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

Journal of Clinical Periodontology

Volumn 37, Issue 12, 2010, Pages 1039-1048

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

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b ASTON UNIVERSITY   (United Kingdom)

Author keywords

bacteria; cytokine; epithelium; HIF 1 ; NF B; oxygen; P.gingivalis

Indexed keywords

AUTACOID; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; OXYGEN; TUMOR NECROSIS FACTOR ALPHA;

ACTINOMYCES VISCOSUS; AGGREGATIBACTER ACTINOMYCETEMCOMITANS; ANAEROBIC GROWTH; ARTICLE; BACTEROIDES; CELL CULTURE; EPITHELIUM; EPITHELIUM CELL; ESCHERICHIA COLI; FUSOBACTERIUM NUCLEATUM; HUMAN; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOUTH MUCOSA; PEPTOSTREPTOCOCCUS; PERIODONTAL POCKET; PORPHYROMONAS GINGIVALIS; PREVOTELLA INTERMEDIA; STREPTOCOCCUS MITIS;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; ACTINOMYCES VISCOSUS; ANAEROBIOSIS; BACTEROIDES; CELLS, CULTURED; CYTOKINES; 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;

EID: 78649286140     PISSN: 03036979     EISSN: 1600051X     Source Type: Journal    
DOI: 10.1111/j.1600-051X.2010.01622.x     Document Type: Article

References (62)

1. Acosta-Iborra, B., Elorza, A., Olazabal, I. M., Martin-Cofreces, N. A., Martin-Puig, S., Miro, M., Calzada, M. J., Aragones, J., Sanchez-Madrid, F., &, Landazuri, M. O., (2009) Macrophage oxygen sensing modulates antigen presentation and phagocytic functions involving IFNgamma production through HIF-1± transcription factor. Journal of Immunology 182, 3155 - 3164.
2. Arenzana-Seisdedos, F., Fernandez, B., Dominguez, I., Jacque, J. M., Thomas, D., Diaz-Meco, M. T., Moscat, J., &, Virelizier, J. L., (1993) Phosphatidylcholine hydrolysis activates NF-kB and increases human immunodeficiency virus replication in human monocytes and T lymphocytes. Journal of Virology 67, 6596 - 6604.
3. Bhandari, V., &, Elias, J., (2006) Cytokines in tolerance to hyperoxia-induced injury in the developing and adult lung. Free Radical Biology and Medicine 41, 4 - 18.
4. Bjornheden, T., Levin, M., Evaldsson, M., &, Wiklund, O., (1999) Evidence of hypoxic areas within the arterial wall in vivo. Arteriosclerosis, Thrombosis and Vascular Biology 19, 870 - 876.
5. Bostanci, N., Emingil, G., Afacan, B., Han, B., Ilgenli, T., Atilla, G., Hughes, F. J., &, Belibasakis, G. N., (2008) Tumour necrosis factor-alpha-converting enzyme (TACE) levels in periodontal diseases. Journal of Dental Research 87, 273 - 277.
6. Buchmann, R., Hasilik, A., Nunn, M. E., Van Dyke, T. E., &, Lange, D. E., (2002) PMN responses in chronic periodontal disease: evaluation by gingival crevicular fluid enzymes and elastase-alpha-1-proteinase inhibitor complex. Journal of Clinical Periodontology 29, 563 - 572.
7. Burke, B., Giannoudis, A., Corke, K. P., Gill, D., Wells, M., Ziegler-Heitbrock, L., &, Lewis, C. E., (2003) Hypoxia-induced gene expression in human macrophages: implications for ischemic tissues and hypoxia-regulated gene therapy. American Journal of Pathology 163, 1233 - 1243.
8. Chapple, I. L. C., &, Matthews, J. B., (2007) The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontology 2000 43, 160 - 232.
9. Charbonneau, M., Harper, K., Grondin, F., Pelmus, M., McDonald, P. P., &, Dubois, C. M., (2007) Hypoxia-inducible factor mediates hypoxic and tumor necrosis factor alpha-induced increases in tumor necrosis factor-alpha converting enzyme/ADAM17 expression by synovial cells. Journal of Biological Chemistry 282, 33714 - 33724.
10. Chung, R. M., Grbc, J. T., &, Lamster, I. B., (1997) Interleukin-8 and beta-glucuronidase in gingival crevicular fluid. Journal of Clinical Periodontology 24, 146 - 152.
11. Dale, B. A., (2002) Periodontal epithelium: a newly recognized role in health and disease. Periodontology 2000 30, 70 - 78.
12. Darveau, R. P., Belton, C. M., Reife, R. A., &, Lamont, R. J., (1998) Local chemokine paralysis, a novel pathogenic mechanism for Porphyromonas gingivalis. Infection and Immunity 66, 1660 - 1665.
13. Derevianko, A., D'Amico, R., &, Simms, H., (1996) Polymorphonuclear leucocytes (PMN)-derived inflammatory cytokines - regulation by oxygen tension and extracellular matrix. Clinical and Experimental Immunology 106, 560 - 567.
14. Déry, M. A., Michaud, M. D., &, Richard, DE., (2005) Hypoxia-inducible factor 1: regulation by hypoxic and non-hypoxic activators. International Journal of Biochemistry and Cell Biology 37, 535 - 540.
15. Dias, I. H., Marshall, L., Lambert, P. A., Chapple, I. L., Matthews, J. B., &, Griffiths, H. R., (2008) Gingipains from Porphyromonas gingivalis increase the chemotactic and respiratory burst-priming properties of the 77-amino-acid interleukin-8 variant. Infection and Immunity 76, 317 - 323.
16. Erdemir, E. O., Duran, I., &, Haliloglu, S., (2004) Effects of smoking on clinical parameters and the gingival crevicular fluid levels of IL-6 and TNF-alpha in patients with chronic periodontitis. Journal of Clinical Periodontology 31, 99 - 104.
17. Farida, R., Marsh, P. D., Newman, H. N., Rule, D. C., &, Ivanyi, L., (1986) Serological investigation of various forms of inflammatory periodontitis. Journal of Periodontal Research 21, 365 - 374.
18. Frede, S., Stockmann, C., Freitag, P., &, Fandrey, J., (2006) Bacterial lipopolysaccharide induces HIF-1 activation in human monocytes via p44/42 MAPK and NF-kappaB. Biochemical Journal 396, 517 - 527.
19. Gamonal, J., Acevedo, A., Bascones, A., Jorge, O., &, Silva, A., (2001) Characterization of cellular infiltrate, detection of chemokine receptor CCR5 and interleukin-8 and RANTES chemokines in adult periodontitis. Journal of Periodontal Research 36, 194 - 203.
20. Grant, M. M., &, Griffiths, H. R., (2007) Cell passage-associated transient high oxygenation causes a transient decrease in cellular glutathione and affects T cell responses to apoptotic and mitogenic stimuli. Environmental Toxicology and Pharmacology 23, 335 - 339.
