TLR5, a novel mediator of innate immunity-induced osteoclastogenesis and bone loss

FASEB Journal

Volumn 29, Issue 11, 2015, Pages 4449-4460

  Kassem, Ali ^a   Henning, Petra ^b   Kindlund, Bert ^b   Lindholm, Catharina ^b,c   Lerner, Ulf H ^a,b  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Flagellin; Inflammation; One resorption; Osteoclasts; Toll like receptors

Indexed keywords

FLAGELLIN; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; TOLL LIKE RECEPTOR 5; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MYD88 PROTEIN, MOUSE; MYELOID DIFFERENTIATION FACTOR 88; TNFRSF11B PROTEIN, MOUSE; TNFSF11 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE EROSION; CONTROLLED STUDY; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; MOUSE; NEWBORN; NONHUMAN; OSTEOBLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; PERIODONTITIS; PRIORITY JOURNAL; REACTIVE ARTHRITIS; RHEUMATOID ARTHRITIS; SKULL; ANIMAL; ARTHRITIS; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; OSTEOCLAST; PATHOLOGY;

ANIMALS; ARTHRITIS; IMMUNITY, INNATE; MICE; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; NF-KAPPA B; OSTEOBLASTS; OSTEOCLASTS; OSTEOPROTEGERIN; PERIODONTITIS; RANK LIGAND; TOLL-LIKE RECEPTOR 5;

EID: 84948783874     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-272559     Document Type: Article

References (48)

1. Walsh, M. C., and Choi, Y. (2014) Biology of the RANKL-RANK-OPG system in immunity, bone, and beyond. Front. Immunol. 5, 511
2. Souza, P. P., and Lerner, U. H. (2013) The role of cytokines in inflammatory bone loss. Immunol. Invest. 42, 555-622
3. Sims, N. A., and Walsh, N. C. (2010) GP130 cytokines and bone remodelling in health and disease. BMB Rep. 43, 513-523
4. Takayanagi, H. (2012) New developments in osteoimmunology. Nat. Rev. Rheumatol. 8, 684-689
5. Schett, G., and Gravallese, E. (2012) Bone erosion in rheumatoid arthritis: mechanisms, diagnosis and treatment. Nat. Rev. Rheumatol. 8, 656-664
6. Bar-Shavit, Z. (2008) Taking a toll on the bones: regulation of bone metabolismby innate immune regulators. Autoimmunity 41, 195-203
7. Grevers, L.C., de Vries, T.J., Vogl, T., Abdollahi-Roodsaz, S., Sloetjes, A. W., Leenen, P. J., Roth, J., Everts, V., van den Berg, W. B., and van Lent, P. L. (2011) S100A8 enhances osteoclastic bone resorption in vitro through activation of Toll-like receptor 4: implications for bone destruction in murine antigen-induced arthritis. Arthritis Rheum. 63, 1365-1375
8. Chakravarti, A., and Raquil, M. A., Tessier, P., and Poubelle, P. E. (2009) Surface RANKL of Toll-like receptor 4-stimulated human neutrophils activates osteoclastic bone resorption. Blood 114, 1633-1644
9. Koh, J. M., Lee, Y.S., Kim, Y.S., Park, S.H., Lee, S.H., and Kim, H. H., Lee, M. S., Lee, K. U., and Kim, G. S. (2009) Heat shock protein 60 causes osteoclastic bone resorption via toll-like receptor-2 in estrogen deficiency. Bone 45, 650-660
10. Kumar, H., Kawai, T., and Akira, S. (2011) Pathogen recognition by the innate immune system. Int. Rev. Immunol. 30, 16-34
11. Kawai, T., and Akira, S. (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. 11, 373-384
12. Ausubel, F. M. (2005) Are innate immune signaling pathways in plants and animals conserved? Nat Immunol. 6, 973-979
13. Itoh, K., Udagawa, N., Kobayashi, K, Suda, K, Li, X., Takami, M., Okahashi, N., Nishihara, T., and Takahashi, N. (2003) Lipopolysaccharide promotes the survival of osteoclasts via Tolllike receptor 4, but cytokine production of osteoclasts in response to lipopolysaccharide is different from that of macrophages. J. Immunol. 170, 3688-3695
14. Nakamura, H., Fukusaki, Y., Yoshimura, A, Shiraishi, C, Kishimoto, M., Kaneko, T., and Hara, Y (2008) Lack of Toll-like receptor 4 decreases lipopolysaccharide-induced bone resorption in C3H/HeJ mice in vivo. Oral Microbiol. Immunol. 23, 190-195
15. Shi, H., and Kokoeva, M. V., Inouye, K, Tzameli, I., Yin, H., and Flier, J. S. (2006) TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116, 3015-3025
16. Vabulas, R. M., Ahmad-Nejad, P., da Costa, C, Miethke, T., Kirschning, C. J., Hacker, H., and Wagner, H. (2001) Endocytosed HSP60s use toll-like receptor 2 (TLR2) and TLR4 to activate the toll/interleukin-1 receptor signaling pathway in innate immune cells. J. Biol. Chem. 276, 31332-31339
17. Klingelhofer, J., Senolt, L., Baslund, B., Nielsen, G. H., Skibshøj, I., Pavelka, K, Neidhart, M., Gay, S., Ambartsumian, N., Hansen, B. S., Petersen, J., Lukanidin, E., and Grigorian, M. (2007) Up-regulation of metastasis-promoting S100A4 (Mts-1) in rheumatoid arthritis: putative involvement in the pathogenesis of rheumatoid arthritis. Arthritis Rheum. 56, 779-789
18. O'Neill, L. A (2008) Primer: Toll-like receptor signaling pathways - what do rheumatologists need to know? Nat Clin. Pract. Rheumatol. 4, 319-327
19. Hayashi, F., Smith, K D., Ozinsky, A, Hawn, T. R, Yi, E. C., Goodlett, D. R, Eng, J. K., Akira, S., Underhill, D. M., and Aderem, A (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410, 1099-1103
20. Ramos, H. C, Rumbo, M., and Sirard J.C. (2004) Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol. 12, 509-517
21. Honko, A. N., and Mizel, S. B. (2005) Effects of flagellin on innate and adaptive immunity. Immunol. Res. 33, 83-101
22. Chamberlain, N. D., and Vila, O. M., Volin, M. V., Volkov, S., Pope, R M., Swedler, W., Mandelin II, A M., and Shahrara, S. (2012) TLR5, a novel and unidentified inflammatory mediator in rheumatoid arthritis that correlates with disease activity score and joint TNF-alpha levels. J. Immunol. 189, 475-483
23. Kim, S. J., Chen, Z., Chamberlain, N. D., Volin, M. V, Swedler, W., Volkov, S., Sweiss, N., and Shahrara, S. (2013) Angiogenesis in rheumatoid arthritis is fostered directly by toll-like receptor 5 ligation and indirectly through interleukin-17 induction. Arthritis Rheum. 65, 2024-2036
24. Leirisalo-Repo, M., Helenius, P., Hannu, T., Lehtinen, A, Kreula, J., Taavitsainen, M., and Koskimies, S. (1997) Long-term prognosis of reactive salmonella arthritis. Ann. Rheum. Dis. 56, 516-520
25. Zhang, X., and Aubin, J. E., Kim, T. H., Payne, U., Chiu, B., and Inman, R D. (2004) Synovial fibroblasts infected with Salmonella enterica serovar Typhimurium mediate osteoclast differentiation and activation. Infect. Immun. 72, 7183-7189
26. Beklen, A, Hukkanen, M., Richardson, R, and Konttinen, Y T. (2008) Immunohistochemical localization of Toll-like receptors 1-10 in periodontitis. Oral Microbiol. Immunol. 23, 425-431
27. Beklen, A., Sorsa, T., and Konttinen, Y T. (2009) Toll-like receptors 2 and 5 in human gingival epithelial cells co-operate with T-cell cytokine interleukin-17. Oral Microbiol. Immunol. 24, 38-42
28. Papadopoulos, G., and Weinberg, E. O., Massari, P., Gibson III, F. C., Wetzler, L. M., Morgan, E. F., and Genco, C. A. (2013) Macrophage-specific TLR2 signaling mediates pathogen-induced TNF-dependent inflammatory oral boneloss. J. Immunol. 190, 1148-1157
29. Kim, S. J., Chen, Z., Chamberlain, N. D., and Essani, A. B., Volin, M. V., Amin, M. A., Volkov, S., and Gravallese, E. M., Arami, S., Swedler, W., Lane, N.E., Mehta, A., Sweiss, N., and Shahrara, S. (2014) Ligation of TLR5 promotes myeloid cell infiltration and differentiation into mature osteoclasts in rheumatoid arthritis and experimental arthritis. J. Immunol. 193, 3092-3913
30. Adachi, O., Kawai, T., Takeda, K., Matsumoto, M., Tsutsui, H., Sakagami, M., Nakanishi, K., and Akira, S. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9, 143-150
31. Ljunggren, O., Ransjo, M., and Lerner, U. H. (1991) In vitro studies on bone resorption in neonatal mouse calvariae using a modified dissection technique giving four samples ofbone from each calvaria. J. Bone Miner. Res. 6, 543-550
32. Lerner, U. H. (1987) Modifications of the mouse calvarial technique improve the responsiveness to stimulators of bone resorption. J. Bone Miner. Res. 2, 375-383
33. Granholm, S., Henning, P., Lindholm, C., and Lerner, U. H. (2013) Osteoclast progenitor cells present in significant amounts in mouse calvarial osteoblast isolations and osteoclastogenesis increased by BMP-2. Bone 52, 83-92
34. Takeshita, S., Kaji, K., and Kudo, A. (2000) Identification and characterization of the new osteoclast progenitor with macrophage phenotypes being able to differentiate into mature osteoclasts. J. Bone Miner. Res. 15, 1477-1488
35. Granholm, S., Lundberg, P., and Lerner, U. H. (2007) Calcitonin inhibits osteoclast formation in mouse haematopoetic cells independently of transcriptional regulation by receptor activator of NF-kappaB and c-Fms. J. Endocrinol. 195, 415-427
36. Conaway, H. H., Pirhayati, A., Persson, E., Pettersson, U., Svensson, O., Lindholm, C., Henning, P., Tuckermann, J., and Lerner, U. H. (2011) Retinoids stimulate periosteal bone resorption by enhancing the protein RANKL, a response inhibited by monomeric glucocorticoid receptor. J. Biol. Chem. 286, 31425-31436
37. Schwab, A. M., Granholm, S., Persson, E., Wilkes, B., and Lerner, U. H., and Conaway, H. H. (2005) Stimulation of resorption in cultured mouse calvarial bones by thiazolidinediones. Endocrinology 146, 4349-4361
38. Palmqvist, P., Lundberg, P., Persson, E., Johansson, A., Lundgren, I., Lie, A., Conaway, H. H., and Lerner, U. H. (2006) Inhibition of hormone and cytokine-stimulated osteoclastogenesis and bone resorption by interleukin-4 and interleukin-13 is associated with increased osteoprotegerin and decreased RANKL and RANK in a STAT6-dependent pathway. J. Biol. Chem. 281, 2414-2429
39. Takami, M., Kim, N., Rho, J., and Choi, Y. (2002) Stimulation by tolllike receptors inhibits osteoclast differentiation. J. Immunol. 169, 1516-1523
40. Ji, J. D., Park-Min, K. H., Shen, Z., Fajardo, R. J., Goldring, S. R., McHugh, K. P., and Ivashkiv, L. B. (2009) Inhibition of RANK expression and osteoclastogenesis by TLRs and IFN-gamma in human osteoclast precursors. J. Immunol. 183, 7223-7233
41. Xiong, J., Onal, M., Jilka, R. L., and Weinstein, R. S., Manolagas, S. C., and O'Brien, C. A. (2011) Matrix-embedded cells control osteoclast formation. Nat. Med. 17, 1235-1241
42. Nakashima, T., Hayashi, M., Fukunaga, T., Kurata, K., Oh-Hora, M., Feng, J. Q., and Bonewald, L. F., Kodama, T., Wutz, A., Wagner, E. F., and Penninger, J. M., and Takayanagi, H. (2011) Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat. Med. 17, 1231-1234
43. Kawai, T., and Akira, S. (2007) Signaling to NF-kappaB by Toll-like receptors. Trends Mol. Med. 13, 460-469
44. Mizel, S. B., and Snipes, J.A. (2002) Gram-negativeflagellin-induced self-tolerance is associated with a block in interleukin-1 receptor-associated kinase release from toll-like receptor 5. J. Biol. Chem. 277, 22414-22420
45. Gohda, J., Matsumura, T., and Inoue, J. (2004) Cutting edge: TNFR-associated factor (TRAF) 6 is essential for MyD88-dependent pathway but not toll/IL-1 receptor domain-containing adaptor-inducing IFN-beta (TRIF)-dependent pathway in TLR signaling. J. Immunol. 173, 2913-2917
46. Idris, A. I., Krishnan, M., Simic, P., Landao-Bassonga, E., Mollat, P., Vukicevic, S., and Ralston, S. H. (2010) Small molecule inhibitors of IkappaB kinase signaling inhibit osteoclast formation in vitro and prevent ovariectomy-induced bone loss in vivo. FASEB J. 24, 4545-4555
47. Zou, W., and Bar-Shavit, Z. (2002) Dual modulation of osteoclast differentiation by lipopolysaccharide. J. Bone Miner. Res. 17, 1211-1218
48. Ha, H., and Lee, J. H., Kim, H. N., Kwak, H. B., and Kim, H. M., Lee, S. E., Rhee, J. H., and Kim, H. H., and Lee, Z. H. (2008) Stimulation by TLR5 modulates osteoclast differentiation through STAT1/IFN-beta. J. Immunol. 180, 1382-1389