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. 1991 Nov;59(11):4221–4226. doi: 10.1128/iai.59.11.4221-4226.1991

Release of leukotriene B4 from human neutrophils after interaction with nontypeable Haemophilus influenzae.

R Garofalo 1, H Faden 1, S Sharma 1, P L Ogra 1
PMCID: PMC259019  PMID: 1657784

Abstract

Opsonization of nontypeable Haemophilus influenzae with antibody is critical for the interaction between the organism and human polymorphonuclear leukocytes (PMNs). Nontypeable H. influenzae opsonized in fresh antibody-positive serum induced the release of 42.5 +/- 17.9 ng of leukotriene B4 per ml from PMNs after 20 min of incubation at 37 degrees C. On the other hand, opsonization of the organisms in fresh antibody-negative serum stimulated the release of significantly smaller amounts of leukotriene B4 by the PMNs. Simultaneous determinations of phagocytosis demonstrated similar patterns of response. A small amount (26.7 +/- 7.6%) of unopsonized nontypeable H. influenzae was phagocytosed by PMNs during 20 min of incubation at 37 degrees C. In contrast, 89.3 +/- 2.0% of nontypeable H. influenzae opsonized in fresh antibody-positive serum was phagocytosed during the same incubation period (P less than 0.001). Removal of complement through heat inactivation at 56 degrees C for 30 min did not significantly affect phagocytosis. These data suggest that the humoral immune response to nontypeable H. influenzae plays an important role in the inflammatory process and may contribute to the production of middle ear effusions in otitis media.

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Selected References

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  1. Bluestone C. D. Management of otitis media in infants and children: current role of old and new antimicrobial agents. Pediatr Infect Dis J. 1988 Nov;7(11 Suppl):S129–S136. doi: 10.1097/00006454-198811001-00002. [DOI] [PubMed] [Google Scholar]
  2. Brodsky L., Faden H., Bernstein J., Stanievich J., DeCastro G., Volovitz B., Ogra P. L. Arachidonic acid metabolites in middle ear effusions of children. Ann Otol Rhinol Laryngol. 1991 Jul;100(7):589–592. doi: 10.1177/000348949110000714. [DOI] [PubMed] [Google Scholar]
  3. Carlin S. A., Marchant C. D., Shurin P. A., Johnson C. E., Murdell-Panek D., Barenkamp S. J. Early recurrences of otitis media: reinfection or relapse? J Pediatr. 1987 Jan;110(1):20–25. doi: 10.1016/s0022-3476(87)80281-0. [DOI] [PubMed] [Google Scholar]
  4. Chauncey J. B., Simon R. H., Peters-Golden M. Rat alveolar macrophages synthesize leukotriene B4 and 12-hydroxyeicosatetraenoic acid from alveolar epithelial cell-derived arachidonic acid. Am Rev Respir Dis. 1988 Oct;138(4):928–935. doi: 10.1164/ajrccm/138.4.928. [DOI] [PubMed] [Google Scholar]
  5. Dahlén S. E., Björk J., Hedqvist P., Arfors K. E., Hammarström S., Lindgren J. A., Samuelsson B. Leukotrienes promote plasma leakage and leukocyte adhesion in postcapillary venules: in vivo effects with relevance to the acute inflammatory response. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3887–3891. doi: 10.1073/pnas.78.6.3887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Faden H., Bernstein J., Brodsky L., Stanievich J., Krystofik D., Shuff C., Hong J. J., Ogra P. L. Otitis media in children. I. The systemic immune response to nontypable Hemophilus influenzae. J Infect Dis. 1989 Dec;160(6):999–1004. doi: 10.1093/infdis/160.6.999. [DOI] [PubMed] [Google Scholar]
  7. Faden H., Brodsky L., Bernstein J., Stanievich J., Krystofik D., Shuff C., Hong J. J., Ogra P. L. Otitis media in children: local immune response to nontypeable Haemophilus influenzae. Infect Immun. 1989 Nov;57(11):3555–3559. doi: 10.1128/iai.57.11.3555-3559.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Faden H., Stanievich J., Brodsky L., Bernstein J., Ogra P. L. Changes in nasopharyngeal flora during otitis media of childhood. Pediatr Infect Dis J. 1990 Sep;9(9):623–626. [PubMed] [Google Scholar]
  9. Ford-Hutchinson A. W. Leukotriene B4 in inflammation. Crit Rev Immunol. 1990;10(1):1–12. [PubMed] [Google Scholar]
  10. Goldyne M. E., Stobo J. D. Human monocytes synthesize eicosanoids from T lymphocyte-derived arachidonic acid. Prostaglandins. 1982 Nov;24(5):623–630. doi: 10.1016/0090-6980(82)90032-6. [DOI] [PubMed] [Google Scholar]
  11. Hansen E. J., Hart D. A., McGehee J. L., Toews G. B. Immune enhancement of pulmonary clearance of nontypable Haemophilus influenzae. Infect Immun. 1988 Jan;56(1):182–190. doi: 10.1128/iai.56.1.182-190.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Harrison C. J., Marks M. I., Welch D. F. Microbiology of recently treated acute otitis media compared with previously untreated acute otitis media. Pediatr Infect Dis. 1985 Nov-Dec;4(6):641–646. doi: 10.1097/00006454-198511000-00009. [DOI] [PubMed] [Google Scholar]
  13. Hirata F., Corcoran B. A., Venkatasubramanian K., Schiffmann E., Axelrod J. Chemoattractants stimulate degradation of methylated phospholipids and release of arachidonic acid in rabbit leukocytes. Proc Natl Acad Sci U S A. 1979 Jun;76(6):2640–2643. doi: 10.1073/pnas.76.6.2640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Howard A. J., Dunkin K. T., Millar G. W. Nasopharyngeal carriage and antibiotic resistance of Haemophilus influenzae in healthy children. Epidemiol Infect. 1988 Apr;100(2):193–203. doi: 10.1017/s0950268800067327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Juhn S. K., Jung T. T. Inflammatory changes reflected in middle ear effusion in otitis media. Auris Nasus Larynx. 1985;12 (Suppl 1):S63–S66. doi: 10.1016/s0385-8146(85)80103-6. [DOI] [PubMed] [Google Scholar]
  16. Jung T. T. Prostaglandins, leukotrienes, and other arachidonic acid metabolites in the pathogenesis of otitis media. Laryngoscope. 1988 Sep;98(9):980–993. doi: 10.1288/00005537-198809000-00013. [DOI] [PubMed] [Google Scholar]
  17. Karasic R. B., Trumpp C. E., Gnehm H. E., Rice P. A., Pelton S. I. Modification of otitis media in chinchillas rechallenged with nontypable Haemophilus influenzae and serological response to outer membrane antigens. J Infect Dis. 1985 Feb;151(2):273–279. doi: 10.1093/infdis/151.2.273. [DOI] [PubMed] [Google Scholar]
  18. Kilian M., Heine-Jensen J., Bülow P. Haemophilus in the upper respiratory tract of children. A bacteriological, serological and clinical investigation. Acta Pathol Microbiol Scand B Microbiol Immunol. 1972;80(4):571–578. doi: 10.1111/j.1699-0463.1972.tb00181.x. [DOI] [PubMed] [Google Scholar]
  19. Liston T. E., Foshee W. S., McCleskey F. K. The bacteriology of recurrent otitis media and the effect of sulfisoxazole chemoprophylaxis. Pediatr Infect Dis. 1984 Jan-Feb;3(1):20–24. doi: 10.1097/00006454-198401000-00006. [DOI] [PubMed] [Google Scholar]
  20. Long S. S., Henretig F. M., Teter M. J., McGowan K. L. Nasopharyngeal flora and acute otitis media. Infect Immun. 1983 Sep;41(3):987–991. doi: 10.1128/iai.41.3.987-991.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mackowiak P. A. The normal microbial flora. N Engl J Med. 1982 Jul 8;307(2):83–93. doi: 10.1056/NEJM198207083070203. [DOI] [PubMed] [Google Scholar]
  22. Marcus A. J., Broekman M. J., Safier L. B., Ullman H. L., Islam N., Sherhan C. N., Rutherford L. E., Korchak H. M., Weissmann G. Formation of leukotrienes and other hydroxy acids during platelet-neutrophil interactions in vitro. Biochem Biophys Res Commun. 1982 Nov 16;109(1):130–137. doi: 10.1016/0006-291x(82)91575-3. [DOI] [PubMed] [Google Scholar]
  23. Martin T. R., Pistorese B. P., Chi E. Y., Goodman R. B., Matthay M. A. Effects of leukotriene B4 in the human lung. Recruitment of neutrophils into the alveolar spaces without a change in protein permeability. J Clin Invest. 1989 Nov;84(5):1609–1619. doi: 10.1172/JCI114338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Musher D. M., Hague-Park M., Baughn R. E., Wallace R. J., Jr, Cowley B. Opsonizing and bactericidal effects of normal human serum on nontypable Haemophilus influenzae. Infect Immun. 1983 Jan;39(1):297–304. doi: 10.1128/iai.39.1.297-304.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Payan D. G., Missirian-Bastian A., Goetzl E. J. Human T-lymphocyte subset specificity of the regulatory effects of leukotriene B4. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3501–3505. doi: 10.1073/pnas.81.11.3501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rola-Pleszczynski M. Differential effects of leukotriene B4 on T4+ and T8+ lymphocyte phenotype and immunoregulatory functions. J Immunol. 1985 Aug;135(2):1357–1360. [PubMed] [Google Scholar]
  27. Shurin P. A., Pelton S. I., Tager I. B., Kasper D. L. Bactericidal antibody and susceptibility to otitis media caused by nontypable strains of Haemophilus influenzae. J Pediatr. 1980 Sep;97(3):364–369. doi: 10.1016/s0022-3476(80)80182-x. [DOI] [PubMed] [Google Scholar]
  28. Sloyer J. L., Jr, Cate C. C., Howie V. M., Ploussard J. H., Johnston R. B., Jr The immune response to acute otitis media in children. II. Serum and middle ear fluid antibody in otitis media due to Haemophilus influenza. J Infect Dis. 1975 Dec;132(6):685–688. doi: 10.1093/infdis/132.6.685. [DOI] [PubMed] [Google Scholar]
  29. Smith M. J., Ford-Hutchinson A. W., Bray M. A. Leukotriene B: a potential mediator of inflammation. J Pharm Pharmacol. 1980 Jul;32(7):517–518. doi: 10.1111/j.2042-7158.1980.tb12985.x. [DOI] [PubMed] [Google Scholar]
  30. Smith R. J., Yein F. S., Speziale S. C., Bowman B. J. A possible requirement for arachidonic acid lipoxygenation in the mechanism of phagocytic degranulation by human neutrophils stimulated with aggregated immunoglobulin G. Biochem Biophys Res Commun. 1986 Apr 14;136(1):310–315. doi: 10.1016/0006-291x(86)90911-3. [DOI] [PubMed] [Google Scholar]
  31. Waite M., DeChatelet L. R., King L., Shirley P. S. Phagocytosis-induced release of arachidonic acid from human neutrophils. Biochem Biophys Res Commun. 1979 Oct 12;90(3):984–992. doi: 10.1016/0006-291x(79)91924-7. [DOI] [PubMed] [Google Scholar]

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