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. 1981 Sep;78(9):5406–5410. doi: 10.1073/pnas.78.9.5406

Specific gangliosides function as host cell receptors for Sendai virus.

M A Markwell, L Svennerholm, J C Paulson
PMCID: PMC348754  PMID: 6272300

Abstract

The ability of specific gangliosides to function as host cell receptors for Sendai virus was investigated by using Madin-Darby bovine kidney cells which become resistant to infection upon treatment with Vibrio cholerae sialidase. Sialidase-treated cells were incubated for 20 min at 37 degrees C with individual, highly purified gangliosides containing homogeneous carbohydrate moieties and then inoculated with virus for 10 min. Susceptibility of the cells to infection was monitored by hemagglutination titer of the virus produced 48 hr after inoculation. Incubation of the cells with gangliosides containing the sequence NeuAc alpha 2,3Gal beta 1,3GalNAc (i.e., GD1a, GT1b, and GQ1b) fully restored susceptibility to infection to the cells. However, the ganglioside GQ1b in which the sequence ends with two sialic acids in a NeuAc alpha 2,8NeuAc linkage instead of a single sialic acid as in GD1a and GT1b, was effective as a receptor at a concentration 1/100th that of any of the other gangliosides tested. Incubation with gangliosides similar in structure to GD1a, GT1b, and GQ1b but lacking the sialic acid attached to the terminal galactose (i.e., GM1 and GD1b) had no effect. The results from control experiments in which gangliosides were incubated at 0 degrees C with cells or in which trypsin was used to remove gangliosides adsorbed to cells were consistent with the premise that the gangliosides must actually insert into the cellular membrane to function as Sendai virus receptors. Addition of 4 X 10(6) molecules of 14C-labeled GD1a per cell made the cells fully susceptible to infection. Analysis of the ganglioside content of cell membranes showed that gangliosides GD1a, GT1b, and GQ1b are natural components of these cells and are present in quantities sufficient to act as receptors. These results demonstrate that gangliosides with the proper carbohydrate sequence, such as GD1a, GT1b, and GQ1b, function as natural receptors for Sendai virus in host cells.

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Selected References

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

  1. BABLANIAN R., EGGERS H. J., TAMM I. STUDIES ON THE MECHANISM OF POLIOVIRUS-INDUCED CELL DAMAGE. I. THE RELATION BETWEEN POLIOVIRUS,-INDUCED METABOLIC AND MORPHOLOGICAL ALTERATIONS IN CULTURED CELLS. Virology. 1965 May;26:100–113. doi: 10.1016/0042-6822(65)90030-9. [DOI] [PubMed] [Google Scholar]
  2. BUTLER W. T. HEMAGGLUTINATION STUDIES WITH FORMALINIZED ERYTHROCYTES. EFFECT OF BIS-DIAZO-BENZIDINE AND TANNIC ACID TREATMENT ON SENSITIZATION BY SOLUBLE ANTIGEN. J Immunol. 1963 May;90:663–671. [PubMed] [Google Scholar]
  3. Callies R., Schwarzmann G., Radsak K., Siegert R., Wiegandt H. Characterization of the cellular binding of exogenous gangliosides. Eur J Biochem. 1977 Nov 1;80(2):425–432. doi: 10.1111/j.1432-1033.1977.tb11897.x. [DOI] [PubMed] [Google Scholar]
  4. Cuatrecasas P. Gangliosides and membrane receptors for cholera toxin. Biochemistry. 1973 Aug 28;12(18):3558–3566. doi: 10.1021/bi00742a032. [DOI] [PubMed] [Google Scholar]
  5. Drzeniek R. Substrate specificity of neuraminidases. Histochem J. 1973 May;5(3):271–290. doi: 10.1007/BF01004994. [DOI] [PubMed] [Google Scholar]
  6. Fredman P., Nilsson O., Tayot J. L., Svennerholm L. Separation of gangliosides on a new type of anion-exchange resin. Biochim Biophys Acta. 1980 Apr 18;618(1):42–52. doi: 10.1016/0005-2760(80)90052-1. [DOI] [PubMed] [Google Scholar]
  7. HAFF R. F., STEWART R. C. ROLE OF SIALIC ACID RECEPTORS IN ADSORPTION OF INFLUENZA VIRUS TO CHICK EMBRYO CELLS. J Immunol. 1965 Jun;94:842–851. [PubMed] [Google Scholar]
  8. Haywood A. M. Characteristics of Sendai virus receptors in a model membrane. J Mol Biol. 1974 Mar 15;83(4):427–436. doi: 10.1016/0022-2836(74)90504-x. [DOI] [PubMed] [Google Scholar]
  9. Haywood A. M. Characteristics of Sendai virus receptors in a model membrane. J Mol Biol. 1974 Mar 15;83(4):427–436. doi: 10.1016/0022-2836(74)90504-x. [DOI] [PubMed] [Google Scholar]
  10. Holmgren J., Lönnroth I., Månsson J., Svennerholm L. Interaction of cholera toxin and membrane GM1 ganglioside of small intestine. Proc Natl Acad Sci U S A. 1975 Jul;72(7):2520–2524. doi: 10.1073/pnas.72.7.2520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Holmgren J., Svennerholm L., Elwing H., Fredman P., Strannegård O. Sendai virus receptor: proposed recognition structure based on binding to plastic-adsorbed gangliosides. Proc Natl Acad Sci U S A. 1980 Apr;77(4):1947–1950. doi: 10.1073/pnas.77.4.1947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Klenk H. D., Choppin P. W. Glycosphingolipids of plasma membranes of cultured cells and an enveloped virus (SV5) grown in these cells. Proc Natl Acad Sci U S A. 1970 May;66(1):57–64. doi: 10.1073/pnas.66.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. MARCUS P. I. Symposium on the biology of cells modified by viruses or antigens. IV. Single-cell techniques in tracing virus-host interactions. Bacteriol Rev. 1959 Dec;23(4):232–249. doi: 10.1128/br.23.4.232-249.1959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Maggio B., Cumar F. A., Caputto R. Induction of membrane fusion by polysialogangliosides. FEBS Lett. 1978 Jun 1;90(1):149–152. doi: 10.1016/0014-5793(78)80318-4. [DOI] [PubMed] [Google Scholar]
  15. Mansson J. E., Vanier M. T., Svennerholm L. Changes in the fatty acid and sphingosine composition of the major gangliosides of human brain with age. J Neurochem. 1978 Jan;30(1):273–275. doi: 10.1111/j.1471-4159.1978.tb07064.x. [DOI] [PubMed] [Google Scholar]
  16. Markwell M. A., Fox C. F. Protein-protein interactions within paramyxoviruses identified by native disulfide bonding or reversible chemical cross-linking. J Virol. 1980 Jan;33(1):152–166. doi: 10.1128/jvi.33.1.152-166.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Markwell M. A., Fox C. F. Surface-specific iodination of membrane proteins of viruses and eucaryotic cells using 1,3,4,6-tetrachloro-3alpha,6alpha-diphenylglycoluril. Biochemistry. 1978 Oct 31;17(22):4807–4817. doi: 10.1021/bi00615a031. [DOI] [PubMed] [Google Scholar]
  18. Markwell M. A., Paulson J. C. Sendai virus utilizes specific sialyloligosaccharides as host cell receptor determinants. Proc Natl Acad Sci U S A. 1980 Oct;77(10):5693–5697. doi: 10.1073/pnas.77.10.5693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Moss J., Fishman P. H., Manganiello V. C., Vaughan M., Brady R. O. Functional incorporation of ganglioside into intact cells: induction of choleragen responsiveness. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1034–1037. doi: 10.1073/pnas.73.4.1034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Paulson J. C., Sadler J. E., Hill R. L. Restoration of specific myxovirus receptors to asialoerythrocytes by incorporation of sialic acid with pure sialyltransferases. J Biol Chem. 1979 Mar 25;254(6):2120–2124. [PubMed] [Google Scholar]
  21. Rearick J. I., Sadler J. E., Paulson J. C., Hill R. L. Enzymatic characterization of beta D-galactoside alpha2 leads to 3 sialyltransferase from porcine submaxillary gland. J Biol Chem. 1979 Jun 10;254(11):4444–4451. [PubMed] [Google Scholar]
  22. Sharom F. J., Barratt D. G., Thede A. E., Grant C. W. Glycolipids in model membranes. Spin label and freeze-etch studies. Biochim Biophys Acta. 1976 Dec 2;455(2):485–492. doi: 10.1016/0005-2736(76)90319-9. [DOI] [PubMed] [Google Scholar]
  23. Svennerholm L., Fredman P. A procedure for the quantitative isolation of brain gangliosides. Biochim Biophys Acta. 1980 Jan 18;617(1):97–109. doi: 10.1016/0005-2760(80)90227-1. [DOI] [PubMed] [Google Scholar]
  24. Svennerholm L., Vanier M. T., Månsson J. E. Krabbe disease: a galactosylsphingosine (psychosine) lipidosis. J Lipid Res. 1980 Jan;21(1):53–64. [PubMed] [Google Scholar]
  25. Tiffany J. M., Blough H. A. Attachment of myxoviruses to artificial membranes: electron microscopic studies. Virology. 1971 Apr;44(1):18–28. doi: 10.1016/0042-6822(71)90148-6. [DOI] [PubMed] [Google Scholar]
  26. WARREN L. The thiobarbituric acid assay of sialic acids. J Biol Chem. 1959 Aug;234(8):1971–1975. [PubMed] [Google Scholar]
  27. Weinstein D. B., Marsh J. B., Glick M. C., Warren L. Membranes of animal cells. VI. The glycolipids of the L cell and its surface membrane. J Biol Chem. 1970 Aug 10;245(15):3928–3937. [PubMed] [Google Scholar]
  28. Wu P. S., Ledeen R. W., Udem S., Isaacson Y. A. Nature of the Sendai virus receptor: glycoprotein versus ganglioside. J Virol. 1980 Jan;33(1):304–310. doi: 10.1128/jvi.33.1.304-310.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]

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