Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1977 Mar;15(3):817–827. doi: 10.1128/iai.15.3.817-827.1977

Ethylenediaminetetraacetic acid-sensitive antiphagocytic activity of Neisseria gonorrhoeae.

R S Rosenthal, R S Fulbright, M E Eads, W D Sawyer
PMCID: PMC421446  PMID: 404246

Abstract

Colonial types of Neisseria gonorrhoeae were examined for the presence of pilus-independent antiphagocytic activity. Type 3 and depiliated type 1 gonococci had a shearing- and protease-resistant antiphagocytic activity that was eliminated by treatment with ethylenediaminetetraacetic acid (EDTA) and that was not present on type 4 bacteria. Incubation of EDTA-treated bacteria 37 degrees C for 90 min resulted in fas prevented by antibiotics that block the final assembly of cell wall macromolecules that depend on the C55-isoprenoid carrier for export. These include both lipopolysaccharide and peptidoglycan. Restoration was, however, unaffected by drugs that interfere with the synthesis of peptidoglycan, but not that of lipopolysaccharide, and by inhibitors of protein synthesis. These data suggested that gonococci have an antiphagocytic mechanism in addition to the previously described determinant (presumably pili) that was removed by blending or by treatment with proteases. Of the two antiphagocytic activities, type 1 had both, type 3 had only the EDTA-sensitive component, and type 4 had neither.

