Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1986 May;52(2):384–389. doi: 10.1128/iai.52.2.384-389.1986

Neisseria gonorrhoeae survive intraleukocytic oxygen-independent antimicrobial capacities of anaerobic and aerobic granulocytes in the presence of pyocin lethal for extracellular gonococci.

S G Casey, W M Shafer, J K Spitznagel
PMCID: PMC261010  PMID: 2870986

Abstract

The resistance of a piliated, transparent variant of Neisseria gonorrhoeae FA19 to intraleukocytic killing by human polymorphonuclear neutrophils (PMN) was examined. In both aerobic and anaerobic PMN monolayers, approximately 2% of the intracellular gonococci survived for as long as 165 min. Anaerobic PMN were as effective as aerobic PMN in the intracellular killing of gonococci. Hence, O2-independent antimicrobial systems of PMN performed a significant role in the intraleukocytic killing of gonococci were intracellular was supported by the elimination of extracellular bacteria by the addition of pyocin 103 and confirmed by the fluorescent antibody staining of intact gonococci after the PMN were permeabilized to antibody with a Formalin-acetone treatment of PMN monolayers. Our data indicate that while the majority of ingested gonococci are killed by O2-independent antimicrobial systems, a small number (about 2%), survive even when care is taken to eliminate extracellular bacteria.

