Home LiteratureArticle Details
PMID: 1673923 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Phase variation of the opacity outer membrane protein controls invasion by Neisseria gonorrhoeae into human epithelial cells.

The EMBO journal ·Vol. 10 ·No. 6 ·1991-06-00 ·Pages 1307-15

Makino S, van Putten JP, Meyer TF

Abstract

Neisseria gonorrhoeae is a facultative intracellular bacterium capable of penetrating into certain human epithelial cell types. In order to identify gonococcal factors essential for invading Chang human conjunctiva cells, a gentamicin selection assay for the quantification of viable intracellular bacteria was used in conjunction with microscopy. The results demonstrate a correlation between the invasive behaviour of gonococci and the expression of Opa proteins, a family of variable outer membrane proteins present in all pathogenic Neisseria species. However, only particular Opa proteins supported invasion into Chang cells as indicated by the use of two unrelated gonococcal strains. Invasion was sensitive to cytochalasin D, and strong adherence mediated by the Opa proteins appeared to be essential for the internalization of gonococci. In contrast pili, which also conferred binding to Chang conjunctiva cells, did not support cellular invasion but rather were inhibitory.

MeSH Terms
Bacterial Adhesion Bacterial Outer Membrane Proteins/chemistry,metabolism Blotting, Western Cells, Cultured Conjunctiva/cytology Epithelium/microbiology Fimbriae, Bacterial Fluorescent Antibody Technique Humans In Vitro Techniques Microscopy, Electron Molecular Weight Neisseria gonorrhoeae/immunology,pathogenicity
Chemicals
Bacterial Outer Membrane Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Makino S
Max-Planck-Institut für Biologie, Abteilung Infektionsbiologie, Tübingen, FRG.
van Putten J P
Meyer T F
References (55)
55 references, click to expand
  1. The use of immunogold-silver staining to study antigen variation and bacterial entry into eukaryotic cells by conventional light microscopy.
    J Med Microbiol. 1990 Sep;33(1):35-41 PMID: 2121989
  2. Biochemical purification and crystallographic characterization of the fiber-forming protein pilin from Neisseria gonorrhoeae.
    J Biol Chem. 1990 Feb 5;265(4):2278-85 PMID: 1967608
  3. Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells.
    Proc Natl Acad Sci U S A. 1989 Aug;86(16):6383-7 PMID: 2548211
  4. Pilin expression in Neisseria gonorrhoeae is under both positive and negative transcriptional control.
    EMBO J. 1988 Dec 20;7(13):4367-78 PMID: 2854063
  5. The repertoire of silent pilus genes in Neisseria gonorrhoeae: evidence for gene conversion.
    Cell. 1986 Jan 17;44(1):107-15 PMID: 2866848
  6. Piliation control mechanisms in Neisseria gonorrhoeae.
    Proc Natl Acad Sci U S A. 1986 Jun;83(11):3890-4 PMID: 2872674
  7. Interactions of gonococci with HeLa cells: attachment, detachment, replication, penetration, and the role of protein II.
    Infect Immun. 1986 Oct;54(1):154-60 PMID: 2875950
  8. Gonococcal cell wall lectin-adhesin with vaccine potential.
    Lancet. 1986 May 31;1(8492):1269-70 PMID: 2872407
  9. The effect of protein II and pili on the interaction of Neisseria gonorrhoeae with human polymorphonuclear leucocytes.
    J Gen Microbiol. 1986 Feb;132(2):503-12 PMID: 2872268
  10. Monoclonal antibodies to outer membrane protein PII block interactions of Neisseria gonorrhoeae with human neutrophils.
    Infect Immun. 1990 Apr;58(4):1078-84 PMID: 2108088
  11. Erythrocyte gangliosides act as receptors for Neisseria subflava: identification of the Sia-1 adhesin.
    Infect Immun. 1990 Aug;58(8):2555-63 PMID: 2370108
  12. Interactions of Neisseria gonorrhoeae with human neutrophils: effects of serum and gonococcal opacity on phagocyte killing and chemiluminescence.
    Infect Immun. 1982 May;36(2):737-44 PMID: 6806195
  13. Pilus expression in Neisseria gonorrhoeae involves chromosomal rearrangement.
    Cell. 1982 Aug;30(1):45-52 PMID: 6127165
  14. Rates in vitro changes of gonococcal colony opacity phenotypes.
    Infect Immun. 1982 Aug;37(2):481-5 PMID: 6126433
  15. Opacity determinants of Neisseria gonorrhoeae: gene expression and chromosomal linkage to the gonococcal pilus gene.
    Cell. 1984 Jun;37(2):447-56 PMID: 6144397
  16. Inhibition of Neisseria gonorrhoeae attachment to HeLa cells with monoclonal antibody directed against a protein II.
    Infect Immun. 1983 Dec;42(3):980-5 PMID: 6139341
  17. Mechanisms of mucosal invasion by pathogenic Neisseria.
    Rev Infect Dis. 1983 Sep-Oct;5 Suppl 4:S708-14 PMID: 6415784
  18. Comparative virulence of opacity variants of Neisseria gonorrhoeae strain P9.
    Infect Immun. 1981 Mar;31(3):965-70 PMID: 6785243
  19. Studies on gonococcus infection. XV. Identification of surface proteins of Neisseria gonorrhoeae correlated with leukocyte association.
    Infect Immun. 1978 Aug;21(2):575-84 PMID: 211086
  20. Variations in surface protein composition associated with virulence properties in opacity types of Neisseria gonorrhoeae.
    J Gen Microbiol. 1979 Oct;114(2):305-12 PMID: 120407
  21. Gonococcal interactions with polymorphonuclear neutrophils: importance of the phagosome for bactericidal activity.
    J Clin Invest. 1978 Dec;62(6):1161-71 PMID: 107196
  22. Surface components affecting interactions between Neisserai gonorrhoeae and eucaryotic cells.
    J Infect Dis. 1977 Aug;136 Suppl:S138-43 PMID: 408429
  23. Role of pili in the virulence of Neisseria gonorrhoeae.
    Infect Immun. 1973 Aug;8(2):255-63 PMID: 4200266
  24. Role of chromosomal rearrangement in N. gonorrhoeae pilus phase variation.
    Cell. 1985 Feb;40(2):293-300 PMID: 2857113
  25. Intragenic recombination leads to pilus antigenic variation in Neisseria gonorrhoeae.
    Nature. 1985 May 9-15;315(6015):156-8 PMID: 2859529
  26. A single genetic locus encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli K-12.
    Nature. 1985 Sep 19-25;317(6034):262-4 PMID: 2995819
  27. Model for invasion of human tissue culture cells by Neisseria gonorrhoeae.
    Infect Immun. 1988 Jun;56(6):1625-32 PMID: 3131248
  28. Gonococci possessing only certain P.II outer membrane proteins interact with human neutrophils.
    Infect Immun. 1988 Jun;56(6):1574-9 PMID: 3131247
  29. The interaction between Neisseria gonorrhoeae and the human cornea in organ culture. An electron microscopic study.
    Graefes Arch Clin Exp Ophthalmol. 1988;226(4):341-5 PMID: 3139497
  30. Expression of outer membrane protein II by gonococci in experimental gonorrhea.
    J Exp Med. 1988 Dec 1;168(6):2121-9 PMID: 3143800
  31. Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation.
    Cell. 1986 Oct 10;47(1):61-71 PMID: 3093085
  32. Reassortment of pilin genes in Neisseria gonorrhoeae occurs by two distinct mechanisms.
    Nature. 1989 Apr 20;338(6217):651-2 PMID: 2468090
  33. Pilus- gonococcal variants. Evidence for multiple forms of piliation control.
    J Exp Med. 1985 Aug 1;162(2):729-44 PMID: 2410533
  34. Expression of gonococcal protein II in Escherichia coli by translational fusion.
    Mol Microbiol. 1989 May;3(5):663-71 PMID: 2503682
  35. Interactions of Neisseria gonorrhoeae with human neutrophils.
    Clin Microbiol Rev. 1989 Apr;2 Suppl:S83-91 PMID: 2497966
  36. Phase variation of gonococcal protein II: regulation of gene expression by slipped-strand mispairing of a repetitive DNA sequence.
    Cell. 1989 Feb 24;56(4):539-47 PMID: 2492905
  37. Penetration of human intestinal epithelial cells by Salmonella: molecular cloning and expression of Salmonella typhi invasion determinants in Escherichia coli.
    Proc Natl Acad Sci U S A. 1989 Jul;86(13):5173-7 PMID: 2662196
  38. Genetic mechanisms and biological implications of phase variation in pathogenic neisseriae.
    Clin Microbiol Rev. 1989 Apr;2 Suppl:S139-45 PMID: 2655883
  39. Identification of carbohydrate structures that are possible receptors for Neisseria gonorrhoeae.
    Proc Natl Acad Sci U S A. 1988 Jul;85(13):4902-6 PMID: 2898784
  40. Proteins that appear to be associated with pili in Neisseria gonorrhoeae.
    Infect Immun. 1988 Jul;56(7):1743-7 PMID: 2898429
  41. Release of soluble pilin antigen coupled with gene conversion in Neisseria gonorrhoeae.
    Proc Natl Acad Sci U S A. 1987 Dec;84(24):9079-83 PMID: 2892194
  42. Effects of recA mutations on pilus antigenic variation and phase transitions in Neisseria gonorrhoeae.
    Genetics. 1987 Nov;117(3):391-8 PMID: 2891588
  43. A determinant of resistance of Neisseria gonorrhoeae to killing by human phagocytes: an outer membrane lipoprotein of about 20 kDa with a high content of glutamic acid.
    J Gen Microbiol. 1986 Dec;132(12):3277-87 PMID: 2888833
  44. Pilus genes of Neisseria gonorrheae: chromosomal organization and DNA sequence.
    Proc Natl Acad Sci U S A. 1984 Oct;81(19):6110-4 PMID: 6148752
  45. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells.
    Cell. 1987 Aug 28;50(5):769-78 PMID: 3304658
  46. Resistance of Neisseria gonorrhoeae to phagocytosis: relationship to colonial morphology and surface pili.
    J Infect Dis. 1974 Mar;129(3):310-6 PMID: 4205880
  47. 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):373-9 PMID: 4197389
  48. Genetic transformation of Neisseria gonorrhoeae to streptomycin resistance.
    J Bacteriol. 1966 Nov;92(5):1364-71 PMID: 4958881
  49. Differential ability of colonial types of Neisseria gonorrhoeae to produce infection cutaneous perforated plastic chambers in guinea-pigs and rabbits.
    J Med Microbiol. 1975 May;8(2):325-35 PMID: 806688
  50. A genetic determinant required for continuous reinfection of adjacent cells on large plasmid in S. flexneri 2a.
    Cell. 1986 Aug 15;46(4):551-5 PMID: 3524856
  51. Multiplication of Shigella flexneri within HeLa cells: lysis of the phagocytic vacuole and plasmid-mediated contact hemolysis.
    Infect Immun. 1986 Feb;51(2):461-9 PMID: 3510976
  52. Stimulation of human leukocytes by protein II+ gonococci is mediated by lectin-like gonococcal components.
    Infect Immun. 1985 Oct;50(1):116-22 PMID: 3930402
  53. Identification and characterization of a Neisseria gonorrhoeae gene encoding a glycolipid-binding adhesin.
    Proc Natl Acad Sci U S A. 1990 Jan;87(1):333-7 PMID: 2153292
  54. Identification of the integrin binding domain of the Yersinia pseudotuberculosis invasin protein.
    EMBO J. 1990 Jun;9(6):1979-89 PMID: 1693333
  55. Variation and control of protein expression in Neisseria.
    Annu Rev Microbiol. 1990;44:451-77 PMID: 2252390
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1991-06-00
Pages
1307-15
Language
English
Region
England
NLM ID
8208664
PMCID
PMC452788
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com