Full text

PDF
817

Selected References

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

  1. Anderson J. S., Matsuhashi M., Haskin M. A., Strominger J. L. Biosythesis of the peptidoglycan of bacterial cell walls. II. Phospholipid carriers in the reaction sequence. J Biol Chem. 1967 Jul 10;242(13):3180–3190. [PubMed] [Google Scholar]
  2. BRINTON C. C., Jr, BUZZELL A., LAUFFER M. A. Electrophoresis and phage susceptibility studies on a filament-producing variant of the E. coli B bacterium. Biochim Biophys Acta. 1954 Dec;15(4):533–542. doi: 10.1016/0006-3002(54)90011-6. [DOI] [PubMed] [Google Scholar]
  3. Carpenter R. R. Phagocytosis by guinea pig splenic cells of Escherichia coli and protein-coated bentonite particles labeled with iodine-125. J Immunol. 1966 Jun;96(6):992–999. [PubMed] [Google Scholar]
  4. 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]
  5. Elmros T., Burman L. G., Bloom G. D. Autolysis of Neisseria gonorrhoeae. J Bacteriol. 1976 May;126(2):969–976. doi: 10.1128/jb.126.2.969-976.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. FOLEY M. J., SMITH M. R., WOOD W. B., Jr Studies on the pathogenicity of group A Streptococci. I. Its relation to surface phagocytosis. J Exp Med. 1959 Oct 1;110:603–616. doi: 10.1084/jem.110.4.603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gibbs D. L., Roberts R. B. The interaction in vitro between human polymorphonuclear leukocytes and Neisseria gonorrhoeae cultivated in the chick embryo. J Exp Med. 1975 Jan 1;141(1):155–171. doi: 10.1084/jem.141.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. James-Holmquest A. N., Swanson J., Buchanan T. M., Wende R. D., Williams R. P. Differential attachment by piliated and nonpiliated Neisseria gonorrhoeae to human sperm. Infect Immun. 1974 May;9(5):897–902. doi: 10.1128/iai.9.5.897-902.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. James A. N., Knox J. M., Williams R. P. Attachment of gonococci to sperm. Influence of physical and chemical factors. Br J Vener Dis. 1976 Apr;52(2):128–135. doi: 10.1136/sti.52.2.128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. KELLOGG D. S., Jr, PEACOCK W. L., Jr, DEACON W. E., BROWN L., PIRKLE D. I. NEISSERIA GONORRHOEAE. I. VIRULENCE GENETICALLY LINKED TO CLONAL VARIATION. J Bacteriol. 1963 Jun;85:1274–1279. doi: 10.1128/jb.85.6.1274-1279.1963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  12. La Scolea L. J., Jr, Young F. E. Development of a defined minimal medium for the growth of Neisseria gonorrhoeae. Appl Microbiol. 1974 Jul;28(1):70–76. doi: 10.1128/am.28.1.70-76.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Leive L. Release of lipopolysaccharide by EDTA treatment of E. coli. Biochem Biophys Res Commun. 1965 Nov 22;21(4):290–296. doi: 10.1016/0006-291x(65)90191-9. [DOI] [PubMed] [Google Scholar]
  14. McCutchan J. A., Levine S., Braude A. I. Influence of colony type on susceptibility of gonococci to killing by human serum. J Immunol. 1976 Jun;116(6):1652–1655. [PubMed] [Google Scholar]
  15. McGee Z. A., Gross J., Dourmashkin R. R., Taylor-Robinson D. Nonpilar surface appendages of colony type 1 and colony type 4 gonococci. Infect Immun. 1976 Jul;14(1):266–270. doi: 10.1128/iai.14.1.266-270.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Medearis D. N., Jr, Camitta B. M., Heath E. C. Cell wall composition and virulence in Escherichia coli. J Exp Med. 1968 Sep 1;128(3):399–414. doi: 10.1084/jem.128.3.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. OREN R., FARNHAM A. E., SAITO K., MILOFSKY E., KARNOVSKY M. L. Metabolic patterns in three types of phagocytizing cells. J Cell Biol. 1963 Jun;17:487–501. doi: 10.1083/jcb.17.3.487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. OSBORN M. J. STUDIES ON THE GRAM-NEGATIVE CELL WALL. I. EVIDENCE FOR THE ROLE OF 2-KETO- 3-DEOXYOCTONATE IN THE LIPOPOLYSACCHARIDE OF SALMONELLA TYPHIMURIUM. Proc Natl Acad Sci U S A. 1963 Sep;50:499–506. doi: 10.1073/pnas.50.3.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Payne S. M., Finkelstein R. A. Pathogenesis and immunology of experimental gonococcal infection: role of iron in virulence. Infect Immun. 1975 Dec;12(6):1313–1318. doi: 10.1128/iai.12.6.1313-1318.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Perry M. B., Daoust V. The lipopolysaccharides of Neisseria gonorrhoeae colony types 1 and 4. Can J Biochem. 1975 May;53(5):623–629. doi: 10.1139/o75-084. [DOI] [PubMed] [Google Scholar]
  23. Plaut A. G., Gilbert J. V., Artenstein M. S., Capra J. D. Neisseria gonorrhoeae and neisseria meningitidis: extracellular enzyme cleaves human immunoglobulin A. Science. 1975 Dec 12;190(4219):1103–1105. doi: 10.1126/science.810892. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Rogers S. W., Gilleland H. E., Jr, Eagon R. G. Characterization of a protein-lipopolysaccharide complex released from cell walls of Pseudomonas aeruginosa by ethylenediaminetetraacetic acid. Can J Microbiol. 1969 Jul;15(7):743–748. doi: 10.1139/m69-130. [DOI] [PubMed] [Google Scholar]
  26. Rothfield L., Romeo D. Role of lipids in the biosynthesis of the bacterial cell envelope. Bacteriol Rev. 1971 Mar;35(1):14–38. doi: 10.1128/br.35.1.14-38.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. SMITH M. R., FLEMING D. O., WOOD W. B., Jr THE EFFECT OF ACUTE RADIATION INJURY ON PHAGOCYTIC MECHANISMS OF ANTIBACTERIAL DEFENSE. J Immunol. 1963 Jun;90:914–924. [PubMed] [Google Scholar]
  28. Sawyer W. D. Interaction of influenza virus with leukocytes and its effect on phagocytosis. J Infect Dis. 1969 Jun;119(6):541–556. doi: 10.1093/infdis/119.6.541. [DOI] [PubMed] [Google Scholar]
  29. Smith M. R., Wood W. B., Jr Heat labile opsonins to pneumococcus. I. Participation of complement. J Exp Med. 1969 Dec 1;130(6):1209–1227. doi: 10.1084/jem.130.6.1209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Stead A., Main J. S., Ward M. E., Watt P. J. Studies on lipopolysaccharides isolated from strains of Neisseria gonorrhoeae. J Gen Microbiol. 1975 May;88(1):123–131. doi: 10.1099/00221287-88-1-123. [DOI] [PubMed] [Google Scholar]
  31. Stendahl O., Edebo L. Phagocytosis of mutants of Salmonella typhimurium by rabbit polymorphonuclear cells. Acta Pathol Microbiol Scand B Microbiol Immunol. 1972;80(4):481–488. doi: 10.1111/j.1699-0463.1972.tb00169.x. [DOI] [PubMed] [Google Scholar]
  32. Swanson J., King G., Zeligs B. Studies on gonococcus infection. VII. In vitro killing of gonococci by human leukocytes. Infect Immun. 1975 Jan;11(1):65–68. doi: 10.1128/iai.11.1.65-68.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Swanson J., Sparks E., Young D., King G. Studies on Gonococcus infection. X. Pili and leukocyte association factor as mediators of interactions between gonococci and eukaryotic cells in vitro. Infect Immun. 1975 Jun;11(6):1352–1361. doi: 10.1128/iai.11.6.1352-1361.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Swanson J. Studies on gonococcus infection. IV. Pili: their role in attachment of gonococci to tissue culture cells. J Exp Med. 1973 Mar 1;137(3):571–589. doi: 10.1084/jem.137.3.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Thomas D. W., Hill J. C., Tyeryar F. J., Jr Interaction of gonococci with phagocytic leukocytes from men and mice. Infect Immun. 1973 Jul;8(1):98–104. doi: 10.1128/iai.8.1.98-104.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Tucker A. N., White D. C. Release of membrane components from viable Haemophilus parainfluenzae by ethylenediaminetetraacetic acid-tris(hydroxymethyl)-aminomethane. J Bacteriol. 1970 May;102(2):498–507. doi: 10.1128/jb.102.2.498-507.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Walker T. S., Haak R. A., Wegener W. S. Plasmid DNA in virulent and avirulent gonococci. Can J Microbiol. 1975 Nov;21(11):1705–1710. doi: 10.1139/m75-250. [DOI] [PubMed] [Google Scholar]
  40. Ward M. E., Watt P. J., Glynn A. A. Gonococci in urethral exudates possess a virulence factor lost on subculture. Nature. 1970 Jul 25;227(5256):382–384. doi: 10.1038/227382a0. [DOI] [PubMed] [Google Scholar]
  41. Ward M. E., Watt P. J., Robertson J. N. The human fallopian tube: a laboratory model for gonococcal infection. J Infect Dis. 1974 Jun;129(6):650–659. doi: 10.1093/infdis/129.6.650. [DOI] [PubMed] [Google Scholar]
  42. Watt P. J. The fate of gonococci in polymorphonuclear leucocytes. J Med Microbiol. 1970 Aug;3(3):501–509. doi: 10.1099/00222615-3-3-501. [DOI] [PubMed] [Google Scholar]
  43. Witt K., Veale D. R., Smith H. Resistance of Neisseria gonorrhoeae to ingestion and digestion by phagocytes of human buffy coat. J Med Microbiol. 1976 Feb;9(1):1–12. doi: 10.1099/00222615-9-1-1. [DOI] [PubMed] [Google Scholar]
  44. Wood W. B., Jr, Smith M. R. Intercellular Surface Phagocytosis. Science. 1947 Jul 25;106(2743):86–87. doi: 10.1126/science.106.2743.86. [DOI] [PubMed] [Google Scholar]

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

RESOURCES