1887

Abstract

The carbohydrate epitope Galα1-3Galβ1-4GlcNAc-R (α-galactosyl) is abundantly expressed on cells of non-primate mammals, prosimians and New World monkeys, where it is synthesized by the enzyme α1,3-galactosyltransferase (α1,3GT). Old World monkeys, apes and humans lack α1,3GT and hence do not synthesize α-galactosyl epitopes. Instead, these species produce a natural antibody, anti-Gal, which interacts specifically with α-galactosyl epitopes and which constitutes up to 1% of circulating immunoglobulins in humans. We have used eastern equine encephalitis (EEE) virus as a model to examine the differential expression of α-galactosyl epitopes on the glycoproteins of virus propagated in cells that either produce or lack α1,3GT. As predicted, virus propagated in Vero cells (derived from the African green monkey, an Old World monkey) did not express α-galactosyl epitopes. In contrast, virus propagated in mouse 3T3 cells (EEE) expressed approximately 80 α-galactosyl epitopes per virion on both the E1 and the E2 envelope glycoproteins. Thus, expression of the α-galactosyl epitope on virions paralleled that on host cells. The binding of anti-Gal antibody to these epitopes on EEE virions partially neutralized virus infectivity, raising the possibility that anti-Gal production in hosts may influence the initial infectious stage of viruses expressing α-galactosyl epitopes.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-75-5-1177
1994-05-01
2022-01-22
Loading full text...

Full text loading...

/deliver/fulltext/jgv/75/5/JV0750051177.html?itemId=/content/journal/jgv/10.1099/0022-1317-75-5-1177&mimeType=html&fmt=ahah

References

  1. Avila J. L., Rojas M., Galili U. 1989; Immunogenic Galα1→3Gal carbohydrate epitopes are present on pathogenic American Trypanosoma and Leishmania. Journal of Immunology 142:2828–2834
    [Google Scholar]
  2. Blake D. A., Goldstein I. J. 1980; Resolution of nucleotide sugars and oligosaccharides by lectin affinity chromatography. Analytical Biochemistry 102:103–109
    [Google Scholar]
  3. Burke D. J., Keegstra K. 1976; Purification and composition of the proteins from Sindbis virus grown in chick and BHK cells. Journal of Virology 20:676–686
    [Google Scholar]
  4. Chang G. -J. J., Trent D. W. 1987; Nucleotide sequence of the genome region encoding the 26S mRNA of eastern equine encephalomyelitis virus and the deduced amino acid sequence of the viral structural proteins. Journal of General Virology 68:2129–2142
    [Google Scholar]
  5. Davidson S. K., Hunt L. A. 1985; Hazelhurst vesicular stomatitis virus G and Sindbis virus El glycoproteins undergo similar host-cell- dependent variation in oligosaccharide processing. Biochemical Journal 229:47–55
    [Google Scholar]
  6. Davin J. C., Malaise M., Foidart J., Mahieu P. 1987; Anti α-galactosyl antibodies and immune complexes in children with Henoch-Schlonlein purpura or IgA nephropathy. Kidney International 31:1132–1139
    [Google Scholar]
  7. Fuller S. D. 1987; The T = 4 envelope of Sindbis virus is organized by interactions with a complementary T = 3 capsid. Cell 48:923–934
    [Google Scholar]
  8. Galili U. 1993; Evolution and pathophysiology of the human natural anti-α-galactosyl IgG (anti-Gal) antibody. Springer Seminars in Immunopathology 15:155–171
    [Google Scholar]
  9. Galili U., Rachmilewitz E. A., Peleg A., Flechner I. 1984; A unique natural human IgG antibody with anti-α-galactosyl specificity. Journal of Experimental Medicine 60:1519–1531
    [Google Scholar]
  10. Galili U., Macher B. A., Buehler J., Shohet S. B. 1985; Human natural anti-α-galactosyl IgG. II. The specific recognition of α(l-3)-linked galactose residues. Journal of Experimental Medicine 162:573–582
    [Google Scholar]
  11. Galili U., Buehler J., Shohet S. B., Macher B. A. 1987a; The human natural anti-Gal IgG. III. The subtlety of immune tolerance in man as demonstrated by crossreactivity between natural anti-Gal and anti-B antibodies. Journal of Experimental Medicine 165:693–704
    [Google Scholar]
  12. Galili U., Clark M. R., Shohet S. B., Buehler J., Macher B. A. 1987b; Evolutionary relationship between the anti-Gal antibody and the Galαl-3Gal epitope in primates. Proceedings of the National Academy of Sciences, U.S.A 84:1369–1373
    [Google Scholar]
  13. Galili U., Shohet S. B., Kobrin E., Stults C. L. M., Macher B. A. 1988; Man, apes, and Old World monkeys differ from other mammals in the expression of α-galactosyl epitopes on nucleated cells. Journal of Biological Chemistry 263:17755–17762
    [Google Scholar]
  14. Geyer R., Geyer H., Strim S., Hunsmann G., Schneider J., Dabrowski U., Dabrowski J. 1984; Major oligosaccharides in the glycoprotein of Friend murine leukemia virus: struture eluci-dation by one and two dimensional proton nuclear magnetic resonance and methylation analysis. Biochemistry 23:5628–5634
    [Google Scholar]
  15. Hsieh P., Rosner M. R., Robbins P. W. 1983; Host-dependent variation of asparagine-linked oligosaccharides at individual glyco-sylation sites of Sindbis virus glycoproteins. Journal of Biological Chemistry 258:2548–2554
    [Google Scholar]
  16. Hunt L. A. 1980; Altered synthesis and processing of oligosac�charides of vesicular stomatitis virus glycoprotein in different lectin- resistant Chinese hamster ovary cell lines. Journal of Virology 35:362–370
    [Google Scholar]
  17. Joziasse D. H., Shaper J. H., Van Den Eunden D. H., Van Tunen A. H., Shaper N. L. 1989; Bovine αl-3 galactosyltransferase: Isolation and characterization of a cDNA clone. Identification of homologous sequences in human genomic DNA. Journal of Biological Chemistry 264:14290–14297
    [Google Scholar]
  18. Klenk H. -D. 1990; Influence of glycosylation on antigenicity of viral proteins. In Immunochemistry of Viruses, II. The Basis for Sero-diagnosis and Vaccines pp. 25–37 Van Regen-mortel M. H. V., Neurath A. R. Edited by New York: Elsevier;
    [Google Scholar]
  19. Klenk H. -D., Rott R. 1980; Cotranslational and post�translational processing of viral glycoproteins. Current Topics in Microbiology and Immunology 90:19–48
    [Google Scholar]
  20. Koblet H. 1990; The ‘merry-go-round’: alphaviruses between vertebrate and invertebrate cells. Advances in Virus Research 38:343–402
    [Google Scholar]
  21. Kornfeld R., Kornfeld S. 1976; Comparative aspects of glycoprotein structure. Annual Review of Biochemistry 45:217–237
    [Google Scholar]
  22. Kornfeld R., Kornfeld S. 1985; Assembly of asparagine-linked oligosaccharides. Annual Review of Biochemistry 54:631–664
    [Google Scholar]
  23. Morris C. D. 1988; Eastern equine encephalomyelitis. In The Arboviruses: Epidemiology and Ecology 3 pp. 1–20 Monath T. P. Edited by Boca Raton: CRC Press;
    [Google Scholar]
  24. Rademacher T. W., Parekh R. B., Dwek R. A. 1988; Glyco-biology. Annual Review of Biochemistry 51:785–838
    [Google Scholar]
  25. Repik P. M., Dalrymple J. M., Brandt W. E., McCown J. M., Russell P. K. 1983; RNA fingerprinting as a method for distinguishing dengue 1 virus strains. American Journal of Tropical Medicine and Hygiene 32:577–589
    [Google Scholar]
  26. Russell P. K., Nisalak A., Sukhavachana P., Vivona S. 1967; A plaque reduction test for dengue virus neutralizing antibodies. Journal of Immunology 99:285–290
    [Google Scholar]
  27. Santer U. V., DeSantis R., Hård K. J., Van Kuik J. A., Vliegen-Thart J. F. G., Won B., Glick M. C. 1989; N-linked oligosaccharide changes with oncogenic transformation require sialylation of multiantennae. European Journal of Biochemistry 181:249–260
    [Google Scholar]
  28. Schlesinger M. J., Schlesinger S. 1986; Formation and assembly of alphavirus glycoproteins. In The Togaviridae and Flaviviridae pp. 121–148 Schlesinger S., Schlesinger M. J. Edited by New York: Plenum Press;
    [Google Scholar]
  29. Schlesinger M. J., Schlesinger S. 1987; Domains of virus glycoproteins. Advances in Virus Research 33:1–44
    [Google Scholar]
  30. Schmaljohn C. S., Hasty S. E., Harrison S. A., Dalrymple J. M. 1983; Characterization of Hantaan virions, the prototype virus of hemorrhagic fever with renal syndrome. Journal of Infectious Diseases 148:1005–1012
    [Google Scholar]
  31. Spiro R. G., Bhoyroo V. D. 1984; Occurrence of α-d-galactosyl residues in thyroglobulins from several species. Localization of the saccharide chains of the complex carbohydrate units. Journal of Biological Chemistry 259:9858–9866
    [Google Scholar]
  32. Stollar V., Stollar B. D., Koo K., Harrap K. A., Schlesinger W. R. 1976; Sialic acid contents of Sindbis virus from vertebrate and mosquito cells: Equivalence of biological and immunological viral properties. Virology 69:104–115
    [Google Scholar]
  33. Strauss J. H., Strauss E. G. 1977; Togaviruses. In The Molecular Biology of Animal Viruses 1 pp. 111–166 Nayak D. P. Edited by New York: Marcel Dekker;
    [Google Scholar]
  34. Strauss J. H.Jr Burge B. W., Darnell J. E. 1970; Carbo�hydrate content of the membrane protein of Sindbis virus. Journal of Molecular Biology 47:437–448
    [Google Scholar]
  35. Thall A., Galili U. 1990; Distribution of Galαl-3Galβl- 4GlcNAc residues on secreted mammalian glycoproteins (thyro-globulin, fibrogen and immunoglobulin G) as measured by a sensitive solid-phase radioimmunoassay. Biochemistry 29:3959–3965
    [Google Scholar]
  36. Thall A., Etienne-Decerf J., Winand R. J., Galili U. 1991; The α-galactosyl epitope on mammalian thyroid cells. Acta endo-crinologica 88:7401–7404
    [Google Scholar]
  37. Weaver S. C., Scott T. W., Lorenz L. H., Repik P. M. 1991; Detection of eastern equine encephalomyelitis virus deposition in Culiseta melanura following ingestion of radiolabeled virus in blood meals. American Journal of Tropical Medicine and Hygiene 44:250–259
    [Google Scholar]
  38. Wood C., Kabat E. A., Murphy L. A., Goldstein I. J. 1979; Immunochemical studies on the combining sites of two isolectins A4 and B4 isolated from Bandeiraea simplicifolia. Archives of Biochemistry and Biophysics 198:1–9
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-75-5-1177
Loading
/content/journal/jgv/10.1099/0022-1317-75-5-1177
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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