Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1997 Aug;65(8):2997–3002. doi: 10.1128/iai.65.8.2997-3002.1997

Role of pili in Haemophilus influenzae adherence and colonization.

J R Gilsdorf 1, K W McCrea 1, C F Marrs 1
PMCID: PMC175422  PMID: 9234745

Full Text

The Full Text of this article is available as a PDF (206.7 KB).

Selected References

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

  1. 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]
  2. Apicella M. A., Shero M., Dudas K. C., Stack R. R., Klohs W., LaScolea L. J., Murphy T. F., Mylotte J. M. Fimbriation of Haemophilus species isolated from the respiratory tract of adults. J Infect Dis. 1984 Jul;150(1):40–43. doi: 10.1093/infdis/150.1.40. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Barenkamp S. J., St Geme J. W., 3rd Identification of a second family of high-molecular-weight adhesion proteins expressed by non-typable Haemophilus influenzae. Mol Microbiol. 1996 Mar;19(6):1215–1223. doi: 10.1111/j.1365-2958.1996.tb02467.x. [DOI] [PubMed] [Google Scholar]
  6. Brinton C. C., Jr, Carter M. J., Derber D. B., Kar S., Kramarik J. A., To A. C., To S. C., Wood S. W. Design and development of pilus vaccines for Haemophilus influenzae diseases. Pediatr Infect Dis J. 1989 Jan;8(1 Suppl):S54–S61. [PubMed] [Google Scholar]
  7. Coleman T., Grass S., Munson R., Jr Molecular cloning, expression, and sequence of the pilin gene from nontypeable Haemophilus influenzae M37. Infect Immun. 1991 May;59(5):1716–1722. doi: 10.1128/iai.59.5.1716-1722.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. DAVIS D. J., PITTMAN M., GRIFFITTS J. J. Hemagglutination by the Koch-Weeks bacillus (Hemophilus aegyptius). J Bacteriol. 1950 Mar;59(3):427–431. doi: 10.1128/jb.59.3.427-431.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Erwin A. L., Kenny G. E., Smith A. L., Stull T. L. Human antibody response to outer membrane proteins and fimbriae of Haemophilus influenzae type b. Can J Microbiol. 1988 Jun;34(6):723–729. doi: 10.1139/m88-123. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Farley M. M., Stephens D. S., Mulks M. H., Cooper M. D., Bricker J. V., Mirra S. S., Wright A. Pathogenesis of IgA1 protease-producing and -nonproducing Haemophilus influenzae in human nasopharyngeal organ cultures. J Infect Dis. 1986 Nov;154(5):752–759. doi: 10.1093/infdis/154.5.752. [DOI] [PubMed] [Google Scholar]
  13. Fleischmann R. D., Adams M. D., White O., Clayton R. A., Kirkness E. F., Kerlavage A. R., Bult C. J., Tomb J. F., Dougherty B. A., Merrick J. M. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science. 1995 Jul 28;269(5223):496–512. doi: 10.1126/science.7542800. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Forsgren J., Samuelson A., Ahlin A., Jonasson J., Rynnel-Dagö B., Lindberg A. Haemophilus influenzae resides and multiplies intracellularly in human adenoid tissue as demonstrated by in situ hybridization and bacterial viability assay. Infect Immun. 1994 Feb;62(2):673–679. doi: 10.1128/iai.62.2.673-679.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Geme J. W., 3rd, Cutter D. Evidence that surface fibrils expressed by Haemophilus influenzae type b promote attachment to human epithelial cells. Mol Microbiol. 1995 Jan;15(1):77–85. doi: 10.1111/j.1365-2958.1995.tb02222.x. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Gilsdorf J. R., Ferrieri P. Adherence of Haemophilus influenzae to human epithelial cells. Scand J Infect Dis. 1984;16(3):271–278. doi: 10.3109/00365548409070400. [DOI] [PubMed] [Google Scholar]
  19. Gilsdorf J. R., Ferrieri P. Role of nasopharyngeal colonization with and without bacteremia in the protection of infant rats against Haemophilus influenzae type b challenge. Infect Immun. 1985 Mar;47(3):648–653. doi: 10.1128/iai.47.3.648-653.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gilsdorf J. R., Forney L. J., LiPuma J. J. Reactivity of Haemophilus influenzae type b anti-pili antibodies. Microb Pathog. 1989 Oct;7(4):311–316. doi: 10.1016/0882-4010(89)90049-1. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Gilsdorf J. R., McCrea K., Forney L. Conserved and nonconserved epitopes among Haemophilus influenzae type b pili. Infect Immun. 1990 Jul;58(7):2252–2257. doi: 10.1128/iai.58.7.2252-2257.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gilsdorf J. R., Tucci M., Forney L. J., Watson W., Marrs C. F., Hansen E. J. Paradoxical effect of pilus expression on binding of antibodies by Haemophilus influenzae. Infect Immun. 1993 Aug;61(8):3375–3381. doi: 10.1128/iai.61.8.3375-3381.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gilsdorf J. R., Tucci M., Marrs C. F. Role of pili in Haemophilus influenzae adherence to, and internalization by, respiratory cells. Pediatr Res. 1996 Feb;39(2):343–348. doi: 10.1203/00006450-199602000-00025. [DOI] [PubMed] [Google Scholar]
  26. Hacker J. Genetic determinants coding for fimbriae and adhesins of extraintestinal Escherichia coli. Curr Top Microbiol Immunol. 1990;151:1–27. doi: 10.1007/978-3-642-74703-8_1. [DOI] [PubMed] [Google Scholar]
  27. Holmgren A., Kuehn M. J., Brändén C. I., Hultgren S. J. Conserved immunoglobulin-like features in a family of periplasmic pilus chaperones in bacteria. EMBO J. 1992 Apr;11(4):1617–1622. doi: 10.1002/j.1460-2075.1992.tb05207.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hultgren S. J., Lindberg F., Magnusson G., Kihlberg J., Tennent J. M., Normark S. The PapG adhesin of uropathogenic Escherichia coli contains separate regions for receptor binding and for the incorporation into the pilus. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4357–4361. doi: 10.1073/pnas.86.12.4357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Jackson A. D., Cole P. J., Wilson R. Comparison of haemophilus influenzae type b interaction with respiratory mucosa organ cultures maintained with an air interface or immersed in medium. Infect Immun. 1996 Jun;64(6):2353–2355. doi: 10.1128/iai.64.6.2353-2355.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Johnson P. D., Oppedisano F., Bennett-Wood V., Gilbert G. L., Robins-Browne R. M. Sporadic invasion of cultured epithelial cells by Haemophilus influenzae type b. Infect Immun. 1996 Mar;64(3):1051–1053. doi: 10.1128/iai.64.3.1051-1053.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kar S., To S. C., Brinton C. C., Jr Cloning and expression in Escherichia coli of LKP pilus genes from a nontypeable Haemophilus influenzae strain. Infect Immun. 1990 Apr;58(4):903–908. doi: 10.1128/iai.58.4.903-908.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Krogfelt K. A. Bacterial adhesion: genetics, biogenesis, and role in pathogenesis of fimbrial adhesins of Escherichia coli. Rev Infect Dis. 1991 Jul-Aug;13(4):721–735. doi: 10.1093/clinids/13.4.721. [DOI] [PubMed] [Google Scholar]
  33. Kubiet M., Ramphal R. Adhesion of nontypeable Haemophilus influenzae from blood and sputum to human tracheobronchial mucins and lactoferrin. Infect Immun. 1995 Mar;63(3):899–902. doi: 10.1128/iai.63.3.899-902.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Lampe R. M., Mason E. O., Jr, Kaplan S. L., Umstead C. L., Yow M. D., Feigin R. D. Adherence of Haemophilus influenzae to buccal epithelial cells. Infect Immun. 1982 Jan;35(1):166–172. doi: 10.1128/iai.35.1.166-172.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Langermann S., Wright A. Molecular analysis of the Haemophilus influenzae type b pilin gene. Mol Microbiol. 1990 Feb;4(2):221–230. doi: 10.1111/j.1365-2958.1990.tb00589.x. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. 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]
  38. McCrea K. W., Watson W. J., Gilsdorf J. R., Marrs C. F. Identification of hifD and hifE in the pilus gene cluster of Haemophilus influenzae type b strain Eagan. Infect Immun. 1994 Nov;62(11):4922–4928. doi: 10.1128/iai.62.11.4922-4928.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Murphy T. F., Sethi S. Bacterial infection in chronic obstructive pulmonary disease. Am Rev Respir Dis. 1992 Oct;146(4):1067–1083. doi: 10.1164/ajrccm/146.4.1067. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. 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]
  42. 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]
  43. Pichichero M. E., Loeb M., Anderson, Smith D. H. Do pili play a role in pathogenicity of Haemophilus influenzae type B? Lancet. 1982 Oct 30;2(8305):960–962. doi: 10.1016/s0140-6736(82)90161-1. [DOI] [PubMed] [Google Scholar]
  44. Read T. D., Dowdell M., Satola S. W., Farley M. M. Duplication of pilus gene complexes of Haemophilus influenzae biogroup aegyptius. J Bacteriol. 1996 Nov;178(22):6564–6570. doi: 10.1128/jb.178.22.6564-6570.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Reddy M. S., Bernstein J. M., Murphy T. F., Faden H. S. Binding between outer membrane proteins of nontypeable Haemophilus influenzae and human nasopharyngeal mucin. Infect Immun. 1996 Apr;64(4):1477–1479. doi: 10.1128/iai.64.4.1477-1479.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Rosenau A., Sizaret P. Y., Musser J. M., Goudeau A., Quentin R. Adherence to human cells of a cryptic Haemophilus genospecies responsible for genital and neonatal infections. Infect Immun. 1993 Oct;61(10):4112–4118. doi: 10.1128/iai.61.10.4112-4118.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. 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]
  48. Sirakova T., Kolattukudy P. E., Murwin D., Billy J., Leake E., Lim D., DeMaria T., Bakaletz L. Role of fimbriae expressed by nontypeable Haemophilus influenzae in pathogenesis of and protection against otitis media and relatedness of the fimbrin subunit to outer membrane protein A. Infect Immun. 1994 May;62(5):2002–2020. doi: 10.1128/iai.62.5.2002-2020.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. St Geme J. W., 3rd, Cutter D., Barenkamp S. J. Characterization of the genetic locus encoding Haemophilus influenzae type b surface fibrils. J Bacteriol. 1996 Nov;178(21):6281–6287. doi: 10.1128/jb.178.21.6281-6287.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. St Geme J. W., 3rd, Falkow S., Barenkamp S. J. High-molecular-weight proteins of nontypable Haemophilus influenzae mediate attachment to human epithelial cells. Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2875–2879. doi: 10.1073/pnas.90.7.2875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. 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]
  52. St Geme J. W., 3rd, Falkow S. Isolation, expression, and nucleotide sequencing of the pilin structural gene of the Brazilian purpuric fever clone of Haemophilus influenzae biogroup aegyptius. Infect Immun. 1993 May;61(5):2233–2237. doi: 10.1128/iai.61.5.2233-2237.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. St Geme J. W., 3rd, Falkow S. Loss of capsule expression by Haemophilus influenzae type b results in enhanced adherence to and invasion of human cells. Infect Immun. 1991 Apr;59(4):1325–1333. doi: 10.1128/iai.59.4.1325-1333.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. St Geme J. W., Pinkner J. S., 3rd, Krasan G. P., Heuser J., Bullitt E., Smith A. L., Hultgren S. J. Haemophilus influenzae pili are composite structures assembled via the HifB chaperone. Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11913–11918. doi: 10.1073/pnas.93.21.11913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Stenfors L. E., Räisänen S. Abundant attachment of bacteria to nasopharyngeal epithelium in otitis-prone children. J Infect Dis. 1992 Jun;165(6):1148–1150. doi: 10.1093/infdis/165.6.1148. [DOI] [PubMed] [Google Scholar]
  56. 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]
  57. 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]
  58. 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]
  59. Watson W. J., Gilsdorf J. R., Tucci M. A., McCrea K. W., Forney L. J., Marrs C. F. Identification of a gene essential for piliation in Haemophilus influenzae type b with homology to the pilus assembly platform genes of gram-negative bacteria. Infect Immun. 1994 Feb;62(2):468–475. doi: 10.1128/iai.62.2.468-475.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. 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]
  61. Weller P. F., Smith A. L., Anderson P., Smith D. H. The role of encapsulation and host age in the clearance of Haemophilus influenzae bacteremia. J Infect Dis. 1977 Jan;135(1):34–41. doi: 10.1093/infdis/135.1.34. [DOI] [PubMed] [Google Scholar]
  62. Whitney A. M., Farley M. M. Cloning and sequence analysis of the structural pilin gene of Brazilian purpuric fever-associated Haemophilus influenzae biogroup aegyptius. Infect Immun. 1993 Apr;61(4):1559–1562. doi: 10.1128/iai.61.4.1559-1562.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Zwahlen A., Winkelstein J. A., Moxon E. R. Surface determinants of Haemophilus influenzae pathogenicity: comparative virulence of capsular transformants in normal and complement-depleted rats. J Infect Dis. 1983 Sep;148(3):385–394. doi: 10.1093/infdis/148.3.385. [DOI] [PubMed] [Google Scholar]
  64. van Alphen L., Geelen-van den Broek L., Blaas L., van Ham M., Dankert J. Blocking of fimbria-mediated adherence of Haemophilus influenzae by sialyl gangliosides. Infect Immun. 1991 Dec;59(12):4473–4477. doi: 10.1128/iai.59.12.4473-4477.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. van Alphen L., Levene C., Geelen-van den Broek L., Poole J., Bennett M., Dankert J. Combined inheritance of epithelial and erythrocyte receptors for Haemophilus influenzae. Infect Immun. 1990 Nov;58(11):3807–3809. doi: 10.1128/iai.58.11.3807-3809.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. van Alphen L., Poole J., Geelen L., Zanen H. C. The erythrocyte and epithelial cell receptors for Haemophilus influenzae are expressed independently. Infect Immun. 1987 Oct;55(10):2355–2358. doi: 10.1128/iai.55.10.2355-2358.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. 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]
  68. van Ham S. M., van Alphen L., Mooi F. R., van Putten J. P. Phase variation of H. influenzae fimbriae: transcriptional control of two divergent genes through a variable combined promoter region. Cell. 1993 Jun 18;73(6):1187–1196. doi: 10.1016/0092-8674(93)90647-9. [DOI] [PubMed] [Google Scholar]
  69. van Ham S. M., van Alphen L., Mooi F. R., van Putten J. P. The fimbrial gene cluster of Haemophilus influenzae type b. Mol Microbiol. 1994 Aug;13(4):673–684. doi: 10.1111/j.1365-2958.1994.tb00461.x. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES