A bone-protective role for IL-17 receptor signaling in ovariectomy-induced bone loss

European Journal of Immunology

Volumn 39, Issue 10, 2009, Pages 2831-2839

  Goswami, Jaya ^a,b   Hernández Santos, Nydiaris ^b   Zuniga, Luis A ^c   Gaffen, Sarah L ^a,b,d  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c STANFORD UNIVERSITY   (United States)

^d UNIVERSITY AT BUFFALO   (United States)

Author keywords

Bone loss; Cytokine; IL 17; Knockout; T cells

Indexed keywords

INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; LEPTIN;

ADIPOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DESTRUCTION; BONE TURNOVER; CONTROLLED STUDY; ESTROGEN DEFICIENCY; FEMALE; HORMONE ACTION; HORMONE SYNTHESIS; METABOLIC REGULATION; MOUSE; NONHUMAN; OSTEOLYSIS; OVARIECTOMY; POSTMENOPAUSE OSTEOPOROSIS; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN EXPRESSION; SATIETY; SIGNAL TRANSDUCTION; TH1 CELL; TH17 CELL; TH2 CELL;

3T3-L1 CELLS; ADIPOCYTES; ADIPOGENESIS; ANIMALS; BONE DENSITY; CYTOKINES; DOWN-REGULATION; ESTROGENS; FEMALE; INTERLEUKIN-17; LEPTIN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; OSTEOPOROSIS; OVARIECTOMY; RECEPTORS, INTERLEUKIN-17; SIGNAL TRANSDUCTION; SPINE; TUMOR NECROSIS FACTOR-ALPHA; WEIGHT GAIN;

EID: 70350545726     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939670     Document Type: Article

References (48)

1. Lubberts, E., IL-17/Th17 targeting: on the road to prevent chronic destructive arthritis? Cytokine 2008. 41: 84-91.
2. Langrish, C. L., Chen, Y., Blumenschein, W. M., Mattson, J., Basham, B., Sedgwick, J. D., McClanahan, T. et al., IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 2005. 201: 233-240.
3. Weaver, C. T., Hatton, R. D., Mangan, P. R. and Harrington, L. E., IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 2007. 25: 821-852.
4. Lubberts, E., van den Bersselaar, L., Oppers-Walgreen, B., Schwarzenberger, P., Coenen-de Roo, C. J., Kolls, J. K., Joosten, L. A. and van den Berg, W. B., IL-17 promotes bone erosion in murine collagen-induced arthritis through loss of the receptor activator of NF-kappa B ligand/osteoprotegerin balance. J. Immunol. 2003. 170: 2655-2662. (Pubitemid 36245658)
5. Sato, K., Suematsu, A., Okamoto, K., Yamaguchi, A., Morishita, Y., Kadono, Y., Tanaka, S. et al., Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J. Exp. Med. 2006. 203: 2673-2682.
6. Jovanovic, D., di Battista, J. A., Martel-Pelletier, J., Jolicoeur, F. C., He, Y., Zhang, M., Mineau, F. and Pelletier, J.-P., IL-17 stimulates the production and expression of proinflammatory cytokines, IL-1β and TNF-α, by human macrophages. J. Immunol. 1998. 160: 3513-3521. (Pubitemid 28164746)
7. Fossiez, F., Djossou, O., Chomarat, P., Flores-Romo, L., Ait-Yahia, S., Maat, C., Pin, J. J. et al., T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J. Exp. Med. 1996. 183: 2593-2603.
8. Ruddy, M. J., Wong, G. C., Liu, X. K., Yamamoto, H., Kasayama, S., Kirkwood, K. L. and Gaffen, S. L., Functional cooperation between interleukin-17 and tumor necrosis factor-alpha is mediated by CCAAT/enhancer-binding protein family members. J. Biol. Chem. 2004. 279: 2559-2567.
9. Jilka, R. L., Hangoc, G., Girasole, G., Passeri, G., Williams, D. C., Abrams, J. S., Boyce, B. et al., Increased osteoclast development after estrogen loss: mediated by interleukin-6. Science 1992. 257: 88-91.
10. Poli, V., Balena, R., Fattori, E., Markatos, A., Yamamoto, M., Tanaka, H., Ciliberto, G. et al., Interleukin-6 deficient mice are protected from bone loss caused by estrogen depletion. EMBO J. 1994. 13: 1189-1196. (Pubitemid 24074725)
11. Cenci, S., Toraldo, G., Weitzmann, M. N., Roggia, C., Gao, Y., Qian, W. P., Sierra, O. and Pacifici, R., Estrogen deficiency induces bone loss by increasing T cell proliferation and lifespan through IFN-gamma-induced class II transactivator. Proc. Natl. Acad. Sci. USA 2003. 100: 10405-10410.
12. Wei, S., Kitaura, H., Zhou, P., Ross, F. P. and Teitelbaum, S. L., IL-1 mediates TNF-induced osteoclastogenesis. J. Clin. Invest. 2005. 115: 282-290.
13. Roggia, C., Gao, Y., Cenci, S., Weitzmann, M. N., Toraldo, G., Isaia, G. and Pacifici, R., Up-regulation of TNF-producing T cells in the bone marrow: a key mechanism by which estrogen deficiency induces bone loss in vivo. Proc. Natl. Acad. Sci. USA 2001. 98: 13960-13965.
14. Yu, J. J., Ruddy, M. J., Conti, H. R., Boonanantanasarn, K. and Gaffen, S. L., The interleukin-17 receptor plays a gender-dependent role in host protection against Porphyromonas gingivalis-induced periodontal bone loss. Infect. Immun. 2008. 76: 8.
15. Yu, J. J., Ruddy, M. J., Wong, G. C., Sfintescu, C., Baker, P. J., Smith, J. B., Evans, R. T. and Gaffen, S. L., 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 2007. 109: 3794-3802. (Pubitemid 46641730)
16. Gaffen, S. L. and Hajishengallis, G., A new inflammatory cytokine on the block: re-thinking periodontal disease and the Th1/Th2 paradigm in the context of Th17 cells and IL-17. J Dent. Res. 2008. 87: 817-828.
17. Quinn, J. M., Sims, N. A., Saleh, H., Mirosa, D., Thompson, K., Bouralexis, S., Walker, E. C. et al. IL-23 inhibits osteoclastogenesis indirectly through lymphocytes and is required for the maintenance of bone mass in mice. J. Immunol. 2008. 181: 5720-5729.
18. Weitzmann, M. N. and Pacifici, R., Estrogen deficiency and bone loss: an inflammatory tale. J. Clin. Invest. 2006. 116: 1186-1194.
19. Cenci, S., Weitzmann, M. N., Roggia, C., Namba, N., Novack, D., Woodring, J. and Pacifici, R., Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J. Clin. Invest. 2000. 106: 1229-1237.
20. Bouxsein, M. L., Myers, K. S., Shultz, K. L., Donahue, L. R., Rosen, C. J. and Beamer, W. G., Ovariectomy-induced bone loss varies among inbred strains of mice. J. Bone Miner. Res. 2005. 20: 1085-1092.
21. Beamer, W. G., Donahue, L. R., Rosen, C. J. and Baylink, D. J., Genetic variability in adult bone density among inbred strains of mice. Bone 1996. 18: 397-403.
22. Gao, Y., Qian, W. P., Dark, K., Toraldo, G., Lin, A. S., Guldberg, R. E., Flavell, R. A. et al., Estrogen prevents bone loss through transforming growth factor beta signaling in T cells. Proc. Natl. Acad. Sci. USA 2004. 101: 16618-16623.
23. Wu, J., Wang, X., Chiba, H., Higuchi, M., Nakatani, T., Ezaki, O., Cui, H. et al., Combined intervention of soy isoflavone and moderate exercise prevents body fat elevation and bone loss in ovariectomized mice. Metabolism 2004. 53: 942-948. (Pubitemid 38829472)
24. Weitzmann, M. N. and Pacifici, R., The role of T lymphocytes in bone metabolism. Immunol. Rev. 2005. 208: 154-168.
25. Bluher, S. and Mantzoros, C. S., Leptin in humans: lessons from translational research. Am. J. Clin. Nutr. 2009. 89: 991S-997S.
26. Karsenty, G. and Ducy, P., The hypothalamic control of bone mass, implication for the treatment of osteoporosis. Ann. Endocrinol. (Paris) 2006. 67: 123.
27. Ducy, P., Schinke, T. and Karsenty, G., The osteoblast: a sophisticated fibroblast under central surveillance. Science 2000. 289: 1501-1504. (Pubitemid 30677463)
28. Lee, N. J., Wong, I. P., Baldock, P. A. and Herzog, H., Leptin as an endocrine signal in bone. Curr. Osteoporos. Rep. 2008. 6: 62-66.
29. Thomas, T., Gori, F., Khosla, S., Jensen, M. D., Burguera, B. and Riggs, B. L., Leptin acts on human marrow stromal cells to enhance differentiation to osteoblasts and to inhibit differentiation to adipocytes. Endocrinology 1999. 140: 1630-1638. (Pubitemid 29149231)
30. Ruddy, M. J., Shen, F., Smith, J. B., Sharma, A. and Gaffen, S. L., Interleukin-17 regulates expression of the CXC chemokine LIX/CXCL5 in osteoblasts: implications for inflammation and neutrophil recruitment. J. Leukoc. Biol. 2004. 76: 135-144.
31. Theill, L., Boyle, W. and Penninger, J., RANK-L and RANK: T cells, bone loss and mammalian evolution. Annu. Rev. Immunol. 2002. 20: 795-823.
32. Khosla, S., Minireview: the OPG/RANKL/RANK system. Endocrinology 2001. 142: 5050-5055.
33. Manolagas, S. C., Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr. Rev. 2000. 21: 115-137.
34. Riggs, B. L., Khosla, S. and Melton, L. J., 3rd, Sex steroids and the construction and conservation of the adult skeleton. Endocr. Rev. 2002. 23: 279-302.
35. Pacifici, R., Estrogen, cytokines, and pathogenesis of postmenopausal osteoporosis. J. Bone Miner. Res. 1996. 11: 1043-1051.
36. Shen, F., Ruddy, M. J., Plamondon, P. and Gaffen, S. L., Cytokines link osteoblasts and inflammation: microarray analysis of interleukin-17-and TNF-alpha-induced genes in bone cells. J. Leukoc. Biol. 2005. 77: 388-399.
37. Gillespie, M. T., Impact of cytokines and T lymphocytes upon osteoclast differentiation and function. Arthritis Res. Ther. 2007. 9: 103.
38. Gao, Y., Grassi, F., Ryan, M. R., Terauchi, M., Page, K., Yang, X., Weitzmann, M. N. et al., IFN-gamma stimulates osteoclast formation and bone loss in vivo via antigen-driven T cell activation. J. Clin. Invest. 2007. 117: 122-132.
39. Kimble, R. B., Bain, S. and Pacifici, R., The functional block of TNF but not of IL-6 prevents bone loss in ovariectomized mice. J. Bone Miner. Res. 1997. 12: 935-941.
40. Kimble, R. B., Srivastava, S., Ross, F. P., Matayoshi, A. and Pacifici, R., 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. J. Biol. Chem. 1996. 271: 28890-28897.
41. Kimble, R. B., Matayoshi, A. B., Vannice, J. L., Kung, V. T., Williams, C. and Pacifici, R., Simultaneous block of interleukin-1 and tumor necrosis factor is required to completely prevent bone loss in the early postovariectomy period. Endocrinology 1995. 136: 3054-3061.
42. Frost, A., Jonsson, K. B., Brandstrom, H., Ohlsson, C., Ljunghall, S. and Ljunggren, O., Interleukin-13 inhibits cell proliferation and stimulates interleukin-6 formation in isolated human osteoblasts. J. Clin. Endocrinol. Metab. 1998. 83: 3285-3289.
43. Nagata, T., McKinley, L., Peschon, J. J., Alcorn, J. F., Aujla, S. J. and Kolls, J. K., Requirement of IL-17RA in Con A induced hepatitis and negative regulation of IL-17 production in mouse T cells. J. Immunol. 2008. 181: 7473-7479.
44. Shin, J. H., Shin, D. W. and Noh, M., Interleukin-17A inhibits adipocyte differentiation in human mesenchymal stem cells and regulates proinflammatory responses in adipocytes. Biochem. Pharmacol. 2009. 77: 1835-1844.
45. Huang, H., Kim, H. J., Chang, E. J., Lee, Z. H., Hwang, S. J., Kim, H. M., Lee, Y. and Kim, H. H., IL-17 stimulates the proliferation and differentiation of human mesenchymal stem cells: implications for bone remodeling. Cell Death Differ. 2009. doi.10.1038/cdd.2009.74
46. Sumarac-Dumanovic, M., Stevanovic, D., Ljubic, A., Jorga, J., Simic, M., Stamenkovic-Pejkovic, D., Starcevic, V. et al., Increased activity of interleukin-23/interleukin-17 proinflammatory axis in obese women. Int. J. Obes. (Lond.) 2009. 33: 151-156.
47. Rickel, E. A., Siegel, L. A., Yoon, B. R., Rottman, J. B., Kugler, D. G., Swart, D. A., Anders, P. M. et al., Identification of functional roles for both IL-17RB and IL-17RA in mediating IL-25-induced activities. J. Immunol. 2008. 181: 4299-4310.
48. Rong, Z., Wang, A., Li, Z., Ren, Y., Cheng, L., Li, Y., Wang, Y. et al., IL-17RD (Sef or IL-17RLM) interacts with IL-17 receptor and mediates IL-17 signaling. Cell Res. 2008. 19: 208-215.