Oxygen tension modulates the cytokine response of oral epithelium to periodontal bacteria

Melissa M. Grant, Rajitha T Kolamunne, Frances E. Lock, John B. Matthews, Iain L.C. Chapple, Helen R Griffiths

Research output: Contribution to journalArticle

Abstract

Background: There is an inverse relationship between pocket depth and pocket oxygen tension with deep pockets being associated with anaerobic bacteria. However, little is known about how the host tissues respond to bacteria under differing oxygen tensions within the periodontal pocket.

Aim: To investigate the effect of different oxygen tensions upon nuclear factor-kappa B (NF-?B) activation and the inflammatory cytokine response of oral epithelial cells when exposed to nine species of oral bacteria.

Materials and Methods: H400 oral epithelial cells were equilibrated at 2%, 10% or 21% oxygen. Cells were stimulated with heat-killed oral bacteria at multiplicity of infection 10:1, Escherichia coli lipopolysaccharide (15 µg/ml) or vehicle control. Interleukin-8 (IL-8) and tumour necrosis factor-alpha (TNF-a) levels were measured by enzyme-linked immunosorbent assay and NF-?B activation was measured by reporter vector or by immunohistochemical analysis.

Results: Tannerella forsythensis, Porphyromonas gingivalis and Prevotella intermedia elicited the greatest epithelial NF-?B activation and cytokine responses. An oxygen-tension-dependent trend in cytokine production was observed with the highest IL-8 and TNF-a production observed at 2% oxygen and lowest at 21% oxygen.

Conclusions: These data demonstrate a greater pro-inflammatory host response and cell signalling response to bacteria present in more anaerobic conditions, and hypersensitivity of epithelial cells to pro-inflammatory stimuli at 2% oxygen, which may have implications for disease pathogenesis and/or therapy.
Original languageEnglish
Pages (from-to)1039-1048
Number of pages10
JournalJournal of Clinical Periodontology
Volume37
Issue number12
Early online date18 Oct 2010
DOIs
Publication statusPublished - Dec 2010

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Epithelium
Cytokines
Oxygen
Bacteria
Epithelial Cells
Interleukin-8
Tumor Necrosis Factor-alpha
Prevotella intermedia
Periodontal Pocket
Porphyromonas gingivalis
Anaerobic Bacteria
NF-kappa B
Lipopolysaccharides
Hypersensitivity
Hot Temperature
Enzyme-Linked Immunosorbent Assay
Escherichia coli
Infection

Keywords

  • actinobacillus actinomycetemcomitans
  • actinomyces viscosus
  • anaerobiosis
  • bacteroides
  • cultured cells
  • cytokine
  • epithelial cells
  • epithelium
  • escherichia coli
  • fusobacterium nucleatum
  • humans
  • inflammation mediators
  • interleukin-8
  • lipopolysaccharides
  • mouth mucosa
  • NF-kappa B
  • oxygen
  • peptostreptococcus
  • periodontal pocket
  • porphyromonas gingivalis
  • prevotella intermedia
  • streptococcus mitis
  • tumor necrosis factor-alpha
  • bacteria
  • HIF-1α
  • NF-κB

Cite this

Grant, M. M., Kolamunne, R. T., Lock, F. E., Matthews, J. B., Chapple, I. L. C., & Griffiths, H. R. (2010). Oxygen tension modulates the cytokine response of oral epithelium to periodontal bacteria. Journal of Clinical Periodontology, 37(12), 1039-1048. https://doi.org/10.1111/j.1600-051X.2010.01622.x
Grant, Melissa M. ; Kolamunne, Rajitha T ; Lock, Frances E. ; Matthews, John B. ; Chapple, Iain L.C. ; Griffiths, Helen R. / Oxygen tension modulates the cytokine response of oral epithelium to periodontal bacteria. In: Journal of Clinical Periodontology. 2010 ; Vol. 37, No. 12. pp. 1039-1048.
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abstract = "Background: There is an inverse relationship between pocket depth and pocket oxygen tension with deep pockets being associated with anaerobic bacteria. However, little is known about how the host tissues respond to bacteria under differing oxygen tensions within the periodontal pocket.Aim: To investigate the effect of different oxygen tensions upon nuclear factor-kappa B (NF-?B) activation and the inflammatory cytokine response of oral epithelial cells when exposed to nine species of oral bacteria.Materials and Methods: H400 oral epithelial cells were equilibrated at 2{\%}, 10{\%} or 21{\%} oxygen. Cells were stimulated with heat-killed oral bacteria at multiplicity of infection 10:1, Escherichia coli lipopolysaccharide (15 µg/ml) or vehicle control. Interleukin-8 (IL-8) and tumour necrosis factor-alpha (TNF-a) levels were measured by enzyme-linked immunosorbent assay and NF-?B activation was measured by reporter vector or by immunohistochemical analysis.Results: Tannerella forsythensis, Porphyromonas gingivalis and Prevotella intermedia elicited the greatest epithelial NF-?B activation and cytokine responses. An oxygen-tension-dependent trend in cytokine production was observed with the highest IL-8 and TNF-a production observed at 2{\%} oxygen and lowest at 21{\%} oxygen.Conclusions: These data demonstrate a greater pro-inflammatory host response and cell signalling response to bacteria present in more anaerobic conditions, and hypersensitivity of epithelial cells to pro-inflammatory stimuli at 2{\%} oxygen, which may have implications for disease pathogenesis and/or therapy.",
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Grant, MM, Kolamunne, RT, Lock, FE, Matthews, JB, Chapple, ILC & Griffiths, HR 2010, 'Oxygen tension modulates the cytokine response of oral epithelium to periodontal bacteria', Journal of Clinical Periodontology, vol. 37, no. 12, pp. 1039-1048. https://doi.org/10.1111/j.1600-051X.2010.01622.x

Oxygen tension modulates the cytokine response of oral epithelium to periodontal bacteria. / Grant, Melissa M.; Kolamunne, Rajitha T; Lock, Frances E.; Matthews, John B.; Chapple, Iain L.C.; Griffiths, Helen R.

In: Journal of Clinical Periodontology, Vol. 37, No. 12, 12.2010, p. 1039-1048.

Research output: Contribution to journalArticle

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T1 - Oxygen tension modulates the cytokine response of oral epithelium to periodontal bacteria

AU - Grant, Melissa M.

AU - Kolamunne, Rajitha T

AU - Lock, Frances E.

AU - Matthews, John B.

AU - Chapple, Iain L.C.

AU - Griffiths, Helen R

N1 - © 2010 John Wiley & Sons A/S.

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N2 - Background: There is an inverse relationship between pocket depth and pocket oxygen tension with deep pockets being associated with anaerobic bacteria. However, little is known about how the host tissues respond to bacteria under differing oxygen tensions within the periodontal pocket.Aim: To investigate the effect of different oxygen tensions upon nuclear factor-kappa B (NF-?B) activation and the inflammatory cytokine response of oral epithelial cells when exposed to nine species of oral bacteria.Materials and Methods: H400 oral epithelial cells were equilibrated at 2%, 10% or 21% oxygen. Cells were stimulated with heat-killed oral bacteria at multiplicity of infection 10:1, Escherichia coli lipopolysaccharide (15 µg/ml) or vehicle control. Interleukin-8 (IL-8) and tumour necrosis factor-alpha (TNF-a) levels were measured by enzyme-linked immunosorbent assay and NF-?B activation was measured by reporter vector or by immunohistochemical analysis.Results: Tannerella forsythensis, Porphyromonas gingivalis and Prevotella intermedia elicited the greatest epithelial NF-?B activation and cytokine responses. An oxygen-tension-dependent trend in cytokine production was observed with the highest IL-8 and TNF-a production observed at 2% oxygen and lowest at 21% oxygen.Conclusions: These data demonstrate a greater pro-inflammatory host response and cell signalling response to bacteria present in more anaerobic conditions, and hypersensitivity of epithelial cells to pro-inflammatory stimuli at 2% oxygen, which may have implications for disease pathogenesis and/or therapy.

AB - Background: There is an inverse relationship between pocket depth and pocket oxygen tension with deep pockets being associated with anaerobic bacteria. However, little is known about how the host tissues respond to bacteria under differing oxygen tensions within the periodontal pocket.Aim: To investigate the effect of different oxygen tensions upon nuclear factor-kappa B (NF-?B) activation and the inflammatory cytokine response of oral epithelial cells when exposed to nine species of oral bacteria.Materials and Methods: H400 oral epithelial cells were equilibrated at 2%, 10% or 21% oxygen. Cells were stimulated with heat-killed oral bacteria at multiplicity of infection 10:1, Escherichia coli lipopolysaccharide (15 µg/ml) or vehicle control. Interleukin-8 (IL-8) and tumour necrosis factor-alpha (TNF-a) levels were measured by enzyme-linked immunosorbent assay and NF-?B activation was measured by reporter vector or by immunohistochemical analysis.Results: Tannerella forsythensis, Porphyromonas gingivalis and Prevotella intermedia elicited the greatest epithelial NF-?B activation and cytokine responses. An oxygen-tension-dependent trend in cytokine production was observed with the highest IL-8 and TNF-a production observed at 2% oxygen and lowest at 21% oxygen.Conclusions: These data demonstrate a greater pro-inflammatory host response and cell signalling response to bacteria present in more anaerobic conditions, and hypersensitivity of epithelial cells to pro-inflammatory stimuli at 2% oxygen, which may have implications for disease pathogenesis and/or therapy.

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KW - actinomyces viscosus

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KW - bacteroides

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KW - fusobacterium nucleatum

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KW - lipopolysaccharides

KW - mouth mucosa

KW - NF-kappa B

KW - oxygen

KW - peptostreptococcus

KW - periodontal pocket

KW - porphyromonas gingivalis

KW - prevotella intermedia

KW - streptococcus mitis

KW - tumor necrosis factor-alpha

KW - bacteria

KW - HIF-1α

KW - NF-κB

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