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PMID: 8440254 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Variable opacity (Opa) outer membrane proteins account for the cell tropisms displayed by Neisseria gonorrhoeae for human leukocytes and epithelial cells.

The EMBO journal ·Vol. 12 ·No. 2 ·1993-02-00 ·Pages 641-50

Kupsch EM, Knepper B, Kuroki T, Heuer I, Meyer TF

Abstract

Opacity proteins (Opa) of Neisseria gonorrhoeae, a family of variant outer membrane proteins implicated in pathogenesis, are subject to phase variation. In strain MS11, 11 different opa gene alleles have been identified, the expression of which can be turned on and off independently. Using a reverse genetic approach, we demonstrate that a single Opa protein variant of strain MS11, Opa50, enables gonococci to invade epithelial cells. The remaining variant Opa proteins show no, or very little, specificity for epithelial cells but instead confer interaction with human polymorphonuclear neutrophils (PMNs). Thus, depending on the opa allele expressed, gonococci are capable of invading epithelial cells or of interacting with human leukocytes. The respective properties of Opa proteins are maintained independent of the gonococcal strain; thus, the specificity for epithelial cells or leukocytes is intrinsic to Opa proteins. Significant homology exists in the surface exposed variable regions of two invasion supporting Opa proteins from independent strains. Efficient epithelial cell invasion is favoured by high level Opa production, however, a 10-fold reduction still allows significant invasion by gonococci. In contrast, recombinant Escherichia coli expressing Opa proteins adhered or invaded poorly under similar experimental conditions, thus indicating that additional factors besides Opa are required in the Opa-mediated interaction with human cells.

