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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
. 1979 Apr;76(4):1673–1676. doi: 10.1073/pnas.76.4.1673

Choleragen (cholera toxin): a bacterial lectin.

R L Richards, J Moss, C R Alving, P H Fishman, R O Brady
PMCID: PMC383452  PMID: 287006

Abstract

Choleragen (cholera toxin) agglutinated erythrocytes and liposomes containing the toxin receptor, galactosyl-N-acetylgalactosaminyl-(N-acetylneuraminyl)-galactosylglucosylceramide (ganglioside GM1). Cells that had been exposed to GM1 were agglutinated, but agglutination was not observed when cells had been exposed to other gangliosides (GM2, GM3, GD1a, GD1b). Choleragen-dependent agglutination of liposomes was slightly less specific, because liposomes containing either GM1 or GD1b, but neither GM2, GD1a, nor GM3 were agglutinated. The oligosaccharide isolated from GM1 inhibited both the agglutination of cells and liposomes containing GM1 and the binding of choleragen to liposomes containing GM1. Galactose and sialic acid were less effective inhibitors of liposomal agglutination and did not inhibit cellular agglutination or binding of choleragen to liposomes. Liposomal agglutination was dependent on choleragen concentration and occurred with the B but not the A protomer of choleragen. These results suggest that choleragen, through its binding to the oligosaccharide portion of a glycolipid, exhibits lectinlike activity, which results in agglutination of liposomes and erythrocytes.

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Selected References

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  1. Alving C. R., Joseph K. C., Wistar R. Influence of membrane composition on the interaction of a human monoclonal "anti-Forssman" immunoglobulin with liposomes. Biochemistry. 1974 Nov 5;13(23):4818–4824. doi: 10.1021/bi00720a021. [DOI] [PubMed] [Google Scholar]
  2. Boldt D. H., Speckart S. F., Richards R. L., Alving C. R. Interactions of lectins with glycolipids in liposomes. Biochem Biophys Res Commun. 1977 Jan 10;74(1):208–214. doi: 10.1016/0006-291x(77)91395-x. [DOI] [PubMed] [Google Scholar]
  3. Bowles D. J., Kauss H. Isolation of a lectin from liver plasma membrane and its binding to cellular membrane receptors in vitro. FEBS Lett. 1976 Jul 1;66(1):16–19. doi: 10.1016/0014-5793(76)80574-1. [DOI] [PubMed] [Google Scholar]
  4. Craig S. W., Cuatrecasas P. Mobility of cholera toxin receptors on rat lymphocyte membranes. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3844–3848. doi: 10.1073/pnas.72.10.3844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Cuatrecasas P. Interaction of Vibrio cholerae enterotoxin with cell membranes. Biochemistry. 1973 Aug 28;12(18):3547–3558. doi: 10.1021/bi00742a031. [DOI] [PubMed] [Google Scholar]
  7. Den H., Malinzak D. A. Isolation and properties of beta-D-galactoside-specific lectin from chick embryo thigh muscle. J Biol Chem. 1977 Aug 10;252(15):5444–5448. [PubMed] [Google Scholar]
  8. Fishman P. H., Moss J., Osborne J. C., Jr Interaction of choleragen with the oligosaccharide of ganglioside GM1: evidence for multiple oligosaccharide binding sites. Biochemistry. 1978 Feb 21;17(4):711–716. doi: 10.1021/bi00597a024. [DOI] [PubMed] [Google Scholar]
  9. Gill D. M. Mechanism of action of cholera toxin. Adv Cyclic Nucleotide Res. 1977;8:85–118. [PubMed] [Google Scholar]
  10. Holmgren J., Lönnroth I., Svennerholm L. Tissue receptor for cholera exotoxin: postulated structure from studies with GM1 ganglioside and related glycolipids. Infect Immun. 1973 Aug;8(2):208–214. doi: 10.1128/iai.8.2.208-214.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Holmgren J., Månsson J. E., Svennerholm L. Tissue receptor for cholera exotoxin: structural requirements of G11 ganglioside in toxin binding and inactivation. Med Biol. 1974 Aug;52(4):229–233. [PubMed] [Google Scholar]
  12. Hudgin R. L., Pricer W. E., Jr, Ashwell G., Stockert R. J., Morell A. G. The isolation and properties of a rabbit liver binding protein specific for asialoglycoproteins. J Biol Chem. 1974 Sep 10;249(17):5536–5543. [PubMed] [Google Scholar]
  13. King C. A., Van Heyningen W. E. Deactivation of cholera toxin by a sialidase-resistant monosialosylganglioside. J Infect Dis. 1973 Jun;127(6):639–647. doi: 10.1093/infdis/127.6.639. [DOI] [PubMed] [Google Scholar]
  14. Kinsky S. C. Preparation of liposomes and a spectrophotometric assay for release of trapped glucose marker. Methods Enzymol. 1974;32:501–513. doi: 10.1016/0076-6879(74)32050-2. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Moss J., Fishman P. H., Richards R. L., Alving C. R., Vaughan M., Brady R. O. Choleragen-mediated release of trapped glucose from liposomes containing ganglioside GM1. Proc Natl Acad Sci U S A. 1976 Oct;73(10):3480–3483. doi: 10.1073/pnas.73.10.3480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Moss J., Richards R. L., Alving C. R., Fishman P. H. Effect of the A and B protomers of choleragen on release of trapped glucose from liposomes containing or lacking ganglioside GM1. J Biol Chem. 1977 Jan 25;252(2):797–798. [PubMed] [Google Scholar]
  18. Osawa T., Nagai Y., Wiegandt H. Functional incorporation of gangliosides into liposomes. Jpn J Exp Med. 1977 Jun;47(3):221–222. [PubMed] [Google Scholar]
  19. Pacuszka T., Duffard R. O., Nishimura R. N., Brady R. O., Fishman P. H. Biosynthesis of bovine thyroid gangliosides. J Biol Chem. 1978 Aug 25;253(16):5839–5846. [PubMed] [Google Scholar]
  20. Read B. D., Demel R. A., Wiegandt H., van Deenen L. L. Specific interaction of concanavalin A with glycolipid monolayers. Biochim Biophys Acta. 1977 Oct 17;470(2):325–330. doi: 10.1016/0005-2736(77)90110-9. [DOI] [PubMed] [Google Scholar]
  21. Redwood W. R., Polefka T. G. Lectin-receptor interactions in liposomes. II. Interaction of wheat germ agglutinin with phosphatidylcholine liposomes containing incorporated monosialoganglioside. Biochim Biophys Acta. 1976 Dec 14;455(3):631–643. doi: 10.1016/0005-2736(76)90037-7. [DOI] [PubMed] [Google Scholar]
  22. Révész T., Greaves M. Ligand-induced redistribution of lymphocyte membrane ganglioside GM1. Nature. 1975 Sep 11;257(5522):103–106. doi: 10.1038/257103a0. [DOI] [PubMed] [Google Scholar]
  23. Sattler J., Schwarzmann G., Knack I., Röhm K. H., Wiegandt H. Studies of ligand binding to cholera toxin, III. Cooperativity of oligosaccharide binding. Hoppe Seylers Z Physiol Chem. 1978 Jun;359(6):719–723. doi: 10.1515/bchm.1978.359.1.719. [DOI] [PubMed] [Google Scholar]
  24. Sattler J., Schwarzmann G., Staerk J., Ziegler W., Wiegandt H. Studies of the ligand binding to cholera toxin, II. The hydrophilic moiety of sialoglycolipids. Hoppe Seylers Z Physiol Chem. 1977 Feb;358(2):159–163. doi: 10.1515/bchm2.1977.358.1.159. [DOI] [PubMed] [Google Scholar]
  25. Sedlacek H. H., Stärk J., Seiler F. R., Ziegler W., Wiegandt H. Cholera toxin induced redistribution of sialoglycolipid receptor at the lymphocyte membrane. FEBS Lett. 1976 Jan 15;61(2):272–276. doi: 10.1016/0014-5793(76)81055-1. [DOI] [PubMed] [Google Scholar]
  26. Simpson D. L., Thorne D. R., Loh H. H. Developmentally regulated lectin in neonatal rat brain. Nature. 1977 Mar 24;266(5600):367–369. doi: 10.1038/266367a0. [DOI] [PubMed] [Google Scholar]
  27. Staerk J., Ronneberger J., Wiegandt H., Ziegler W. Interaction of ganglioside G Gtet1 and its derivatives with choleragen. Eur J Biochem. 1974 Oct 1;48(1):103–110. doi: 10.1111/j.1432-1033.1974.tb03747.x. [DOI] [PubMed] [Google Scholar]
  28. Surolia A., Bachhawat B. K., Podder S. K. Interaction between lectin from Ricinus communis and liposomes containing gangliosides. Nature. 1975 Oct 30;257(5529):802–804. doi: 10.1038/257802a0. [DOI] [PubMed] [Google Scholar]
  29. de Waard A., Hickman S., Kornfeld S. Isolation and properties of beta-galactoside binding lectins of calf heart and lung. J Biol Chem. 1976 Dec 10;251(23):7581–7587. [PubMed] [Google Scholar]
  30. van Heyningen S. Cholera toxin. Biol Rev Camb Philos Soc. 1977 Nov;52(4):509–509. doi: 10.1111/j.1469-185x.1977.tb00858.x. [DOI] [PubMed] [Google Scholar]

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