21. Grenier, D., &, Mayrand, D., (1987) Selected characteristics of pathogenic and nonpathogenic strains of Bacteroides gingivalis. Journal of Clinical Microbiology 25, 738 - 740.
22. Grossi, S. G., Zambon, J. J., Ho, A. W., Koch, G., Dunford, R. G., Machtei, E. E., Nordeyrd, O. M., &, Genco, R. J., (1994) Assessment of risk for periodontal disease. 1. Risk indicators for attachment loss. Journal of Periodontology 65, 260 - 267.
23. Hanioka, T., Tanaka, M., Takaya, K., Matsumori, Y., &, Shizukuishi, S., (2000) Pocket oxygen tension in smokers and non-smokers with periodontal disease. Journal of Periodontology 71, 550 - 554.
24. Hasegawa, Y., Tribble, G. D., Baker, H. V., Mans, J. J., Handfield, M., &, Lamont, R. J., (2008) Role of Porphyromonas gingivalis SerB in gingival epithelial cell cytoskeletal remodeling and cytokine production. Infection and Immunity 76, 2420 - 2427.
25. Hoffmann, E., Dittrich-Breiholz, O., Holtmann, H., &, Kracht, M., (2002) Multiple control of interleukin-8 gene expression. Journal of Leukocyte Biology 72, 847 - 855.
26. Jin, L. J., Leung, W. K., Corbet, E. F., &, Söder, B., (2002) Relationship of changes in interleukin-8 levels and granulocyte elastase activity in gingival crevicular fluid to subgingival periodontopathogens following non-surgical periodontal therapy in subjects with chronic periodontitis. Journal of Clinical Periodontology 29, 604 - 614.
27. Jung, Y., Isaacs, J. S., Lee, S., Trepel, J., Liu, Z. G., &, Neckers, L., (2003) Hypoxia-inducible factor induction by tumour necrosis factor in normoxic cells requires receptor-interacting protein-dependent nuclear factor kappa B activation. Biochemical Journal 370, 1011 - 1017.
28. Kivisaari, J., (1975) Oxygen and carbon dioxide tensions in healing tissue. Acta Chirurgica Scandinavica 141, 693 - 696.
29. Koong, A. C., Chen, E. Y., &, Giaccia, A. J., (1994) Hypoxia causes the activation of nuclear factor kappa B through the phosphorylation of I kappa B alpha on tyrosine residues. Cancer Research 54, 1425 - 1430.
30. Krisanaprakornkit, S., Kimball, J. R., Weinberg, A., Darveau, R. P., Bainbridge, B. W., &, Dale, B. A., (2000) Inducible expression of human beta-defensin 2 by Fusobacterium nucleatum in oral epithelial cells: multiple signaling pathways and role of commensal bacteria in innate immunity and the epithelial barrier. Infection and Immunity 68, 2907 - 2915.
31. Kusumoto, Y., Hirano, H., Saitoh, K., Yamada, S., Takedachi, M., Nozaki, T., Ozawa, Y., Nakahira, Y., Saho, T., Ogo, H., Shimabukuro, Y., Okada, H., &, Murakami, S., (2004) Human gingival epithelial cells produce chemotactic factors interleukin-8 and monocyte chemoattractant protein-1 after stimulation with Porphyromonas gingivalis via toll-like receptor 2. Journal of Periodontology 75, 370 - 379.
32. Laine, M. L., &, Van Winkelhoff, A. J., (1998) Virulence of six capsular serotypes of Porphyromonas gingivalis in a mouse model. Oral Microbiology and Immunology 13, 322 - 325.
33. Lin, L., Chen, L., Liu, J., Zhang, D., Zhao, J., Kou, Y., Yu, N., &, Pan, Y., (2009) Virulence genes of Porphyromonas gingivalis W83 in chronic periodontitis. Acta Odontologica Scandinavica 67, 258 - 264.
34. Loesche, W. J., Gusberti, F., Mettraux, G., Higgins, T., &, Syed, S., (1983) Relationship between oxygen tension and subgingival bacterial flora in untreated human periodontal pockets. Infection and Immunity 42, 659 - 667.
35. Madianos, P. N., Papapanou, P. N., &, Sandros, J., (1997) Porphyromonas gingivalis infection of oral epithelium inhibits neutrophil transepithelial migration. Infection and Immunity 65, 3983 - 3990.
36. Matthews, J. B., Wright, H. J., Roberts, A., Cooper, P. R., &, Chapple, I. L., (2007a) Hyperactivity and reactivity of peripheral blood neutrophils in chronic periodontitis. Clinical and Experimental Immunology 147, 255 - 264.
37. Matthews, J. B., Wright, H. J., Roberts, A., Ling-Mountford, N., Cooper, P. R., &, Chapple, I. L., (2007b) Neutrophil hyper-responsiveness in periodontitis. Journal of Dental Research 86, 718 - 722.
38. Matuschak, G. M., Munoz, C. F., Johanns, C. A., Rahman, R., &, Lechner, A. J., (1998) Upregulation of postbacteremic YNF alpha and IL1alpha gene expression by alveolar hypoxia/regeneration in perfused rat lungs. American Journal of Respiratory and Critical Care Medicine 157, 629 - 637.
39. 2) in untreated human periodontal pockets. Journal of Periodontology 55, 516 - 521.
40. Mikolajczyk-Pawlinska, J., Travis, J., &, Potempa, J., (1998) Modulation of interleukin-8 activity by gingipains from Porphyromonas gingivalis: implications for pathogenicity of periodontal disease. FEBS Letters 440, 282 - 286.
41. Milward, M. R., Chapple, I. L., Wright, H. J., Millard, J. L., Matthews, J. B., &, Cooper, P. R., (2007) Differential activation of NF-kappaB and gene expression in oral epithelial cells by periodontal pathogens. Clinical and Experimental Immunology 148, 307 - 324.
42. Mori, Y., Yoshimura, A., Ukai, T., Lien, E., Espevik, T., &, Hara, Y., (2003) Immunohistochemical localization of Toll-like receptors 2 and 4 in gingival tissue from patients with periodontitis. Oral Microbiology and Immunology 18, 54 - 58.
43. Offenbacher, S., Barros, S. P., Singer, R. E., Moss, K., Williams, R. C., &, Beck, J. D., (2007) Periodontal disease at the biofilm-gingival interface. Journal of Periodontology 78, 1911 - 1925.
44. Prime, S. S., Game, S. M., Matthews, J. B., Stone, A., Donnelly, M. J., Yeudall, W. A., Patel, V., Sposto, R., Silverthorne, A., &, Scully, C., (1994a) Epidermal growth factor and transforming growth factor alpha characteristics of human oral carcinoma cell lines. British Journal of Cancer 69, 8 - 15.
45. Prime, S. S., Matthews, J. B., Patel, V., Game, S. M., Donnelly, M., Stone, A., Paterson, I. C., Sandy, J. R., &, Yeudall, W. A., (1994b) TGF-beta receptor regulation mediates the response to exogenous ligand but is independent of the degree of cellular differentiation in human oral keratinocytes. International Journal of Cancer 56, 406 - 412.
46. Prime, S. S., Nixon, S. V. R., Crane, I. J., Stone, A., Matthews, J. B., Maitland, N. J., Remnant, L., Powell, S. K., Game, S. M., &, Scully, C. M., (1990) The behaviour of human oral squamous cell carcinoma in cell culture. Journal of Pathology 160, 259 - 269.
47. Roberts, A., Matthews, J. B., Socransky, S. S., Freestone, P. P., Williams, P. H., &, Chapple, I. L., (2005) Stress and the periodontal diseases: growth responses of periodontal bacteria to Escherichia coli stress-associated autoinducer and exogenous Fe. Oral Microbiology and Immunology 20, 147 - 153.
48. Sandros, J., Karlsson, C., Lappin, D. F., Madianos, P. N., Kinane, D. F., &, Papapanou, P. N., (2000) Cytokine responses of oral epithelial cells to Porphyromonas gingivalis infection. Journal of Dental Research 79, 1808 - 1814.
49. Sarada, S., Himadri, P., Mishra, C., Geetali, P., Ram, M. S., &, Ilavazhagan, G., (2008) Role of oxidative stress and NFkB in hypoxia-induced pulmonary edema. Experimental Biology and Medicine (Maywood) 233, 1088 - 1098.
50. Shi, Q., Abbruzzese, J. L., Huang, S., Fidler, I. J., Xiong, Q., &, Xie, K., (1999) Constitutive and inducible interleukin 8 expression by hypoxia and acidosis renders human pancreatic cancer cells more tumorigenic and metastatic. Clinical Cancer Research 5, 3711 - 3721.
51. Shin, J., Ji, S., &, Choi, Y., (2008) Ability of oral bacteria to induce tissue-destructive molecules from human neutrophils. Oral Diseases 14, 327 - 334.
52. Smith, A. J., &, Humphries, S. E., (2009) Cytokine and cytokine receptor gene polymorphisms and their functionality. Cytokine Growth Factor Review 20, 43 - 59.
53. Socransky, S. S., Haffajee, A. D., Cugini, M. A., Smith, C., &, Kent, R. L. Jr., (1998) Microbial complexes in subgingival plaque. Journal of Clinical Periodontology 25, 134 - 144.
54. Stathopoulou, P. G., Benakanakere, M. R., Galicia, J. C., &, Kinane, DF., (2010) Epithelial cell pro-inflammatory cytokine response differs across dental plaque bacterial species. Journal of Clinical Periodontology 37, 24 - 29.
55. Stevens, C. R., Williams, R. B., Farrell, A. J., &, Blake, D. R., (1991) Hypoxia and inflammatory synovitis: observations and speculation. Annals of the Rheumatic Diseases 50, 124 - 132.
56. Sundqvist, G., Figdor, D., Hnström, L., Sörlin, S., ;amp, Sandström, G., (1991) Phagocytosis and virulence of different strains of Porphyromonas gingivalis. Scandinavian Journal of Dental Research 99, 117 - 129.
57. Tonetti, M. S., Imboden, M. A., Gerber, L., Lang, N. P., Laissue, J., &, Mueller, C., (1994) Localized expression of mRNA for phagocyte-specific chemotactic cytokines in human periodontal infections. Infection and Immunity 62, 4005 - 4014.
58. Van Uden, P., Kenneth, N. S., &, Rocha, S., (2008) Regulation of hypoxia-inducible factor-1alpha by NF-kappaB. Biochemical Journal 412, 477 - 484.
59. Vaupel, P., Kallinowski, F., &, Okunieff, P., (1989) Blood flow, oxygen and nutrient supply, and metabolic environment of human tumors: a review. Cancer Research 49, 6449 - 6465.
60. Yavuzyilmaz, E., Yamalik, N., Bulut, S., Ozen, S., Ersoy, F., &, Saat, U., (1995) The gingival crevicular fluid interleukin-1 and tumour necrosis factor-alpha levels in patients with rapidly progressive periodontitis. Australian Dental Journal 40, 46 - 49.
61. Yin, L., &, Dale, B. A., (2007) Activation of protective responses in oral epithelial cells by Fusobacterium nucleatum and human beta-defensin-2. Journal of Medical Microbiology 56, 976 - 987.
62. Zhang, J., Dong, H., Kashket, S., &, Duncan, M. J., (1999) IL-8 degradation by Porphyromonas gingivalis proteases. Microbial Pathogen 26, 275 - 280.