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. 1991 Nov;59(11):4168–4172. doi: 10.1128/iai.59.11.4168-4172.1991

Extracellular release of reactive oxygen species from human neutrophils upon interaction with Escherichia coli strains causing renal scarring.

H Mundi 1, B Björkstén 1, C Svanborg 1, L Ohman 1, C Dahlgren 1
PMCID: PMC259012  PMID: 1937773

Abstract

The production of reactive oxygen metabolites by neutrophils plays a key role in the host defense against invading microorganisms and in tissue damage resulting from infection. In the present study we measured the ability of different uropathogenic Escherichia coli strains to induce generation of oxygen metabolites upon interaction with human neutrophils. The strains were selected to represent two groups of patients with recurrent episodes of acute pyelonephritis: one with renal scars (12 strains) and one without renal scarring (11 strains). The majority of strains (from both groups) induced a pronounced neutrophil respiratory burst activity. When the intracellular and extracellular oxidative responses were measured separately, it was found that the response induced by nonscarring strains was primarily of intracellular (intraphagosomal) origin, whereas a proportionally larger fraction of the response induced by the scarring strains was extracellular. Since reactive oxygen products are toxic to the renal tissue, this release can be of importance in the development of renal scars.

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Selected References

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  1. Bar-Shavit Z., Ofek I., Goldman R., Mirelman D., Sharon N. Mannose residues on phagocytes as receptors for the attachment of Escherichia coli and Salmonella typhi. Biochem Biophys Res Commun. 1977 Sep 9;78(1):455–460. doi: 10.1016/0006-291x(77)91276-1. [DOI] [PubMed] [Google Scholar]
  2. Bellavite P. The superoxide-forming enzymatic system of phagocytes. Free Radic Biol Med. 1988;4(4):225–261. doi: 10.1016/0891-5849(88)90044-5. [DOI] [PubMed] [Google Scholar]
  3. Bender J. G., Van Epps D. E. Analysis of the bimodal chemiluminescence pattern stimulated in human neutrophils by chemotactic factors. Infect Immun. 1983 Sep;41(3):1062–1070. doi: 10.1128/iai.41.3.1062-1070.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bjerrum O. W., Borregaard N. Dual granule localization of the dormant NADPH oxidase and cytochrome b559 in human neutrophils. Eur J Haematol. 1989 Jul;43(1):67–77. doi: 10.1111/j.1600-0609.1989.tb01254.x. [DOI] [PubMed] [Google Scholar]
  5. Briheim G., Stendahl O., Dahlgren C. Intra- and extracellular events in luminol-dependent chemiluminescence of polymorphonuclear leukocytes. Infect Immun. 1984 Jul;45(1):1–5. doi: 10.1128/iai.45.1.1-5.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Böyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Invest Suppl. 1968;97:77–89. [PubMed] [Google Scholar]
  7. Clark R. A. The human neutrophil respiratory burst oxidase. J Infect Dis. 1990 Jun;161(6):1140–1147. doi: 10.1093/infdis/161.6.1140. [DOI] [PubMed] [Google Scholar]
  8. Dahlgren C. Analysis of luminol-dependent chemiluminescence from granule depleted neutrophil cytoplasts reveals two different light-emitting mechanisms. J Biolumin Chemilumin. 1988 Jan-Mar;2(1):25–33. doi: 10.1002/bio.1170020106. [DOI] [PubMed] [Google Scholar]
  9. Dahlgren C. Difference in extracellular radical release after chemotactic factor and calcium ionophore activation of the oxygen radical-generating system in human neutrophils. Biochim Biophys Acta. 1987 Aug 19;930(1):33–38. doi: 10.1016/0167-4889(87)90152-2. [DOI] [PubMed] [Google Scholar]
  10. Dahlgren C. Effects on extra- and intracellularly localized, chemoattractant-induced, oxygen radical production in neutrophils following modulation of conditions for ligand-receptor interaction. Inflammation. 1988 Aug;12(4):335–349. doi: 10.1007/BF00915769. [DOI] [PubMed] [Google Scholar]
  11. Dahlgren C., Stendahl O. Role of myeloperoxidase in luminol-dependent chemiluminescence of polymorphonuclear leukocytes. Infect Immun. 1983 Feb;39(2):736–741. doi: 10.1128/iai.39.2.736-741.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. DeChatelet L. R., Long G. D., Shirley P. S., Bass D. A., Thomas M. J., Henderson F. W., Cohen M. S. Mechanism of the luminol-dependent chemiluminescence of human neutrophils. J Immunol. 1982 Oct;129(4):1589–1593. [PubMed] [Google Scholar]
  13. Edwards S. W. Luminol- and lucigenin-dependent chemiluminescence of neutrophils: role of degranulation. J Clin Lab Immunol. 1987 Jan;22(1):35–39. [PubMed] [Google Scholar]
  14. Glauser M. P., Lyons J. M., Braude A. I. Prevention of chronic experimental pyelonephritis by suppression of acute suppuration. J Clin Invest. 1978 Feb;61(2):403–407. doi: 10.1172/JCI108951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hallett M. B., Campbell A. K. Two distinct mechanisms for stimulation of oxygen-radical production by polymorphonuclear leucocytes. Biochem J. 1983 Nov 15;216(2):459–465. doi: 10.1042/bj2160459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hodson C. J., Wilson S. Natural History of Chronic Pyelonephritic Scarring. Br Med J. 1965 Jul 24;2(5455):191–194. doi: 10.1136/bmj.2.5455.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hurst N. P. Molecular basis of activation and regulation of the phagocyte respiratory burst. Ann Rheum Dis. 1987 Apr;46(4):265–272. doi: 10.1136/ard.46.4.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jesaitis A. J., Buescher E. S., Harrison D., Quinn M. T., Parkos C. A., Livesey S., Linner J. Ultrastructural localization of cytochrome b in the membranes of resting and phagocytosing human granulocytes. J Clin Invest. 1990 Mar;85(3):821–835. doi: 10.1172/JCI114509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jodal U., Lindberg U., Lincoln K. Level diagnosis of symptomatic urinary tract infections in childhood. Acta Paediatr Scand. 1975 Mar;64(2):201–208. doi: 10.1111/j.1651-2227.1975.tb03822.x. [DOI] [PubMed] [Google Scholar]
  20. Linder H., Engberg I., van Kooten C., de Man P., Svanborg-Edén C. Effects of anti-inflammatory agents on mucosal inflammation induced by infection with gram-negative bacteria. Infect Immun. 1990 Jul;58(7):2056–2060. doi: 10.1128/iai.58.7.2056-2060.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lock R., Dahlgren C. Characteristics of the granulocyte chemiluminescence reaction following an interaction between human neutrophils and Salmonella typhimurium bacteria. APMIS. 1988 Apr;96(4):299–305. [PubMed] [Google Scholar]
  22. Lock R., Dahlgren C., Lindén M., Stendahl O., Svensbergh A., Ohman L. Neutrophil killing of two type 1 fimbria-bearing Escherichia coli strains: dependence on respiratory burst activation. Infect Immun. 1990 Jan;58(1):37–42. doi: 10.1128/iai.58.1.37-42.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lock R., Johansson A., Orselius K., Dahlgren C. Analysis of horseradish peroxidase-amplified chemiluminescence produced by human neutrophils reveals a role for the superoxide anion in the light emitting reaction. Anal Biochem. 1988 Sep;173(2):450–455. doi: 10.1016/0003-2697(88)90213-8. [DOI] [PubMed] [Google Scholar]
  24. Lomberg H., Hellström M., Jodal U., Orskov I., Svanborg Edén C. Properties of Escherichia coli in patients with renal scarring. J Infect Dis. 1989 Mar;159(3):579–582. doi: 10.1093/infdis/159.3.579. [DOI] [PubMed] [Google Scholar]
  25. Marre R., Hacker J., Henkel W., Goebel W. Contribution of cloned virulence factors from uropathogenic Escherichia coli strains to nephropathogenicity in an experimental rat pyelonephritis model. Infect Immun. 1986 Dec;54(3):761–767. doi: 10.1128/iai.54.3.761-767.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ransley P. G., Risdon R. A. Reflux nephropathy: effects of antimicrobial therapy on the evolution of the early pyelonephritic scar. Kidney Int. 1981 Dec;20(6):733–742. doi: 10.1038/ki.1981.204. [DOI] [PubMed] [Google Scholar]
  27. Roberts J. A., Roth J. K., Jr, Domingue G., Lewis R. W., Kaack B., Baskin G. Immunology of pyelonephritis in the primate model. V. Effect of superoxide dismutase. J Urol. 1982 Dec;128(6):1394–1400. doi: 10.1016/s0022-5347(17)53516-8. [DOI] [PubMed] [Google Scholar]
  28. Segal A. W. The molecular and cellular pathology of chronic granulomatous disease. Eur J Clin Invest. 1988 Oct;18(5):433–443. doi: 10.1111/j.1365-2362.1988.tb01037.x. [DOI] [PubMed] [Google Scholar]
  29. Stevens P., Winston D. J., Van Dyke K. In vitro evaluation of opsonic and cellular granulocyte function by luminol-dependent chemiluminescence: utility in patients with severe neutropenia and cellular deficiency states. Infect Immun. 1978 Oct;22(1):41–51. doi: 10.1128/iai.22.1.41-51.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Svanborg Edén C., Bjursten L. M., Hull R., Hull S., Magnusson K. E., Moldovano Z., Leffler H. Influence of adhesins on the interaction of Escherichia coli with human phagocytes. Infect Immun. 1984 Jun;44(3):672–680. doi: 10.1128/iai.44.3.672-680.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Svanborg-Edén C., Hagberg L., Hull R., Hull S., Magnusson K. E., Ohman L. Bacterial virulence versus host resistance in the urinary tracts of mice. Infect Immun. 1987 May;55(5):1224–1232. doi: 10.1128/iai.55.5.1224-1232.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Topley N., Steadman R., Mackenzie R., Knowlden J. M., Williams J. D. Type 1 fimbriate strains of Escherichia coli initiate renal parenchymal scarring. Kidney Int. 1989 Oct;36(4):609–616. doi: 10.1038/ki.1989.237. [DOI] [PubMed] [Google Scholar]
  33. Weiss J., Kao L., Victor M., Elsbach P. Oxygen-independent intracellular and oxygen-dependent extracellular killing of Escherichia coli S15 by human polymorphonuclear leukocytes. J Clin Invest. 1985 Jul;76(1):206–212. doi: 10.1172/JCI111947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Winberg J., Bollgren I., Källenius G., Möllby R., Svenson S. B. Clinical pyelonephritis and focal renal scarring. A selected review of pathogenesis, prevention, and prognosis. Pediatr Clin North Am. 1982 Aug;29(4):801–814. doi: 10.1016/s0031-3955(16)34213-4. [DOI] [PubMed] [Google Scholar]
  35. de Man P., Cläeson I., Johanson I. M., Jodal U., Svanborg Edén C. Bacterial attachment as a predictor of renal abnormalities in boys with urinary tract infection. J Pediatr. 1989 Dec;115(6):915–922. doi: 10.1016/s0022-3476(89)80742-5. [DOI] [PubMed] [Google Scholar]

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