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Clinical and Developmental Immunology
Volume 2013, Article ID 503754, 7 pages
http://dx.doi.org/10.1155/2013/503754
Review Article

Periodontal Disease: Linking the Primary Inflammation to Bone Loss

Department of Basic Medical Sciences, Neurosciences and Sense Organs, Section of Human Anatomy and Histology “R. Amprino”, University of Bari, Piazza Giulio Cesare 11, 70124 Bari, Italy

Received 1 March 2013; Accepted 6 May 2013

Academic Editor: Giorgio Mori

Copyright © 2013 Adriana Di Benedetto et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. T. Graves and D. Cochran, “The contribution of interleukin-1 and tumor necrosis factor to periodontal tissue destruction,” Journal of Periodontology, vol. 74, no. 3, pp. 391–401, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. G. P. Garlet, C. R. Cardoso, T. A. Silva et al., “Cytokine pattern determines the progression of experimental periodontal disease induced by Actinobacillus actinomycetemcomitans through the modulation of MMPs, RANKL, and their physiological inhibitors,” Oral Microbiology and Immunology, vol. 21, no. 1, pp. 12–20, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. G. K. Hansson and K. Edfeldt, “Toll to be paid at the gateway to the vessel wall,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 6, pp. 1085–1087, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. F. Hayashi, T. K. Means, and A. D. Luster, “Toll-like receptors stimulate human neutrophil function,” Blood, vol. 102, no. 7, pp. 2660–2669, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Benakanakere and D. F. Kinane, “Innate cellular responses to the periodontal biofilm,” Frontiers of Oral Biology, vol. 1, pp. 41–55, 2012. View at Google Scholar
  6. N. Bostanci and G. N. Belibasakis, “Porphyromonas gingivalis: an invasive and evasive opportunistic oral pathogen,” FEMS Microbiology Letters, vol. 333, no. 1, pp. 1–9, 2012. View at Publisher · View at Google Scholar
  7. R. Mahanonda and S. Pichyangkul, “Toll-like receptors and their role in periodontal health and disease,” Periodontology 2000, vol. 43, no. 1, pp. 41–55, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Hayashi, C. V. Gudino, F. C. Gibson III, and C. A. Genco, “Pathogen-induced inflammation at sites distant from oral infection: bacterial persistence and induction of cell-specific innate immune inflammatory pathways,” Molecular Oral Microbiology, vol. 25, no. 5, pp. 305–316, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Hans and V. M. Hans, “Toll-like receptors and their dual role in periodontitis: a review,” Journal of Oral Science, vol. 53, no. 3, pp. 263–271, 2011. View at Publisher · View at Google Scholar
  10. G. P. Garlet, “Destructive and protective roles of cytokines in periodontitis: a re-appraisal from host defense and tissue destruction viewpoints,” Journal of Dental Research, vol. 89, no. 12, pp. 1349–1363, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. D. L. Cochran, “Inflammation and bone loss in periodontal disease,” Journal of Periodontology, vol. 79, no. 8, pp. 1569–1576, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. J. B. Payne and L. M. Golub, “Using tetracyclines to treat osteoporotic/osteopenic bone loss: from the basic science laboratory to the clinic,” Pharmacological Research, vol. 63, no. 2, pp. 121–129, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. W. Han, W. Shi, G. T. J. Huang et al., “Interactions between periodontal bacteria and human oral epithelial cells: fusobacterium nucleatum adheres to and invades epithelial cells,” Infection and Immunity, vol. 68, no. 6, pp. 3140–3146, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. A. S. Trevani, A. Chorny, G. Salamone et al., “Bacterial DNA activates human neutrophils by a CpG-independent pathway,” European Journal of Immunology, vol. 33, no. 11, pp. 3164–3174, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Nanbara, N. Wara-Aswapati, T. Nagasawa et al., “Modulation of Wnt5a expression by periodontopathic bacteria,” PLoS ONE, vol. 7, no. 4, Article ID e34434, 2012. View at Publisher · View at Google Scholar
  16. J. G. Tew, M. E. El Shikh, R. M. El Sayed, and H. A. Schenkein, “Dendritic cells, antibodies reactive with oxLDL, and inflammation,” Journal of Dental Research, vol. 91, no. 1, pp. 8–16, 2012. View at Publisher · View at Google Scholar
  17. S. Ekhlassi, L. Y. Scruggs, T. Garza, D. Montufar-Solis, A. J. Moretti, and J. R. Klein, “Porphyromonas gingivalis lipopolysaccharide induces tumor necrosis factor-α and interleukin-6 secretion, and CCL25 gene expression, in mouse primary gingival cell lines: interleukin-6-driven activation of CCL2,” Journal of Periodontal Research, vol. 43, no. 4, pp. 431–439, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. T. Ara, K. Kurata, K. Hirai et al., “Human gingival fibroblasts are critical in sustaining inflammation in periodontal disease,” Journal of Periodontal Research, vol. 44, no. 1, pp. 21–27, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. A. C. F. Morandini, C. R. Sipert, T. H. Gasparoto et al., “Differential production of macrophage inflammatory protein-1α, stromal-derived factor-1, and IL-6 by human cultured periodontal ligament and gingival fibroblasts challenged with lipopolysaccharide from P. gingivalis,” Journal of Periodontology, vol. 81, no. 2, pp. 310–317, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. Y. C. Chang, S. F. Yang, C. C. Lai, J. Y. Liu, and Y. S. Hsieh, “Regulation of matrix metalloproteinase production by cytokines, pharmacological agents and periodontal pathogens in human periodontal ligament fibroblast cultures,” Journal of Periodontal Research, vol. 37, no. 3, pp. 196–203, 2002. View at Google Scholar · View at Scopus
  21. M. Ohshima, Y. Yamaguchi, K. Otsuka, M. Sato, and M. Ishikawa, “Laminin expression by human periodontal ligament fibroblasts,” Connective Tissue Research, vol. 47, no. 3, pp. 149–156, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. N. Scheres, M. L. Laine, T. J. de Vries, V. Everts, and A. J. van Winkelhoff, “Gingival and periodontal ligament fibroblasts differ in their inflammatory response to viable Porphyromonas gingivalis,” Journal of Periodontal Research, vol. 45, no. 2, pp. 262–270, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. I. H. Jung, D. E. Lee, J. H. Yun et al., “Anti-inflammatory effect of (-)-epigallocatechin-3-gallate on Porphyromonas gingivalis lipopolysaccharide-stimulated fibroblasts and stem cells derived from human periodontal ligament,” Journal of Periodontal & Implant Science, vol. 42, no. 6, pp. 185–195, 2012. View at Publisher · View at Google Scholar
  24. W. Zhang, E. B. Swearingen, J. Ju, T. Rigney, and G. D. Tribble, “Porphyromonas gingivalis invades osteoblasts and inhibits bone formation,” Microbes and Infection, vol. 12, no. 11, pp. 838–845, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. W. Zhang, J. Ju, T. Rigney, and G. Tribble, “Integrin alpha5beta1-fimbriae binding and actin rearrangement are essential for Porphyromonas gingivalis invasion of osteoblasts and subsequent activation of the JNK pathway,” BMC Microbiology, vol. 13, no. 1, article 5, 2013. View at Google Scholar
  26. M. Kim, H. K. Jun, B. K. Choi, J. H. Cha, and Y. J. Yoo, “Td92, an outer membrane protein of Treponema denticola, induces osteoclastogenesis via prostaglandin-E2-mediated RANKL/osteoprotegerin regulation,” Journal of Periodontal Research, vol. 45, no. 6, pp. 772–779, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Tang, F. Sun, X. Li, Y. Zhou, S. Yin, and X. Zhou, “Porphyromonas endodontalis lipopolysaccharides induce RANKL by mouse osteoblast in a way different from that of Escherichia coli lipopolysaccharide,” Journal of Endodontics, vol. 37, no. 12, pp. 1653–1658, 2011. View at Publisher · View at Google Scholar
  28. C. W. Cutler and R. Jotwani, “Antigen-presentation and the role of dendritic cells in periodontitis,” Periodontology 2000, vol. 35, pp. 135–157, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. K. M. Murphy and S. L. Reiner, “The lineage decisions of helper T cells,” Nature Reviews Immunology, vol. 2, no. 12, pp. 933–944, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. V. Appay, R. A. W. van Lier, F. Sallusto, and M. Roederer, “Phenotype and function of human T lymphocyte subsets: consensus and issues,” Cytometry A, vol. 73, no. 11, pp. 975–983, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. C. T. Weaver and R. D. Hatton, “Interplay between the TH17 and TReg cell lineages: a (co-)evolutionary perspective,” Nature Reviews Immunology, vol. 9, no. 12, pp. 883–889, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. J. M. Berthelot and B. Le Goff, “Rheumatoid arthritis and periodontal disease,” Joint Bone Spine, vol. 77, no. 6, pp. 537–541, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. E. J. Ohlrich, M. P. Cullinan, and G. J. Seymour, “The immunopathogenesis of periodontal disease,” Australian Dental Journal, vol. 54, supplement 1, pp. S2–S10, 2009. View at Google Scholar · View at Scopus
  34. C. Matsumoto, T. Oda, S. Yokoyama et al., “Toll-like receptor 2 heterodimers, TLR2/6 and TLR2/1 induce prostaglandin E production by osteoblasts, osteoclast formation and inflammatory periodontitis,” Biochemical and Biophysical Research Communications, vol. 428, no. 1, pp. 110–115, 2012. View at Publisher · View at Google Scholar
  35. U. H. Lerner, “Inflammation-induced bone remodeling in periodontal disease and the influence of post-menopausal osteoporosis,” Journal of Dental Research, vol. 85, no. 7, pp. 596–607, 2006. View at Google Scholar · View at Scopus
  36. Y. D. Park, Y. S. Kim, Y. M. Jung et al., “Porphyromonas gingivalis lipopolysaccharide regulates interleukin (IL)-17 and IL-23 expression via SIRT1 modulation in human periodontal ligament cells,” Cytokine, vol. 60, no. 1, pp. 284–293, 2012. View at Publisher · View at Google Scholar
  37. D. Liu, J. K. Xu, L. Figliomeni et al., “Expression of RANKL and OPG mRNA in periodontal disease: possible involvement in bone destruction,” International Journal of Molecular Medicine, vol. 11, no. 1, pp. 17–21, 2003. View at Google Scholar · View at Scopus
  38. H. K. Lu, Y. L. Chen, H. C. Chang, C. L. Li, and M. Y. P. Kuo, “Identification of the osteoprotegerin/receptor activator of nuclear factor-kappa B ligand system in gingival crevicular fluid and tissue of patients with chronic periodontitis,” Journal of Periodontal Research, vol. 41, no. 4, pp. 354–360, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. G. Brunetti, S. Colucci, P. Pignataro et al., “T cells support osteoclastogenesis in an in vitro model derived from human periodontitis patients,” Journal of Periodontology, vol. 76, no. 10, pp. 1675–1680, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. G. N. Belibasakis and N. Bostanci, “The RANKL-OPG system in clinical periodontology,” Journal of Clinical Periodontology, vol. 39, no. 3, pp. 239–248, 2012. View at Publisher · View at Google Scholar
  41. X. Han, X. Lin, A. R. Seliger, J. Eastcott, T. Kawai, and M. A. Taubman, “Expression of receptor activator of nuclear factor-κB ligand by B cells in response to oral bacteria,” Oral Microbiology and Immunology, vol. 24, no. 3, pp. 190–196, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. T. Kawai, T. Matsuyama, Y. Hosokawa et al., “B and T lymphocytes are the primary sources of RANKL in the bone resorptive lesion of periodontal disease,” American Journal of Pathology, vol. 169, no. 3, pp. 987–998, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Yamaguchi, T. Ukai, T. Kaneko et al., “T cells are able to promote lipopolysaccharide-induced bone resorption in mice in the absence of B cells,” Journal of Periodontal Research, vol. 43, no. 5, pp. 549–555, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Crotti, M. D. Smith, R. Hirsch et al., “Receptor activator NF κB ligand (RANKL) and osteoprotegerin (OPG) protein expression in periodontitis,” Journal of Periodontal Research, vol. 38, no. 4, pp. 380–387, 2003. View at Google Scholar · View at Scopus
  45. A. Yarilina, K. Xu, J. Chen, and L. B. Ivashkiv, “TNF activates calcium-nuclear factor of activated T cells (NFAT)c1 signaling pathways in human macrophages,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 4, pp. 1573–1578, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. D. Graves, “Cytokines that promote periodontal tissue destruction,” Journal of Periodontology, vol. 79, no. 8, pp. 1585–1591, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. C. T. Ritchlin, S. A. Haas-Smith, P. Li, D. G. Hicks, and E. M. Schwarz, “Mechanisms of TNF-α- and RANKL-mediated osteoclastogenesis and bone resorption in psoriatic arthritis,” The Journal of Clinical Investigation, vol. 111, no. 6, pp. 821–831, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. G. P. Garlet, W. Martins Jr., B. A. L. Fonseca, B. R. Ferreira, and J. S. Silva, “Matrix metalloproteinases, their physiological inhibitors and osteoclast factors are differentially regulated by the cytokine profile in human periodontal disease,” Journal of Clinical Periodontology, vol. 31, no. 8, pp. 671–679, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. S. T. S. Tjoa, T. J. de Vries, T. Schoenmaker, A. Kelder, B. G. Loos, and V. Everts, “Formation of osteoclast-like cells from peripheral blood of periodontitis patients occurs without supplementation of macrophage colony-stimulating factor,” Journal of Clinical Periodontology, vol. 35, no. 7, pp. 568–575, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Hernández, N. Dutzan, J. García-Sesnich et al., Host-Pathogen Interactions in Progressive Chronic Periodontitis, Journal of Dental Research, vol. 90, no. 10, pp. 1164–1170, 2011.
  51. H. Huang, N. Zhao, X. Xu et al., “Dose-specific effects of tumor necrosis factor alpha on osteogenic differentiation of mesenchymal stem cells,” Cell Proliferation, vol. 44, no. 5, pp. 420–427, 2011. View at Publisher · View at Google Scholar
  52. R. Vernal, N. Dutzan, A. Chaparro, J. Puente, M. A. Valenzuela, and J. Gamonal, “Levels of interleukin-17 in gingival crevicular fluid and in supernatants of cellular cultures of gingival tissue from patients with chronic periodontitis,” Journal of Clinical Periodontology, vol. 32, no. 4, pp. 383–389, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. C. R. Cardoso, G. P. Garlet, G. E. Crippa et al., “Evidence of the presence of T helper type 17 cells in chronic lesions of human periodontal disease,” Oral Microbiology and Immunology, vol. 24, no. 1, pp. 1–6, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. M. N. Kelly, J. K. Kolls, K. Happel et al., “Interteukin-17/interleukin-17 receptor-mediated signaling is important for generation of an optimal polymorphonuclear response against Toxoplasma gondii infection,” Infection and Immunity, vol. 73, no. 1, pp. 617–621, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. J. J. Yu, M. J. Ruddy, G. C. Wong et al., “An essential role for IL-17 in preventing pathogen-initiated bone destruction: recruitment of neutrophils to inflamed bone requires IL-17 receptor-dependent signals,” Blood, vol. 109, no. 9, pp. 3794–3802, 2007. View at Publisher · View at Google Scholar · View at Scopus
  56. W. J. Boyle, W. S. Simonet, and D. L. Lacey, “Osteoclast differentiation and activation,” Nature, vol. 423, no. 6937, pp. 337–342, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. C. T. Weaver, L. E. Harrington, P. R. Mangan, M. Gavrieli, and K. M. Murphy, “Th17: an effector CD4 T cell lineage with regulatory T cell ties,” Immunity, vol. 24, no. 6, pp. 677–688, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. S. A. Marsters, R. A. Pitti, J. P. Sheridan, and A. Ashkenazi, “Control of apoptosis signaling by Apo2 ligand,” Recent Progress in Hormone Research, vol. 54, pp. 225–234, 1999. View at Google Scholar · View at Scopus
  59. G. Zauli and P. Secchiero, “The role of the TRAIL/TRAIL receptors system in hematopoiesis and endothelial cell biology,” Cytokine and Growth Factor Reviews, vol. 17, no. 4, pp. 245–257, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. S. Roux, P. Lambert-Comeau, C. Saint-Pierre, M. Lépine, B. Sawan, and J. L. Parent, “Death receptors, Fas and TRAIL receptors, are involved in human osteoclast apoptosis,” Biochemical and Biophysical Research Communications, vol. 333, no. 1, pp. 42–50, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. S. Colucci, G. Brunetti, F. P. Cantatore et al., “The death receptor DR5 is involved in TRAIL-mediated human osteoclast apoptosis,” Apoptosis, vol. 12, no. 9, pp. 1623–1632, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. G. Brunetti, A. Oranger, G. Mori et al., “Trail is involved in human osteoclast apoptosis,” Annals of the New York Academy of Sciences, vol. 1116, pp. 316–322, 2007. View at Publisher · View at Google Scholar
  63. P. Secchiero, A. Gonelli, P. Mirandola et al., “Tumor necrosis factor-related apoptosis-inducing ligand induces monocytic maturation of leukemic and normal myeloid precursors through a caspase-dependent pathway,” Blood, vol. 100, no. 7, pp. 2421–2429, 2002. View at Publisher · View at Google Scholar · View at Scopus
  64. P. Secchiero, E. Melloni, M. Heikinheimo et al., “TRAIL regulates normal erythroid maturation through an ERK-dependent pathway,” Blood, vol. 103, no. 2, pp. 517–522, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. G. Zauli, E. Rimondi, V. Nicolin, E. Melloni, C. Celeghini, and P. Secchiero, “TNF-related apoptosis-inducing ligand (TRAIL) blocks osteoclastic differentiation induced by RANKL plus M-CSF,” Blood, vol. 104, no. 7, pp. 2044–2050, 2004. View at Publisher · View at Google Scholar · View at Scopus
  66. G. Mori, G. Brunetti, S. Colucci et al., “Alteration of activity and survival of osteoblasts obtained from human periodontitis patients: role of TRAIL,” Journal of Biological Regulators and Homeostatic Agents, vol. 21, no. 3-4, pp. 105–114, 2007. View at Google Scholar · View at Scopus
  67. E. H. Alexander, F. A. Rivera, I. Marriott, J. Anguita, K. L. Bost, and M. C. Hudson, “Staphylococcus aureus—induced tumor necrosis factor—related apoptosis—inducing ligand expression mediates apoptosis and caspase-8 activation in infected osteoblasts,” BMC Microbiology, vol. 3, article 5, 2003. View at Publisher · View at Google Scholar
  68. G. Brunetti, A. Oranger, G. Mori et al., “TRAIL effect on osteoclast formation in physiological and pathological conditions,” Frontiers in Bioscience, vol. 1, no. 3, pp. 1154–1161, 2011. View at Google Scholar
  69. S. Vitovski, J. S. Phillips, J. Sayers, and P. I. Croucher, “Investigating the interaction between osteoprotegerin and receptor activator of NF-κB or tumor necrosis factor-related apoptosis-inducing ligand: evidence for a pivotal role for osteoprotegerin in regulating two distinct pathways,” The Journal of Biological Chemistry, vol. 282, no. 43, pp. 31601–31609, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. G. Mori, G. Brunetti, S. Collucci et al., “Osteoblast apoptosis in periodontal disease: role of TNF-related apoptosis-inducing ligand,” International Journal of Immunopathology and Pharmacology, vol. 22, no. 1, pp. 95–103, 2009. View at Google Scholar · View at Scopus
  71. G. Brunetti, A. Oranger, C. Carbone et al., “Osteoblasts display different responsiveness to TRAIL-induced apoptosis during their differentiation process,” Cell Biochemistry and Biophysics. View at Publisher · View at Google Scholar
  72. H. Lucas, P. M. Bartold, A. A. Dharmapatni, C. A. Holding, and D. R. Haynes, “Inhibition of apoptosis in periodontitis,” Journal of Dental Research, vol. 89, no. 1, pp. 29–33, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. P. M. Bartold, M. D. Cantley, and D. R. Haynes, “Mechanisms and control of pathologic bone loss in periodontitis,” Periodontology 2000, vol. 53, no. 1, pp. 55–69, 2010. View at Publisher · View at Google Scholar · View at Scopus