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. 1988 May;56(5):1334–1340. doi: 10.1128/iai.56.5.1334-1340.1988

Identification of a human erythrocyte receptor for colonization factor antigen I pili expressed by H10407 enterotoxigenic Escherichia coli.

P Pieroni 1, E A Worobec 1, W Paranchych 1, G D Armstrong 1
PMCID: PMC259823  PMID: 2895745

Abstract

We have identified a receptor for colonization factor antigen I (CFA/I) pili in human erythrocyte membranes. Erythrocyte binding assays, using whole organisms, suggested that the CFA/I receptor was a glycoprotein containing important sialic acid moieties. Subsequently, human erythrocyte membranes were extracted with lithium diiodosalicylate to obtain a soluble glycoprotein fraction from which to isolate receptors. The extracted material caused agglutination of the CFA/I+ but not the CFA/I- organisms at a protein concentration of 0.5 mg/ml. The CFA/I receptor was identified in iodinated extract by an affinity isolation procedure, using whole bacterial cells. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis and autoradiography of the washed, extract-coated H10407 CFA/I+ organisms revealed a band with an apparent molecular weight of 26,000 which was present in the original extract but was not observed on extract-coated H10407 CFA/I- bacteria. The addition of purified CFA/I pili reduced binding of the 26,000-molecular-weight receptor to CFA/I+ bacteria. The CFA/I-specific receptor species also bound to wheat germ agglutinin-agarose. This observation supported the suggestion that the CFA/I receptor identified in this report is a sialoglycoprotein.

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Selected References

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  1. Abraham S. N., Goguen J. D., Sun D., Klemm P., Beachey E. H. Identification of two ancillary subunits of Escherichia coli type 1 fimbriae by using antibodies against synthetic oligopeptides of fim gene products. J Bacteriol. 1987 Dec;169(12):5530–5536. doi: 10.1128/jb.169.12.5530-5536.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Armstrong G. D., Frost L. S., Vogel H. J., Paranchych W. Nature of the carbohydrate and phosphate associated with ColB2 and EDP208 pilin. J Bacteriol. 1981 Mar;145(3):1167–1176. doi: 10.1128/jb.145.3.1167-1176.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Armstrong G. D., Peppler M. S. Maintenance of biological activity of pertussis toxin radioiodinated while bound to fetuin-agarose. Infect Immun. 1987 May;55(5):1294–1299. doi: 10.1128/iai.55.5.1294-1299.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bartus H., Actor P., Snipes E., Sedlock D., Zajac I. Indications that the erythrocyte receptor involved in enterotoxigenic Escherichia coli attachment is a sialoglycoconjugate. J Clin Microbiol. 1985 Jun;21(6):951–954. doi: 10.1128/jcm.21.6.951-954.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beachey E. H. Bacterial adherence: adhesin-receptor interactions mediating the attachment of bacteria to mucosal surface. J Infect Dis. 1981 Mar;143(3):325–345. doi: 10.1093/infdis/143.3.325. [DOI] [PubMed] [Google Scholar]
  6. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cheney C. P., Boedeker E. C. Adherence of an enterotoxigenic Escherichia coli strain, serotype O78:H11, to purified human intestinal brush borders. Infect Immun. 1983 Mar;39(3):1280–1284. doi: 10.1128/iai.39.3.1280-1284.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Deneke C. F., McGowan K., Larson A. D., Gorbach S. L. Attachment of human and pig (K88) enterotoxigenic Escherichia coli strains to either human or porcine small intestinal cells. Infect Immun. 1984 Aug;45(2):522–524. doi: 10.1128/iai.45.2.522-524.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eshdat Y., Silverblatt F. J., Sharon N. Dissociation and reassembly of Escherichia coli type 1 pili. J Bacteriol. 1981 Oct;148(1):308–314. doi: 10.1128/jb.148.1.308-314.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Evans D. G., Evans D. J., Jr, Clegg S., Pauley J. A. Purification and characterization of the CFA/I antigen of enterotoxigenic Escherichia coli. Infect Immun. 1979 Aug;25(2):738–748. doi: 10.1128/iai.25.2.738-748.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Evans D. G., Evans D. J., Jr, Tjoa W. S., DuPont H. L. Detection and characterization of colonization factor of enterotoxigenic Escherichia coli isolated from adults with diarrhea. Infect Immun. 1978 Feb;19(2):727–736. doi: 10.1128/iai.19.2.727-736.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Evans D. G., Evans D. J., Jr, Tjoa W. Hemagglutination of human group A erythrocytes by enterotoxigenic Escherichia coli isolated from adults with diarrhea: correlation with colonization factor. Infect Immun. 1977 Nov;18(2):330–337. doi: 10.1128/iai.18.2.330-337.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Evans D. J., Jr, Evans D. G., Young L. S., Pitt J. Hemagglutination typing of Escherichia coli: definition of seven hemagglutination types. J Clin Microbiol. 1980 Aug;12(2):235–242. doi: 10.1128/jcm.12.2.235-242.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Finlay B. B., Frost L. S., Paranchych W. Nucleotide sequence of the tra YALE region from IncFV plasmid pED208. J Bacteriol. 1986 Nov;168(2):990–998. doi: 10.1128/jb.168.2.990-998.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gaastra W., de Graaf F. K. Host-specific fimbrial adhesins of noninvasive enterotoxigenic Escherichia coli strains. Microbiol Rev. 1982 Jun;46(2):129–161. doi: 10.1128/mr.46.2.129-161.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Germani Y., Brethes B., Bégaud E., Moreau J. P. Etude comparative entre l'adhérence aux entérocytes de lapins, la présence des facteurs de colonisation CFA/I et CFA/II et la toxinogénie de 55 souches de Escherichia coli. Ann Inst Pasteur Microbiol. 1985 Mar-Apr;136A(2):203–212. doi: 10.1016/s0769-2609(85)80059-4. [DOI] [PubMed] [Google Scholar]
  17. Klemm P. Fimbrial adhesions of Escherichia coli. Rev Infect Dis. 1985 May-Jun;7(3):321–340. doi: 10.1093/clinids/7.3.321. [DOI] [PubMed] [Google Scholar]
  18. Klemm P. Primary structure of the CFA1 fimbrial protein from human enterotoxigenic Escherichia coli strains. Eur J Biochem. 1982 May 17;124(2):339–348. doi: 10.1111/j.1432-1033.1982.tb06597.x. [DOI] [PubMed] [Google Scholar]
  19. Knutton S., Lloyd D. R., Candy D. C., McNeish A. S. In vitro adhesion of enterotoxigenic Escherichia coli to human intestinal epithelial cells from mucosal biopsies. Infect Immun. 1984 May;44(2):514–518. doi: 10.1128/iai.44.2.514-518.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Knutton S., Lloyd D. R., Candy D. C., McNeish A. S. Ultrastructural study of adhesion of enterotoxigenic Escherichia coli to erythrocytes and human intestinal epithelial cells. Infect Immun. 1984 May;44(2):519–527. doi: 10.1128/iai.44.2.519-527.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kronis K. A., Carver J. P. Thermodynamics of wheat germ agglutinin-sialyloligosaccharide interactions by proton nuclear magnetic resonance. Biochemistry. 1985 Feb 12;24(4):834–840. doi: 10.1021/bi00325a004. [DOI] [PubMed] [Google Scholar]
  22. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  23. Labigne-Roussel A. F., Lark D., Schoolnik G., Falkow S. Cloning and expression of an afimbrial adhesin (AFA-I) responsible for P blood group-independent, mannose-resistant hemagglutination from a pyelonephritic Escherichia coli strain. Infect Immun. 1984 Oct;46(1):251–259. doi: 10.1128/iai.46.1.251-259.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Lindahl M., Faris A., Wadstrom T. Colonization factor antigen on enterotoxigenic Escherichia coli is a sialic-specific lectin. Lancet. 1982 Jul 31;2(8292):280–280. doi: 10.1016/s0140-6736(82)90368-3. [DOI] [PubMed] [Google Scholar]
  26. Lindberg F., Lund B., Johansson L., Normark S. Localization of the receptor-binding protein adhesin at the tip of the bacterial pilus. Nature. 1987 Jul 2;328(6125):84–87. doi: 10.1038/328084a0. [DOI] [PubMed] [Google Scholar]
  27. Marchesi V. T., Andrews E. P. Glycoproteins: isolation from cellmembranes with lithium diiodosalicylate. Science. 1971 Dec 17;174(4015):1247–1248. doi: 10.1126/science.174.4015.1247. [DOI] [PubMed] [Google Scholar]
  28. Maurer L., Orndorff P. E. Identification and characterization of genes determining receptor binding and pilus length of Escherichia coli type 1 pili. J Bacteriol. 1987 Feb;169(2):640–645. doi: 10.1128/jb.169.2.640-645.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. McMichael J. C., Ou J. T. Structure of common pili from Escherichia coli. J Bacteriol. 1979 Jun;138(3):969–975. doi: 10.1128/jb.138.3.969-975.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Montreuil J. Spatial conformation of glycans and glycoproteins. Biol Cell. 1984;51(2):115–131. doi: 10.1111/j.1768-322x.1984.tb00291.x. [DOI] [PubMed] [Google Scholar]
  31. Norgren M., Normark S., Lark D., O'Hanley P., Schoolnik G., Falkow S., Svanborg-Edén C., Båga M., Uhlin B. E. Mutations in E coli cistrons affecting adhesion to human cells do not abolish Pap pili fiber formation. EMBO J. 1984 May;3(5):1159–1165. doi: 10.1002/j.1460-2075.1984.tb01945.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ofek I., Mirelman D., Sharon N. Adherence of Escherichia coli to human mucosal cells mediated by mannose receptors. Nature. 1977 Feb 17;265(5595):623–625. doi: 10.1038/265623a0. [DOI] [PubMed] [Google Scholar]
  33. Peppler M. S., Judd R. C., Munoz J. J. Effect of proteolytic enzymes, storage and reduction on the structure and biological activity of pertussigen, a toxin from Bordetella pertussis. Dev Biol Stand. 1985;61:75–87. [PubMed] [Google Scholar]
  34. Salit I. E., Gotschlich E. C. Type I Escherichia coli pili: characterization of binding to monkey kidney cells. J Exp Med. 1977 Nov 1;146(5):1182–1194. doi: 10.1084/jem.146.5.1182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sastry P. A., Pearlstone J. R., Smillie L. B., Paranchych W. Studies on the primary structure and antigenic determinants of pilin isolated from Pseudomonas aeruginosa K. Can J Biochem Cell Biol. 1985 Apr;63(4):284–291. doi: 10.1139/o85-042. [DOI] [PubMed] [Google Scholar]
  36. Schoolnik G. K., Fernandez R., Tai J. Y., Rothbard J., Gotschlich E. C. Gonococcal pili. Primary structure and receptor binding domain. J Exp Med. 1984 May 1;159(5):1351–1370. doi: 10.1084/jem.159.5.1351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Spivak J. L., Small D., Hollenberg M. D. Erythropoietin: isolation by affinity chromatography with lectin-agarose derivatives. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4633–4635. doi: 10.1073/pnas.74.10.4633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Steck T. L., Ramos B., Strapazon E. Proteolytic dissection of band 3, the predominant transmembrane polypeptide of the human erythrocyte membrane. Biochemistry. 1976 Mar 9;15(5):1153–1161. doi: 10.1021/bi00650a030. [DOI] [PubMed] [Google Scholar]
  39. Tomita M., Marchesi V. T. Amino-acid sequence and oligosaccharide attachment sites of human erythrocyte glycophorin. Proc Natl Acad Sci U S A. 1975 Aug;72(8):2964–2968. doi: 10.1073/pnas.72.8.2964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Worobec E. A., Shastry P., Smart W., Bradley R., Singh B., Paranchych W. Monoclonal antibodies against colonization factor antigen I pili from enterotoxigenic Escherichia coli. Infect Immun. 1983 Sep;41(3):1296–1301. doi: 10.1128/iai.41.3.1296-1301.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]

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