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PMID: 7629509 Published · ppublish English Journal Article

Adherence of pilus- Opa+ gonococci to epithelial cells in vitro involves heparan sulfate.

The Journal of experimental medicine ·Vol. 182 ·No. 2 ·1995-08-01 ·Pages 511-7

Chen T, Belland RJ, Wilson J, Swanson J

Abstract

Neisseria gonorrhoeae attaches to host epithelial cells via pili and opacity-associated (Opa) outer membrane proteins. Pilus- gonococci (Gc) of strain MS11 adhere to both human and nonhuman cells, but only when particular Opa proteins are expressed; OpaA+ variants adhere best, OpaC+ variants are next best, and the seven other Opa+ variants adhere poorly or not at all. The adherence of OpaA+ Gc to Chinese hamster ovary (CHO) cells is inhibited by heparin or heparan sulfate (HS), but not by chondroitin sulfate. OpaA+ Gc do not adhere to CHO cells devoid of HS proteoglycans; low concentrations of heparin restore OpaA+ Gc adherence to these HS-deficient CHO cells and high concentrations inhibit it. 3H-heparin binding to whole Gc parallels their adherence abilities (OpaA+ > OpaC+ > OpaH+ >> Opas B, D, E, F, G, I = Opa- = 0). Opa proteins separated by SDS-PAGE also bind 3H-heparin. These data suggest that adherence of pilus-, Opa+ Gc involves HS-proteoglycan of eukaryotic cells.

Related Genes
MeSH Terms
Animals Antigens, Bacterial/metabolism Bacterial Adhesion Bacterial Outer Membrane Proteins/metabolism CHO Cells Cricetinae Epithelium/microbiology Fimbriae, Bacterial/physiology Heparin/pharmacology Heparitin Sulfate/metabolism Neisseria gonorrhoeae/pathogenicity Protein Binding Protein Denaturation
Chemicals
Antigens, Bacterial Bacterial Outer Membrane Proteins opacity proteins Heparin Heparitin Sulfate
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Chen T
Laboratory of Microbial Structure and Function, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana 59840, USA.
Belland R J
Wilson J
Swanson J
References (46)
46 references, click to expand
  1. Herpes simplex viruses lacking glycoprotein D are unable to inhibit virus penetration: quantitative evidence for virus-specific cell surface receptors.
    J Virol. 1988 Dec;62(12):4605-12 PMID: 2846873
  2. Model for invasion of human tissue culture cells by Neisseria gonorrhoeae.
    Infect Immun. 1988 Jun;56(6):1625-32 PMID: 3131248
  3. Expression of outer membrane protein II by gonococci in experimental gonorrhea.
    J Exp Med. 1988 Dec 1;168(6):2121-9 PMID: 3143800
  4. 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
  5. Undersulfated heparan sulfate in a Chinese hamster ovary cell mutant defective in heparan sulfate N-sulfotransferase.
    J Biol Chem. 1989 May 15;264(14):8059-65 PMID: 2524478
  6. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells.
    Cell. 1990 Mar 9;60(5):861-71 PMID: 2311122
  7. Soluble forms of herpes simplex virus glycoprotein D bind to a limited number of cell surface receptors and inhibit virus entry into cells.
    J Virol. 1990 Jun;64(6):2569-76 PMID: 2159532
  8. 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
  9. Proteoglycans: structures and interactions.
    Annu Rev Biochem. 1991;60:443-75 PMID: 1883201
  10. 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
  11. Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans.
    J Cell Biol. 1992 Mar;116(5):1273-81 PMID: 1310996
  12. Cloning, expression, and DNA sequence analysis of genes encoding nontypeable Haemophilus influenzae high-molecular-weight surface-exposed proteins related to filamentous hemagglutinin of Bordetella pertussis.
    Infect Immun. 1992 Apr;60(4):1302-13 PMID: 1548058
  13. A single mutation affects both N-acetylglucosaminyltransferase and glucuronosyltransferase activities in a Chinese hamster ovary cell mutant defective in heparan sulfate biosynthesis.
    Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2267-71 PMID: 1532254
  14. 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
  15. Structure of a heparan sulphate oligosaccharide that binds to basic fibroblast growth factor.
    Biochem J. 1992 Aug 1;285 ( Pt 3):805-13 PMID: 1497618
  16. 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
  17. Variable opacity (Opa) outer membrane proteins account for the cell tropisms displayed by Neisseria gonorrhoeae for human leukocytes and epithelial cells.
    EMBO J. 1993 Feb;12(2):641-50 PMID: 8440254
  18. Binding of lipoprotein lipase to heparin. Identification of five critical residues in two distinct segments of the amino-terminal domain.
    J Biol Chem. 1993 Apr 25;268(12):8447-57 PMID: 8473288
  19. Neuraminic acid is alpha 2-->3 linked in the lipooligosaccharide of Neisseria meningitidis serogroup B strain 6275.
    J Bacteriol. 1993 Jul;175(14):4565-8 PMID: 8331087
  20. Comparative analysis of structurally defined heparin binding sequences reveals a distinct spatial distribution of basic residues.
    J Biol Chem. 1993 Sep 15;268(26):19228-31 PMID: 8366075
  21. Isolation of a putative fimbrial adhesin from Bordetella pertussis and the identification of its gene.
    Mol Microbiol. 1993 Aug;9(3):623-34 PMID: 8105363
  22. Minimal sequence in heparin/heparan sulfate required for binding of basic fibroblast growth factor.
    J Biol Chem. 1993 Nov 15;268(32):23898-905 PMID: 8226930
  23. Localization of a functional site on herpes simplex virus type 1 glycoprotein C involved in binding to cell surface heparan sulphate.
    J Gen Virol. 1994 Apr;75 ( Pt 4):743-52 PMID: 7512117
  24. Glycoprotein C-independent binding of herpes simplex virus to cells requires cell surface heparan sulphate and glycoprotein B.
    J Gen Virol. 1994 Jun;75 ( Pt 6):1211-22 PMID: 8207388
  25. High-molecular-weight proteins of nontypeable Haemophilus influenzae mediate bacterial adhesion to cellular proteoglycans.
    Infect Immun. 1994 Sep;62(9):4028-33 PMID: 8063423
  26. Escherichia coli that express Neisseria gonorrhoeae opacity-associated proteins attach to and invade human fallopian tube epithelium.
    Ann N Y Acad Sci. 1994 Aug 15;730:286-9 PMID: 8080188
  27. Sulfated glycoconjugate receptors for the Bordetella pertussis adhesin filamentous hemagglutinin (FHA) and mapping of the heparin-binding domain on FHA.
    Infect Immun. 1994 Nov;62(11):5010-9 PMID: 7927782
  28. The pathology of gonorrhoea.
    Br J Vener Dis. 1948 Dec;24(4):137-47 PMID: 18099876
  29. Neisseria gonorrhoeae. II. Colonial variation and pathogenicity during 35 months in vitro.
    J Bacteriol. 1968 Sep;96(3):596-605 PMID: 4979098
  30. Gonococci in urethral exudates possess a virulence factor lost on subculture.
    Nature. 1970 Jul 25;227(5256):382-4 PMID: 4987874
  31. Studies on gonococcus infection. IV. Pili: their role in attachment of gonococci to tissue culture cells.
    J Exp Med. 1973 Mar 1;137(3):571-89 PMID: 4631989
  32. Role of pili in the virulence of Neisseria gonorrhoeae.
    Infect Immun. 1973 Aug;8(2):255-63 PMID: 4200266
  33. The human fallopian tube: a laboratory model for gonococcal infection.
    J Infect Dis. 1974 Jun;129(6):650-9 PMID: 4209721
  34. Studies on gonococcus infection. VII. In vitro killing of gonococci by human leukocytes.
    Infect Immun. 1975 Jan;11(1):65-8 PMID: 803924
  35. Human fallopian tubes in organ culture: preparation, maintenance, and quantitation of damage by pathogenic microorganisms.
    Infect Immun. 1976 Feb;13(2):608-18 PMID: 816745
  36. Ultrastructural study of cervical gonorrhea.
    J Infect Dis. 1977 Aug;136(2):248-55 PMID: 408425
  37. 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
  38. Detailed analysis of the portion of the herpes simplex virus type 1 genome encoding glycoprotein C.
    J Virol. 1983 Feb;45(2):634-47 PMID: 6300426
  39. Immunological characteristics of gonococcal outer membrane protein II assessed by immunoprecipitation, immunoblotting, and coagglutination.
    J Exp Med. 1983 May 1;157(5):1405-20 PMID: 6406636
  40. Nucleotide sequence specifying the glycoprotein gene, gB, of herpes simplex virus type 1.
    Virology. 1984 Mar;133(2):301-14 PMID: 6324454
  41. Animal cell mutants defective in glycosaminoglycan biosynthesis.
    Proc Natl Acad Sci U S A. 1985 May;82(10):3197-201 PMID: 3858816
  42. 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
  43. Gonococcal pilin variants in experimental gonorrhea.
    J Exp Med. 1987 May 1;165(5):1344-57 PMID: 3106555
  44. Inhibition of chondroitin and heparan sulfate biosynthesis in Chinese hamster ovary cell mutants defective in galactosyltransferase I.
    J Biol Chem. 1987 Sep 5;262(25):12189-95 PMID: 2957376
  45. Use of organ cultures in microbiological research.
    Annu Rev Microbiol. 1987;41:291-300 PMID: 3318672
  46. 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
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
1995-08-01
Pages
511-7
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2192128
Subset
IM
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