Inflammation-Induced Bone Loss: Can it Be Prevented?

Rheumatic Disease Clinics of North America

Volumn 32, Issue 4, 2006, Pages 759-773

  Romas, Evange ^a   Gillespie, Matthew T ^b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ABATACEPT; ADAM PROTEIN; ALENDRONIC ACID; BISPHOSPHONIC ACID DERIVATIVE; COLONY STIMULATING FACTOR 1; CYTOKINE; DENOSUMAB; DISEASE MODIFYING ANTIRHEUMATIC DRUG; IBANDRONIC ACID; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 17; INTERLEUKIN 6; METHOTREXATE; OSTEOCLAST DIFFERENTIATION FACTOR; PARATHYROID HORMONE; RISEDRONIC ACID; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ANTIBODY; ZOLEDRONIC ACID;

BONE DESTRUCTION; BONE REMODELING; DRUG POTENCY; HUMAN; INFLAMMATION; NUCLEAR MAGNETIC RESONANCE IMAGING; OSTEOCLAST; OSTEOLYSIS; OSTEOPENIA; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; T LYMPHOCYTE ACTIVATION;

ARTHRITIS, RHEUMATOID; BONE RESORPTION; DIPHOSPHONATES; HUMANS; INFLAMMATION; OSTEOCLASTS; OSTEOPOROSIS; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 34247125697     PISSN: 0889857X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.rdc.2006.07.004     Document Type: Review

References (99)

1. Goldring S. Osteoporosis and rheumatic diseases. In: Favus M.J. (Ed). Primer of the metabolic bone diseases and disorders of mineral metabolism. 5th edition (2003), Lippincott Williams & Wilkins, Philadelphia 379-382
2. Drossaers-Bakker K.W., de Buck M., van Zeben D., et al. Long-term course and outcome of functional capacity in rheumatoid arthritis: the effect of disease activity and radiologic damage over time. Arthritis Rheum 42 9 (1999) 1854-1860
3. Forsblad D'Elia H., Larsen A., Waltbrand E., et al. Radiographic joint destruction in postmenopausal rheumatoid arthritis is strongly associated with generalised osteoporosis. Ann Rheum Dis 62 7 (2003) 617-623
4. Gough A.K., Lilley J., Eyre S., et al. Generalised bone loss in patients with early rheumatoid arthritis. Lancet 344 8914 (1994) 23-27
5. Goldring S.R. Pathogenesis of bone and cartilage destruction in rheumatoid arthritis. Rheumatology (Oxford) 42 Suppl 2 (2003) ii11-ii16
6. Gravallese E.M., Harada Y., Wang J.T., et al. Identification of cell types responsible for bone resorption in rheumatoid arthritis and juvenile rheumatoid arthritis. Am J Pathol 152 4 (1998) 943-951
7. Redlich K., Hayer S., Maier A., et al. Tumor necrosis factor alpha-mediated joint destruction is inhibited by targeting osteoclasts with osteoprotegerin. Arthritis Rheum 46 3 (2002) 785-792
8. Redlich K., Hayer S., Ricci R., et al. Osteoclasts are essential for TNF-alpha-mediated joint destruction. J Clin Invest 110 10 (2002) 1419-1427
9. Schett G., Redlich K., Hayer S., et al. Osteoprotegerin protects against generalized bone loss in tumor necrosis factor-transgenic mice. Arthritis Rheum 48 7 (2003) 2042-2051
10. Zwerina J., Hayer S., Tohidast-Akrad M., et al. Single and combined inhibition of tumor necrosis factor, interleukin-1, and RANKL pathways in tumor necrosis factor-induced arthritis: effects on synovial inflammation, bone erosion, and cartilage destruction. Arthritis Rheum 50 1 (2004) 277-290
11. Pettit A.R., Ji H., von Stechow D., et al. TRANCE/RANKL knockout mice are protected from bone erosion in a serum transfer model of arthritis. Am J Pathol 159 5 (2001) 1689-1699
12. Romas E., Sims N.A., Hards D.K., et al. Osteoprotegerin reduces osteoclast numbers and prevents bone erosion in collagen-induced arthritis. Am J Pathol 161 4 (2002) 1419-1427
13. Bertolini D.R., Nedwin G.E., Bringman T.S., et al. Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature 319 6053 (1986) 516-518
14. Herrak P., Gortz B., Hayer S., et al. Zoledronic acid protects against local and systemic bone loss in tumor necrosis factor-mediated arthritis. Arthritis Rheum 50 7 (2004) 2327-2337
15. Sims N.A., Green J.R., Glatt M., et al. Targeting osteoclasts with zoledronic acid prevents bone destruction in collagen-induced arthritis. Arthritis Rheum 50 7 (2004) 2338-2346
16. Smolen J.S., and Steiner G. Therapeutic strategies for rheumatoid arthritis. Nat Rev Drug Discov 2 6 (2003) 473-488
17. Sambrook P.N. The skeleton in rheumatoid arthritis: common mechanisms for bone erosion and osteoporosis?. J Rheumatol 27 11 (2000) 2541-2542
18. Vincent C., Nogueira L., Clavel C., et al. Autoantibodies to citrullinated proteins: ACPA. Autoimmunity 38 1 (2005) 17-24
19. Cappellen D., Luong-Nguyen N.H., Bongiovanni S., et al. Transcriptional program of mouse osteoclast differentiation governed by the macrophage colony-stimulating factor and the ligand for the receptor activator of NFkappa B. J Biol Chem 277 24 (2002) 21971-21982
20. Ostergaard M., Hansen M., Stoltenberg M., et al. New radiographic bone erosions in the wrists of patients with rheumatoid arthritis are detectable with magnetic resonance imaging a median of two years earlier. Arthritis Rheum 48 8 (2003) 2128-2131
21. Mc Gonagle D., Gibbon W., O'Connor P., et al. A preliminary study of ultrasound aspiration of bone erosion in early rheumatoid arthritis. Rheumatology (Oxford) 38 4 (1999) 329-331
22. Shimizu S., Shiozawa S., Shiozawa K., et al. Quantitative histologic studies on the pathogenesis of periarticular osteoporosis in rheumatoid arthritis. Arthritis Rheum 28 1 (1985) 25-31
