Porphyromonas gingivalis LPS inhibits osteoblastic differentiation and promotes pro-inflammatory cytokine production in human periodontal ligament stem cells

Archives of Oral Biology

Volumn 59, Issue 2, 2014, Pages 167-175

  Kato, Hirohito ^a   Taguchi, Yoichiro ^a   Tominaga, Kazuya ^a   Umeda, Makoto ^a   Tanaka, Akio ^a  

^a OSAKA DENTAL UNIVERSITY   (Japan)

Author keywords

Cell differentiation; Cytokines; Lipopolysaccharides; Osteoblasts; Periodontal ligament; Stem cells

Indexed keywords

ALKALINE PHOSPHATASE; COLLAGEN; CYTOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; OSTEOCALCIN;

ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECT; HUMAN; MESENCHYMAL STROMA CELL; METABOLISM; MOLAR TOOTH; OSTEOBLAST; PERIODONTAL LIGAMENT; PORPHYROMONAS GINGIVALIS; STAINING; STEM CELL;

CELL DIFFERENTIATION; CYTOKINES; LIPOPOLYSACCHARIDES; OSTEOBLASTS; PERIODONTAL LIGAMENT; STEM CELLS;

ALKALINE PHOSPHATASE; CELL PROLIFERATION; COLLAGEN; HUMANS; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTERLEUKIN-8; LIPOPOLYSACCHARIDES; MESENCHYMAL STROMAL CELLS; MOLAR, THIRD; OSTEOBLASTS; OSTEOCALCIN; PERIODONTAL LIGAMENT; PORPHYROMONAS GINGIVALIS; STAINING AND LABELING;

EID: 84890065640     PISSN: 00039969     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.archoralbio.2013.11.008     Document Type: Article

References (50)

1. A. Nanci, and D.D. Bosshardt Structure of periodontal tissues in health and disease Periodontology 2000 40 1 2006 11 28 (Pubitemid 43434239)
2. B.J. Paster, I. Olsen, J.A. Aas, and F.E. Dewhirst The breadth of bacterial diversity in the human periodontal pocket and other oral sites Periodontology 2000 42 1 2006 80 87 (Pubitemid 44286048)
3. B.L. Pihlstrom, B.S. Michalowicz, and N.W. Johnson Periodontal Dis Lancet 366 2005 1809 1820
4. G.R. Persson Immune responses and vaccination against periodontal infections J Clin Periodontol 32 6 2005 39 53 (Pubitemid 41391055)
5. F.C. Nichols Distribution of 3-hydroxy iC17:0 in subgingival plaque and gingival tissue samples: relationship to adult periodontitis Infect Immun 62 9 1994 3753 3760
6. F. Nichols, and B. Maraj Relationship between hydroxy fatty acids and prostaglandin E2 in gingival tissue Infect Immun 66 12 1998 5805 5811 (Pubitemid 28531838)
7. Y. Jiang, C.K. Mehta, T.Y. Hsu, and F.F. Alsulaimani Bacteria induce osteoclastogenesis via an osteoblast-independent pathway Infect Immun 70 6 2002 3143 3148 (Pubitemid 34564177)
8. T. Nakashima, Y. Kobayashi, S. Yamasaki, A. Kawakami, K. Eguchi, and H. Sasaki Protein expression and functional difference of membrane-bound and soluble receptor activator of NF-kappaB ligand: modulation of the expression by osteotropic factors and cytokines Biochem Biophys Res Commun 7 3 2000 768 775
9. D.T. Graves, T. Oates, and G.P. Garlet Review of osteoimmunology and the host response in endodontic and periodontal lesions J Oral Microbiol 3 2011 1 15
10. F.J. Hughes, M. Ghuman, and A. Talal Periodontal regeneration: a challenge for the tissue engineer? Proc Inst Mech Eng H 224 12 2010 1345 1358
11. P.R. Garant Collagen resorption by fibroblasts. A theory of fibroblastic maintenance of the periodontal ligament J Periodontol 47 7 1976 380 390
12. R.M. Nohutcu, L.K. McCauley, A.J. Koh, and M.J. Somerman Expression of extracellular matrix proteins in human periodontal ligament cells during mineralization in vitro J Periodontol 68 4 1997 320 327 (Pubitemid 127524519)
13. L.T. Hou, C.M. Liu, J.Y. Lei, M.Y. Wong, and J.K. Chen Biological effects of cementum and bone extracts on human periodontal fibroblasts J Periodontol 71 7 2000 1100 1109
14. D.G. Lin, D.J. Kenny, E.J. Barrett, P. Lekic, and C.A. McCulloch Storage conditions of avulsed teeth affect the phenotype of cultured human periodontal ligament cells J Periodontal Res 35 1 2000 42 50
15. K. Nagatomo, M. Komaki, I. Sekiya, Y. Sakaguchi, K. Noguchi, and S. Oda Stem cell properties of human periodontal ligament cells J Periodontal Res 41 4 2006 303 310 (Pubitemid 44392300)
16. B.M. Seo, M. Miura, S. Gronthos, P.M. Bartold, S. Batouli, and J. Brahim Investigation of multipotent postnatal stem cells from human periodontal ligament Lancet 364 9429 2004 149 155 (Pubitemid 38891686)
17. J.C. Park, J.M. Kim, I.H. Jung, J.C. Kim, S.H. Choi, and K.S. Cho Isolation and characterization of human periodontal ligament (PDL) stem cells (PDLSCs) from the inflamed PDL tissue: in vitro and in vivo evaluations J Clin Periodontol 38 8 2011 721 731
18. Y. Liu, Y. Zheng, G. Ding, D. Fang, C. Zhang, and P.M. Bartold Periodontal ligament stem cell-mediated treatment for periodontitis in miniature swine Stem Cells 26 4 2008 1065 1073
19. Y. Tsumanuma, T. Iwata, K. Washio, T. Yoshida, A. Yamada, and R. Takagi Comparison of different tissue-derived stem cell sheets for periodontal regeneration in a canine 1-wall defect model Biomaterials 32 25 2011 5819 5825
20. W. Sonoyama, Y. Liu, D. Fang, T. Yamaza, B.M. Seo, and C. Zhang Mesenchymal stem cell-mediated functional tooth regeneration in swine PLoS One 20 1 2006 e79
21. S. Gronthos, K. Mrozik, S. Shi, and P.M. Bartold Ovine periodontal ligament stem cells: isolation, characterization, and differentiation potential Calcif Tissue Int 79 2006 310 317 (Pubitemid 44900154)
22. H. Kato, N. Katayama, Y. Taguchi, K. Tominaga, M. Umeda, and A. Tanaka A Synthetic oligopeptide derived from enamel matrix derivative promotes the differentiation of human periodontal ligament stem cells into osteoblast-like cells with increased mineralization J Periodontol 84 10 2013 1476 1483
23. E.J. Gang, D. Bosnakovski, C.A. Figueiredo, J.W. Visser, and R.C. Perlingeiro SSEA-4 identifies mesenchymal stem cells from bone marrow Blood 109 4 2007 1743 1751 (Pubitemid 46239610)
24. H. Fukushima, N. Kawanabe, S. Murata, Y. Ishihara, T. Yanagita, and T.A. Balam SSEA-4 is a marker of human deciduous periodontal ligament stem cells J Dent Res 91 10 2012 955 960
25. C.O. Morsczeck, J. Dress, and M. Gosau Lipopolysaccharide from Escherichia coli but not from Porphyromonas gingivalis induce pro-inflammatory cytokines and alkaline phosphatase in dental follicle cells Arch Oral Biol 57 12 2012 1595 1601
26. Y. Yamaji, T. Kubota, K. Sasaguri, S. Sato, Y. Suzuki, and H. Kumada Inflammatory cytokine gene expression in human periodontal ligament fibroblasts stimulated with bacterial lipopolysaccharides Infect Immun 63 9 1995 3576 3581
27. A. Takemura, N. Matsuda, S. Kimura, T. Fujiwara, I. Nakagawa, and S. Hamada Porphyromonas gingivalis lipopolysaccharide modulates the responsiveness of human periodontal ligament fibroblasts to platelet-derived growth factor J Periodontal Res 33 7 1998 400 407 (Pubitemid 128527123)
28. Z.J. Wang, F.M. Zhang, L.S. Wang, Y.W. Yao, Q. Zhao, and X. Gao Lipopolysaccharides can protect mesenchymal stem cells (MSCs) from oxidative stress-induced apoptosis and enhance proliferation of MSCs via Toll-like receptor(TLR)-4 and PI3K/Akt Cell Biol Int 33 6 2009 665 674
29. N. Wada, D. Menicanin, S. Shi, P.M. Bartold, and S. Gronthos Immunomodulatory properties of human periodontal ligament stem cells J Cell Physiol 219 3 2009 667 676
30. D. Jönsson, D. Nebel, G. Bratthall, and B.O. Nilsson The human periodontal ligament cell: a fibroblast-like cell acting as an immune cell J Periodontal Res 46 2 2011 153 157
31. T. Mattern, A. Thanhäuser, N. Reiling, K.M. Toellner, M. Duchrow, and S. Kusumoto Endotoxin and lipid A stimulate proliferation of human T cells in the presence of autologous monocytes J Immunol 153 7 1994 2996 3004 (Pubitemid 24292525)
32. H.C. Blair, M. Zaidi, and P.H. Schlesinger Mechanisms balancing skeletal matrix synthesis and degradation Biochem J 364 2 2002 329 341 (Pubitemid 34620792)
33. T. Seo, S. Cha, T.I. Kim, J.S. Lee, and K.M. Woo Porphyromonas gingivalis-derived lipopolysaccharide-mediated activation of MAPK signaling regulates inflammatory response and differentiation in human periodontal ligament fibroblasts J Microbiol 50 2 2012 311 319
34. Y.H. Wang, J. Jiang, Q. Zhu, A.Z. AlAnezi, R.B. Clark, and X. Jiang Porphyromonas gingivalis lipids inhibit osteoblastic differentiation and function Infect Immun 78 9 2010 3726 3735
35. M. Weinreb, D. Shinar, and G.A. Rodan Different pattern of alkaline phosphatase, osteopontin, and osteocalcin expression in developing rat bone visualized by in situ hybridization J Bone Miner Res 5 8 1990 831 842 (Pubitemid 20294767)
36. J.E. Aubin, F. Liu, L. Malaval, and A.K. Gupta Osteoblast and chondroblast differentiation Bone 17 2 Suppl. 1995 77S 83S
37. K. Nomiyama, C. Kitamura, T. Tsujisawa, M. Nagayoshi, T. Morotomi, and M. Terashita Effects of lipopolysaccharide on newly established rat dental pulp-derived cell line with odontoblastic properties J Endod 33 10 2007 1187 1191
38. Q. Xing, Q. Ye, M. Fan, Y. Zhou, Q. Xu, and A. Sandham Porphyromonas gingivalis lipopolysaccharide inhibits the osteoblastic differentiation of preosteoblasts by activating Notch1 signaling J Cell Physiol 225 1 2010 106 114
39. T. Ikeda, S. Nomura, A. Yamaguchi, T. Suda, and S. Yoshiki In situ hybridization of bone matrix proteins in undecalcified adult rat bone sections J Histochem Cytochem 40 8 1992 1079 1088
40. K. Bandow, A. Maeda, K. Kakimoto, J. Kusuyama, M. Shamoto, and T. Ohnishi Molecular mechanisms of the inhibitory effect of lipopolysaccharide (LPS) on osteoblast differentiation Biochem Biophys Res Commun 402 4 2010 755 761
41. H. Kadono, J. Kido, M. Kataoka, N. Yamauchi, and T. Nagata Inhibition of osteoblastic cell differentiation by lipopolysaccharide extract from Porphyromonas gingivalis Infect Immun 67 6 1999 2841 2846 (Pubitemid 29244698)
42. A.A. Bom-van Noorloos, J.W. van der Meer, J.S. van de Gevel, E. Schepens, T.J. van Steenbergen, and E.H. Burger Bacteroides gingivalis stimulates bone resorption via interleukin-1 production by mononuclear cells. The relative role for B. gingivalis endotoxin J Clin Periodontol 17 7 Pt 1 1990 409 413 (Pubitemid 20231065)
43. Y. Iino, and R.M. Hopps The bone-resorbing activities in tissue culture of lipopolysaccharides from the bacteria Actinobacillus actinomycetemcomitans, Bacteroides gingivalis and Capnocytophaga ochracea isolated from human mouths Arch Oral Biol 29 1 1984 59 63
44. Z. Diya, C. Lili, L. Shenglai, G. Zhiyuan, and Y. Jie Lipopolysaccharide (LPS) of Porphyromonas gingivalis induces IL-1beta, TNF-alpha and IL-6 production by THP-1 cells in a way different from that of Escherichia coli LPS Innate Immun 14 2 2008 99 107
45. K.J. Jones, S. Ekhlassi, D. Montufar-Solis, J.R. Klein, and J.S. Schaefer Differential cytokine patterns in mouse macrophages and gingival fibroblasts after stimulation with Porphyromonas gingivalis or Escherichia coli lipopolysaccharide J Periodontol 81 12 2010 1850 1857
46. T.D. Herath, Y. Wang, C.J. Seneviratne, Q. Lu, R.P. Darveau, and C.Y. Wang Porphyromonas gingivalis lipopolysaccharide lipid A heterogeneity differentially modulates the expression of IL-6 and IL-8 in human gingival fibroblasts J Clin Periodontol 38 8 2011 694 701
47. Y. Sun, R. Shu, C.L. Li, and M.Z. Zhang Gram-negative periodontal bacteria induce the activation of Toll-like receptors 2 and 4, and cytokine production in human periodontal ligament cells J Periodontol 81 10 2010 1488 1496
48. D. Nebel, J. Arvidsson, J. Lillqvist, A. Holm, and B.O. Nilsson Differential effects of LPS from Escherichia coli and Porphyromonas gingivalis on IL-6 production in human periodontal ligament cells Acta Odontol Scand 71 3-4 2013 892 898
49. O. Uehara, Y. Abiko, M. Saitoh, H. Miyakawa, and F. Nakazawa Lipopolysaccharide extracted from Porphyromonas gingivalis induces DNA hypermethylation of runt-related transcription factor 2 in human periodontal fibroblasts J Microbiol Immunol Infect 2013 (in press)
50. H.C. Roberts, R. Moseley, A.J. Sloan, S.J. Youde, and R.J. Waddington Lipopolysaccharide alters decorin and biglycan synthesis in rat alveolar bone osteoblasts: consequences for bone repair during periodontal disease Eur J Oral Sci 116 3 2008 207 216