Gingival and periodontal ligament fibroblasts differ in their inflammatory response to viable Porphyromonas gingivalis

Journal of Periodontal Research

Volumn 45, Issue 2, 2010, Pages 262-270

  Scheres, N ^a   Laine, M L ^a   de Vries, T J ^b   Everts, V ^a   van Winkelhoff, A J ^a  

^a Department of Oral Microbiology ^*  (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Fibroblast; Gingiva; Inflammatory response; P. gingivalis; Periodontal ligament; Periodontitis

Indexed keywords

ALKALINE PHOSPHATASE; AUTACOID; COLONY STIMULATING FACTOR 1; CYTOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOPROTEGERIN; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ADOLESCENT; ADULT; ARTICLE; CELL CULTURE; COMPARATIVE STUDY; CYTOLOGY; FEMALE; FIBROBLAST; GINGIVA; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MALE; MICROBIOLOGY; PERIODONTAL LIGAMENT; PORPHYROMONAS GINGIVALIS; T LYMPHOCYTE;

ADOLESCENT; ADULT; ALKALINE PHOSPHATASE; CELLS, CULTURED; CHEMOKINE CCL2; CHEMOKINE CCL5; CYTOKINES; FEMALE; FIBROBLASTS; GINGIVA; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTERLEUKIN-8; LYMPHOCYTE ACTIVATION; MACROPHAGE COLONY-STIMULATING FACTOR; MALE; OSTEOPROTEGERIN; PERIODONTAL LIGAMENT; PORPHYROMONAS GINGIVALIS; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA; YOUNG ADULT;

EID: 77950264849     PISSN: 00223484     EISSN: 16000765     Source Type: Journal    
DOI: 10.1111/j.1600-0765.2009.01229.x     Document Type: Article

References (52)

1. Darveau RP, Tanner A, Page RC. The microbial challenge in periodontitis. Periodontol 2000 1997, 14:12-32.
2. Feng Z, Weinberg A. Role of bacteria in health and disease of periodontal tissues. Periodontol 2000 2006, 40:50-76.
3. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL. Microbial complexes in subgingival plaque. J Clin Periodontol 1998, 25:134-144.
4. Socransky SS, Haffajee AD. Implications of periodontal microbiology for the treatment of periodontal infections. Compend Suppl 1994, 685:688-693.
5. Slots J, Ting M. Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in human periodontal disease: occurrence and treatment. Periodontol 2000 1999, 20:82-121.
6. Van Winkelhoff AJ, Loos BG, Van der Reijden WA, Van der Velden U. Porphyromonas gingivalis, Bacteroides forsythus and other putative periodontal pathogens in subjects with and without periodontal destruction. J Clin Periodontol 2002, 29:1023-1028.
7. O'Brien-Simpson NM, Veith PD, Dashper SG, Reynolds EC. Antigens of bacteria associated with periodontitis. Periodontol 2000 2004, 35:101-134.
8. Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet 2005, 366:1809-1820.
9. Oshiro T, Shiotani A, Shibasaki Y, Sasaki T. Osteoclast induction in periodontal tissue during experimental movement of incisors in osteoprotegerin-deficient mice. Anat Rec 2002, 266:218-225.
10. Berkovitz BK. Periodontal ligament: structural and clinical correlates. Dent Update 2004, 52:54.
11. Beertsen W, McCulloch CA, Sodek J. The periodontal ligament: a unique, multifunctional connective tissue. Periodontol 2000 1997, 13:20-40.
12. Sakata M, Shiba H, Komatsuzawa H. Expression of osteoprotegerin (osteoclastogenesis inhibitory factor) in cultures of human dental mesenchymal cells and epithelial cells. J Bone Miner Res 1999, 14:1486-1492.
13. Nagasawa T, Kobayashi H, Kiji M. LPS-stimulated human gingival fibroblasts inhibit the differentiation of monocytes into osteoclasts through the production of osteoprotegerin. Clin Exp Immunol 2002, 130:338-344.
14. Kanzaki H, Chiba M, Shimizu Y, Mitani H. Dual regulation of osteoclast differentiation by periodontal ligament cells through RANKL stimulation and OPG inhibition. J Dent Res 2001, 80:887-891.
15. Datta HK, Ng WF, Walker JA, Tuck SP, Varanasi SS. The cell biology of bone metabolism. J Clin Pathol 2008, 61:577-587.
16. Fujita T, Iwata T, Shiba H. Identification of marker genes distinguishing human periodontal ligament cells from human mesenchymal stem cells and human gingival fibroblasts. J Periodont Res 2007, 42:283-286.
17. Groeneveld MC, Everts V, Beertsen W. Alkaline phosphatase activity in the periodontal ligament and gingiva of the rat molar: its relation to cementum formation. J Dent Res 1995, 74:1374-1381.
18. Han X, Amar S. Identification of genes differentially expressed in cultured human periodontal ligament fibroblasts vs. human gingival fibroblasts by DNA microarray analysis. J Dent Res 2002, 81:399-405.
19. de Vries TJ, Schoenmaker T, Wattanaroonwong N. Gingival fibroblasts are better at inhibiting osteoclast formation than periodontal ligament fibroblasts. J Cell Biochem 2006, 98:370-382.
20. Hormdee D, Nagasawa T, Kiji M. Protein kinase-A-dependent osteoprotegerin production on interleukin-1 stimulation in human gingival fibroblasts is distinct from periodontal ligament fibroblasts. Clin Exp Immunol 2005, 142:490-497.
21. Yashiro R, Nagasawa T, Kiji M. Transforming growth factor-beta stimulates interleukin-11 production by human periodontal ligament and gingival fibroblasts. J Clin Periodontol 2006, 33:165-171.
22. Girasole G, Passeri G, Jilka RL, Manolagas SC. Interleukin-11: a new cytokine critical for osteoclast development. J Clin Invest 1994, 93:1516-1524.
23. Zhou J, Windsor LJ. Heterogeneity in the collagen-degrading ability of Porphyromonas gingivalis-stimulated human gingival fibroblasts. J Periodont Res 2007, 42:77-84.
24. Yamamoto T, Kita M, Oseko F, Nakamura T, Imanishi J, Kanamura N. Cytokine production in human periodontal ligament cells stimulated with Porphyromonas gingivalis. J Periodont Res 2006, 41:554-559.
25. Wang PL, Ohura K. Porphyromonas gingivalis lipopolysaccharide signaling in gingival fibroblasts-CD14 and Toll-like receptors. Crit Rev Oral Biol Med 2002, 13:132-142.
26. Wang PL, Azuma Y, Shinohara M, Ohura K. Toll-like receptor 4-mediated signal pathway induced by Porphyromonas gingivalis lipopolysaccharide in human gingival fibroblasts. Biochem Biophys Res Commun 2000, 273:1161-1167.
27. Takeshita A, Imai K, Hanazawa S. CpG motifs in Porphyromonas gingivalis DNA stimulate interleukin-6 expression in human gingival fibroblasts. Infect Immun 1999, 67:4340-4345.
28. Belibasakis GN, Bostanci N, Hashim A. Regulation of RANKL and OPG gene expression in human gingival fibroblasts and periodontal ligament cells by Porphyromonas gingivalis: a putative role of the Arg-gingipains. Microb Pathog 2007, 43:46-53.
29. Tabeta K, Yamazaki K, Akashi S. Toll-like receptors confer responsiveness to lipopolysaccharide from Porphyromonas gingivalis in human gingival fibroblasts. Infect Immun 2000, 68:3731-3735.
30. Wang PL, Oido-Mori M, Fujii T. Heterogeneous expression of Toll-like receptor 4 and downregulation of Toll-like receptor 4 expression on human gingival fibroblasts by Porphyromonas gingivalis lipopolysaccharide. Biochem Biophys Res Commun 2001, 288:863-867.
31. Urnowey S, Ansai T, Bitko V, Nakayama K, Takehara T, Barik S. Temporal activation of anti- and pro-apoptotic factors in human gingival fibroblasts infected with the periodontal pathogen, Porphyromonas gingivalis: potential role of bacterial proteases in host signalling. BMC Microbiol 2006, 6:26.
32. Morioka M, Hinode D, Nagata A. Cytotoxicity of Porphyromonas gingivalis toward cultured human gingival fibroblasts. Oral Microbiol Immunol 1993, 8:203-207.
33. Boutaga K, van Winkelhoff AJ, Vandenbroucke-Grauls CM, Savelkoul PH. Comparison of real-time PCR and culture for detection of Porphyromonas gingivalis in subgingival plaque samples. J Clin Microbiol 2003, 41:4950-4954.
34. Kumar A, Takada Y, Boriek AM, Aggarwal BB. Nuclear factor-kappaB: its role in health and disease. J Mol Med 2004, 82:434-448.
35. van Winkelhoff AJ, Appelmelk BJ, Kippuw N, de Graaff J. K-antigens in Porphyromonas gingivalis are associated with virulence. Oral Microbiol Immunol 1993, 8:259-265.
36. Davey ME, Duncan MJ. Enhanced biofilm formation and loss of capsule synthesis: deletion of a putative glycosyltransferase in Porphyromonas gingivalis. J Bacteriol 2006, 188:5510-5523.
37. Laine ML, van Winkelhoff AJ. Virulence of six capsular serotypes of Porphyromonas gingivalis in a mouse model. Oral Microbiol Immunol 1998, 13:322-325.
38. Zhou Q, Desta T, Fenton M, Graves DT, Amar S. Cytokine profiling of macrophages exposed to Porphyromonas gingivalis, its lipopolysaccharide, or its FimA protein. Infect Immun 2005, 73:935-943.
39. Zhou Q, Amar S. Identification of signaling pathways in macrophage exposed to Porphyromonas gingivalis or to its purified cell wall components. J Immunol 2007, 179:7777-7790.
40. Zhou Q, Amar S. Identification of proteins differentially expressed in human monocytes exposed to Porphyromonas gingivalis and its purified components by high-throughput immunoblotting. Infect Immun 2006, 74:1204-1214.
41. Vernal R, Leon R, Herrera D, Garcia-Sanz JA, Silva A, Sanz M. Variability in the response of human dendritic cells stimulated with Porphyromonas gingivalis or Aggregatibacter actinomycetemcomitans. J Periodont Res 2008, 43:689-697.
42. Kusumoto Y, Hirano H, Saitoh K. Human gingival epithelial cells produce chemotactic factors interleukin-8 and monocyte chemoattractant protein-1 after stimulation with Porphyromonas gingivalis via toll-like receptor 2. J Periodontol 2004, 75:370-379.
43. Wada N, Maeda H, Yoshimine Y, Akamine A. Lipopolysaccharide stimulates expression of osteoprotegerin and receptor activator of NF-kappa B ligand in periodontal ligament fibroblasts through the induction of interleukin-1 beta and tumor necrosis factor-alpha. Bone 2004, 35:629-635.
44. Mikolajczyk-Pawlinska J, Travis J, Potempa J. Modulation of interleukin-8 activity by gingipains from Porphyromonas gingivalis: implications for pathogenicity of periodontal disease. FEBS Lett 1998, 440:282-286.
45. Fletcher J, Reddi K, Poole S. Interactions between periodontopathogenic bacteria and cytokines. J Periodont Res 1997, 32:200-205.
46. Fletcher J, Nair S, Poole S, Henderson B, Wilson M. Cytokine degradation by biofilms of Porphyromonas gingivalis. Curr Microbiol 1998, 36:216-219.
47. Bodet C, Chandad F, Grenier D. Modulation of cytokine production by Porphyromonas gingivalis in a macrophage and epithelial cell co-culture model. Microbes Infect 2005, 7:448-456.
48. Calkins CC, Platt K, Potempa J, Travis J. Inactivation of tumor necrosis factor-alpha by proteinases (gingipains) from the periodontal pathogen, Porphyromonas gingivalis. Implications of immune evasion. J Biol Chem 1998, 273:6611-6614.
49. Steffen MJ, Holt SC, Ebersole JL. Porphyromonas gingivalis induction of mediator and cytokine secretion by human gingival fibroblasts. Oral Microbiol Immunol 2000, 15:172-180.
50. Stathopoulou PG, Benakanakere MR, Galicia JC, Kinane DF. The host cytokine response to Porphyromonas gingivalis is modified by gingipains. Oral Microbiol Immunol 2009, 24:11-17.
51. Flavell SJ, Hou TZ, Lax S, Filer AD, Salmon M, Buckley CD. Fibroblasts as novel therapeutic targets in chronic inflammation. Br J Pharmacol 2008, 153(suppl 1):S241-S246.
52. Buckley CD, Pilling D, Lord JM, Akbar AN, Scheel-Toellner D, Salmon M. Fibroblasts regulate the switch from acute resolving to chronic persistent inflammation. Trends Immunol 2001, 22:199-204.