Full text

PDF
384

Selected References

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

  1. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  2. Casey S. G., Shafer W. M., Spitznagel J. K. Anaerobiosis increases resistance of Neisseria gonorrhoeae to O2-independent antimicrobial proteins from human polymorphonuclear granulocytes. Infect Immun. 1985 Feb;47(2):401–407. doi: 10.1128/iai.47.2.401-407.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Casey S. G., Veale D. R., Smith H. Demonstration of intracellular growth of gonococci in human phagocytes using spectinomycin to kill extracellular organisms. J Gen Microbiol. 1979 Aug;113(2):395–398. doi: 10.1099/00221287-113-2-395. [DOI] [PubMed] [Google Scholar]
  4. Daly J. A., Lee T. J., Spitznagel J. K., Sparling P. F. Gonococci with mutations to low-level penicillin resistance exhibit increased sensitivity to the oxygen-independent bactericidal activity of human polymorphonuclear leukocyte granule extracts. Infect Immun. 1982 Mar;35(3):826–833. doi: 10.1128/iai.35.3.826-833.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Densen P., Mandell G. L. Gonococcal interactions with polymorphonuclear neutrophils: importance of the phagosome for bactericidal activity. J Clin Invest. 1978 Dec;62(6):1161–1171. doi: 10.1172/JCI109235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dilworth J. A., Hendley J. O., Mandell G. L. Attachment and ingestion of gonococci human neutrophils. Infect Immun. 1975 Mar;11(3):512–516. doi: 10.1128/iai.11.3.512-516.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Evans B. A. Ultrastructural study of cervical gonorrhea. J Infect Dis. 1977 Aug;136(2):248–255. doi: 10.1093/infdis/136.2.248. [DOI] [PubMed] [Google Scholar]
  8. Fontaine E. A., Taylor-Robinson D., Hanna N. F., Coufalik E. D. Anaerobes in men with urethritis. Br J Vener Dis. 1982 Oct;58(5):321–326. doi: 10.1136/sti.58.5.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Guymon L. F., Esser M., Shafer W. M. Pyocin-resistant lipopolysaccharide mutans of Neisseria gonorrhoeae: alterations in sensitivity to normal human serum and polymyxin B. Infect Immun. 1982 May;36(2):541–547. doi: 10.1128/iai.36.2.541-547.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kellogg D. S., Jr, Cohen I. R., Norins L. C., Schroeter A. L., Reising G. Neisseria gonorrhoeae. II. Colonial variation and pathogenicity during 35 months in vitro. J Bacteriol. 1968 Sep;96(3):596–605. doi: 10.1128/jb.96.3.596-605.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Morse S. A., Vaughan P., Johnson D., Iglewski B. H. Inhibition of Neisseria gonorrhoeae by a bacteriocin from Pseudomonas aeruginosa. Antimicrob Agents Chemother. 1976 Aug;10(2):354–362. doi: 10.1128/aac.10.2.354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Novotny P., Short J. A., Walker P. D. An electron-microscope study of naturally occurring and cultured cells of Neisseria Gonorrhoeae. J Med Microbiol. 1975 Aug;8(3):413–427. doi: 10.1099/00222615-8-3-413. [DOI] [PubMed] [Google Scholar]
  13. Ofek I., Beachey E. H., Bisno A. L. Resistance of Neisseria gonorrhoeae to phagocytosis: relationship to colonial morphology and surface pili. J Infect Dis. 1974 Mar;129(3):310–316. doi: 10.1093/infdis/129.3.310. [DOI] [PubMed] [Google Scholar]
  14. Okamura N., Spitznagel J. K. Outer membrane mutants of Salmonella typhimurium LT2 have lipopolysaccharide-dependent resistance to the bactericidal activity of anaerobic human neutrophils. Infect Immun. 1982 Jun;36(3):1086–1095. doi: 10.1128/iai.36.3.1086-1095.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ovcinnikov N. M., Delektorskij V. V., Dmitriev G. A. Ultrastructure of gonococci in acute, chronic, and asymptomatic gonorrhoea. Br J Vener Dis. 1976 Aug;52(4):230–245. doi: 10.1136/sti.52.4.230. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Pryzwansky K. B., MacRae E. K., Spitznagel J. K., Cooney M. H. Early degranulation of human neutrophils: immunocytochemical studies of surface and intracellular phagocytic events. Cell. 1979 Dec;18(4):1025–1033. doi: 10.1016/0092-8674(79)90215-0. [DOI] [PubMed] [Google Scholar]
  17. Pryzwansky K. B., Martin L. E., Spitznagel J. K. Immunocytochemical localization of myeloperoxidase, lactoferrin, lysozyme and neutral proteases in human monocytes and neutrophilic granulocytes. J Reticuloendothel Soc. 1978 Sep;24(3):295–310. [PubMed] [Google Scholar]
  18. Punsalang A. P., Jr, Sawyer W. D. Role of pili in the virulence of Neisseria gonorrhoeae. Infect Immun. 1973 Aug;8(2):255–263. doi: 10.1128/iai.8.2.255-263.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rest R. F., Fischer S. H., Ingham Z. Z., Jones J. F. Interactions of Neisseria gonorrhoeae with human neutrophils: effects of serum and gonococcal opacity on phagocyte killing and chemiluminescence. Infect Immun. 1982 May;36(2):737–744. doi: 10.1128/iai.36.2.737-744.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rest R. F. Killing of Neisseria gonorrhoeae by human polymorphonuclear neutrophil granule extracts. Infect Immun. 1979 Aug;25(2):574–579. doi: 10.1128/iai.25.2.574-579.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Segal A. W., Cross A. R., Garcia R. C., Borregaard N., Valerius N. H., Soothill J. F., Jones O. T. Absence of cytochrome b-245 in chronic granulomatous disease. A multicenter European evaluation of its incidence and relevance. N Engl J Med. 1983 Feb 3;308(5):245–251. doi: 10.1056/NEJM198302033080503. [DOI] [PubMed] [Google Scholar]
  22. Spitznagel J. K. Nonoxidative antimicrobial reactions of leukocytes. Contemp Top Immunobiol. 1984;14:283–343. doi: 10.1007/978-1-4757-4862-8_10. [DOI] [PubMed] [Google Scholar]
  23. Swanson J., Sparks E., Zeligs B., Siam M. A., Parrott C. Studies on gonococcus infection. V. Observations on in vitro interactions of gonococci and human neutrophils. Infect Immun. 1974 Sep;10(3):633–644. doi: 10.1128/iai.10.3.633-644.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Thongthai C., Sawyer W. D. Studies on the virulence of Neisseria gonorrhoeae. I. Relation of colonial morphology and resistance to phagocytosis by polymorphonuclear leukocytes. Infect Immun. 1973 Mar;7(3):373–379. doi: 10.1128/iai.7.3.373-379.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Veale D. R., Finch H., Smith H. Penetration of penicillin into human phagocytes containing Neisseria gonorrhoeae: intracellular survival and growth at optimum concentrations of antibiotic. J Gen Microbiol. 1976 Aug;96(2):353–363. doi: 10.1099/00221287-95-2-353. [DOI] [PubMed] [Google Scholar]
  26. Veale D. R., Goldner M., Penn C. W., Ward J., Smith H. The intracellular survival and growth of gonococci in human phagocytes. J Gen Microbiol. 1979 Aug;113(2):383–393. doi: 10.1099/00221287-113-2-383. [DOI] [PubMed] [Google Scholar]

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

RESOURCES