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. 1993 Oct;61(10):4112–4118. doi: 10.1128/iai.61.10.4112-4118.1993

Adherence to human cells of a cryptic Haemophilus genospecies responsible for genital and neonatal infections.

A Rosenau 1, P Y Sizaret 1, J M Musser 1, A Goudeau 1, R Quentin 1
PMCID: PMC281132  PMID: 8104893

Abstract

Haemophilus strains usually identified as Haemophilus influenzae biotype IV belonging to a cryptic genospecies are responsible for genital and neonatal infections. As a first approach to identifying the bacterial factors involved in the pathogenesis of these unusual diseases, we studied the piliation, adherence, and invasion properties of 17 strains assigned to this cryptic genospecies. Twelve strains spontaneously displayed abundant peritrichous piliation, and two strains expressed peritrichous pili after enrichment procedures. For virtually all strains, piliation correlated with adhesion to cultured HeLa cells of genital origin and to a lesser extent with adhesion to HEp-2 cells of laryngeal origin. A variation in the adherence properties of the various strains was observed: all piliated strains except one adhered to 50 to 100% of HeLa cells, with a mean number of bacteria per cell varying from 4 to 50. Adherence was not dependent on the state of growth for most strains, was more pronounced with HeLa cells than with HEp-2 cells for 10 of the 12 highly adherent strains, was time and inoculum dependent, and was not followed by significant invasion of cells. Most of the strains belonging to this unusual Haemophilus clone possess adhesins that do not recognize erythrocyte receptors, since agglutination of human erythrocytes was observed with only 3 of the 14 piliated strains.

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Selected References

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  1. Albritton W. L., Brunton J. L., Meier M., Bowman M. N., Slaney L. A. Haemophilus influenzae: comparison of respiratory tract isolates with genitourinary tract isolates. J Clin Microbiol. 1982 Nov;16(5):826–831. doi: 10.1128/jcm.16.5.826-831.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson P. W., Pichichero M. E., Connor E. M. Enhanced nasopharyngeal colonization of rats by piliated Haemophilus influenzae type b. Infect Immun. 1985 May;48(2):565–568. doi: 10.1128/iai.48.2.565-568.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bakaletz L. O., Tallan B. M., Hoepf T., DeMaria T. F., Birck H. G., Lim D. J. Frequency of fimbriation of nontypable Haemophilus influenzae and its ability to adhere to chinchilla and human respiratory epithelium. Infect Immun. 1988 Feb;56(2):331–335. doi: 10.1128/iai.56.2.331-335.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Connor E. M., Loeb M. R. A hemadsorption method for detection of colonies of Haemophilus influenzae type b expressing fimbriae. J Infect Dis. 1983 Nov;148(5):855–860. doi: 10.1093/infdis/148.5.855. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Friesen C. A., Cho C. T. Characteristic features of neonatal sepsis due to Haemophilus influenzae. Rev Infect Dis. 1986 Sep-Oct;8(5):777–780. doi: 10.1093/clinids/8.5.777. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Gilsdorf J. R., Judd W. J., Cinat M. Relationship of Haemophilus influenzae type b pilus structure and adherence to human erythrocytes. Infect Immun. 1989 Oct;57(10):3259–3260. doi: 10.1128/iai.57.10.3259-3260.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Horne R. W., Ronchetti I. P. A negative staining-carbon film technique for studying viruses in the electron microscope. I. Preparative procedures for examining icosahedral and filamentous viruses. J Ultrastruct Res. 1974 Jun;47(3):361–383. doi: 10.1016/s0022-5320(74)90015-x. [DOI] [PubMed] [Google Scholar]
  11. Kahn M. E., Gromkova R. Occurrence of pili on and adhesive properties of Haemophilus parainfluenzae. J Bacteriol. 1981 Feb;145(2):1075–1078. doi: 10.1128/jb.145.2.1075-1078.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kleiman M. B., Reynolds J. K., Schreiner R. L., Smith J. W. Failure to demonstrate special virulence of nontypable Haemophilus influenzae biotype 4 in neonatal sepsis. J Infect Dis. 1983 Sep;148(3):615–615. doi: 10.1093/infdis/148.3.615. [DOI] [PubMed] [Google Scholar]
  13. Lee C. A., Falkow S. The ability of Salmonella to enter mammalian cells is affected by bacterial growth state. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4304–4308. doi: 10.1073/pnas.87.11.4304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Murphy T. F., Kirkham C., Sikkema D. J. Neonatal, urogenital isolates of biotype 4 nontypeable Haemophilus influenzae express a variant P6 outer membrane protein molecule. Infect Immun. 1992 May;60(5):2016–2022. doi: 10.1128/iai.60.5.2016-2022.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Musser J. M., Barenkamp S. J., Granoff D. M., Selander R. K. Genetic relationships of serologically nontypable and serotype b strains of Haemophilus influenzae. Infect Immun. 1986 Apr;52(1):183–191. doi: 10.1128/iai.52.1.183-191.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Patrick C. C., Patrick G. S., Kaplan S. L., Barrish J., Mason E. O., Jr Adherence kinetics of Haemophilus influenzae type b to eucaryotic cells. Pediatr Res. 1989 Nov;26(5):500–503. doi: 10.1203/00006450-198911000-00028. [DOI] [PubMed] [Google Scholar]
  17. Pichichero M. E. Adherence of Haemophilus influenzae to human buccal and pharyngeal epithelial cells: relationship to pilation. J Med Microbiol. 1984 Aug;18(1):107–116. doi: 10.1099/00222615-18-1-107. [DOI] [PubMed] [Google Scholar]
  18. Porras O., Dillon H. C., Jr, Gray B. M., Svanborg-Edén C. Lack of correlation of in vitro adherence of Haemophilus influenzae to epithelial cells with frequent occurrence of otitis media. Pediatr Infect Dis J. 1987 Jan;6(1):41–45. doi: 10.1097/00006454-198701000-00011. [DOI] [PubMed] [Google Scholar]
  19. Quentin R., Martin C., Musser J. M., Pasquier-Picard N., Goudeau A. Genetic characterization of a cryptic genospecies of Haemophilus causing urogenital and neonatal infections. J Clin Microbiol. 1993 May;31(5):1111–1116. doi: 10.1128/jcm.31.5.1111-1116.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Quentin R., Musser J. M., Mellouet M., Sizaret P. Y., Selander R. K., Goudeau A. Typing of urogenital, maternal, and neonatal isolates of Haemophilus influenzae and Haemophilus parainfluenzae in correlation with clinical source of isolation and evidence for a genital specificity of H. influenzae biotype IV. J Clin Microbiol. 1989 Oct;27(10):2286–2294. doi: 10.1128/jcm.27.10.2286-2294.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sable N. S., Connor E. M., Hall C. B., Loeb M. R. Variable adherence of fimbriated Haemophilus influenzae type b to human cells. Infect Immun. 1985 Apr;48(1):119–123. doi: 10.1128/iai.48.1.119-123.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Simonet M., Falkow S. Invasin expression in Yersinia pseudotuberculosis. Infect Immun. 1992 Oct;60(10):4414–4417. doi: 10.1128/iai.60.10.4414-4417.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. St Geme J. W., 3rd, Falkow S. Haemophilus influenzae adheres to and enters cultured human epithelial cells. Infect Immun. 1990 Dec;58(12):4036–4044. doi: 10.1128/iai.58.12.4036-4044.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Turk D. C. The pathogenicity of Haemophilus influenzae. J Med Microbiol. 1984 Aug;18(1):1–16. doi: 10.1099/00222615-18-1-1. [DOI] [PubMed] [Google Scholar]
  25. Wallace R. J., Jr, Baker C. J., Quinones F. J., Hollis D. G., Weaver R. E., Wiss K. Nontypable Haemophilus influenzae (biotype 4) as a neonatal, maternal, and genital pathogen. Rev Infect Dis. 1983 Jan-Feb;5(1):123–136. doi: 10.1093/clinids/5.1.123. [DOI] [PubMed] [Google Scholar]
  26. Weber A., Harris K., Lohrke S., Forney L., Smith A. L. Inability to express fimbriae results in impaired ability of Haemophilus influenzae b to colonize the nasopharynx. Infect Immun. 1991 Dec;59(12):4724–4728. doi: 10.1128/iai.59.12.4724-4728.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. van Alphen L., van den Berghe N., Geelen-van den Broek L. Interaction of Haemophilus influenzae with human erythrocytes and oropharyngeal epithelial cells is mediated by a common fimbrial epitope. Infect Immun. 1988 Jul;56(7):1800–1806. doi: 10.1128/iai.56.7.1800-1806.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. van Ham S. M., Mooi F. R., Sindhunata M. G., Maris W. R., van Alphen L. Cloning and expression in Escherichia coli of Haemophilus influenzae fimbrial genes establishes adherence to oropharyngeal epithelial cells. EMBO J. 1989 Nov;8(11):3535–3540. doi: 10.1002/j.1460-2075.1989.tb08519.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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