Skip to main content
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1979 Mar 1;149(3):669–685. doi: 10.1084/jem.149.3.669

Form variation in Escherichia coli K1: determined by O-acetylation of the capsular polysaccharide

PMCID: PMC2184817  PMID: 372481

Abstract

The chemical basis for the alternating antigenic change called form variation noted for the Escherichia coli K1-capsular polysaccharide has been shown by 13C nuclear magnetic resonance to be a result of random O- acetylation of C7 and C9 carbons of the alpha-2-8-linked sialic acid homopolymer. A serologic method (antiserum agar) was developed to identify and isolate the form variants. The O-acetyl positive and O- acetyl negative K1 polysaccharides had unique biochemical and immunologic properties. The O-acetyl-positive variants resisted neuraminidase hydrolysis in contrast to the susceptibility of the O- acetyl negative variant to this enzyme. In addition, O-acetylation altered the antigenicity of the O-acetyl polysaccharides. When injected as whole organisms, O-acetyl positive organisms produced anti-K1 - antibodies in rabbits specific for this polysaccharide variant. O- acetyl negative organisms were comparatively less immunogenic; however, antibodies induced by these organisms reacted with both K1 polysaccharide variants. Burros, injected with either variant, produced antibodies reactive with both K1 polysaccharides.

Full Text

The Full Text of this article is available as a PDF (1.7 MB).

Selected References

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

  1. Avery O. T., Goebel W. F. CHEMOIMMUNOLOGICAL STUDIES ON THE SOLUBLE SPECIFIC SUBSTANCE OF PNEUMOCOCCUS : I. THE ISOLATION AND PROPERTIES OF THE ACETYL POLYSACCHARIDE OF PNEUMOCOCCUS TYPE I. J Exp Med. 1933 Nov 30;58(6):731–755. doi: 10.1084/jem.58.6.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BARRY G. T. Colominic acid, a polymer of N-acetylneuraminic acid. J Exp Med. 1958 Apr 1;107(4):507–521. doi: 10.1084/jem.107.4.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BARRY G. T., GOEBEL W. F. Colominic acid, a substance of bacterial origin related to sialic acid. Nature. 1957 Jan 26;179(4552):206–206. doi: 10.1038/179206a0. [DOI] [PubMed] [Google Scholar]
  4. Bhattacharjee A. K., Jennings H. J., Kenny C. P., Martin A., Smith I. C. Structural determination of the sialic acid polysaccharide antigens of Neisseria meningitidis serogroups B and C with carbon 13 nuclear magnetic resonance. J Biol Chem. 1975 Mar 10;250(5):1926–1932. [PubMed] [Google Scholar]
  5. Björkstén B., Bortolussi R., Gothefors L., Quie P. G. Interaction of E. coli strains with human serum: lack of relationship to K1 antigen. J Pediatr. 1976 Dec;89(6):892–897. doi: 10.1016/s0022-3476(76)80592-6. [DOI] [PubMed] [Google Scholar]
  6. Bolaños R., DeWitt C. W. Isolation and characterization of the K1 (L) antigen of Escherichia coli. J Bacteriol. 1966 Mar;91(3):987–996. doi: 10.1128/jb.91.3.987-996.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brodribb A. J. Treatment of symptomatic diverticular disease with a high-fibre diet. Lancet. 1977 Mar 26;1(8013):664–666. doi: 10.1016/s0140-6736(77)92112-2. [DOI] [PubMed] [Google Scholar]
  8. Cheasty T., Gross R. J., Rowe B. Incidence of K1 antigen in Escherichia coli isolated from blood and cerebrospinal fluid of patients in the United Kingdom. J Clin Pathol. 1977 Oct;30(10):945–947. doi: 10.1136/jcp.30.10.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Craven D. E., Frasch C. E., Robbins J. B., Feldman H. A. Serogroup identification of Neisseria meningitidis: comparison of an antiserum agar method with bacterial slide agglutination. J Clin Microbiol. 1978 May;7(5):410–414. doi: 10.1128/jcm.7.5.410-414.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. DEWITT C. W., ROWE J. A. Sialic acids (N,7-O-diacetylneuraminic acid and N-acetylneuraminic acid) in Escherichia coli. I. Isolation and identification. J Bacteriol. 1961 Dec;82:838–848. doi: 10.1128/jb.82.6.838-848.1961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. DEWITT C. W., ZELL E. A. Sialic acids (N,7-O-diacetylneuraminic acid and N-acetylneuraminic adcid) in Escherichia coli. II. Their presence on the cell wall surface and relationship to K antigen. J Bacteriol. 1961 Dec;82:849–856. doi: 10.1128/jb.82.6.849-856.1961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dickson J. J., Messer M. Intestinal neuraminidase activity of suckling rats and other mammals. Relationship to the sialic acid content of milk. Biochem J. 1978 Feb 15;170(2):407–413. doi: 10.1042/bj1700407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Egan W., Liu T. Y., Dorow D., Cohen J. S., Robbins J. D., Gotschlich E. C., Robbins J. B. Structural studies on the sialic acid polysaccharide antigen of Escherichia coli strain Bos-12. Biochemistry. 1977 Aug 9;16(16):3687–3692. doi: 10.1021/bi00635a028. [DOI] [PubMed] [Google Scholar]
  14. Gotschlich E. C., Rey M., Etienne J., Sanborn W. R., Triau R., Cvjetanović B. The immunological responses observed in field studies in Africa with group A meningococcal vaccines. Prog Immunobiol Stand. 1971;5:485–491. [PubMed] [Google Scholar]
  15. Grados O., Ewing W. H. Antigenic relationship between Escherichia coli and Neisseria meningitidis. J Infect Dis. 1970 Jul-Aug;122(1):100–103. doi: 10.1093/infdis/122.1-2.100. [DOI] [PubMed] [Google Scholar]
  16. Gross R. J., Cheasty T., Rowe B. Isolation of bacteriophages specific for the K1 polysaccharide antigen of Escherichia coli. J Clin Microbiol. 1977 Dec;6(6):548–550. doi: 10.1128/jcm.6.6.548-550.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. HESTRIN S. The reaction of acetylcholine and other carboxylic acid derivatives with hydroxylamine, and its analytical application. J Biol Chem. 1949 Aug;180(1):249–261. [PubMed] [Google Scholar]
  18. Hochstein H. D., Elfin R. J., Cooper J. F., Seligmann E. B., Jr, Wolff S. M. Further developments of Limulus Amebocyte Lysate test. Bull Parenter Drug Assoc. 1973 May-Jun;27(3):139–148. [PubMed] [Google Scholar]
  19. Kaijser B., Ahlstedt S. Protective capacity of antibodies against Escherichia coli and K antigens. Infect Immun. 1977 Aug;17(2):286–289. doi: 10.1128/iai.17.2.286-289.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kasper D. L., Winkelhake J. L., Zollinger W. D., Brandt B. L., Artenstein M. S. Immunochemical similarity between polysaccharide antigens of Escherichia coli 07: K1(L):NM and group B Neisseria meningitidis. J Immunol. 1973 Jan;110(1):262–268. [PubMed] [Google Scholar]
  21. 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]
  22. Liu T. Y., Chang Y. H. Hydrolysis of proteins with p-toluenesulfonic acid. Determination of tryptophan. J Biol Chem. 1971 May 10;246(9):2842–2848. [PubMed] [Google Scholar]
  23. Liu T. Y., Gotschlich E. C., Dunne F. T., Jonssen E. K. Studies on the meningococcal polysaccharides. II. Composition and chemical properties of the group B and group C polysaccharide. J Biol Chem. 1971 Aug 10;246(15):4703–4712. [PubMed] [Google Scholar]
  24. McCracken G. H., Jr, Sarff L. D., Glode M. P., Mize S. G., Schiffer M. S., Robbins J. B., Gotschlich E. C., Orskov I., Orskov F. Relation between Escherichia coli K1 capsular polysaccharide antigen and clinical outcome in neonatal meningitis. Lancet. 1974 Aug 3;2(7875):246–250. doi: 10.1016/s0140-6736(74)91413-5. [DOI] [PubMed] [Google Scholar]
  25. Myerowitz R. L., Albers A. C., Yee R. B., Orskov F. Relationship of K1 antigen to biotype in clinical isolates of Escherichia coli. J Clin Microbiol. 1977 Aug;6(2):124–127. doi: 10.1128/jcm.6.2.124-127.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Orskov F. Agarose electrophoresis combined with second dimensional Cetavlon precipitation. A new method for demonstration of acidic polysaccharide K antigens. Acta Pathol Microbiol Scand B. 1976 Oct;84B(5):319–320. [PubMed] [Google Scholar]
  27. Orskov F., Orskov I. Immunoelectrophoretic patterns of extracts from Escherichia coli O antigen test strains O1 to O157 examinations in homologous OK sera. Further comments on the classification of Escherichia K antigens. Acta Pathol Microbiol Scand B Microbiol Immunol. 1972;80(6):905–910. [PubMed] [Google Scholar]
  28. Orskov F., Orskov I., Jann B., Jann K. Immunoelectrophoretic patterns of extracts from all Escherichia coli O and K antigen test strains: correlation with pathogenicity. Acta Pathol Microbiol Scand B Microbiol Immunol. 1971;79(2):142–152. doi: 10.1111/j.1699-0463.1971.tb02141.x. [DOI] [PubMed] [Google Scholar]
  29. Orskov F., Sorenson K. B. Escherichia coli serogroups in breast-fed and bottle-fed infants. Acta Pathol Microbiol Scand B. 1975 Feb;83(1):25–30. [PubMed] [Google Scholar]
  30. Orskov I., Orskov F., Jann B., Jann K. Serology, chemistry, and genetics of O and K antigens of Escherichia coli. Bacteriol Rev. 1977 Sep;41(3):667–710. doi: 10.1128/br.41.3.667-710.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. ROBBINS P. W., KELLER J. M., WRIGHT A., BERNSTEIN R. L. ENZYMATIC AND KINETIC STUDIES ON THE MECHANISM OF O-ANTIGEN CONVERSION BY BACTERIOPHAGE EPSILON-15. J Biol Chem. 1965 Jan;240:384–390. [PubMed] [Google Scholar]
  32. Robbins J. B., McCracken G. H., Jr, Gotschlich E. C., Orskov F., Orskov I., Hanson L. A. Escherichia coli K1 capsular polysaccharide associated with neonatal meningitis. N Engl J Med. 1974 May 30;290(22):1216–1220. doi: 10.1056/NEJM197405302902202. [DOI] [PubMed] [Google Scholar]
  33. SVENNERHOLM L. Quantitative estimation of sialic acids. II. A colorimetric resorcinol-hydrochloric acid method. Biochim Biophys Acta. 1957 Jun;24(3):604–611. doi: 10.1016/0006-3002(57)90254-8. [DOI] [PubMed] [Google Scholar]
  34. Sarff L. D., McCracken G. H., Schiffer M. S., Glode M. P., Robbins J. B., Orskov I., Orskov F. Epidemiology of Escherichia coli K1 in healthy and diseased newborns. Lancet. 1975 May 17;1(7916):1099–1104. doi: 10.1016/s0140-6736(75)92496-4. [DOI] [PubMed] [Google Scholar]
  35. Schiffer M. S., Oliveira E., Glode M. P., McCracken G. H., Jr, Sarff L. M., Robbins J. B. A review: relation between invasiveness and the K1 capsular polysaccharide of Escherichia coli. Pediatr Res. 1976 Feb;10(2):82–87. doi: 10.1203/00006450-197602000-00002. [DOI] [PubMed] [Google Scholar]
  36. Semjen G., Orskov I., Orskov F. K antigen determination of Escherichia coli by counter-current immunoelectrophoresis (CIE). Acta Pathol Microbiol Scand B. 1977 Feb;85B(1):103–107. doi: 10.1111/j.1699-0463.1977.tb01680.x. [DOI] [PubMed] [Google Scholar]
  37. Shindo H., Egan W., Cohen J. S. Studies of individual carboxyl groups in proteins by carbon 13 nuclear magnetic resonance spectroscopy. J Biol Chem. 1978 Oct 10;253(19):6751–6755. [PubMed] [Google Scholar]
  38. Sivonen A., Renkonen O. V., Robbins J. B. Use of antiserum agar plates for serogrouping of meningococci. J Clin Pathol. 1977 Sep;30(9):834–837. doi: 10.1136/jcp.30.9.834. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Vann W. F., Liu T. Y., Robbins J. B. Cell-free biosynthesis of the O-acetylated N-acetylneuraminic acid capsular polysaccharide of group C meningococci. J Bacteriol. 1978 Mar;133(3):1300–1306. doi: 10.1128/jb.133.3.1300-1306.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. WARREN L. The thiobarbituric acid assay of sialic acids. J Biol Chem. 1959 Aug;234(8):1971–1975. [PubMed] [Google Scholar]
  41. Weeke B. Crossed immunoelectrophoresis. Scand J Immunol Suppl. 1973;1:47–56. doi: 10.1111/j.1365-3083.1973.tb03778.x. [DOI] [PubMed] [Google Scholar]
  42. Wolberg G., DeWitt C. W. Mouse virulence of K(L) antigen-containing strains of Escherichia coli. J Bacteriol. 1969 Nov;100(2):730–737. doi: 10.1128/jb.100.2.730-737.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wong K. H., Barrera O., Sutton A., May J., Hochstein D. H., Robbins J. D., Robbins J. B., Parkman P. D., Seligmann E. B., Jr Standardization and control of meningococcal vaccines, group A and group C polysaccharides. J Biol Stand. 1977;5(3):197–215. doi: 10.1016/s0092-1157(77)80005-x. [DOI] [PubMed] [Google Scholar]
  44. Wyle F. A., Artenstein M. S., Brandt B. L., Tramont E. C., Kasper D. L., Altieri P. L., Berman S. L., Lowenthal J. P. Immunologic response of man to group B meningococcal polysaccharide vaccines. J Infect Dis. 1972 Nov;126(5):514–521. doi: 10.1093/infdis/126.5.514. [DOI] [PubMed] [Google Scholar]
  45. Zieg J., Silverman M., Hilmen M., Simon M. Recombinational switch for gene expression. Science. 1977 Apr 8;196(4286):170–172. doi: 10.1126/science.322276. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES