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PMID: 9529095 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Local chemokine paralysis, a novel pathogenic mechanism for Porphyromonas gingivalis.

Infection and immunity ·Vol. 66 ·No. 4 ·1998-04-00 ·Pages 1660-5

Darveau RP, Belton CM, Reife RA, Lamont RJ

Abstract

Periodontitis, which is widespread in the adult population, is a persistent bacterial infection associated with Porphyromonas gingivalis. Gingival epithelial cells are among the first cells encountered by both P. gingivalis and commensal oral bacteria. The chemokine interleukin 8 (IL-8), a potent chemoattractant and activator of polymorphonuclear leukocytes, was secreted by gingival epithelial cells in response to components of the normal oral flora. In contrast, P. gingivalis was found to strongly inhibit IL-8 accumulation from gingival epithelial cells. Inhibition was associated with a decrease in mRNA for IL-8. Antagonism of IL-8 accumulation did not occur in KB cells, an epithelial cell line that does not support high levels of intracellular invasion by P. gingivalis. Furthermore, a noninvasive mutant of P. gingivalis was unable to antagonize IL-8 accumulation. Invasion-dependent destruction of the gingival IL-8 chemokine gradient at sites of P. gingivalis colonization (local chemokine paralysis) will severely impair mucosal defense and represents a novel mechanism for bacterial colonization of host tissue.

