Anti IL-17A therapy inhibits bone loss in TNF-α-mediated murine arthritis by modulation of the T-cell balance

European Journal of Immunology

Volumn 42, Issue 2, 2012, Pages 413-423

  Zwerina, Karin ^a   Koenders, Marije ^b   Hueber, Axel ^a,c   Marijnissen, Renoud J ^b   Baum, Wolfgang ^a   Heiland, Gisela Ruiz ^a   Zaiss, Mario ^a   Mclnnes, Iain ^c   Joosten, Leo ^b   van den Berg, Wim ^b   Zwerina, Jochen ^a,d   Schett, Georg ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d LUDWIG BOLTZMANN INSTITUTE FOR LUNG VASCULAR RESEARCH   (Austria)

Author keywords

Arthritis; Cytokine; IL 17; Osteoclast; T cells

Indexed keywords

INTERLEUKIN 1; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 17 ANTIBODY; INTERLEUKIN 4; LYMPHOKINE; T CELL FACTOR PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE INJURY; BONE MASS; CHRONIC ARTHRITIS; CONTROLLED STUDY; IMMUNOMODULATION; IN VIVO STUDY; LYMPHOCYTE COUNT; MOUSE; NONHUMAN; OSTEOCLASTOGENESIS; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; TH2 CELL;

ANIMALS; ANTIBODIES, MONOCLONAL; ARTHRITIS, EXPERIMENTAL; BONE RESORPTION; CELLS, CULTURED; HUMANS; IMMUNOTHERAPY; INFLAMMATION; INTERLEUKIN-1; INTERLEUKIN-17; MICE; MICE, KNOCKOUT; T-LYMPHOCYTES, REGULATORY; TH1-TH2 BALANCE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84856040620     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201141871     Document Type: Article

References (47)

1. Karsenty, G., The complexities of skeletal biology. Nature 2003. 423: 316-318.
2. Nakashima, T. and Takayanagi, H., Osteoclasts and the immune system. J. Bone Miner. Metab. 2009. 27: 519-529.
3. van Staa, T. P., Geusens, P., Bijlsma, J. W., Leufkens, H. G. and Cooper, C., Clinical assessment of the long-term risk of fracture in patients with rheumatoid arthritis. Arthritis Rheum. 2006. 54: 3104-3112.
4. Schett, G., Hayer, S., Zwerina, J., Redlich, K. and Smolen, J. S., Mechanisms of disease: the link between RANKL and arthritic bone disease. Nat. Clin. Pract. Rheumatol. 2005. 1: 47-54.
5. Lam, J., Takeshita, S., Barker, J. E., Kanagawa, O., Ross, F. P. and Teitelbaum, S. L., TNF-alpha induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J. Clin. Invest. 2000. 106: 1481-1488.
6. Zwerina, J., Redlich, K., Polzer, K., Joosten, L., Krönke, G., Distler, J., Hess, A. et al., TNF-induced structural joint damage is mediated by IL-1. Proc. Natl. Acad. Sci. USA 2007. 104: 11742-11747.
7. Kong, Y. Y., Feige, U., Sarosi, I., Bolon, B., Tafuri, A., Morony, S., Capparelli, C. et al., Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 1999. 402: 304-309.
8. 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.
9. Yamada, H., Nakashima, Y., Okazaki, K., Mawatari, T., Fukushi, J. I., Kaibara, N., Hori, A. et al., Th1 but not Th17 cells predominate in the joints of patients with rheumatoid arthritis. Ann. Rheum. Dis. 2008; 67: 1299-1304.
10. Hueber, A. J., Asquith, D. L., Miller, A. M., Reilly, J., Kerr, S., Leipe, J., Melendez, A. J. and McInnes, I. B., Mast cells express IL-17A in rheumatoid arthritis synovium. J. Immunol. 2010; 184: 3336-3340.
11. Horwood, N. J., Elliott, J., Martin, T. J., and Gillespie, M. T., IL-12 alone and in synergy with IL-18 inhibits osteoclast formation in vitro. J. Immunol. 2001. 166: 4915-4921.
12. Wei, S., Wang, M. W., Teitelbaum, S. L. and Ross, F. P., Interleukin-4 reversibly inhibits osteoclastogenesis via inhibition of NF-kappa B and mitogen-activated protein kinase signaling. J. Biol. Chem. 2002. 277: 6622-6630.
13. Takayanagi, H., Ogasawara, K., Hida, S., Chiba, T., Murata, S., Sato, K., Takaoka, A. et al., T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-gamma. Nature 2000. 408: 600-605.
14. Zaiss, M. M., Axmann, R., Zwerina, J., Polzer, K., Gückel, E., Skapenko, A., Schulze-Koops, H. et al., Treg cells suppress osteoclast formation: a new link between the immune system and bone. Arthritis Rheum. 2007. 56: 4104-4112.
15. Lubberts, E., Koenders, M. I., Oppers-Walgreen, B., van den Bersselaar, L., Coenen-de Roo, C. J., Joosten, L. A. and van den Berg, W. B., Treatment with a neutralizing anti-murine interleukin-17 antibody after the onset of collagen-induced arthritis reduces joint inflammation, cartilage destruction, and bone erosion. Arthritis Rheum. 2004. 50: 650-659.
16. 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.
17. Staschke, K. A., Dong, S., Saha, J., Zhao, J., Brooks, N. A., Hepburn, D. L., Xia, J. et al., IRAK4 kinase activity is required for Th17 differentiation and Th17-mediated disease. J. Immunol. 2009. 183: 568-577.
18. Takayanagi, H., Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems. Nat. Rev. Immunol. 2007. 7: 292-304.
19. Schett, G. and Teitelbaum, S. L., Osteoclasts and arthritis. J. Bone Miner. Res. 2009. 24: 1142-1146.
20. Azuma, Y., Kaji, K., Katogi, R., Takeshita, S. and Kudo, A., Tumor necrosis factor-alpha induces differentiation of and bone resorption by osteoclasts. J. Biol. Chem. 2000. 275: 4858-4864.
21. Diarra, D., Stolina, M., Polzer, K., Zwerina, J., Ominsky, M. S., Dwyer, D., Korb, A. et al., Dickkopf-1 is a master regulator of joint remodeling. Nat. Med. 2007. 13: 156-163.
22. Walsh, N. C., Crotti, T. N., Goldring, S. R. and Gravallese, E. M., Rheumatic diseases: the effects of inflammation on bone. Immunol. Rev. 2005. 208: 228-251.
23. Schett, G., Stach, C., Zwerina, J., Voll, R. and Manger, B., How antirheumatic drugs protect joints from damage in rheumatoid arthritis. Arthritis Rheum. 2008. 58: 2936-2948.
24. Stein, N. C., Kreutzmann, C., Zimmermann, S. P., Niebergall, U., Hellmeyer, L., Goettsch, C., Schoppet, M. et al., Interleukin-4 and interleukin-13 stimulate the osteoclast inhibitor osteoprotegerin by human endothelial cells through the STAT6 pathway. J. Bone Miner. Res. 2008. 23: 750-758.
25. Lacey, D. L., Erdmann, J. M., Teitelbaum, S. L., Tan, H. L., Ohara, J. and Shioi, A., Interleukin 4, interferon-gamma, and prostaglandin E impact the osteoclastic cell-forming potential of murine bone marrow macrophages. Endocrinology 1995. 136: 2367-2376.
26. Bendixen, A. C., Shevde, N. K., Dienger, K. M., Willson, T. M., Funk, C. D. and Pike, J. W., IL-4 inhibits osteoclast formation through a direct action on osteoclast precursors via peroxisome proliferator-activated receptor gamma 1. Proc. Natl. Acad. Sci. USA 2001. 98: 2443-2448.
27. Wan, Y., Chong, L. W. and Evans, R. M., PPAR-gamma regulates osteoclastogenesis in mice. Nat. Med. 2007. 13: 1496-1503.
28. Kitaura, H., Nagata, N., Fujimura, Y., Hotokezaka, H., Tatamiya, M., Nakao, N., Yoshida, N. et al., Interleukin-4 directly inhibits tumor necrosis factor-alpha-mediated osteoclast formation in mouse bone marrow macrophages. Immunol Lett. 2003. 88: 193-198.
29. Kitaura, H., Nagata, N., Fujimura, Y., Hotokezaka, H., Yoshida, N. and Nakayama, K., Effect of IL-12 on TNF-alpha-mediated osteoclast formation in bone marrow cells: apoptosis mediated by Fas/Fas ligand interaction. J. Immunol. 2002. 169: 4732-4738.
30. Kelchtermans, H., Schurgers, E., Geboes, L., Mitera, T., Van Damme, J., Van Snick, J., Uyttenhove, C. et al., Effector mechanisms of interleukin-17 in collagen-induced arthritis in the absence of interferon-gamma and counteraction by interferon-gamma. Arthritis Res. Ther. 2009. 11: R122.
31. Plater-Zyberk, C., Joosten, L. A., Helsen, M. M., Koenders, M. I., Baeuerle, P. A. and van den Berg, W. B., Combined blockade of granulocyte-macrophage colony stimulating factor and interleukin 17 pathways potently suppresses chronic destructive arthritis in a tumour necrosis factor alpha-independent mouse model. Ann. Rheum. Dis. 2009. 68: 721-728.
32. Lubberts, E., Koenders, M. I., and van den Berg, W. B., The role of T-cell interleukin-17 in conducting destructive arthritis: lessons from animal models. Arthritis Res Ther. 2005. 7: 29-37.
33. Lubberts, E., IL-17/Th17 targeting: on the road to prevent chronic destructive arthritis? Cytokine. 2008. 41: 84-91.
34. Li, X., Yuan, F. L., Lu, W. G., Zhao, Y. Q., Li, C. W., Li, J. P., and Xu, R. S., The role of interleukin-17 in mediating joint destruction in rheumatoid arthritis. Biochem. Biophys. Res. Commun. 2010. 397: 131-135.
35. Koenders, M. I., Lubberts, E., Oppers-Walgreen, B., van den Bersselaar, L., Helsen, M. M., Di Padova, F. E., Boots, A. M. et al., Blocking of interleukin-17 during reactivation of experimental arthritis prevents joint inflammation and bone erosion by decreasing RANKL and interleukin-1. Am. J. Pathol. 2005. 167: 141-149.
36. Van Bezooijen, R. L., Van Der Wee-Pals, L., Papapoulos, S. E., and Löwik, C. W., Interleukin 17 synergises with tumour necrosis factor alpha to induce cartilage destruction in vitro. Ann. Rheum. Dis. 2002. 61: 870-876.
37. Dudler, J., Renggli- Zulliger, N., Busso, N., Lotz, M. and So, A., Effect of interleukin 17 on proteoglycan degradation in murine knee joints. Ann Rheum Dis. 2000. 59: 529-532.
38. Polzer, K., Joosten, L., Gasser, J., Distler, J. H., Ruiz, G., Baum, W., Redlich, K. et al., IL-1 is essential for systemic inflammatory bone loss. Ann. Rheum. Dis. 2010. 69: 284-290.
39. Chabaud, M., Page, G. and Miossec, P., Enhancing effect of IL-1, IL-17, and TNF-alpha on macrophage inflammatory protein-3alpha production in rheumatoid arthritis: regulation by soluble receptors and Th2 cytokines. J. Immunol. 2001. 167: 6015-6020.
40. Genovese, M. C., Van den Bosch, F., Roberson, S. A., Bojin, S., Biagini, I. M., Ryan, P., Sloan-Lancaster, J., LY2439821, a humanized anti-interleukin-17 monoclonal antibody, in the treatment of patients with rheumatoid arthritis: a phase I randomized, double-blind, placebo-controlled, proof-of-concept study. Arthritis Rheum. 2010. 62: 929-939.
41. Hueber, W., Patel, D. D., Dryja, T., Wright, A. M., Koroleva, I., Bruin, G., Antoni, C. et al., Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Sci. Transl. Med. 2010. 2: 52ra72.
42. Keffer, J., Probert, L., Cazlaris, H., Georgopoulos, S., Kaslaris, E., Kioussis, D. and Kollias, G., Transgenic mice expressing human tumour necrosis factor: a predictive genetic model of arthritis. EMBO J. 1991. 10: 4025-4031.
43. Horai, R., Asano, M., Sudo, K., Kanuka, H., Suzuki, M., Nishihara, M., Takahashi, M. et al., Production of mice deficient in genes for interleukin (IL)-1alpha, IL-1beta, IL-1alpha/beta, and IL-1 receptor antagonist shows that IL-1beta is crucial in turpentine-induced fever development and glucocorticoid secretion. J. Exp. Med. 1998. 187: 1463-1475.
44. Parfitt, A. M., Drezner, M. K., Glorieux, F. H., Kanis, J. A., Malluche, H., Meunier, P. J., Ott, S. M. et al., Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J. Bone Miner. Res. 1987. 2: 595-610.
45. Hildebrand, T., Laib, A., Muller, R., Dequeker, J. and Ruegsegger, P., Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J. Bone Miner. Res. 1999. 14: 1167-1174.
46. Bouxsein, M. L., Boyd, S. K., Christiansen, B. A., Guldberg, R. E., Jepsen, K. J. and Müller, R., Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J. Bone Miner. Res. 2010. 25: 1468-1486.
47. Gortz, B., Hayer, S., Redlich, K., Zwerina, J., Tohidast-Akrad, M., Tuerk, B., Hartmann, C. et al., Arthritis induces lymphocytic bone marrow inflammation and endosteal bone formation. J. Bone Miner. Res. 2004. 19: 990-998.