Related Genes
opa
MeSH Terms
Amino Acid Sequence Antigens, Bacterial/genetics,metabolism Bacterial Outer Membrane Proteins/genetics,metabolism Base Sequence Cells, Cultured Cloning, Molecular DNA, Bacterial Epithelium/microbiology Escherichia coli Gene Expression Humans Leukocytes/microbiology Molecular Sequence Data Neisseria gonorrhoeae/physiology Sequence Alignment Tumor Cells, Cultured
Chemicals
Antigens, Bacterial Bacterial Outer Membrane Proteins DNA, Bacterial opacity proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Kupsch E M
Max-Planck-Institut für Biologie, Abteilung Infektionsbiologie, Tübingen, Germany.
Knepper B
Kuroki T
Heuer I
Meyer T F
References (46)
46 references, click to expand
  1. Purification and immunological studies of the cross-reaction between the 65-kilodalton gonococcal parietal lectin and an antigen common to a wide range of bacteria.
    Infect Immun. 1992 Aug;60(8):3468-71 PMID: 1639519
  2. Human neutrophil response to recombinant neisserial Opa proteins.
    Mol Microbiol. 1992 Jul;6(13):1729-37 PMID: 1630313
  3. Interaction of two variable proteins (PilE and PilC) required for pilus-mediated adherence of Neisseria gonorrhoeae to human epithelial cells.
    Mol Microbiol. 1992 Nov;6(22):3439-50 PMID: 1362447
  4. Genetic variation in pathogenic bacteria.
    Trends Genet. 1992 Dec;8(12):422-7 PMID: 1362826
  5. The human fallopian tube: a laboratory model for gonococcal infection.
    J Infect Dis. 1974 Jun;129(6):650-9 PMID: 4209721
  6. 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
  7. Biological properties of two distinct pilus types produced by isogenic variants of Neisseria gonorrhoeae P9.
    J Bacteriol. 1980 Jan;141(1):393-6 PMID: 6101593
  8. Pathogenic mechanisms of Neisseria gonorrhoeae: observations on damage to human fallopian tubes in organ culture by gonococci of colony type 1 or type 4.
    J Infect Dis. 1981 Mar;143(3):413-22 PMID: 6785363
  9. Roles of lipopolysaccharide and outer membrane protein OmpC of Escherichia coli K-12 in the receptor function for bacteriophage T4.
    J Bacteriol. 1982 Aug;151(2):718-22 PMID: 7047495
  10. Pilus expression in Neisseria gonorrhoeae involves chromosomal rearrangement.
    Cell. 1982 Aug;30(1):45-52 PMID: 6127165
  11. Studies on transformation of Escherichia coli with plasmids.
    J Mol Biol. 1983 Jun 5;166(4):557-80 PMID: 6345791
  12. Opacity determinants of Neisseria gonorrhoeae: gene expression and chromosomal linkage to the gonococcal pilus gene.
    Cell. 1984 Jun;37(2):447-56 PMID: 6144397
  13. 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
  14. 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
  15. Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation.
    Cell. 1986 Oct 10;47(1):61-71 PMID: 3093085
  16. Antigenic and physical diversity of Neisseria gonorrhoeae lipooligosaccharides.
    Infect Immun. 1986 Oct;54(1):63-9 PMID: 2428752
  17. Frequency and distribution in the United States of strains of Neisseria gonorrhoeae with plasmid-mediated, high-level resistance to tetracycline.
    J Infect Dis. 1987 Apr;155(4):819-22 PMID: 3102635
  18. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells.
    Cell. 1987 Aug 28;50(5):769-78 PMID: 3304658
  19. 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
  20. 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
  21. Surface proteins of pathogenic "Neisseria": antigenic variation and conserved epitopes.
    Ann Sclavo Collana Monogr. 1986;3(1-2):407-14 PMID: 2447924
  22. Gonococci possessing only certain P.II outer membrane proteins interact with human neutrophils.
    Infect Immun. 1988 Jun;56(6):1574-9 PMID: 3131247
  23. Model for invasion of human tissue culture cells by Neisseria gonorrhoeae.
    Infect Immun. 1988 Jun;56(6):1625-32 PMID: 3131248
  24. Recombination among protein II genes of Neisseria gonorrhoeae generates new coding sequences and increases structural variability in the protein II family.
    Mol Microbiol. 1988 Mar;2(2):227-36 PMID: 2454382
  25. Ultrastructural localization of gonococcal antigens in infected epithelial cells as visualized by post-embedding immuno-electronmicroscopy.
    Microb Pathog. 1988 Mar;4(3):213-22 PMID: 3143041
  26. Three copies of a single protein II-encoding sequence in the genome of Neisseria gonorrhoeae JS3: evidence for gene conversion and gene duplication.
    Mol Microbiol. 1988 Nov;2(6):797-806 PMID: 3145386
  27. 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
  28. Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli.
    Gene. 1988 Sep 30;69(2):301-15 PMID: 3069586
  29. Fast and sensitive multiple sequence alignments on a microcomputer.
    Comput Appl Biosci. 1989 Apr;5(2):151-3 PMID: 2720464
  30. Interactions of Neisseria gonorrhoeae with human neutrophils.
    Clin Microbiol Rev. 1989 Apr;2 Suppl:S83-91 PMID: 2497966
  31. Expression and phase variation of gonococcal P.II genes in Escherichia coli involves ribosomal frameshifting and slipped-strand mispairing.
    Mol Microbiol. 1989 Jun;3(6):777-86 PMID: 2501632
  32. Expression of gonococcal protein II in Escherichia coli by translational fusion.
    Mol Microbiol. 1989 May;3(5):663-71 PMID: 2503682
  33. 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
  34. Erythrocyte gangliosides act as receptors for Neisseria subflava: identification of the Sia-1 adhesin.
    Infect Immun. 1990 Aug;58(8):2555-63 PMID: 2370108
  35. Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly.
    EMBO J. 1991 Feb;10(2):477-88 PMID: 1671354
  36. Phase variation of the opacity outer membrane protein controls invasion by Neisseria gonorrhoeae into human epithelial cells.
    EMBO J. 1991 Jun;10(6):1307-15 PMID: 1673923
  37. In situ expression and localization of Neisseria gonorrhoeae opacity proteins in infected epithelial cells: apparent role of Opa proteins in cellular invasion.
    J Exp Med. 1991 Jun 1;173(6):1395-405 PMID: 1903430
  38. Discrimination between intracellular uptake and surface adhesion of bacterial pathogens.
    Science. 1991 May 17;252(5008):934-8 PMID: 1674624
  39. The role of pili in the interactions of pathogenic Neisseria with cultured human endothelial cells.
    Mol Microbiol. 1991 Aug;5(8):1831-41 PMID: 1722554
  40. The opacity proteins of Neisseria gonorrhoeae strain MS11 are encoded by a family of 11 complete genes.
    Mol Microbiol. 1991 Aug;5(8):1889-901 PMID: 1815562
  41. Enhancement of the invasive ability of Neisseria gonorrhoeae by contact with HecIB, an adenocarcinoma endometrial cell line.
    Mol Microbiol. 1991 Jun;5(6):1531-8 PMID: 1787801
  42. Physical and genetic map of the Neisseria gonorrhoeae strain MS11-N198 chromosome.
    Mol Microbiol. 1991 Oct;5(10):2529-39 PMID: 1791763
  43. The opacity proteins of Neisseria gonorrhoeae strain MS11 are encoded by a family of 11 complete genes.
    Mol Microbiol. 1992 Apr;6(8):1073-6 PMID: 1584024
  44. Escherichia coli expressing a Neisseria gonorrhoeae opacity-associated outer membrane protein invade human cervical and endometrial epithelial cell lines.
    Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5512-6 PMID: 1608963
  45. Further antigenic similarities of Neisseria gonorrhoeae lipooligosaccharides and human glycosphingolipids.
    Infect Immun. 1992 Jul;60(7):3017-20 PMID: 1612771
  46. Expression of the Opc protein correlates with invasion of epithelial and endothelial cells by Neisseria meningitidis.
    Mol Microbiol. 1992 Oct;6(19):2785-95 PMID: 1435257
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1993-02-00
Pages
641-50
Language
English
Region
England
NLM ID
8208664
PMCID
PMC413248
Subset
IM
Databases
GENBANK
Z18927, Z18928, Z18929, Z18930, Z18931, Z18932, Z18933, Z18934, Z18935, Z18936, Z18937, Z18938, Z18939, Z18940, Z18941
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