Phospholipase C, p38/MAPK, and NF-κBmediated induction of MIP-3±/CCL20 by Porphyromonas gingivalis

Innate Immunity

Volumn 16, Issue 4, 2010, Pages 226-234

  Dommisch, Henrik ^a,b   Chung, Whasun O ^a   Jepsen, Søren ^b   Hacker, Beth M ^a   Dale, Beverly A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

C C chemokine ligand 20; gingival epithelial cells; mitogen activated protein kinase; nuclear factor kappa B; phospholipase C

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C;

ARTICLE; CONTROLLED STUDY; EPITHELIUM CELL; GENE EXPRESSION; GENE INDUCTION; HUMAN; HUMAN CELL; INNATE IMMUNITY; KERATINOCYTE; NONHUMAN; PORPHYROMONAS GINGIVALIS; SIGNAL TRANSDUCTION;

CHEMOKINE CCL20; EPITHELIAL CELLS; GINGIVA; HUMANS; INDICATORS AND REAGENTS; INTERLEUKIN-6; NF-KAPPA B; NFATC TRANSCRIPTION FACTORS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; PORPHYROMONAS GINGIVALIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; TRANSCRIPTION FACTOR RELA; TRANSFECTION; TYPE C PHOSPHOLIPASES;

PORPHYROMONAS GINGIVALIS;

EID: 77955256741     PISSN: 17534259     EISSN: 17534267     Source Type: Journal    
DOI: 10.1177/1753425909339237     Document Type: Article

References (42)

1. Dale BA Periodontal epithelium: a newly recognized role in health and disease. Periodontol 2000 2002 ; 30: 70-78.
2. Chung WO, Dommisch H., Yin L., Dale BA Expression of defensins in gingiva and their role in periodontal health and disease. Curr Pharm Des 2007 ; 13: 3073-3083.
3. Lehrer RI Primate defensins. Nat Rev Microbiol 2004 ; 2: 727-738.
4. Yang D., Chen Q., Hoover DM et al. Many chemokines including CCL20/MIP-3alpha display antimicrobial activity. J Leukoc Biol 2003 ; 74: 448-455.
5. Yang D., Chertov O., Bykovskaia SN et al. Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 1999 ; 286: 525-528.
6. Yang D., Chen Q., Chertov O., Oppenheim JJ Human neutrophil defensins selectively chemoattract naive T and immature dendritic cells. J Leukoc Biol 2000 ; 68: 9-14.
7. Hoover DM, Boulegue C., Yang D. et al. The structure of human macrophage inflammatory protein-3alpha /CCL20. Linking antimicrobial and CC chemokine receptor-6-binding activities with human beta-defensins. J Biol Chem 2002 ; 277: 37647-37654.
8. Schutyser E., Struyf S., Van Damme J. The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev 2003 ; 14: 409-426.
9. Yang D., Biragyn A., Kwak LW, Oppenheim JJ Mammalian defensins in immunity: more than just microbicidal. Trends Immunol 2002 ; 23: 291-296.
10. Socransky SS, Haffajee AD, Cugini MA, Smith C., Kent Jr RL Microbial complexes in subgingival plaque. J Clin Periodontol 1998 ; 25: 134-144.
11. Lamont RJ, Jenkinson HF Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev 1998 ; 62: 1244-1263.
12. Holt SC, Kesavalu L., Walker S., Genco CA Virulence factors of Porphyromonas gingivalis. Periodontol 2000 1999 ; 20: 168-238.
13. Sandros J., Papapanou PN, Nannmark U., Dahlen G. Porphyromonas gingivalis invades human pocket epithelium in vitro. J Periodontal Res 1994 ; 29: 62-69.
14. Rudney JD, Chen R., Sedgewick GJ Intracellular Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in buccal epithelial cells collected from human subjects. Infect Immun 2001 ; 69: 2700-2707.
15. Lamont RJ, Chan A., Belton CM, Izutsu KT, Vasel D., Weinberg A. Porphyromonas gingivalis invasion of gingival epithelial cells. Infect Immun 1995 ; 63: 3878-3885.
16. Hintermann E., Haake SK, Christen U., Sharabi A., Quaranta V. Discrete proteolysis of focal contact and adherens junction components in Porphyromonas gingivalis-infected oral keratinocytes: a strategy for cell adhesion and migration disabling. Infect Immun 2002 ; 70: 5846-5856.
17. Belton CM, Izutsu KT, Goodwin PC, Park Y., Lamont RJ Fluorescence image analysis of the association between Porphyromonas gingivalis and gingival epithelial cells. Cell Microbiol 1999 ; 1: 215-223.
18. Dommisch H., Chung WO, Rohani MG et al. Protease-activated receptor 2 mediates human beta-defensin 2 and CC chemokine ligand 20 mRNA expression in response to proteases secreted by Porphyromonas gingivalis. Infect Immun 2007 ; 75: 4326-4333.
19. Chung WO, Dale BA Innate immune response of oral and foreskin keratinocytes: utilization of different signaling pathways by various bacterial species. Infect Immun 2004 ; 72: 352-358.
20. Shpacovitch VM, Brzoska T., Buddenkotte J. et al. Agonists of proteinase-activated receptor 2 induce cytokine release and activation of nuclear transcription factor kappaB in human dermal microvascular endothelial cells. J Invest Dermatol 2002 ; 118: 380-385.
21. Ye RD Regulation of nuclear factor kappaB activation by G-protein-coupled receptors. J Leukoc Biol 2001 ; 70: 839-848.
22. Uehara A., Sugawara Y., Sasano T., Takada H., Sugawara S. Proinflammatory cytokines induce proteinase 3 as membrane-bound and secretory forms in human oral epithelial cells and antibodies to proteinase 3 activate the cells through protease-activated receptor-2. J Immunol 2004 ; 173: 4179-4189.
23. Dickson MA, Hahn WC, Ino Y. et al. Human keratinocytes that express hTERT and also bypass a p16(INK4a)-enforced mechanism that limits life span become immortal yet retain normal growth and differentiation characteristics. Mol Cell Biol 2000 ; 20: 1436-1447.
24. Fujimura S., Hirai K., Shibata Y., Nakayama K., Nakamura T. Comparative properties of envelope-associated argininegingipains and lysine-gingipain of Porphyromonas gingivalis. FEMS Microbiol Lett 1998 ; 163: 173-179.
25. Holzhausen M., Spolidorio LC, Ellen RP et al. Protease-activated receptor-2 activation: a major role in the pathogenesis of Porphyromonas gingivalis infection. Am J Pathol 2006 ; 168: 1189-1199.
26. Chung WO, Hansen SR, Rao D., Dale BA Protease-activated receptor signaling increases epithelial antimicrobial peptide expression. J Immunol 2004 ; 173: 5165-5170.
27. Pfaffl MW A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001 ; 29: e45.
28. Desloges N., Schubert C., Wolff MH, Rahaus M. Varicella-zoster virus infection induces the secretion of interleukin-8. Med Microbiol Immunol 2008 ; 197: 277-284.
29. Wang Y., Yang J., Gao Y., Dong LJ, Liu S., Yao Z. Reciprocal regulation of 5-alpha-dihydrotestosterone, interleukin-6 and interleukin-8 during proliferation of epithelial ovarian carcinoma. Cancer Biol Ther 2007 ; 6: 864-871.
30. Macfarlane SR, Sloss CM, Cameron P., Kanke T., McKenzie RC, Plevin R. The role of intracellular Ca2+ in the regulation of proteinase-activated receptor-2 mediated nuclear factor kappa B signalling in keratinocytes. Br J Pharmacol 2005 ; 145: 535-544.
31. Yoshida N., Katada K., Handa O. et al. Interleukin-8 production via protease-activated receptor 2 in human esophageal epithelial cells. Int J Mol Med 2007 ; 19: 335-340.
32. Goon Goh F., Sloss CM, Cunningham MR, Nilsson M., Cadalbert L., Plevin R. G-protein-dependent and -independent pathways regulate proteinase-activated receptor-2 mediated p65 NFkappaB serine 536 phosphorylation in human keratinocytes. Cell Signal 2008 ; 20: 1267-1274.
33. Vliagoftis H., Schwingshackl A., Milne CD et al. Proteinase-activated receptor-2-mediated matrix metalloproteinase-9 release from airway epithelial cells. J Allergy Clin Immunol 2000 ; 106: 537-545.
34. Bretschneider E., Kaufmann R., Braun M. et al. Evidence for proteinase-activated receptor-2 (PAR-2)-mediated mitogenesis in coronary artery smooth muscle cells. Br J Pharmacol 1999 ; 126: 1735-1740.
35. Foster N., Cheetham J., Taylor JJ, Preshaw PM VIP inhibits Porphyromonas gingivalis LPS-induced immune responses in human monocytes. J Dent Res 2005 ; 84: 999-1004.
36. Brozovic S., Sahoo R., Barve S. et al. Porphyromonas gingivalis enhances FasL expression via up-regulation of NFkappaBmediated gene transcription and induces apoptotic cell death in human gingival epithelial cells. Microbiology 2006 ; 152: 797-806.
37. Inomata M., Into T., Ishihara Y., Nakashima M., Noguchi T., Matsushita K. Arginine-specific gingipain A from Porphyromonas gingivalis induces Weibel-Palade body exocytosis and enhanced activation of vascular endothelial cells through protease-activated receptors. Microbes Infect 2007 ; 9: 1500-1506.
38. Yilmaz O., Jungas T., Verbeke P., Ojcius DM Activation of the phosphatidylinositol 3-kinase/Akt pathway contributes to survival of primary epithelial cells infected with the periodontal pathogen Porphyromonas gingivalis. Infect Immun 2004 ; 72: 3743-3751.
39. Duits LA, Ravensbergen B., Rademaker M., Hiemstra PS, Nibbering PH Expression of beta-defensin 1 and 2 mRNA by human monocytes, macrophages and dendritic cells. Immunology 2002 ; 106: 517-525.
40. Biragyn A., Ruffini PA, Leifer CA et al. Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2. Science 2002 ; 298: 1025-1029.
41. Marcet B., Horckmans M., Libert F., Hassid S., Boeynaems JM, Communi D. Extracellular nucleotides regulate CCL20 release from human primary airway epithelial cells, monocytes and monocyte-derived dendritic cells. J Cell Physiol 2007 ; 211: 716-727.
42. Chung WO, Dale BA Differential utilization of nuclear factorkappaB signaling pathways for gingival epithelial cell responses to oral commensal and pathogenic bacteria. Oral Microbiol Immunol 2008 ; 23: 119-126.