MeSH Terms
Dental Plaque/microbiology Humans Interleukin-8/antagonists & inhibitors,genetics,metabolism KB Cells Periodontal Diseases/etiology Porphyromonas gingivalis/pathogenicity RNA, Messenger/analysis
Chemicals
Interleukin-8 RNA, Messenger
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Darveau R P
Bristol-Myers Squibb Pharmaceutical Research Institute, Seattle, Washington 98121, USA. [email protected]
Belton C M
Reife R A
Lamont R J
References (41)
41 references, click to expand
  1. Expression of the endothelial leukocyte adhesion molecule-1 (ELAM-1) on endothelial cells in experimental gingivitis in humans.
    J Periodontol. 1993 May;64(5):355-7 PMID: 7685818
  2. Interactions of Porphyromonas gingivalis with epithelial cells.
    Infect Immun. 1993 May;61(5):2260-5 PMID: 8386706
  3. Interleukin-8 and the neutrophil response to mucosal gram-negative infection.
    J Clin Invest. 1993 Aug;92(2):780-5 PMID: 8349817
  4. Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry.
    Infect Immun. 1993 Nov;61(11):4569-74 PMID: 8406853
  5. Involvement of Porphyromonas gingivalis fimbriae in adherence to Streptococcus gordonii.
    Oral Microbiol Immunol. 1993 Oct;8(5):272-6 PMID: 7903442
  6. Inactivation of the Porphyromonas gingivalis fimA gene blocks periodontal damage in gnotobiotic rats.
    J Bacteriol. 1994 Feb;176(4):1052-9 PMID: 8106316
  7. Localized expression of mRNA for phagocyte-specific chemotactic cytokines in human periodontal infections.
    Infect Immun. 1994 Sep;62(9):4005-14 PMID: 8063420
  8. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion.
    J Clin Invest. 1995 Jan;95(1):55-65 PMID: 7814646
  9. Ability of bacteria associated with chronic inflammatory disease to stimulate E-selectin expression and promote neutrophil adhesion.
    Infect Immun. 1995 Apr;63(4):1311-7 PMID: 7534275
  10. Pathogenic strategies of the oral anaerobe, Porphyromonas gingivalis.
    Trends Microbiol. 1995 Feb;3(2):45-51 PMID: 7728384
  11. CD14 and innate recognition of bacteria.
    J Immunol. 1995 Jul 1;155(1):6-8 PMID: 7541427
  12. Porphyromonas gingivalis invasion of gingival epithelial cells.
    Infect Immun. 1995 Oct;63(10):3878-85 PMID: 7558295
  13. Association of Helicobacter pylori and Chlamydia pneumoniae infections with coronary heart disease and cardiovascular risk factors.
    BMJ. 1995 Sep 16;311(7007):711-4 PMID: 7549683
  14. Porphyromonas gingivalis lipopolysaccharide is poorly recognized by molecular components of innate host defense in a mouse model of early inflammation.
    Infect Immun. 1995 Dec;63(12):4686-94 PMID: 7591124
  15. Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. The Vaginal Infections and Prematurity Study Group.
    N Engl J Med. 1995 Dec 28;333(26):1737-42 PMID: 7491137
  16. Surface attachment of Salmonella typhimurium to intestinal epithelia imprints the subepithelial matrix with gradients chemotactic for neutrophils.
    J Cell Biol. 1995 Dec;131(6 Pt 1):1599-608 PMID: 8522615
  17. Analysis of the prtP gene encoding porphypain, a cysteine proteinase of Porphyromonas gingivalis.
    J Bacteriol. 1996 May;178(10):2734-41 PMID: 8631659
  18. Increased incidence of Chlamydia species within the coronary arteries of patients with symptomatic atherosclerotic versus other forms of cardiovascular disease.
    J Am Coll Cardiol. 1996 Jun;27(7):1555-61 PMID: 8636536
  19. Chlamydia pneumoniae and atherosclerosis.
    Rev Med Interne. 1996;17 Suppl 1:45S-47S PMID: 8760682
  20. Periodontal infection as a possible risk factor for preterm low birth weight.
    J Periodontol. 1996 Oct;67(10 Suppl):1103-13 PMID: 8910829
  21. Periodontal disease and cardiovascular disease.
    J Periodontol. 1996 Oct;67(10 Suppl):1123-37 PMID: 8910831
  22. Release of lipopolysaccharide from intracellular compartments containing Salmonella typhimurium to vesicles of the host epithelial cell.
    Infect Immun. 1997 Jan;65(1):24-34 PMID: 8975888
  23. Role of fimbriae in Porphyromonas gingivalis invasion of gingival epithelial cells.
    Infect Immun. 1997 Jan;65(1):313-6 PMID: 8975930
  24. Secretion of proinflammatory cytokines by epithelial cells in response to Chlamydia infection suggests a central role for epithelial cells in chlamydial pathogenesis.
    J Clin Invest. 1997 Jan 1;99(1):77-87 PMID: 9011579
  25. Molecular factors associated with compartmentalization of gingival immune responses and transepithelial neutrophil migration.
    J Periodontal Res. 1997 Jan;32(1 Pt 2):104-9 PMID: 9085218
  26. Interactions between periodontopathogenic bacteria and cytokines.
    J Periodontal Res. 1997 Jan;32(1 Pt 2):200-5 PMID: 9085235
  27. Porphyromonas gingivalis infection of oral epithelium inhibits neutrophil transepithelial migration.
    Infect Immun. 1997 Oct;65(10):3983-90 PMID: 9316996
  28. Pathogenesis of inflammatory periodontal disease. A summary of current work.
    Lab Invest. 1976 Mar;34(3):235-49 PMID: 765622
  29. Procedure for isolation of bacterial lipopolysaccharides from both smooth and rough Pseudomonas aeruginosa and Salmonella typhimurium strains.
    J Bacteriol. 1983 Aug;155(2):831-8 PMID: 6409884
  30. The severe and moderate phenotypes of heritable Mac-1, LFA-1 deficiency: their quantitative definition and relation to leukocyte dysfunction and clinical features.
    J Infect Dis. 1985 Oct;152(4):668-89 PMID: 3900232
  31. Implantation of Bacteroides gingivalis in nonhuman primates initiates progression of periodontitis.
    Science. 1988 Jan 1;239(4835):55-7 PMID: 3336774
  32. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein.
    Science. 1990 Sep 21;249(4975):1431-3 PMID: 1698311
  33. The bacterial etiology of destructive periodontal disease: current concepts.
    J Periodontol. 1992 Apr;63(4 Suppl):322-31 PMID: 1573546
  34. Purification and characterization of a 50-kDa cysteine proteinase (gingipain) from Porphyromonas gingivalis.
    J Biol Chem. 1992 Sep 15;267(26):18896-901 PMID: 1527017
  35. Direct and indirect effects of Porphyromonas gingivalis lipopolysaccharide on interleukin-6 production by human gingival fibroblasts.
    Oral Microbiol Immunol. 1992 Aug;7(4):218-24 PMID: 1328999
  36. Brief report: recurrent severe infections caused by a novel leukocyte adhesion deficiency.
    N Engl J Med. 1992 Dec 17;327(25):1789-92 PMID: 1279426
  37. Soluble CD14 participates in the response of cells to lipopolysaccharide.
    J Exp Med. 1992 Dec 1;176(6):1665-71 PMID: 1281215
  38. Endothelial cell leukocyte adhesion molecule-1 (ELAM-1) and intercellular adhesion molecule-1 (ICAM-1) expression in gingival tissue during health and experimentally-induced gingivitis.
    J Periodontal Res. 1992 Nov;27(6):623-30 PMID: 1281230
  39. Selective cytokine production by epithelial cells following exposure to Escherichia coli.
    Infect Immun. 1993 Feb;61(2):602-9 PMID: 8423089
  40. Lipopolysaccharide activation of human endothelial and epithelial cells is mediated by lipopolysaccharide-binding protein and soluble CD14.
    Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2744-8 PMID: 7681988
  41. Stimulation of B lymphocytes by lipopolysaccharides from anaerobic bacteria.
    Clin Infect Dis. 1993 Jun;16 Suppl 4:S200-2 PMID: 8324119
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
1998-04-00
Pages
1660-5
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC108102
Subset
IM
Grants
NIDCR NIH HHS · R01 DE011111 · United States
NIDCR NIH HHS · R37 DE011111 · United States
NIDCR NIH HHS · DE11111 · United States
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