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. 1995 Jan;63(1):309–316. doi: 10.1128/iai.63.1.309-316.1995

Nonlethal adherence to human neutrophils mediated by Dr antigen-specific adhesins of Escherichia coli.

J R Johnson 1, K M Skubitz 1, B J Nowicki 1, K Jacques-Palaz 1, R M Rakita 1
PMCID: PMC172993  PMID: 7806371

Abstract

Uropathogenic Escherichia coli strains express a variety of adhesins, including members of the Dr adhesin family such as the Dr hemagglutinin, AFAI, and AFAIII. Certain E. coli adhesins (e.g., type 1 and S fimbriae) are known to mediate adherence to human polymorphonuclear leukocytes (PMNs). The receptor on erythrocytes for Dr family adhesins, decay accelerating factor, is also present on PMNs. To determine whether Dr family adhesins mediate adherence to PMNs and to characterize the specificity and consequences of such adherence, we studied agglutination of PMNs and adherence to PMNs by recombinant E. coli strains expressing various mannose-resistant or mannose-sensitive adhesins, in the presence or absence of inhibitors of adherence. Dr family adhesins, like type 1 fimbriae, mediated concentration-dependent adherence to PMNs. Adherence to PMNs was mannose sensitive for type 1 fimbriae but mannose resistant for Dr family adhesins. Chloramphenicol inhibited PMN adherence for the Dr hemagglutinin with the same potency as that with which it inhibited hemagglutination, but it was inactive against PMN adherence and hemagglutination mediated by other members of the Dr adhesin family. In contrast to PMN adherence mediated by type 1 fimbriae, adherence mediated by the Dr hemagglutinin did not lead to significantly increased bacterial killing. These data suggest that Dr family adhesins mediate a novel pattern of adherence to PMNs, probably by recognizing decay accelerating factor, with minimal consequent bacterial killing.

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Selected References

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  1. Abraham J. M., Freitag C. S., Gander R. M., Clements J. R., Thomas V. L., Eisenstein B. I. Fimbrial phase variation and DNA rearrangements in uropathogenic isolates of Escherichia coli. Mol Biol Med. 1986 Dec;3(6):495–508. [PubMed] [Google Scholar]
  2. Anstee D. J. Blood group-active surface molecules of the human red blood cell. Vox Sang. 1990;58(1):1–20. doi: 10.1111/j.1423-0410.1990.tb02049.x. [DOI] [PubMed] [Google Scholar]
  3. Arduino R. C., Jacques-Palaz K., Murray B. E., Rakita R. M. Resistance of Enterococcus faecium to neutrophil-mediated phagocytosis. Infect Immun. 1994 Dec;62(12):5587–5594. doi: 10.1128/iai.62.12.5587-5594.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bilge S. S., Clausen C. R., Lau W., Moseley S. L. Molecular characterization of a fimbrial adhesin, F1845, mediating diffuse adherence of diarrhea-associated Escherichia coli to HEp-2 cells. J Bacteriol. 1989 Aug;171(8):4281–4289. doi: 10.1128/jb.171.8.4281-4289.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blumenstock E., Jann K. Adhesion of piliated Escherichia coli strains to phagocytes: differences between bacteria with mannose-sensitive pili and those with mannose-resistant pili. Infect Immun. 1982 Jan;35(1):264–269. doi: 10.1128/iai.35.1.264-269.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bock K., Breimer M. E., Brignole A., Hansson G. C., Karlsson K. A., Larson G., Leffler H., Samuelsson B. E., Strömberg N., Edén C. S. Specificity of binding of a strain of uropathogenic Escherichia coli to Gal alpha 1----4Gal-containing glycosphingolipids. J Biol Chem. 1985 Jul 15;260(14):8545–8551. [PubMed] [Google Scholar]
  7. Daniels G. Cromer-related antigens--blood group determinants on decay-accelerating factor. Vox Sang. 1989;56(4):205–211. doi: 10.1111/j.1423-0410.1989.tb02030.x. [DOI] [PubMed] [Google Scholar]
  8. Drevets D. A., Campbell P. A. Macrophage phagocytosis: use of fluorescence microscopy to distinguish between extracellular and intracellular bacteria. J Immunol Methods. 1991 Aug 28;142(1):31–38. doi: 10.1016/0022-1759(91)90289-r. [DOI] [PubMed] [Google Scholar]
  9. Eisenstein B. I. Phase variation of type 1 fimbriae in Escherichia coli is under transcriptional control. Science. 1981 Oct 16;214(4518):337–339. doi: 10.1126/science.6116279. [DOI] [PubMed] [Google Scholar]
  10. Firon N., Ofek I., Sharon N. Carbohydrate-binding sites of the mannose-specific fimbrial lectins of enterobacteria. Infect Immun. 1984 Mar;43(3):1088–1090. doi: 10.1128/iai.43.3.1088-1090.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Goetz M. B., Silverblatt F. J. Stimulation of human polymorphonuclear leukocyte oxidative metabolism by type 1 pili from Escherichia coli. Infect Immun. 1987 Mar;55(3):534–540. doi: 10.1128/iai.55.3.534-540.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Goldhar J., Perry R., Golecki J. R., Hoschutzky H., Jann B., Jann K. Nonfimbrial, mannose-resistant adhesins from uropathogenic Escherichia coli O83:K1:H4 and O14:K?:H11. Infect Immun. 1987 Aug;55(8):1837–1842. doi: 10.1128/iai.55.8.1837-1842.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Goldhar J., Yavzori M., Keisari Y., Ofek I. Phagocytosis of Escherichia coli mediated by mannose resistant non-fimbrial haemagglutinin (NFA-1). Microb Pathog. 1991 Sep;11(3):171–178. doi: 10.1016/0882-4010(91)90047-e. [DOI] [PubMed] [Google Scholar]
  14. Hales B. A., Beverley-Clarke H., High N. J., Jann K., Perry R., Goldhar J., Boulnois G. J. Molecular cloning and characterisation of the genes for a non-fimbrial adhesin from Escherichia coli. Microb Pathog. 1988 Jul;5(1):9–17. doi: 10.1016/0882-4010(88)90076-9. [DOI] [PubMed] [Google Scholar]
  15. Hoschützky H., Nimmich W., Lottspeich F., Jann K. Isolation and characterization of the non-fimbrial adhesin NFA-4 from uropathogenic Escherichia coli O7:K98:H6. Microb Pathog. 1989 May;6(5):351–359. doi: 10.1016/0882-4010(89)90077-6. [DOI] [PubMed] [Google Scholar]
  16. Johnson J. R., Swanson J. L., Neill M. A. Avian P1 antigens inhibit agglutination mediated by P fimbriae of uropathogenic Escherichia coli. Infect Immun. 1992 Feb;60(2):578–583. doi: 10.1128/iai.60.2.578-583.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Johnson J. R. Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev. 1991 Jan;4(1):80–128. doi: 10.1128/cmr.4.1.80. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kröncke K. D., Orskov I., Orskov F., Jann B., Jann K. Electron microscopic study of coexpression of adhesive protein capsules and polysaccharide capsules in Escherichia coli. Infect Immun. 1990 Aug;58(8):2710–2714. doi: 10.1128/iai.58.8.2710-2714.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. König B., König W., Scheffer J., Hacker J., Goebel W. Role of Escherichia coli alpha-hemolysin and bacterial adherence in infection: requirement for release of inflammatory mediators from granulocytes and mast cells. Infect Immun. 1986 Dec;54(3):886–892. doi: 10.1128/iai.54.3.886-892.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Labigne-Roussel A., Falkow S. Distribution and degree of heterogeneity of the afimbrial-adhesin-encoding operon (afa) among uropathogenic Escherichia coli isolates. Infect Immun. 1988 Mar;56(3):640–648. doi: 10.1128/iai.56.3.640-648.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Labigne-Roussel A., Schmidt M. A., Walz W., Falkow S. Genetic organization of the afimbrial adhesin operon and nucleotide sequence from a uropathogenic Escherichia coli gene encoding an afimbrial adhesin. J Bacteriol. 1985 Jun;162(3):1285–1292. doi: 10.1128/jb.162.3.1285-1292.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Le Bouguenec C., Garcia M. I., Ouin V., Desperrier J. M., Gounon P., Labigne A. Characterization of plasmid-borne afa-3 gene clusters encoding afimbrial adhesins expressed by Escherichia coli strains associated with intestinal or urinary tract infections. Infect Immun. 1993 Dec;61(12):5106–5114. doi: 10.1128/iai.61.12.5106-5114.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Low M. G. Biochemistry of the glycosyl-phosphatidylinositol membrane protein anchors. Biochem J. 1987 May 15;244(1):1–13. doi: 10.1042/bj2440001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Macher B. A., Klock J. C. Isolation and chemical characterization of neutral glycosphingolipids of human neutrophils. J Biol Chem. 1980 Mar 10;255(5):2092–2096. [PubMed] [Google Scholar]
  26. Mangan D. F., Snyder I. S. Mannose-sensitive interaction of Escherichia coli with human peripheral leukocytes in vitro. Infect Immun. 1979 Nov;26(2):520–527. doi: 10.1128/iai.26.2.520-527.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nicholson-Weller A., March J. P., Rosen C. E., Spicer D. B., Austen K. F. Surface membrane expression by human blood leukocytes and platelets of decay-accelerating factor, a regulatory protein of the complement system. Blood. 1985 May;65(5):1237–1244. [PubMed] [Google Scholar]
  28. Nicholson-Weller A., Russian D. A., Austen K. F. Natural killer cells are deficient in the surface expression of the complement regulatory protein, decay accelerating factor (DAF). J Immunol. 1986 Aug 15;137(4):1275–1279. [PubMed] [Google Scholar]
  29. Nowicki B., Barrish J. P., Korhonen T., Hull R. A., Hull S. I. Molecular cloning of the Escherichia coli O75X adhesin. Infect Immun. 1987 Dec;55(12):3168–3173. doi: 10.1128/iai.55.12.3168-3173.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nowicki B., Hart A., Coyne K. E., Lublin D. M., Nowicki S. Short consensus repeat-3 domain of recombinant decay-accelerating factor is recognized by Escherichia coli recombinant Dr adhesin in a model of a cell-cell interaction. J Exp Med. 1993 Dec 1;178(6):2115–2121. doi: 10.1084/jem.178.6.2115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nowicki B., Holthöfer H., Saraneva T., Rhen M., Väisänen-Rhen V., Korhonen T. K. Location of adhesion sites for P-fimbriated and for 075X-positive Escherichia coli in the human kidney. Microb Pathog. 1986 Apr;1(2):169–180. doi: 10.1016/0882-4010(86)90019-7. [DOI] [PubMed] [Google Scholar]
  32. Nowicki B., Labigne A., Moseley S., Hull R., Hull S., Moulds J. The Dr hemagglutinin, afimbrial adhesins AFA-I and AFA-III, and F1845 fimbriae of uropathogenic and diarrhea-associated Escherichia coli belong to a family of hemagglutinins with Dr receptor recognition. Infect Immun. 1990 Jan;58(1):279–281. doi: 10.1128/iai.58.1.279-281.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Nowicki B., Moulds J., Hull R., Hull S. A hemagglutinin of uropathogenic Escherichia coli recognizes the Dr blood group antigen. Infect Immun. 1988 May;56(5):1057–1060. doi: 10.1128/iai.56.5.1057-1060.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Nowicki B., Truong L., Moulds J., Hull R. Presence of the Dr receptor in normal human tissues and its possible role in the pathogenesis of ascending urinary tract infection. Am J Pathol. 1988 Oct;133(1):1–4. [PMC free article] [PubMed] [Google Scholar]
  35. Ohman L., Hed J., Stendahl O. Interaction between human polymorphonuclear leukocytes and two different strains of type 1 fimbriae-bearing Escherichia coli. J Infect Dis. 1982 Dec;146(6):751–757. doi: 10.1093/infdis/146.6.751. [DOI] [PubMed] [Google Scholar]
  36. Orndorff P. E., Falkow S. Organization and expression of genes responsible for type 1 piliation in Escherichia coli. J Bacteriol. 1984 Aug;159(2):736–744. doi: 10.1128/jb.159.2.736-744.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rosen H., Michel B. R., Chait A. Phagocytosis of opsonized oil droplets by neutrophils. Adaptation to a microtiter plate format. J Immunol Methods. 1991 Nov 5;144(1):117–125. doi: 10.1016/0022-1759(91)90237-a. [DOI] [PubMed] [Google Scholar]
  38. Silverblatt F. J., Dreyer J. S., Schauer S. Effect of pili on susceptibility of Escherichia coli to phagocytosis. Infect Immun. 1979 Apr;24(1):218–223. doi: 10.1128/iai.24.1.218-223.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Skubitz K. M., Snook R. W., 2nd Monoclonal antibodies that recognize lacto-N-fucopentaose III (CD15) react with the adhesion-promoting glycoprotein family (LFA-1/HMac-1/gp 150,95) and CR1 on human neutrophils. J Immunol. 1987 Sep 1;139(5):1631–1639. [PubMed] [Google Scholar]
  40. Steadman R., Topley N., Jenner D. E., Davies M., Williams J. D. Type 1 fimbriate Escherichia coli stimulates a unique pattern of degranulation by human polymorphonuclear leukocytes. Infect Immun. 1988 Apr;56(4):815–822. doi: 10.1128/iai.56.4.815-822.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Svanborg Edén C., Bjursten L. M., Hull R., Hull S., Magnusson K. E., Moldovano Z., Leffler H. Influence of adhesins on the interaction of Escherichia coli with human phagocytes. Infect Immun. 1984 Jun;44(3):672–680. doi: 10.1128/iai.44.3.672-680.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Topley N., Steadman R., Mackenzie R., Knowlden J. M., Williams J. D. Type 1 fimbriate strains of Escherichia coli initiate renal parenchymal scarring. Kidney Int. 1989 Oct;36(4):609–616. doi: 10.1038/ki.1989.237. [DOI] [PubMed] [Google Scholar]
  43. Ventur Y., Scheffer J., Hacker J., Goebel W., König W. Effects of adhesins from mannose-resistant Escherichia coli on mediator release from human lymphocytes, monocytes, and basophils and from polymorphonuclear granulocytes. Infect Immun. 1990 Jun;58(6):1500–1508. doi: 10.1128/iai.58.6.1500-1508.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Väisänen-Rhen V. Fimbria-like hemagglutinin of Escherichia coli O75 strains. Infect Immun. 1984 Nov;46(2):401–407. doi: 10.1128/iai.46.2.401-407.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Weinstein R., Silverblatt F. J. Antibacterial mechanisms of antibody to mannose-sensitive pili of Escherichia coli. J Infect Dis. 1983 May;147(5):882–889. doi: 10.1093/infdis/147.5.882. [DOI] [PubMed] [Google Scholar]
  46. Westerlund B., Kuusela P., Risteli J., Risteli L., Vartio T., Rauvala H., Virkola R., Korhonen T. K. The O75X adhesin of uropathogenic Escherichia coli is a type IV collagen-binding protein. Mol Microbiol. 1989 Mar;3(3):329–337. doi: 10.1111/j.1365-2958.1989.tb00178.x. [DOI] [PubMed] [Google Scholar]

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