Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1980 Oct;77(10):5693–5697. doi: 10.1073/pnas.77.10.5693

Sendai virus utilizes specific sialyloligosaccharides as host cell receptor determinants.

M A Markwell, J C Paulson
PMCID: PMC350135  PMID: 6255459

Abstract

Purified sialyltransferases (CMP-N-acetyl-neuraminate:D-galactosyl-glycoprotein N-acetylneuraminyl-transferase, EC 2.4.99.1) in conjunction with neuraminidase (acylneuraminyl hydrolase, EC 3.2.1.18) were used to produce cell surface sialyloligosaccharides of defined sequence to investigate their role in paramyxovirus infection of host cells. Infection of Madin-Darby bovine kidney cells by Sendai virus was monitored by hemagglutination titer of the virus produced and by changes in morphological characteristics. By either criterion, treatment of the cells with Vibrio cholerae neuraminidase to remove cell surface sialic acids rendered them resistant to infection by Sendai virus. Endogenous replacement of receptors by the cell occurred slowly but supported maximal levels of infection within 6 hr. In contrast, sialylation during a 20-min incubation with CMP-sialic acid and beta-galactoside alpha 2,3-sialytransferase restored full susceptibility to infection. This enzyme elaborates the NeuAc alpha 2,3Gal beta 1,3GalNAc (NeuAc, N-acetylneuraminic acid) sequence on glycoproteins and glycolipids. No restoration of infectivity was observed when neuraminidase-treated cells were sialylated by using beta-galactoside alpha 2,6-sialytransferase, which elaborates the NeuAc-alpha 2,6Gal beta 1,4GlcNAc sequence. These results suggest that sialyloligosaccharide receptor determinants of defined sequence are required for Sendai virus infection of host cells.

Full text

PDF
5693

Images in this article

5696Image
on p.5696
5696Image
on p.5696
5696Image
on p.5696
5696Image
on p.5696
5696Image
on p.5696
5696Image
on p.5696

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. Drzeniek R. Substrate specificity of neuraminidases. Histochem J. 1973 May;5(3):271–290. doi: 10.1007/BF01004994. [DOI] [PubMed] [Google Scholar]
  3. Glasgow L. R., Paulson J. C., Hill R. L. Systematic purification of five glycosidases from Streptococcus (Diplococcus) pneumoniae. J Biol Chem. 1977 Dec 10;252(23):8615–8623. [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. Helgeland K. Polyoma virus. 3. On the nature of the virus receptors on the mouse embryo cells. Acta Pathol Microbiol Scand. 1966;68(3):439–444. doi: 10.1111/apm.1966.68.3.439. [DOI] [PubMed] [Google Scholar]
  7. Holloway P. W. A simple procedure for removal of Triton X-100 from protein samples. Anal Biochem. 1973 May;53(1):304–308. doi: 10.1016/0003-2697(73)90436-3. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. KODZA H., JUNGEBLUT C. W. Effect of receptor-destroying enzyme on the growth of EMC virus in tissue culture. J Immunol. 1958 Jul;81(1):76–81. [PubMed] [Google Scholar]
  10. Kornfeld R., Kornfeld S. Comparative aspects of glycoprotein structure. Annu Rev Biochem. 1976;45:217–237. doi: 10.1146/annurev.bi.45.070176.001245. [DOI] [PubMed] [Google Scholar]
  11. Kraemer P. M. Cytotoxic, hemolytic and phospholipase contaminants of commerical neuraminidases. Biochim Biophys Acta. 1968 Aug 27;167(1):205–208. doi: 10.1016/0005-2744(68)90296-9. [DOI] [PubMed] [Google Scholar]
  12. Levitt N. H., Crowell R. L. Comparative studies of the regeneration of HeLa cell receptors for poliovirus T1 and coxsackievirus B3. J Virol. 1967 Aug;1(4):693–700. doi: 10.1128/jvi.1.4.693-700.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lyles D. S., Landsberger F. R. Kinetics of Sendai virus envelope fusion with erythrocyte membranes and virus-induced hemolysis. Biochemistry. 1979 Nov 13;18(23):5088–5095. doi: 10.1021/bi00590a011. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. Markwell M. A., Haas S. M., Bieber L. L., Tolbert N. E. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem. 1978 Jun 15;87(1):206–210. doi: 10.1016/0003-2697(78)90586-9. [DOI] [PubMed] [Google Scholar]
  17. Mizuochi T., Yamashita K., Fujikawa K., Kisiel W., Kobata A. The carbohydrate of bovine prothrombin. Occurrence of Gal beta 1 leads to 3GlcNAc grouping in asparagine-linked sugar chains. J Biol Chem. 1979 Jul 25;254(14):6419–6425. [PubMed] [Google Scholar]
  18. Paulson J. C., Beranek W. E., Hill R. L. Purification of a sialyltransferase from bovine colostrum by affinity chromatography on CDP-agarose. J Biol Chem. 1977 Apr 10;252(7):2356–2362. [PubMed] [Google Scholar]
  19. Paulson J. C., Rearick J. I., Hill R. L. Enzymatic properties of beta-D-galactoside alpha2 leads to 6 sialytransferase from bovine colostrum. J Biol Chem. 1977 Apr 10;252(7):2363–2371. [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. Philipson L., Lonberg-Holm K., Pettersson U. Virus-receptor interaction in an adenovirus system. J Virol. 1968 Oct;2(10):1064–1075. doi: 10.1128/jvi.2.10.1064-1075.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Sadler J. E., Rearick J. I., Paulson J. C., Hill R. L. Purification to homogeneity of a beta-galactoside alpha2 leads to 3 sialyltransferase and partial purification of an alpha-N-acetylgalactosaminide alpha2 leads to 6 sialyltransferase from porcine submaxillary glands. J Biol Chem. 1979 Jun 10;254(11):4434–4442. [PubMed] [Google Scholar]
  24. Scheid A., Choppin P. W. Identification of biological activities of paramyxovirus glycoproteins. Activation of cell fusion, hemolysis, and infectivity of proteolytic cleavage of an inactive precursor protein of Sendai virus. Virology. 1974 Feb;57(2):475–490. doi: 10.1016/0042-6822(74)90187-1. [DOI] [PubMed] [Google Scholar]
  25. Shur B. D., Roth S. Cell surface glycosyltransferases. Biochim Biophys Acta. 1975 Dec 29;415(4):473–512. doi: 10.1016/0304-4157(75)90007-6. [DOI] [PubMed] [Google Scholar]
  26. Takasaki S., Yamashita K., Suzuki K., Iwanaga S., Kobata A. The sugar chains of cold-insoluble globulin. A protein related to fibronectin. J Biol Chem. 1979 Sep 10;254(17):8548–8553. [PubMed] [Google Scholar]
  27. 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]
  28. Wassilewa L. Cell receptors for paramyxoviruses. Arch Virol. 1977;54(4):299–305. doi: 10.1007/BF01314775. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. ZAJAC I., CROWELL R. L. LOCATION AND REGENERATION OF ENTERIOVIRUS RECEPTORS OF HELA CELLS. J Bacteriol. 1965 Apr;89:1097–1100. doi: 10.1128/jb.89.4.1097-1100.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES