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Journal of Immunology Research
Volume 2015, Article ID 132765, 12 pages
http://dx.doi.org/10.1155/2015/132765
Research Article

Muramyl Dipeptide Enhances Lipopolysaccharide-Induced Osteoclast Formation and Bone Resorption through Increased RANKL Expression in Stromal Cells

1Division of Orthodontics and Dentofacial Orthopedics, Department of Translational Medicine, Tohoku University Graduate School of Dentistry, 4-1 Seiryo-machi, Aoba-ku, Sendai 980-8575, Japan
2Department of Microbiology and Immunology, Tohoku University Graduate School of Dentistry, 4-1 Seiryo-machi, Aoba-ku, Sendai 980-8575, Japan

Received 12 October 2014; Revised 25 December 2014; Accepted 8 January 2015

Academic Editor: Giacomina Brunetti

Copyright © 2015 Masahiko Ishida 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. P. Orcel, M. Feuga, J. Bielakoff, and M. C. de Vernejoul, “Local bone injections of LPS and M-CSF increase bone resorption by different pathways in vivo in rats,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 264, no. 3, part 1, pp. E391–E397, 1993. View at Google Scholar · View at Scopus
  2. Y. Abu-Amer, F. P. Ross, J. Edwards, and S. L. Teitelbaum, “Lipopolysaccharide-stimulated osteoclastogenesis is mediated by tumor necrosis factor via its P55 receptor,” The Journal of Clinical Investigation, vol. 100, no. 6, pp. 1557–1565, 1997. View at Publisher · View at Google Scholar · View at Scopus
  3. Y. Sakuma, K. Tanaka, M. Suda et al., “Crucial involvement of the EP4 subtype of prostaglandin E receptor in osteoclast formation by proinflammatory cytokines and lipopolysaccharide,” Journal of Bone and Mineral Research, vol. 15, no. 2, pp. 218–227, 2000. View at Google Scholar · View at Scopus
  4. A. L. Dumitrescu, S. A. El-Aleem, B. Morales-Aza, and L. F. Donaldson, “A model of periodontitis in the rat: effect of lipopolysaccharide on bone resorption, osteoclast activity, and local peptidergic innervation,” Journal of Clinical Periodontology, vol. 31, no. 8, pp. 596–603, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. Y.-H. Chung, E.-J. Chang, S.-J. Kim et al., “Lipopolysaccharide from Prevotella nigrescens stimulates osteoclastogenesis in cocultures of bone marrow mononuclear cells and primary osteoblasts,” Journal of Periodontal Research, vol. 41, no. 4, pp. 288–296, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. N. Bostanci, R. P. Allaker, G. N. Belibasakis et al., “Porphyromonas gingivalis antagonises Campylobacter rectus induced cytokine production by human monocytes,” Cytokine, vol. 39, no. 2, pp. 147–156, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. K. Redlich, S. Hayer, R. Ricci et al., “Osteoclasts are essential for TNF-α-mediated joint destruction,” The Journal of Clinical Investigation, vol. 110, no. 10, pp. 1419–1427, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. K. D. Merkel, J. M. Erdmann, K. P. McHugh, Y. Abu-Amer, F. P. Ross, and S. L. Teitelbaum, “Tumor necrosis factor-α mediates orthopedic implant osteolysis,” The American Journal of Pathology, vol. 154, no. 1, pp. 203–210, 1999. View at Publisher · View at Google Scholar · View at Scopus
  9. R. B. Kimble, S. Srivastava, F. P. Ross, A. Matayoshi, and R. Pacifici, “Estrogen deficiency increases the ability of stromal cells to support murine osteoclastogenesis via an interleukin-1-and tumor necrosis factor-mediated stimulation of macrophage colony-stimulating factor production,” The Journal of Biological Chemistry, vol. 271, no. 46, pp. 28890–28897, 1996. View at Publisher · View at Google Scholar · View at Scopus
  10. S. L. Teitelbaum, “Bone resorption by osteoclasts,” Science, vol. 289, no. 5484, pp. 1504–1508, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. S. L. Teitelbaum, “Osteoclasts: what do they do and how do they do it?” The American Journal of Pathology, vol. 170, no. 2, pp. 427–435, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Azuma, K. Kaji, R. Katogi, S. Takeshita, and A. Kudo, “Tumor necrosis factor-α induces differentiation of and bone resorption by osteoclasts,” Journal of Biological Chemistry, vol. 275, no. 7, pp. 4858–4864, 2000. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Kobayashi, N. Takahashi, E. Jimi et al., “Tumor necrosis factor α stimulates osteoclast differentiation by a mechanism independent of the ODF/RANKL-RANK interaction,” The Journal of Experimental Medicine, vol. 191, no. 2, pp. 275–285, 2000. View at Google Scholar · View at Scopus
  14. K. Fuller, C. Murphy, B. Kirstein, S. W. Fox, and T. J. Chambers, “TNFalpha potently activates osteoclasts, through a direct action independent of and strongly synergistic with RANKL,” Endocrinology, vol. 143, no. 3, pp. 1108–1118, 2002. View at Google Scholar · View at Scopus
  15. H. Kitaura, M. S. Sands, K. Aya et al., “Marrow stromal cells and osteoclast precursors differentially contribute to TNF-α-induced osteoclastogenesis in vivo,” The Journal of Immunology, vol. 173, no. 8, pp. 4838–4846, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Kitaura, P. Zhou, H.-J. Kim, D. V. Novack, F. P. Ross, and S. L. Teitelbaum, “M-CSF mediates TNF-induced inflammatory osteolysis,” Journal of Clinical Investigation, vol. 115, no. 12, pp. 3418–3427, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. C.-Y. Chiang, G. Kyritsis, D. T. Graves, and S. Amar, “Interleukin-1 and tumor necrosis factor activities partially account for calvarial bone resorption induced by local injection of lipopolysaccharide,” Infection and Immunity, vol. 67, no. 8, pp. 4231–4236, 1999. View at Google Scholar · View at Scopus
  18. W. Zou and Z. Bar-Shavit, “Dual modulation of osteoclast differentiation by lipopolysaccharide,” Journal of Bone and Mineral Research, vol. 17, no. 7, pp. 1211–1218, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. 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
  20. M. Mörmann, M. Thederan, I. Nackchbandi, T. Giese, C. Wagner, and G. M. Hänsch, “Lipopolysaccharides (LPS) induce the differentiation of human monocytes to osteoclasts in a tumour necrosis factor (TNF) α-dependent manner: a link between infection and pathological bone resorption,” Molecular Immunology, vol. 45, no. 12, pp. 3330–3337, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. H. Takada, S. Yokoyama, and S. Yang, “Enhancement of endotoxin activity by muramyldipeptide,” Journal of Endotoxin Research, vol. 8, no. 5, pp. 337–342, 2002. View at Google Scholar · View at Scopus
  22. H. Takada and C. Galanos, “Enhancement of endotoxin lethality and generation of anaphylactoid reactions by lipopolysaccharides in muramyl-dipeptide-treated mice,” Infection and Immunity, vol. 55, no. 2, pp. 409–413, 1987. View at Google Scholar · View at Scopus
  23. S. Yang, R. Tamai, S. Akashi et al., “Synergistic effect of muramyldipeptide with lipopolysaccharide or lipoteichoic acid to induce inflammatory cytokines in human monocytic cells in culture,” Infection and Immunity, vol. 69, no. 4, pp. 2045–2053, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Yang, N. Takahashi, T. Yamashita et al., “Muramyl dipeptide enhances osteoclast formation induced by lipopolysaccharide, IL-1α, and TNF-α through nucleotide-binding oligomerization domain 2-mediated signaling in osteoblasts,” Journal of Immunology, vol. 175, no. 3, pp. 1956–1964, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Slots and R. J. Genco, “Black-pigmented Bacteroides species, Capnocytophaga species, and Actinobacillus actinomycetemcomitans in human periodontal disease: virulence factors in colonization, survival, and tissue destruction,” Journal of Dental Research, vol. 63, no. 3, pp. 412–421, 1984. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Kimura, H. Kitaura, T. Fujii, Z. W. Hakami, and T. Takano-Yamamoto, “Anti-c-Fms antibody inhibits lipopolysaccharide-induced osteoclastogenesis in vivo,” FEMS Immunology and Medical Microbiology, vol. 64, no. 2, pp. 219–227, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Kimura, H. Kitaura, T. Fujii, M. Ishida, Z. W. Hakami, and T. Takano-Yamamoto, “An anti-c-Fms antibody inhibits osteoclastogenesis in a mouse periodontitis model,” Oral Diseases, vol. 20, no. 3, pp. 319–324, 2014. View at Publisher · View at Google Scholar
  28. T. Kishimoto, T. Kaneko, T. Ukai et al., “Peptidoglycan and lipopolysaccharide synergistically enhance bone resorption and osteoclastogenesis,” Journal of Periodontal Research, vol. 47, no. 4, pp. 446–454, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. J. J. Oppenheim, A. Togawa, L. Chedid, and S. Mizel, “Components of mycobacteria and muramyl dipeptide with adjuvant activity induce lymphocyte activating factor,” Cellular Immunology, vol. 50, no. 1, pp. 71–81, 1980. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Kikuchi, T. Matsuguchi, N. Tsuboi et al., “Gene expression of osteoclast differentiation factor is induced by lipopolysaccharide in mouse osteoblasts via Toll-like receptors,” The Journal of Immunology, vol. 166, no. 5, pp. 3574–3579, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. N. J. Horwood, J. Elliott, T. J. Martin, and M. T. Gillespie, “Osteotropic agents regulate the expression of osteoclast differentiation factor and osteoprotegerin in osteoblastic stromal cells,” Endocrinology, vol. 139, no. 11, pp. 4743–4746, 1998. View at Publisher · View at Google Scholar · View at Scopus
  32. K. Itoh, N. Udagawa, K. Matsuzaki et al., “Importance of membrane- or matrix-associated forms of M-CSF and RANKL/ODF in osteoclastogenesis supported by SaOS-4/3 cells expressing recombinant PTH/PTHrP receptors,” Journal of Bone and Mineral Research, vol. 15, no. 9, pp. 1766–1775, 2000. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Kanzawa, T. Sugimoto, T. Kobayashi, A. Kobayashi, and K. Chihara, “Association between parathyroid hormone (PTH)/PTH-related peptide receptor gene polymorphism and the extent of bone mass reduction in primary hyperparathyroidism,” Hormone and Metabolic Research, vol. 32, no. 9, pp. 355–358, 2000. View at Publisher · View at Google Scholar
  34. S.-K. Lee and J. A. Lorenzo, “Parathyroid hormone stimulates TRANCE and inhibits osteoprotegerin messenger ribonucleic acid expression in murine bone marrow cultures: correlation with osteoclast-like cell formation,” Endocrinology, vol. 140, no. 8, pp. 3552–3561, 1999. View at Google Scholar · View at Scopus
  35. K. Tsukii, N. Shima, S.-I. Mochizuki et al., “Osteoclast differentiation factor mediates an essential signal for bone resorption induced by 1α,25-dihydroxyvitamin D3, prostaglandin E2, or parathyroid hormone in the microenvironment of bone,” Biochemical and Biophysical Research Communications, vol. 246, no. 2, pp. 337–341, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. B. Beutler, “TLR4 as the mammalian endotoxin sensor,” Current Topics in Microbiology and Immunology, vol. 270, pp. 109–120, 2002. View at Google Scholar · View at Scopus
  37. B. Beutler, Z. Jiang, P. Georgel et al., “Genetic analysis of host resistance: toll-like receptor signaling and immunity at large,” Annual Review of Immunology, vol. 24, pp. 353–389, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. E. M. Pålsson-McDermott and L. A. J. O'Neill, “Signal transduction by the lipopolysaccharide receptor, Toll-like receptor-4,” Immunology, vol. 113, no. 2, pp. 153–162, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. J. C. Chow, D. W. Young, D. T. Golenbock, W. J. Christ, and F. Gusovsky, “Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction,” The Journal of Biological Chemistry, vol. 274, no. 16, pp. 10689–10692, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. G. L. Su, R. D. Klein, A. Aminlari et al., “Kupffer cell activation by lipopolysaccharide in rats: role for lipopolysaccharide binding protein and toll-like receptor 4,” Hepatology, vol. 31, no. 4, pp. 932–936, 2000. View at Publisher · View at Google Scholar · View at Scopus
  41. L. Tang, X.-D. Zhou, Q. Wang et al., “Expression of TRAF6 and pro-inflammatory cytokines through activation of TLR2, TLR4, NOD1, and NOD2 in human periodontal ligament fibroblasts,” Archives of Oral Biology, vol. 56, no. 10, pp. 1064–1072, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. K. Bandow, A. Maeda, K. Kakimoto et al., “Molecular mechanisms of the inhibitory effect of lipopolysaccharide (LPS) on osteoblast differentiation,” Biochemical and Biophysical Research Communications, vol. 402, no. 4, pp. 755–761, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Nakao, Y. Fujii, J. Kusuyama et al., “Low-intensity pulsed ultrasound (LIPUS) inhibits LPS-induced inflammatory responses of osteoblasts through TLR4-MyD88 dissociation,” Bone, vol. 58, pp. 17–25, 2014. View at Publisher · View at Google Scholar · View at Scopus