Table of Contents Author Guidelines Submit a Manuscript
Analytical Cellular Pathology
Volume 2018 (2018), Article ID 8047610, 8 pages
https://doi.org/10.1155/2018/8047610
Review Article

Role of Muramyl Dipeptide in Lipopolysaccharide-Mediated Biological Activity and Osteoclast Activity

Division 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

Correspondence should be addressed to Hideki Kitaura; pj.ca.ukohot.m@aruatikh

Received 28 September 2017; Accepted 10 January 2018; Published 14 February 2018

Academic Editor: Jonathan S. Reichner

Copyright © 2018 Hideki Kitaura 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. 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
  2. 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
  3. P. Khedoe, S. de Kleijn, A. M. van Oeveren-Rietdijk et al., “Acute and chronic effects of treatment with mesenchymal stromal cells on LPS-induced pulmonary inflammation, emphysema and atherosclerosis development,” PLoS One, vol. 12, no. 9, article e0183741, 2017. View at Publisher · View at Google Scholar
  4. C. V. Rosadini and J. C. Kagan, “Early innate immune responses to bacterial LPS,” Current Opinion in Immunology, vol. 44, pp. 14–19, 2017. View at Publisher · View at Google Scholar · View at Scopus
  5. P. C. Lopes, “LPS and neuroinflammation: a matter of timing,” Inflammopharmacology, vol. 24, no. 5, pp. 291–293, 2016. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Steven, M. Dib, S. Roohani, F. Kashani, T. Munzel, and A. Daiber, “Time response of oxidative/nitrosative stress and inflammation in LPS-induced endotoxaemia—a comparative study of mice and rats,” International Journal of Molecular Sciences, vol. 18, no. 10, article 2176, 2017. View at Publisher · View at Google Scholar
  7. G. Yucel, Z. Zhao, I. El-Battrawy et al., “Lipopolysaccharides induced inflammatory responses and electrophysiological dysfunctions in human-induced pluripotent stem cell derived cardiomyocytes,” Scientific Reports, vol. 7, no. 1, article 2935, 2017. View at Publisher · View at Google Scholar
  8. S. Hong and J. W. Yu, “Prolonged exposure of lipopolysaccharide induces NLRP3-independent maturation and secretion of interleukin (IL)-1β in macrophages,” Journal of Microbiology and Biotechnology, 2017. View at Publisher · View at Google Scholar
  9. 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 Publisher · View at Google Scholar · View at Scopus
  10. 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
  11. 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
  12. 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
  13. Y. Azuma, K. Kaji, R. Katogi, S. Takeshita, and A. Kudo, “Tumor necrosis factor-α induces differentiation of and bone resorption by osteoclasts,” The Journal of Biological Chemistry, vol. 275, no. 7, pp. 4858–4864, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Kobayashi, N. Takahashi, E. Jimi et al., “Tumor necrosis factor alpha stimulates osteoclast differentiation by a mechanism independent of the ODF/RANKL-RANK interaction,” The Journal of Experimental Medicine, vol. 191, no. 2, pp. 275–286, 2000. View at Google Scholar
  15. K. Fuller, C. Murphy, B. Kirstein, S. W. Fox, and T. J. Chambers, “TNFα 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 Publisher · View at Google Scholar
  16. Y. Cao, I. D. C. Jansen, S. Sprangers, T. J. de Vries, and V. Everts, “TNF-α has both stimulatory and inhibitory effects on mouse monocyte-derived osteoclastogenesis,” Journal of Cellular Physiology, vol. 232, no. 12, pp. 3273–3285, 2017. View at Publisher · View at Google Scholar
  17. 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
  18. H. Kitaura, P. Zhou, H. J. Kim, D. V. Novack, F. P. Ross, and S. L. Teitelbaum, “M-CSF mediates TNF-induced inflammatory osteolysis,” The Journal of Clinical Investigation, vol. 115, no. 12, pp. 3418–3427, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. 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
  20. A. I. Espirito Santo, A. Ersek, A. Freidin, M. Feldmann, A. A. Stoop, and N. J. Horwood, “Selective inhibition of TNFR1 reduces osteoclast numbers and is differentiated from anti-TNF in a LPS-driven model of inflammatory bone loss,” Biochemical and Biophysical Research Communications, vol. 464, no. 4, pp. 1145–1150, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Islam, F. Hassan, G. Tumurkhuu et al., “Bacterial lipopolysaccharide induces osteoclast formation in RAW 264.7 macrophage cells,” Biochemical and Biophysical Research Communications, vol. 360, no. 2, pp. 346–351, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Mormann, M. Thederan, I. Nackchbandi, T. Giese, C. Wagner, and G. M. Hansch, “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
  23. H. Mizutani, Y. Ishihara, A. Izawa et al., “Lipopolysaccharide of Aggregatibacter actinomycetemcomitans up-regulates inflammatory cytokines, prostaglandin E2 synthesis and osteoclast formation in interleukin-1 receptor antagonist-deficient mice,” Journal of Periodontal Research, vol. 48, no. 6, pp. 748–756, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Ishida, H. Kitaura, K. Kimura et al., “Muramyl dipeptide enhances lipopolysaccharide-induced osteoclast formation and bone resorption through increased RANKL expression in stromal cells,” Journal of Immunology Research, vol. 2015, Article ID 132765, 12 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. E. T. Rietschel, T. Kirikae, F. U. Schade et al., “Bacterial endotoxin: molecular relationships of structure to activity and function,” The FASEB Journal, vol. 8, no. 2, pp. 217–225, 1994. View at Google Scholar
  26. A. Steimle, I. B. Autenrieth, and J. S. Frick, “Structure and function: lipid A modifications in commensals and pathogens,” International Journal of Medical Microbiology, vol. 306, no. 5, pp. 290–301, 2016. View at Publisher · View at Google Scholar · View at Scopus
  27. R. R. Schumann, S. R. Leong, G. W. Flaggs et al., “Structure and function of lipopolysaccharide binding protein,” Science, vol. 249, no. 4975, pp. 1429–1431, 1990. View at Publisher · View at Google Scholar
  28. H. Fang, A. Liu, J. Sun, A. Kitz, O. Dirsch, and U. Dahmen, “Granulocyte colony stimulating factor induces lipopolysaccharide (LPS) sensitization via upregulation of LPS binding protein in rat,” PLoS One, vol. 8, no. 2, article e56654, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. S. D. Wright, R. A. Ramos, P. S. Tobias, R. J. Ulevitch, and J. C. Mathison, “CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein,” Science, vol. 249, no. 4975, pp. 1431–1433, 1990. View at Publisher · View at Google Scholar
  30. L. Fang, Z. Xu, G. S. Wang et al., “Directed evolution of an LBP/CD14 inhibitory peptide and its anti-endotoxin activity,” PLoS One, vol. 9, no. 7, article e101406, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. R. Shimazu, S. Akashi, H. Ogata et al., “MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4,” The Journal of Experimental Medicine, vol. 189, no. 11, pp. 1777–1782, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Medzhitov, “Toll-like receptors and innate immunity,” Nature Reviews Immunology, vol. 1, no. 2, pp. 135–145, 2001. View at Publisher · View at Google Scholar
  33. B. S. Park and J. O. Lee, “Recognition of lipopolysaccharide pattern by TLR4 complexes,” Experimental & Molecular Medicine, vol. 45, no. 12, article e66, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. H. D. Brightbill and R. L. Modlin, “Toll-like receptors: molecular mechanisms of the mammalian immune response,” Immunology, vol. 101, no. 1, pp. 1–10, 2000. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Tajima, T. Murata, K. Aritake et al., “Lipopolysaccharide induces macrophage migration via prostaglandin D2 and prostaglandin E2,” The Journal of Pharmacology and Experimental Therapeutics, vol. 326, no. 2, pp. 493–501, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. A. K. Kiemer, C. Muller, and A. M. Vollmar, “Inhibition of LPS-induced nitric oxide and TNF-α production by α-lipoic acid in rat Kupffer cells and in RAW 264.7 murine macrophages,” Immunology & Cell Biology, vol. 80, no. 6, pp. 550–557, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Rossol, H. Heine, U. Meusch et al., “LPS-induced cytokine production in human monocytes and macrophages,” Critical Reviews in Immunology, vol. 31, no. 5, pp. 379–446, 2011. View at Publisher · View at Google Scholar
  38. H. B. Xiao, C. R. Wang, Z. K. Liu, and J. Y. Wang, “LPS induces pro-inflammatory response in mastitis mice and mammary epithelial cells: possible involvement of NF-κBsignaling and OPN,” Pathologie Biologie, vol. 63, no. 1, pp. 11–16, 2015. View at Publisher · View at Google Scholar · View at Scopus
  39. J. van Heijenoort, “Formation of the glycan chains in the synthesis of bacterial peptidoglycan,” Glycobiology, vol. 11, no. 3, pp. 25R–36R, 2001. View at Publisher · View at Google Scholar
  40. R. Wheeler, G. Chevalier, G. Eberl, and I. Gomperts Boneca, “The biology of bacterial peptidoglycans and their impact on host immunity and physiology,” Cellular Microbiology, vol. 16, no. 7, pp. 1014–1023, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Chamaillard, M. Hashimoto, Y. Horie et al., “An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid,” Nature Immunology, vol. 4, no. 7, pp. 702–707, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. S. E. Girardin, I. G. Boneca, J. Viala et al., “Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection,” The Journal of Biological Chemistry, vol. 278, no. 11, pp. 8869–8872, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. F. Ellouz, A. Adam, R. Ciorbaru, and E. Lederer, “Minimal structural requirements for adjuvant activity of bacterial peptidoglycan derivatives,” Biochemical and Biophysical Research Communications, vol. 59, no. 4, pp. 1317–1325, 1974. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Merser, P. Sinay, and A. Adam, “Total synthesis and adjuvant activity of bacterial peptidoglycan derivatives,” Biochemical and Biophysical Research Communications, vol. 66, no. 4, pp. 1316–1322, 1975. View at Publisher · View at Google Scholar · View at Scopus
  45. H. S. Warren, F. R. Vogel, and L. A. Chedid, “Current status of immunological adjuvants,” Annual Review of Immunology, vol. 4, no. 1, pp. 369–388, 1986. View at Publisher · View at Google Scholar
  46. L. Z. Wang, L. Zhang, L. L. Wang et al., “Muramyl dipeptide and anti-CD10 monoclonal antibody immunoconjugate enhances anti-leukemia immunity of T lymphocytes,” APMIS, vol. 124, no. 9, pp. 800–804, 2016. View at Publisher · View at Google Scholar · View at Scopus
  47. T. O'Reilly and O. Zak, “Enhancement of the effectiveness of antimicrobial therapy by muramyl peptide immunomodulators,” Clinical Infectious Diseases, vol. 14, no. 5, pp. 1100–1109, 1992. View at Publisher · View at Google Scholar
  48. E. C. Darcissac, G. M. Bahr, M. A. Parant, L. A. Chedid, and G. J. Riveau, “Selective induction of CD11a,b,c/CD18 and CD54 expression at the cell surface of human leukocytes by muramyl peptides,” Cellular Immunology, vol. 169, no. 2, pp. 294–301, 1996. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Heinzelmann, H. C. Polk Jr, A. Chernobelsky, T. P. Stites, and L. E. Gordon, “Endotoxin and muramyl dipeptide modulate surface receptor expression on human mononuclear cells,” Immunopharmacology, vol. 48, no. 2, pp. 117–128, 2000. View at Publisher · View at Google Scholar · View at Scopus
  50. I. Morisaki, S. M. Michalek, C. C. Harmon, M. Torii, S. Hamada, and J. R. McGhee, “Effective immunity to dental caries: enhancement of salivary anti-Streptococcus mutans antibody responses with oral adjuvants,” Infection and Immunity, vol. 40, no. 2, pp. 577–591, 1983. View at Google Scholar
  51. M. M. Willems, G. G. Zom, N. Meeuwenoord et al., “Lipophilic muramyl dipeptide-antigen conjugates as immunostimulating agents,” ChemMedChem, vol. 11, no. 2, pp. 190–198, 2016. View at Publisher · View at Google Scholar · View at Scopus
  52. L. Chedid, “Muramyl peptides as possible endogenous immunopharmacological mediators,” Microbiology and Immunology, vol. 27, no. 9, pp. 723–732, 1983. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Traub, S. von Aulock, T. Hartung, and C. Hermann, “MDP and other muropeptides—direct and synergistic effects on the immune system,” Journal of Endotoxin Research, vol. 12, no. 2, pp. 69–85, 2006. View at Google Scholar
  54. I. Saiki and I. J. Fidler, “Synergistic activation by recombinant mouse interferon-gamma and muramyl dipeptide of tumoricidal properties in mouse macrophages,” The Journal of Immunology, vol. 135, no. 1, pp. 684–688, 1985. View at Google Scholar
  55. V. Souvannavong, S. Brown, and A. Adam, “Muramyl dipeptide (MDP) synergizes with interleukin 2 and interleukin 4 to stimulate, respectively, the differentiation and proliferation of B cells,” Cellular Immunology, vol. 126, no. 1, pp. 106–116, 1990. View at Publisher · View at Google Scholar · View at Scopus
  56. M. A. Wolfert, T. F. Murray, G. J. Boons, and J. N. Moore, “The origin of the synergistic effect of muramyl dipeptide with endotoxin and peptidoglycan,” The Journal of Biological Chemistry, vol. 277, no. 42, pp. 39179–39186, 2002. View at Publisher · View at Google Scholar · View at Scopus
  57. J. E. Wang, P. F. Jorgensen, E. A. Ellingsen et al., “Peptidoglycan primes for LPS-induced release of proinflammatory cytokines in whole human blood,” Shock, vol. 16, no. 3, pp. 178–182, 2001. View at Publisher · View at Google Scholar
  58. S. Traub, N. Kubasch, S. Morath et al., “Structural requirements of synthetic muropeptides to synergize with lipopolysaccharide in cytokine induction,” The Journal of Biological Chemistry, vol. 279, no. 10, pp. 8694–8700, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. P. F. Jorgensen, J. E. Wang, M. Almlof et al., “Peptidoglycan and lipoteichoic acid modify monocyte phenotype in human whole blood,” Clinical and Vaccine Immunology, vol. 8, no. 3, pp. 515–521, 2001. View at Publisher · View at Google Scholar · View at Scopus
  60. M. G. Netea, G. Ferwerda, D. J. de Jong et al., “Nucleotide-binding oligomerization domain-2 modulates specific TLR pathways for the induction of cytokine release,” The Journal of Immunology, vol. 174, no. 10, pp. 6518–6523, 2005. View at Publisher · View at Google Scholar
  61. T. Selvanantham, N. K. Escalante, M. Cruz Tleugabulova et al., “Nod1 and Nod2 enhance TLR-mediated invariant NKT cell activation during bacterial infection,” The Journal of Immunology, vol. 191, no. 11, pp. 5646–5654, 2013. View at Publisher · View at Google Scholar · View at Scopus
  62. P. R. Pouillart, F. M. Audibert, L. A. Chedid, P. L. Lefrancier, and G. M. Bahr, “Enhancement by muramyl peptides of the protective response of interferon-α/β against encephalomyocarditis virus infection,” International Journal of Immunopharmacology, vol. 18, no. 3, pp. 183–192, 1996. View at Publisher · View at Google Scholar · View at Scopus
  63. J. J. Killion and I. J. Fidler, “Therapy of cancer metastasis by tumoricidal activation of tissue macrophages using liposome-encapsulated immunomodulators,” Pharmacology & Therapeutics, vol. 78, no. 3, pp. 141–154, 1998. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Srividya, R. P. Roy, S. K. Basu, and A. Mukhopadhyay, “Selective activation of antitumor activity of macrophages by the delivery of muramyl dipeptide using a novel polynucleotide-based carrier recognized by scavenger receptors,” Biochemical and Biophysical Research Communications, vol. 268, no. 3, pp. 772–777, 2000. View at Publisher · View at Google Scholar · View at Scopus
  65. Y. Dong, S. Wang, C. Wang, Z. Li, Y. Ma, and G. Liu, “Antagonizing NOD2 signaling with conjugates of paclitaxel and muramyl dipeptide derivatives sensitizes paclitaxel therapy and significantly prevents tumor metastasis,” Journal of Medicinal Chemistry, vol. 60, no. 3, pp. 1219–1224, 2017. View at Publisher · View at Google Scholar · View at Scopus
  66. X. Li, J. Yu, S. Xu et al., “Chemical conjugation of muramyl dipeptide and paclitaxel to explore the combination of immunotherapy and chemotherapy for cancer,” Glycoconjugate Journal, vol. 25, no. 5, pp. 415–425, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. Z. Jakopin, “Murabutide revisited: a review of its pleiotropic biological effects,” Current Medicinal Chemistry, vol. 20, no. 16, pp. 2068–2079, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. L. A. Chedid, M. A. Parant, F. M. Audibert et al., “Biological activity of a new synthetic muramyl peptide adjuvant devoid of pyrogenicity,” Infection and Immunity, vol. 35, no. 2, pp. 417–424, 1982. View at Google Scholar
  69. M. A. Parant, P. Pouillart, C. Le Contel, F. J. Parant, L. A. Chedid, and G. M. Bahr, “Selective modulation of lipopolysaccharide-induced death and cytokine production by various muramyl peptides,” Infection and Immunity, vol. 63, no. 1, pp. 110–115, 1995. View at Google Scholar
  70. T. Goasduff, E. C. Darcissac, V. Vidal, A. Capron, and G. M. Bahr, “The transcriptional response of human macrophages to murabutide reflects a spectrum of biological effects for the synthetic immunomodulator,” Clinical & Experimental Immunology, vol. 128, no. 3, pp. 474–482, 2002. View at Publisher · View at Google Scholar · View at Scopus
  71. E. C. Darcissac, M. J. Truong, J. Dewulf, Y. Mouton, A. Capron, and G. M. Bahr, “The synthetic immunomodulator murabutide controls human immunodeficiency virus type 1 replication at multiple levels in macrophages and dendritic cells,” Journal of Virology, vol. 74, no. 17, pp. 7794–7802, 2000. View at Publisher · View at Google Scholar · View at Scopus
  72. E. M. Jackson and M. M. Herbst-Kralovetz, “Intranasal vaccination with murabutide enhances humoral and mucosal immune responses to a virus-like particle vaccine,” PLoS One, vol. 7, no. 7, article e41529, 2012. View at Publisher · View at Google Scholar · View at Scopus
  73. V. F. Vidal, N. Casteran, C. J. Riendeau et al., “Macrophage stimulation with Murabutide, an HIV-suppressive muramyl peptide derivative, selectively activates extracellular signal-regulated kinases 1 and 2, C / EBPβ and STAT1: role of CD14 and Toll-like receptors 2 and 4,” European Journal of Immunology, vol. 31, no. 7, pp. 1962–1971, 2001. View at Publisher · View at Google Scholar
  74. G. M. Bahr, E. Darcissac, P. R. Pouillart, and L. A. Chedid, “Synergistic effects between recombinant interleukin-2 and the synthetic immunomodulator murabutide: selective enhancement of cytokine release and potentiation of antitumor activity,” Journal of Interferon & Cytokine Research, vol. 16, no. 2, pp. 169–178, 1996. View at Publisher · View at Google Scholar
  75. 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
  76. 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
  77. 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
  78. T. Duong le, A. T. Leung, and B. Langdahl, “Cathepsin K inhibition: a new mechanism for the treatment of osteoporosis,” Calcified Tissue International, vol. 98, no. 4, pp. 381–397, 2016. View at Publisher · View at Google Scholar · View at Scopus
  79. S. A. Hienz, S. Paliwal, and S. Ivanovski, “Mechanisms of bone resorption in periodontitis,” Journal of Immunology Research, vol. 2015, Article ID 615486, 10 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  80. 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
  81. H. Kitaura, K. Kimura, M. Ishida, H. Kohara, M. Yoshimatsu, and T. Takano-Yamamoto, “Immunological reaction in TNF-α-mediated osteoclast formation and bone resorption in vitro and in vivo,” Clinical & Developmental Immunology, vol. 2013, article 181849, 8 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Wei, M. W. Wang, S. L. Teitelbaum, and F. P. Ross, “Interleukin-4 reversibly inhibits osteoclastogenesis via inhibition of NF-ĸB and mitogen-activated protein kinase signaling,” The Journal of Biological Chemistry, vol. 277, no. 8, pp. 6622–6630, 2002. View at Publisher · View at Google Scholar · View at Scopus
  83. H. Kitaura, N. Nagata, Y. Fujimura et al., “Interleukin-4 directly inhibits tumor necrosis factor-α-mediated osteoclast formation in mouse bone marrow macrophages,” Immunology Letters, vol. 88, no. 3, pp. 193–198, 2003. View at Publisher · View at Google Scholar · View at Scopus
  84. T. Fujii, H. Kitaura, K. Kimura, Z. W. Hakami, and T. Takano-Yamamoto, “IL-4 inhibits TNF-α-mediated osteoclast formation by inhibition of RANKL expression in TNF-α-activated stromal cells and direct inhibition of TNF-α-activated osteoclast precursors via a T-cell-independent mechanism in vivo,” Bone, vol. 51, no. 4, pp. 771–780, 2012. View at Publisher · View at Google Scholar · View at Scopus
  85. M. S. Freire, A. P. C. Cantuaria, S. M. F. Lima et al., “NanoUPLC-MSE proteomic analysis of osteoclastogenesis downregulation by IL-4,” Journal of Proteomics, vol. 131, pp. 8–16, 2016. View at Publisher · View at Google Scholar · View at Scopus
  86. Y. Hu, B. Ek-Rylander, M. Wendel, and G. Andersson, “Reciprocal effects of interferon-γ and IL-4 on differentiation to osteoclast-like cells by RANKL or LPS,” Oral Diseases, vol. 20, no. 7, pp. 682–692, 2014. View at Publisher · View at Google Scholar · View at Scopus
  87. M. Yoshimatsu, H. Kitaura, Y. Fujimura, H. Kohara, Y. Morita, and N. Yoshida, “IL-12 inhibits lipopolysaccharide stimulated osteoclastogenesis in mice,” Journal of Immunology Research, vol. 2015, Article ID 214878, 8 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  88. J. Saeed, H. Kitaura, K. Kimura et al., “IL-37 inhibits lipopolysaccharide-induced osteoclast formation and bone resorption in vivo,” Immunology Letters, vol. 175, pp. 8–15, 2016. View at Publisher · View at Google Scholar · View at Scopus
  89. 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,” The Journal of Immunology, vol. 175, no. 3, pp. 1956–1964, 2005. View at Publisher · View at Google Scholar
  90. 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
  91. 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
  92. 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
  93. K. Lucas and M. Maes, “Role of the toll like receptor (TLR) radical cycle in chronic inflammation: possible treatments targeting the TLR4 pathway,” Molecular Neurobiology, vol. 48, no. 1, pp. 190–204, 2013. View at Publisher · View at Google Scholar · View at Scopus
  94. B. Beutler, “TLR4 as the mammalian endotoxin sensor,” Current Topics in Microbiology and Immunology, vol. 270, pp. 109–120, 2002. View at Publisher · View at Google Scholar
  95. 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, no. 1, pp. 353–389, 2006. View at Publisher · View at Google Scholar · View at Scopus
  96. E. M. Palsson-McDermott and L. A. 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
  97. C. Dai, L. Sun, L. Yu, G. Zhu, S. Wu, and W. Bao, “Effects of porcine MyD88 knockdown on the expression of TLR4 pathway-related genes and proinflammatory cytokines,” Bioscience Reports, vol. 36, no. 6, article e00409, 2016. View at Publisher · View at Google Scholar · View at Scopus
  98. 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
  99. 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
  100. 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
  101. L. C. Hofbauer, D. L. Lacey, C. R. Dunstan, T. C. Spelsberg, B. L. Riggs, and S. Khosla, “Interleukin-1β and tumor necrosis factor-α, but not interleukin-6, stimulate osteoprotegerin ligand gene expression in human osteoblastic cells,” Bone, vol. 25, no. 3, pp. 255–259, 1999. View at Publisher · View at Google Scholar · View at Scopus
  102. J. Sun and Y. Ding, “NOD2 agonist promotes the production of inflammatory cytokines in VSMC in synergy with TLR2 and TLR4 agonists,” The Scientific World Journal, vol. 2012, Article ID 607157, 4 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  103. M. C. Walsh and Y. Choi, “Biology of the RANKL-RANK-OPG system in immunity, bone, and beyond,” Frontiers in Immunology, vol. 5, p. 511, 2014. View at Publisher · View at Google Scholar · View at Scopus
  104. J. Lam, S. Takeshita, J. E. Barker, O. Kanagawa, F. P. Ross, and S. L. Teitelbaum, “TNF-α induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand,” The Journal of Clinical Investigation, vol. 106, no. 12, pp. 1481–1488, 2000. View at Publisher · View at Google Scholar
  105. Y. H. Zhang, A. Heulsmann, M. M. Tondravi, A. Mukherjee, and Y. Abu-Amer, “Tumor necrosis factor-α (TNF) stimulates RANKL-induced osteoclastogenesis via coupling of TNF type 1 receptor and RANK signaling pathways,” The Journal of Biological Chemistry, vol. 276, no. 1, pp. 563–568, 2001. View at Publisher · View at Google Scholar · View at Scopus
  106. Z. Yao, W. Lei, R. Duan, Y. Li, L. Luo, and B. F. Boyce, “RANKL cytokine enhances TNF-induced osteoclastogenesis independently of TNF receptor associated factor (TRAF) 6 by degrading TRAF3 in osteoclast precursors,” The Journal of Biological Chemistry, vol. 292, no. 24, pp. 10169–10179, 2017. View at Publisher · View at Google Scholar