heterologous resistance to human virus induced by bovine virus. Science. 1979 Feb 9;203(4380):548–550. doi: 10.1126/science.216077. [DOI] [PubMed] [Google Scholar]
  34. Yolken R. H., Bishop C. A., Townsend T. R., Bolyard E. A., Bartlett J., Santos G. W., Saral R. Infectious gastroenteritis in bone-marrow-transplant recipients. N Engl J Med. 1982 Apr 29;306(17):1010–1012. doi: 10.1056/NEJM198204293061701. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES