Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1992 Jul;174(13):4230–4238. doi: 10.1128/jb.174.13.4230-4238.1992

Variation in antigenicity and molecular weight of Campylobacter coli VC167 flagellin in different genetic backgrounds.

R A Alm 1, P Guerry 1, M E Power 1, T J Trust 1
PMCID: PMC206204  PMID: 1624417

Abstract

Campylobacter coli VC167 has been shown to undergo a reversible flagellar antigenic variation between antigenic type 1 (T1) and antigenic type 2 (T2). VC167 contains two flagellin genes, and the products of both genes are incorporated into a complex flagellar filament in both antigenic types. Although there are only minor amino acid changes in the flagellins expressed by T1 and T2 cells, the two antigenic types of flagellins can be distinguished by differences in apparent M(r) on sodium dodecyl sulfate-polyacrylamide gels and by immunoreactivity with T1-specific (LAH1) or T2-specific (LAH2) antiserum. The isolation of stable variants of T1 and T2 has allowed for the transfer via natural transformation of the flagellin structural genes from the T1 background into the T2 background and from the T2 background into the T1 background. In addition, the flagellin genes from VC167 T1 and T2 have been transferred into strains of Campylobacter jejuni. The results indicate that the observed antigenic variations of VC167 flagellins are dependent on the host genetic background and independent of the primary amino acid sequence. These data provide evidence that posttranslational modifications are responsible for the antigenic variation seen in VC167 flagellins.

Full text

PDF
4230

Images in this article

4233Image
on p.4233
4234Image
on p.4234
4235Image
on p.4235

Selected References

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

  1. AMBLER R. P., REES M. W. Epsilon-N-Methyl-lysine in bacterial flagellar protein. Nature. 1959 Jul 4;184:56–57. doi: 10.1038/184056b0. [DOI] [PubMed] [Google Scholar]
  2. Abimiku A. G., Dolby J. M. Cross-protection of infant mice against intestinal colonisation by Campylobacter jejuni: importance of heat-labile serotyping (Lior) antigens. J Med Microbiol. 1988 Aug;26(4):265–268. doi: 10.1099/00222615-26-4-265. [DOI] [PubMed] [Google Scholar]
  3. Alm R. A., Guerry P., Power M. E., Lior H., Trust T. J. Analysis of the role of flagella in the heat-labile Lior serotyping scheme of thermophilic Campylobacters by mutant allele exchange. J Clin Microbiol. 1991 Nov;29(11):2438–2445. doi: 10.1128/jcm.29.11.2438-2445.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Black R. E., Levine M. M., Clements M. L., Hughes T. P., Blaser M. J. Experimental Campylobacter jejuni infection in humans. J Infect Dis. 1988 Mar;157(3):472–479. doi: 10.1093/infdis/157.3.472. [DOI] [PubMed] [Google Scholar]
  5. Butzler J. P., Skirrow M. B. Campylobacter enteritis. Clin Gastroenterol. 1979 Sep;8(3):737–765. [PubMed] [Google Scholar]
  6. Caldwell M. B., Guerry P., Lee E. C., Burans J. P., Walker R. I. Reversible expression of flagella in Campylobacter jejuni. Infect Immun. 1985 Dec;50(3):941–943. doi: 10.1128/iai.50.3.941-943.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Engvall E., Perlmann P. Enzyme-linked immunosorbent assay, Elisa. 3. Quantitation of specific antibodies by enzyme-labeled anti-immunoglobulin in antigen-coated tubes. J Immunol. 1972 Jul;109(1):129–135. [PubMed] [Google Scholar]
  8. Fedorov O. V., Kostyukova A. S., Pyatibratov M. G. Architectonics of a bacterial flagellin filament subunit. FEBS Lett. 1988 Dec 5;241(1-2):145–148. doi: 10.1016/0014-5793(88)81048-2. [DOI] [PubMed] [Google Scholar]
  9. Fischer S. H., Nachamkin I. Common and variable domains of the flagellin gene, flaA, in Campylobacter jejuni. Mol Microbiol. 1991 May;5(5):1151–1158. doi: 10.1111/j.1365-2958.1991.tb01888.x. [DOI] [PubMed] [Google Scholar]
  10. Gerl L., Sumper M. Halobacterial flagellins are encoded by a multigene family. Characterization of five flagellin genes. J Biol Chem. 1988 Sep 15;263(26):13246–13251. [PubMed] [Google Scholar]
  11. Glazer A. N., De Lange R. J., Martinez R. J. Identification of episilon-N-methyllysine in Spirillum serpens flagella and of episilon-N-dimethyllysine in Salmonella typhimurium flagella. Biochim Biophys Acta. 1969 Aug 12;188(1):164–165. doi: 10.1016/0005-2795(69)90059-2. [DOI] [PubMed] [Google Scholar]
  12. Grogan D. W. Phenotypic characterization of the archaebacterial genus Sulfolobus: comparison of five wild-type strains. J Bacteriol. 1989 Dec;171(12):6710–6719. doi: 10.1128/jb.171.12.6710-6719.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Guerry P., Alm R. A., Power M. E., Logan S. M., Trust T. J. Role of two flagellin genes in Campylobacter motility. J Bacteriol. 1991 Aug;173(15):4757–4764. doi: 10.1128/jb.173.15.4757-4764.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Guerry P., Logan S. M., Thornton S., Trust T. J. Genomic organization and expression of Campylobacter flagellin genes. J Bacteriol. 1990 Apr;172(4):1853–1860. doi: 10.1128/jb.172.4.1853-1860.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Guerry P., Logan S. M., Trust T. J. Genomic rearrangements associated with antigenic variation in Campylobacter coli. J Bacteriol. 1988 Jan;170(1):316–319. doi: 10.1128/jb.170.1.316-319.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Harris L. A., Logan S. M., Guerry P., Trust T. J. Antigenic variation of Campylobacter flagella. J Bacteriol. 1987 Nov;169(11):5066–5071. doi: 10.1128/jb.169.11.5066-5071.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hull R. A., Gill R. E., Hsu P., Minshew B. H., Falkow S. Construction and expression of recombinant plasmids encoding type 1 or D-mannose-resistant pili from a urinary tract infection Escherichia coli isolate. Infect Immun. 1981 Sep;33(3):933–938. doi: 10.1128/iai.33.3.933-938.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Iino T. Genetics of structure and function of bacterial flagella. Annu Rev Genet. 1977;11:161–182. doi: 10.1146/annurev.ge.11.120177.001113. [DOI] [PubMed] [Google Scholar]
  19. Joys T. M. Identification of an antibody binding site in the phase-1 flagellar protein of Salmonella typhimurium. Microbios. 1976;15(61-62):221–228. [PubMed] [Google Scholar]
  20. Joys T. M., Rankis V. The primary structure of the phase-1 flagellar protein of Salmonella typhimurium. I. The tryptic peptides. J Biol Chem. 1972 Aug 25;247(16):5180–5193. [PubMed] [Google Scholar]
  21. Joys T. M. The flagellar filament protein. Can J Microbiol. 1988 Apr;34(4):452–458. doi: 10.1139/m88-078. [DOI] [PubMed] [Google Scholar]
  22. KOBAYASHI T., RINKER J. N., KOFFLER H. Purification and and chemical properties of flagellin. Arch Biochem Biophys. 1959 Oct;84:342–362. doi: 10.1016/0003-9861(59)90598-3. [DOI] [PubMed] [Google Scholar]
  23. Kalmokoff M. L., Jarrell K. F. Cloning and sequencing of a multigene family encoding the flagellins of Methanococcus voltae. J Bacteriol. 1991 Nov;173(22):7113–7125. doi: 10.1128/jb.173.22.7113-7125.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kelly-Wintenberg K., Anderson T., Montie T. C. Phosphorylated tyrosine in the flagellum filament protein of Pseudomonas aeruginosa. J Bacteriol. 1990 Sep;172(9):5135–5139. doi: 10.1128/jb.172.9.5135-5139.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kishimoto A., Nishiyama K., Nakanishi H., Uratsuji Y., Nomura H., Takeyama Y., Nishizuka Y. Studies on the phosphorylation of myelin basic protein by protein kinase C and adenosine 3':5'-monophosphate-dependent protein kinase. J Biol Chem. 1985 Oct 15;260(23):12492–12499. [PubMed] [Google Scholar]
  26. Kuwajima G., Asaka J., Fujiwara T., Fujiwara T., Node K., Kondo E. Nucleotide sequence of the hag gene encoding flagellin of Escherichia coli. J Bacteriol. 1986 Dec;168(3):1479–1483. doi: 10.1128/jb.168.3.1479-1483.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kuwajima G. Flagellin domain that affects H antigenicity of Escherichia coli K-12. J Bacteriol. 1988 Jan;170(1):485–488. doi: 10.1128/jb.170.1.485-488.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Lee A., O'Rourke J. L., Barrington P. J., Trust T. J. Mucus colonization as a determinant of pathogenicity in intestinal infection by Campylobacter jejuni: a mouse cecal model. Infect Immun. 1986 Feb;51(2):536–546. doi: 10.1128/iai.51.2.536-546.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Logan S. M., Guerry P., Rollins D. M., Burr D. H., Trust T. J. In vivo antigenic variation of Campylobacter flagellin. Infect Immun. 1989 Aug;57(8):2583–2585. doi: 10.1128/iai.57.8.2583-2585.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Logan S. M., Trust T. J., Guerry P. Evidence for posttranslational modification and gene duplication of Campylobacter flagellin. J Bacteriol. 1989 Jun;171(6):3031–3038. doi: 10.1128/jb.171.6.3031-3038.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Logan S. M., Trust T. J. Location of epitopes on Campylobacter jejuni flagella. J Bacteriol. 1986 Nov;168(2):739–745. doi: 10.1128/jb.168.2.739-745.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Logan S. M., Trust T. J. Molecular identification of surface protein antigens of Campylobacter jejuni. Infect Immun. 1983 Nov;42(2):675–682. doi: 10.1128/iai.42.2.675-682.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. MCDONOUGH M. W. AMINO ACID COMPOSITION OF ANTIGENICALLY DISTINCT SALMONELLA FLAGELLAR PROTEINS. J Mol Biol. 1965 Jun;12:342–355. doi: 10.1016/s0022-2836(65)80258-3. [DOI] [PubMed] [Google Scholar]
  35. Marshall R. D. Glycoproteins. Annu Rev Biochem. 1972;41:673–702. doi: 10.1146/annurev.bi.41.070172.003325. [DOI] [PubMed] [Google Scholar]
  36. Morooka T., Umeda A., Amako K. Motility as an intestinal colonization factor for Campylobacter jejuni. J Gen Microbiol. 1985 Aug;131(8):1973–1980. doi: 10.1099/00221287-131-8-1973. [DOI] [PubMed] [Google Scholar]
  37. Newell D. G. Monoclonal antibodies directed against the flagella of Campylobacter jejuni: cross-reacting and serotypic specificity and potential use in diagnosis. J Hyg (Lond) 1986 Jun;96(3):377–384. doi: 10.1017/s0022172400066134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Nuijten P. J., van Asten F. J., Gaastra W., van der Zeijst B. A. Structural and functional analysis of two Campylobacter jejuni flagellin genes. J Biol Chem. 1990 Oct 15;265(29):17798–17804. [PubMed] [Google Scholar]
  39. Nuijten P. J., van der Zeijst B. A., Newell D. G. Localization of immunogenic regions on the flagellin proteins of Campylobacter jejuni 81116. Infect Immun. 1991 Mar;59(3):1100–1105. doi: 10.1128/iai.59.3.1100-1105.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Pavlovskis O. R., Rollins D. M., Haberberger R. L., Jr, Green A. E., Habash L., Strocko S., Walker R. I. Significance of flagella in colonization resistance of rabbits immunized with Campylobacter spp. Infect Immun. 1991 Jul;59(7):2259–2264. doi: 10.1128/iai.59.7.2259-2264.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Pinna L. A. Casein kinase 2: an 'eminence grise' in cellular regulation? Biochim Biophys Acta. 1990 Sep 24;1054(3):267–284. doi: 10.1016/0167-4889(90)90098-x. [DOI] [PubMed] [Google Scholar]
  42. Scocca J. J. The role of transformation in the variability of the Neisseria gonorrhoeae cell surface. Mol Microbiol. 1990 Mar;4(3):321–327. doi: 10.1111/j.1365-2958.1990.tb00599.x. [DOI] [PubMed] [Google Scholar]
  43. Seifert H. S., Ajioka R. S., Marchal C., Sparling P. F., So M. DNA transformation leads to pilin antigenic variation in Neisseria gonorrhoeae. Nature. 1988 Nov 24;336(6197):392–395. doi: 10.1038/336392a0. [DOI] [PubMed] [Google Scholar]
  44. Skirrow M. B. Campylobacter enteritis: a "new" disease. Br Med J. 1977 Jul 2;2(6078):9–11. doi: 10.1136/bmj.2.6078.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Southam G., Kalmokoff M. L., Jarrell K. F., Koval S. F., Beveridge T. J. Isolation, characterization, and cellular insertion of the flagella from two strains of the archaebacterium Methanospirillum hungatei. J Bacteriol. 1990 Jun;172(6):3221–3228. doi: 10.1128/jb.172.6.3221-3228.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Thornton S. A., Logan S. M., Trust T. J., Guerry P. Polynucleotide sequence relationships among flagellin genes of Campylobacter jejuni and Campylobacter coli. Infect Immun. 1990 Aug;58(8):2686–2689. doi: 10.1128/iai.58.8.2686-2689.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Trachtenberg S., DeRosier D. J. Three-dimensional reconstruction of the flagellar filament of Caulobacter crescentus. A flagellin lacking the outer domain and its amino acid sequence lacking an internal segment. J Mol Biol. 1988 Aug 20;202(4):787–808. doi: 10.1016/0022-2836(88)90559-1. [DOI] [PubMed] [Google Scholar]
  48. Ueki Y., Umeda A., Fujimoto S., Mitsuyama M., Amako K. Protection against Campylobacter jejuni infection in suckling mice by anti-flagellar antibody. Microbiol Immunol. 1987;31(12):1161–1171. doi: 10.1111/j.1348-0421.1987.tb01350.x. [DOI] [PubMed] [Google Scholar]
  49. Vonderviszt F., Aizawa S., Namba K. Role of the disordered terminal regions of flagellin in filament formation and stability. J Mol Biol. 1991 Oct 20;221(4):1461–1474. doi: 10.1016/0022-2836(91)90946-4. [DOI] [PubMed] [Google Scholar]
  50. Vonderviszt F., Kanto S., Aizawa S., Namba K. Terminal regions of flagellin are disordered in solution. J Mol Biol. 1989 Sep 5;209(1):127–133. doi: 10.1016/0022-2836(89)90176-9. [DOI] [PubMed] [Google Scholar]
  51. Walker R. I., Caldwell M. B., Lee E. C., Guerry P., Trust T. J., Ruiz-Palacios G. M. Pathophysiology of Campylobacter enteritis. Microbiol Rev. 1986 Mar;50(1):81–94. doi: 10.1128/mr.50.1.81-94.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Wang Y., Taylor D. E. Natural transformation in Campylobacter species. J Bacteriol. 1990 Feb;172(2):949–955. doi: 10.1128/jb.172.2.949-955.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Wei L. N., Joys T. M. Covalent structure of three phase-1 flagellar filament proteins of Salmonella. J Mol Biol. 1985 Dec 20;186(4):791–803. doi: 10.1016/0022-2836(85)90397-3. [DOI] [PubMed] [Google Scholar]
  54. Wieland F., Paul G., Sumper M. Halobacterial flagellins are sulfated glycoproteins. J Biol Chem. 1985 Dec 5;260(28):15180–15185. [PubMed] [Google Scholar]
  55. Woodgett J. R., Gould K. L., Hunter T. Substrate specificity of protein kinase C. Use of synthetic peptides corresponding to physiological sites as probes for substrate recognition requirements. Eur J Biochem. 1986 Nov 17;161(1):177–184. doi: 10.1111/j.1432-1033.1986.tb10139.x. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES