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. 1993 Aug;61(8):3375–3381. doi: 10.1128/iai.61.8.3375-3381.1993

Paradoxical effect of pilus expression on binding of antibodies by Haemophilus influenzae.

J R Gilsdorf 1, M Tucci 1, L J Forney 1, W Watson 1, C F Marrs 1, E J Hansen 1
PMCID: PMC281013  PMID: 7687585

Abstract

Haemophilus influenzae type b (Hib) pili are surface proteins that are associated with the ability of Hib to attach to human epithelial cells. Like pilus expression of other bacteria, expression of Hib pili undergoes phase variation. We observed that Hib in the piliated phase (Hib p+) bound monoclonal antibodies directed against six conserved, surface-exposed, nonpilus Hib outer membrane epitopes to a greater extent than Hib in the nonpiliated phase (Hib p-). However, after extended incubation, p+ and p- cells bound these antibodies in a similar fashion. The differential in nonpilus antibody binding to p+ and p- Hib was not related to the presence of the type b capsule. In addition, Hib p+ organisms whose pilin gene was insertionally inactivated and did not produce pili and Hib in the nonpiliated phase bound the nonpilus Hib antibodies similarly. Hib p+ and p- organisms did not differ in their binding of anti-type b capsule antibody, and the binding was specific for the epitopes recognized by the antibodies. In complement-dependent bactericidal assays, the nonpilus antibodies killed Hib p+ more effectively than Hib p-. The increased binding to, and killing of, Hib p+ by a variety of nonpilus antibodies may be important for host defense against invasive Hib.

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Selected References

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  1. Armes L. G., Forney L. J. The complete primary structure of pilin from Haemophilus influenzae type b strain Eagan. J Protein Chem. 1990 Feb;9(1):45–52. doi: 10.1007/BF01024983. [DOI] [PubMed] [Google Scholar]
  2. Björkstén B., Wadström T. Interaction of Escherichia coli with different fimbriae and polymorphonuclear leukocytes. Infect Immun. 1982 Oct;38(1):298–305. doi: 10.1128/iai.38.1.298-305.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Cope L. D., Pelzel S. E., Latimer J. L., Hansen E. J. Characterization of a mutant of Haemophilus influenzae type b lacking the P2 major outer membrane protein. Infect Immun. 1990 Oct;58(10):3312–3318. doi: 10.1128/iai.58.10.3312-3318.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Farley M. M., Stephens D. S., Kaplan S. L., Mason E. O., Jr Pilus- and non-pilus-mediated interactions of Haemophilus influenzae type b with human erythrocytes and human nasopharyngeal mucosa. J Infect Dis. 1990 Feb;161(2):274–280. doi: 10.1093/infdis/161.2.274. [DOI] [PubMed] [Google Scholar]
  6. Forney L. J., Marrs C. F., Bektesh S. L., Gilsdorf J. R. Comparison and analysis of the nucleotide sequences of pilin genes from Haemophilus influenzae type b strains Eagan and M43. Infect Immun. 1991 Jun;59(6):1991–1996. doi: 10.1128/iai.59.6.1991-1996.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gilsdorf J. R., Chang H. Y., McCrea K. W., Bakaletz L. O. Comparison of hemagglutinating pili of Haemophilus influenzae type b with similar structures of nontypeable H. influenzae. Infect Immun. 1992 Feb;60(2):374–379. doi: 10.1128/iai.60.2.374-379.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gilsdorf J. R., Marrs C. F., McCrea K. W., Forney L. J. Cloning, expression, and sequence analysis of the Haemophilus influenzae type b strain M43p+ pilin gene. Infect Immun. 1990 Apr;58(4):1065–1072. doi: 10.1128/iai.58.4.1065-1072.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Goetz M. B., Kuriyama S. M., Silverblatt F. J. Phagolysosome formation by polymorphonuclear neutrophilic leukocytes after ingestion of Escherichia coli that express type 1 pili. J Infect Dis. 1987 Jul;156(1):229–233. doi: 10.1093/infdis/156.1.229. [DOI] [PubMed] [Google Scholar]
  10. Gonzales F. R., Leachman S., Norgard M. V., Radolf J. D., McCracken G. H., Jr, Evans C., Hansen E. J. Cloning and expression in Escherichia coli of the gene encoding the heat-modifiable major outer membrane protein of Haemophilus influenzae type b. Infect Immun. 1987 Dec;55(12):2993–3000. doi: 10.1128/iai.55.12.2993-3000.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gulig P. A., Hansen E. J. Coprecipitation of lipopolysaccharide and the 39,000-molecular-weight major outer membrane protein of Haemophilus influenzae type b by lipopolysaccharide-directed monoclonal antibody. Infect Immun. 1985 Sep;49(3):819–827. doi: 10.1128/iai.49.3.819-827.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hansen E. J., Pelzel S. E., Orth K., Moomaw C. R., Radolf J. D., Slaughter C. A. Structural and antigenic conservation of the P2 porin protein among strains of Haemophilus influenzae type b. Infect Immun. 1989 Nov;57(11):3270–3275. doi: 10.1128/iai.57.11.3270-3275.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Heggeness M. H., Ash J. F. Use of the avidin-biotin complex for the localization of actin and myosin with fluorescence microscopy. J Cell Biol. 1977 Jun;73(3):783–788. doi: 10.1083/jcb.73.3.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Herriott R. M., Meyer E. M., Vogt M. Defined nongrowth media for stage II development of competence in Haemophilus influenzae. J Bacteriol. 1970 Feb;101(2):517–524. doi: 10.1128/jb.101.2.517-524.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kaplan S. L., Mason E. O., Jr, Wiedermann B. L. Role of adherence in the pathogenesis of Haemophilus influenzae type b infection in infant rats. Infect Immun. 1983 Nov;42(2):612–617. doi: 10.1128/iai.42.2.612-617.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kimura A., Gulig P. A., McCracken G. H., Jr, Loftus T. A., Hansen E. J. A minor high-molecular-weight outer membrane protein of Haemophilus influenzae type b is a protective antigen. Infect Immun. 1985 Jan;47(1):253–259. doi: 10.1128/iai.47.1.253-259.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kuratana M., Anderson P. Host metabolites that phenotypically increase the resistance of Haemophilus influenzae type b to clearance mechanisms. J Infect Dis. 1991 May;163(5):1073–1079. doi: 10.1093/infdis/163.5.1073. [DOI] [PubMed] [Google Scholar]
  18. Leunk R. D., Moon R. J. Association of type 1 pili with the ability of livers to clear Salmonella typhimurium. Infect Immun. 1982 Jun;36(3):1168–1174. doi: 10.1128/iai.36.3.1168-1174.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. LiPuma J. J., Gilsdorf J. R. Structural and serological relatedness of Haemophilus influenzae type b pili. Infect Immun. 1988 May;56(5):1051–1056. doi: 10.1128/iai.56.5.1051-1056.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mason E. O., Jr, Kaplan S. L., Wiedermann B. L., Norrod E. P., Stenback W. A. Frequency and properties of naturally occurring adherent piliated strains of Haemophilus influenzae type b. Infect Immun. 1985 Jul;49(1):98–103. doi: 10.1128/iai.49.1.98-103.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Müller W., Keppner W., Rasched I. Versatile kanamycin-resistance cartridges for vector construction in Escherichia coli. Gene. 1986;46(1):131–133. doi: 10.1016/0378-1119(86)90176-9. [DOI] [PubMed] [Google Scholar]
  22. Pruzzo C., Dainelli B., Ricchetti M. Piliated Bacteroides fragilis strains adhere to epithelial cells and are more sensitive to phagocytosis by human neutrophils than nonpiliated strains. Infect Immun. 1984 Jan;43(1):189–194. doi: 10.1128/iai.43.1.189-194.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Shaw S., Smith A. L., Anderson P., Smith D. H. The paradox of Hemophilus infuenzae type B bacteremia in the presence of serum bactericidal activity. J Clin Invest. 1976 Oct;58(4):1019–1029. doi: 10.1172/JCI108525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Stull T. L., Mendelman P. M., Haas J. E., Schoenborn M. A., Mack K. D., Smith A. L. Characterization of Haemophilus influenzae type b fimbriae. Infect Immun. 1984 Dec;46(3):787–796. doi: 10.1128/iai.46.3.787-796.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tosi M. F., Anderson D. C., Barrish J., Mason E. O., Jr, Kaplan S. L. Effect of piliation on interactions of Haemophilus influenzae type b with human polymorphonuclear leukocytes. Infect Immun. 1985 Mar;47(3):780–785. doi: 10.1128/iai.47.3.780-785.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]

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