Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1993 Aug;61(8):3111–3116. doi: 10.1128/iai.61.8.3111-3116.1993

Interleukin-8 enhances nonoxidative intracellular killing of Mycobacterium fortuitum by human granulocytes.

P H Nibbering 1, O Pos 1, A Stevenhagen 1, R Van Furth 1
PMCID: PMC280976  PMID: 8335340

Abstract

The results of this study show that recombinant interleukin-8 (IL-8) enhances the intracellular killing of Mycobacterium fortuitum by human granulocytes. This chemokine did not stimulate the phagocytosis of M. fortuitum by granulocytes at various bacterium-to-cell ratios. The killing process was not affected by the NADPH oxidase inhibitor diphenyleneiodonium bisulfate, which indicates that recombinant IL-8 stimulates oxygen-independent mycobactericidal mechanisms of granulocytes. IL-8 did not stimulate H2O2 production in granulocytes but primed the cells for enhanced H2O2 production upon stimulation with preopsonized M. fortuitum. In sum, the chemokine IL-8 not only is involved in the recruitment of granulocytes to the site of infection but also facilitates the elimination of microorganisms by increasing the efficiency of the bactericidal activity of granulocytes.

Full text

PDF
3111

Selected References

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

  1. Baggiolini M., Imboden P., Detmers P. Neutrophil activation and the effects of interleukin-8/neutrophil-activating peptide 1 (IL-8/NAP-1). Cytokines. 1992;4:1–17. [PubMed] [Google Scholar]
  2. Barnes P. F., Bloch A. B., Davidson P. T., Snider D. E., Jr Tuberculosis in patients with human immunodeficiency virus infection. N Engl J Med. 1991 Jun 6;324(23):1644–1650. doi: 10.1056/NEJM199106063242307. [DOI] [PubMed] [Google Scholar]
  3. Bazzoni F., Cassatella M. A., Rossi F., Ceska M., Dewald B., Baggiolini M. Phagocytosing neutrophils produce and release high amounts of the neutrophil-activating peptide 1/interleukin 8. J Exp Med. 1991 Mar 1;173(3):771–774. doi: 10.1084/jem.173.3.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brown A. E., Holzer T. J., Andersen B. R. Capacity of human neutrophils to kill Mycobacterium tuberculosis. J Infect Dis. 1987 Dec;156(6):985–989. doi: 10.1093/infdis/156.6.985. [DOI] [PubMed] [Google Scholar]
  5. Colditz I. G., Zwahlen R. D., Baggiolini M. Neutrophil accumulation and plasma leakage induced in vivo by neutrophil-activating peptide-1. J Leukoc Biol. 1990 Aug;48(2):129–137. doi: 10.1002/jlb.48.2.129. [DOI] [PubMed] [Google Scholar]
  6. Denis M. Human neutrophils, activated with cytokines or not, do not kill virulent Mycobacterium tuberculosis. J Infect Dis. 1991 Apr;163(4):919–920. doi: 10.1093/infdis/163.4.919. [DOI] [PubMed] [Google Scholar]
  7. Detmers P. A., Lo S. K., Olsen-Egbert E., Walz A., Baggiolini M., Cohn Z. A. Neutrophil-activating protein 1/interleukin 8 stimulates the binding activity of the leukocyte adhesion receptor CD11b/CD18 on human neutrophils. J Exp Med. 1990 Apr 1;171(4):1155–1162. doi: 10.1084/jem.171.4.1155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Detmers P. A., Powell D. E., Walz A., Clark-Lewis I., Baggiolini M., Cohn Z. A. Differential effects of neutrophil-activating peptide 1/IL-8 and its homologues on leukocyte adhesion and phagocytosis. J Immunol. 1991 Dec 15;147(12):4211–4217. [PubMed] [Google Scholar]
  9. Dewald B., Thelen M., Wymann M. P., Baggiolini M. Staurosporine inhibits the respiratory burst and induces exocytosis in human neutrophils. Biochem J. 1989 Dec 15;264(3):879–884. doi: 10.1042/bj2640879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Djeu J. Y., Matsushima K., Oppenheim J. J., Shiotsuki K., Blanchard D. K. Functional activation of human neutrophils by recombinant monocyte-derived neutrophil chemotactic factor/IL-8. J Immunol. 1990 Mar 15;144(6):2205–2210. [PubMed] [Google Scholar]
  11. 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]
  12. Ellis J. A., Mayer S. J., Jones O. T. The effect of the NADPH oxidase inhibitor diphenyleneiodonium on aerobic and anaerobic microbicidal activities of human neutrophils. Biochem J. 1988 May 1;251(3):887–891. doi: 10.1042/bj2510887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Geertsma M. F., Nibbering P. H., Pos O., Van Furth R. Interferon-gamma-activated human granulocytes kill ingested Mycobacterium fortuitum more efficiently than normal granulocytes. Eur J Immunol. 1990 Apr;20(4):869–873. doi: 10.1002/eji.1830200423. [DOI] [PubMed] [Google Scholar]
  14. Horsburgh C. R., Jr Mycobacterium avium complex infection in the acquired immunodeficiency syndrome. N Engl J Med. 1991 May 9;324(19):1332–1338. doi: 10.1056/NEJM199105093241906. [DOI] [PubMed] [Google Scholar]
  15. Hoy J. F., Rolston K. V., Hopfer R. L., Bodey G. P. Mycobacterium fortuitum bacteremia in patients with cancer and long-term venous catheters. Am J Med. 1987 Aug;83(2):213–217. doi: 10.1016/0002-9343(87)90687-5. [DOI] [PubMed] [Google Scholar]
  16. Jackett P. S., Aber V. R., Lowrie D. B. Virulence and resistance to superoxide, low pH and hydrogen peroxide among strains of Mycobacterium tuberculosis. J Gen Microbiol. 1978 Jan;104(1):37–45. doi: 10.1099/00221287-104-1-37. [DOI] [PubMed] [Google Scholar]
  17. Jackett P. S., Aber V. R., Lowrie D. B. Virulence of Mycobacterium tuberculosis and susceptibility to peroxidative killing systems. J Gen Microbiol. 1978 Aug;107(2):273–278. doi: 10.1099/00221287-107-2-273. [DOI] [PubMed] [Google Scholar]
  18. Jones G. S., Amirault H. J., Andersen B. R. Killing of Mycobacterium tuberculosis by neutrophils: a nonoxidative process. J Infect Dis. 1990 Sep;162(3):700–704. doi: 10.1093/infdis/162.3.700. [DOI] [PubMed] [Google Scholar]
  19. Larsen C. G., Anderson A. O., Appella E., Oppenheim J. J., Matsushima K. The neutrophil-activating protein (NAP-1) is also chemotactic for T lymphocytes. Science. 1989 Mar 17;243(4897):1464–1466. doi: 10.1126/science.2648569. [DOI] [PubMed] [Google Scholar]
  20. Larsen C. G., Anderson A. O., Oppenheim J. J., Matsushima K. Production of interleukin-8 by human dermal fibroblasts and keratinocytes in response to interleukin-1 or tumour necrosis factor. Immunology. 1989 Sep;68(1):31–36. [PMC free article] [PubMed] [Google Scholar]
  21. Lehrer R. I., Ganz T. Antimicrobial polypeptides of human neutrophils. Blood. 1990 Dec 1;76(11):2169–2181. [PubMed] [Google Scholar]
  22. Leijh P. C., van den Barselaar M. T., Daha M. R., van Furth R. Participation of immunoglobulins and complement components in the intracellular killing of Staphylococcus aureus and Escherichia coli by human granulocytes. Infect Immun. 1981 Sep;33(3):714–724. doi: 10.1128/iai.33.3.714-724.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Leijh P. C., van den Barselaar M. T., Dubbeldeman-Rempt I., van Furth R. Kinetics of intracellular killing of Staphylococcus aureus and Escherichia coli by human granulocytes. Eur J Immunol. 1980 Oct;10(10):750–757. doi: 10.1002/eji.1830101005. [DOI] [PubMed] [Google Scholar]
  24. Leijh P. C., van den Barselaar M. T., van Zwet T. L., Daha M. R., van Furth R. Requirement of extracellular complement and immunoglobulin for intracellular killing of micro-organisms by human monocytes. J Clin Invest. 1979 Apr;63(4):772–784. doi: 10.1172/JCI109362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Matsushima K., Morishita K., Yoshimura T., Lavu S., Kobayashi Y., Lew W., Appella E., Kung H. F., Leonard E. J., Oppenheim J. J. Molecular cloning of a human monocyte-derived neutrophil chemotactic factor (MDNCF) and the induction of MDNCF mRNA by interleukin 1 and tumor necrosis factor. J Exp Med. 1988 Jun 1;167(6):1883–1893. doi: 10.1084/jem.167.6.1883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Paccaud J. P., Schifferli J. A., Baggiolini M. NAP-1/IL-8 induces up-regulation of CR1 receptors in human neutrophil leukocytes. Biochem Biophys Res Commun. 1990 Jan 15;166(1):187–192. doi: 10.1016/0006-291x(90)91929-m. [DOI] [PubMed] [Google Scholar]
  27. Peveri P., Walz A., Dewald B., Baggiolini M. A novel neutrophil-activating factor produced by human mononuclear phagocytes. J Exp Med. 1988 May 1;167(5):1547–1559. doi: 10.1084/jem.167.5.1547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rampart M., Van Damme J., Zonnekeyn L., Herman A. G. Granulocyte chemotactic protein/interleukin-8 induces plasma leakage and neutrophil accumulation in rabbit skin. Am J Pathol. 1989 Jul;135(1):21–25. [PMC free article] [PubMed] [Google Scholar]
  29. Rook G. A., Steele J., Ainsworth M., Champion B. R. Activation of macrophages to inhibit proliferation of Mycobacterium tuberculosis: comparison of the effects of recombinant gamma-interferon on human monocytes and murine peritoneal macrophages. Immunology. 1986 Nov;59(3):333–338. [PMC free article] [PubMed] [Google Scholar]
  30. Ruch W., Cooper P. H., Baggiolini M. Assay of H2O2 production by macrophages and neutrophils with homovanillic acid and horse-radish peroxidase. J Immunol Methods. 1983 Oct 28;63(3):347–357. doi: 10.1016/s0022-1759(83)80008-8. [DOI] [PubMed] [Google Scholar]
  31. Smith W. B., Gamble J. R., Clark-Lewis I., Vadas M. A. Interleukin-8 induces neutrophil transendothelial migration. Immunology. 1991 Jan;72(1):65–72. [PMC free article] [PubMed] [Google Scholar]
  32. Strieter R. M., Kunkel S. L., Showell H. J., Remick D. G., Phan S. H., Ward P. A., Marks R. M. Endothelial cell gene expression of a neutrophil chemotactic factor by TNF-alpha, LPS, and IL-1 beta. Science. 1989 Mar 17;243(4897):1467–1469. doi: 10.1126/science.2648570. [DOI] [PubMed] [Google Scholar]
  33. Thelen M., Peveri P., Kernen P., von Tscharner V., Walz A., Baggiolini M. Mechanism of neutrophil activation by NAF, a novel monocyte-derived peptide agonist. FASEB J. 1988 Aug;2(11):2702–2706. [PubMed] [Google Scholar]
  34. Thornton A. J., Strieter R. M., Lindley I., Baggiolini M., Kunkel S. L. Cytokine-induced gene expression of a neutrophil chemotactic factor/IL-8 in human hepatocytes. J Immunol. 1990 Apr 1;144(7):2609–2613. [PubMed] [Google Scholar]
  35. Wayne L. G., Sramek H. A. Agents of newly recognized or infrequently encountered mycobacterial diseases. Clin Microbiol Rev. 1992 Jan;5(1):1–25. doi: 10.1128/cmr.5.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Westlin W. F., Kiely J. M., Gimbrone M. A., Jr Interleukin-8 induces changes in human neutrophil actin conformation and distribution: relationship to inhibition of adhesion to cytokine-activated endothelium. J Leukoc Biol. 1992 Jul;52(1):43–51. doi: 10.1002/jlb.52.1.43. [DOI] [PubMed] [Google Scholar]
  37. Woods G. L., Washington J. A., 2nd Mycobacteria other than Mycobacterium tuberculosis: review of microbiologic and clinical aspects. Rev Infect Dis. 1987 Mar-Apr;9(2):275–294. doi: 10.1093/clinids/9.2.275. [DOI] [PubMed] [Google Scholar]

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

RESOURCES