23. Gough A., Sambrook P., Devlin J., et al. Osteoclastic activation is the principal mechanism leading to secondary osteoporosis in rheumatoid arthritis. J Rheumatol 25 7 (1998) 1282-1289
24. Kong Y.Y., Yoshida H., Sarosi I., et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 397 6717 (1999) 315-323
25. Kong Y.Y., Feige U., Sarosi I., et al. Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 402 6759 (1999) 304-309
26. Gravallese E.M., Manning C., Tsay A., et al. Synovial tissue in rheumatoid arthritis is a source of osteoclast differentiation factor. Arthritis Rheum 43 2 (2000) 250-258
27. Takayanagi H., Iizuka H., Juji T., et al. Involvement of receptor activator of nuclear factor kappaB ligand/osteoclast differentiation factor in osteoclastogenesis from synoviocytes in rheumatoid arthritis. Arthritis Rheum 43 2 (2000) 259-269
28. Horwood N.J., Kartsogiannis V., Quinn J.M., et al. Activated T lymphocytes support osteoclast formation in vitro. Biochem Biophys Res Commun 265 1 (1999) 144-150
29. Pettit A.R., Walsh N.C., Manning C., et al. RANKL protein is expressed at the pannus-bone interface at sites of articular bone erosion in rheumatoid arthritis. Rheumatology (Oxford) 45 9 (2006) 1068-1076
30. Ritchlin C.T., Haas-Smith S.A., Li P., et al. Mechanisms of TNF-alpha- and RANKL-mediated osteoclastogenesis and bone resorption in psoriatic arthritis. J Clin Invest 111 6 (2003) 821-831
31. Li P., Schwarz E.M., O'Keefe R.J., et al. Systemic tumor necrosis factor alpha mediates an increase in peripheral CD11bhigh osteoclast precursors in tumor necrosis factor alpha-transgenic mice. Arthritis Rheum 50 1 (2004) 265-276
32. Yao Z., Li P., Zhang Q., et al. TNF increases circulating osteoclast precursor numbers by promoting their proliferation and differentiation in the bone marrow through up-regulation of c-fms expression. J Biol Chem 281 17 (2006) 11846-11855
33. Shigeyama Y., Pap T., Kunzler P., et al. Expression of osteoclast differentiation factor in rheumatoid arthritis. Arthritis Rheum 43 11 (2000) 2523-2530
34. Lubberts E., Oppers-Walgreen B., Pettit A.R., et al. Increase in expression of receptor activator of nuclear factor kappaB at sites of bone erosion correlates with progression of inflammation in evolving collagen-induced arthritis. Arthritis Rheum 46 11 (2002) 3055-3064
35. Schett G., Stolina M., Bolon B., et al. Analysis of the kinetics of osteoclastogenesis in arthritic rats. Arthritis Rheum 52 10 (2005) 3192-3201
36. Teitelbaum S.L. Bone resorption by osteoclasts. Science 289 5484 (2000) 1504-1508
37. Suda T., Takahashi N., Udagawa N., et al. Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr Rev 20 3 (1999) 345-357
38. Fox S.W., and Chambers T.J. Interferon-gamma directly inhibits TRANCE-induced osteoclastogenesis. Biochem Biophys Res Commun 276 3 (2000) 868-872
39. Wei S., Wang M.W., Teitelbaum S.L., et al. Interleukin-4 reversibly inhibits osteoclastogenesis via inhibition of NF-kappa B and mitogen-activated protein kinase signaling. J Biol Chem 277 8 (2002) 6622-6630
40. Takayanagi H., Ogasawara K., Hida S., et al. T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-gamma. Nature 408 6812 (2000) 600-605
41. Takayanagi H., Kim S., Matsuo K., et al. RANKL maintains bone homeostasis through c-Fos-dependent induction of interferon-beta. Nature 416 6882 (2002) 744-749
42. Wyzga N., Varghese S., Wikel S., et al. Effects of activated T cells on osteoclastogenesis depend on how they are activated. Bone 35 3 (2004) 614-620
43. Lam J., Takeshita S., Barker J.E., et al. TNF-alpha induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J Clin Invest 106 12 (2000) 1481-1488
44. Kotake S., Udagawa N., Takahashi N., et al. IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 103 9 (1999) 1345-1352
45. Palmqvist P., Persson E., Conaway H.H., et al. IL-6, leukemia inhibitory factor, and oncostatin M stimulate bone resorption and regulate the expression of receptor activator of NF-kappa B ligand, osteoprotegerin, and receptor activator of NF-kappa B in mouse calvariae. J Immunol 169 6 (2002) 3353-3362
46. Koga T., Inui M., Inoue K., et al. Costimulatory signals mediated by the ITAM motif cooperate with RANKL for bone homeostasis. Nature 428 6984 (2004) 758-763
47. Takayanagi H., Kim S., Koga T., et al. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev Cell 3 6 (2002) 889-901
48. Matsuo K., Galson D.L., Zhao C., et al. Nuclear factor of activated T-cells (NFAT) rescues osteoclastogenesis in precursors lacking c-Fos. J Biol Chem 279 25 (2004) 26475-26480
49. Gohda J., Akiyama T., Koga T., et al. RANK-mediated amplification of TRAF6 signaling leads to NFATc1 induction during osteoclastogenesis. EMBO J 24 4 (2005) 790-799
50. Kaifu T., Nakahara J., Inui M., et al. Osteopetrosis and thalamic hypomyelinosis with synaptic degeneration in DAP12-deficient mice. J Clin Invest 111 3 (2003) 323-332
51. Mocsai A., Humphrey M.B., Van Ziffle J.A., et al. The immunomodulatory adapter proteins DAP12 and Fc receptor gamma-chain (FcRgamma) regulate development of functional osteoclasts through the Syk tyrosine kinase. Proc Natl Acad Sci U S A 101 16 (2004) 6158-6163
52. Takayanagi H. Mechanistic insight into osteoclast differentiation in osteoimmunology. J Mol Med 83 3 (2005) 170-179
53. Jimenez-Boj E., Redlich K., Turk B., et al. Interaction between synovial inflammatory tissue and bone marrow in rheumatoid arthritis. J Immunol 175 4 (2005) 2579-2588
54. Bugatti S., Caporali R., Manzo A., et al. Involvement of subchondral bone marrow in rheumatoid arthritis: lymphoid neogenesis and in situ relationship to subchondral bone marrow osteoclast recruitment. Arthritis Rheum 52 11 (2005) 3448-3459
55. Romas E., Gillespie M.T., and Martin T.J. Involvement of receptor activator of NFkappaB ligand and tumor necrosis factor-alpha in bone destruction in rheumatoid arthritis. Bone 30 2 (2002) 340-346
56. Partsch G., Steiner G., Leeb B.F., et al. Highly increased levels of tumor necrosis factor-alpha and other proinflammatory cytokines in psoriatic arthritis synovial fluid. J Rheumatol 24 3 (1997) 518-523
57. Abu-Amer Y., Ross F.P., Edwards J., et al. Lipopolysaccharide-stimulated osteoclastogenesis is mediated by tumor necrosis factor via its P55 receptor. J Clin Invest 100 6 (1997) 1557-1565
58. McInnes I.B., Leung B.P., Sturrock R.D., et al. Interleukin-15 mediates T cell-dependent regulation of tumor necrosis factor-alpha production in rheumatoid arthritis. Nat Med 3 2 (1997) 189-195
59. Koerner T.J., Adams D.O., and Hamilton T.A. Regulation of tumor necrosis factor (TNF) expression: interferon-gamma enhances the accumulation of mRNA for TNF induced by lipopolysaccharide in murine peritoneal macrophages. Cell Immunol 109 2 (1987) 437-443
60. Debets J.M., Van der Linden C.J., Dieteren I.E., et al. Fc-receptor cross-linking induces rapid secretion of tumor necrosis factor (cachectin) by human peripheral blood monocytes. J Immunol 141 4 (1988) 1197-1201
61. Wei S., Kitaura H., Zhou P., et al. IL-1 mediates TNF-induced osteoclastogenesis. J Clin Invest 115 2 (2005) 282-290
62. Kitaura H., Zhou P., Kim H.J., et al. M-CSF mediates TNF-induced inflammatory osteolysis. J Clin Invest 115 12 (2005) 3418-3427
63. Smolen J.S., Han C., Bala M., et al. Evidence of radiographic benefit of treatment with infliximab plus methotrexate in rheumatoid arthritis patients who had no clinical improvement: a detailed subanalysis of data from the anti-tumor necrosis factor trial in rheumatoid arthritis with concomitant therapy study. Arthritis Rheum 52 4 (2005) 1020-1030
64. Nakae S., Saijo S., Horai R., et al. IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc Natl Acad Sci U S A 100 10 (2003) 5986-5990
65. Takagi N., Mihara M., Moriya Y., et al. Blockage of interleukin-6 receptor ameliorates joint disease in murine collagen-induced arthritis. Arthritis Rheum 41 12 (1998) 2117-2121
66. Wong P.K., Quinn J.M., Sims N.A., et al. Interleukin-6 modulates production of T lymphocyte-derived cytokines in antigen-induced arthritis and drives inflammation-induced osteoclastogenesis. Arthritis Rheum 54 1 (2006) 158-168
67. Strand V., and Kavanaugh A.F. The role of interleukin-1 in bone resorption in rheumatoid arthritis. Rheumatology (Oxford) 43 Suppl 3 (2004) iii10-iii16
68. Joosten L.A., Helsen M.M., van de Loo F.A., et al. Anticytokine treatment of established type II collagen-induced arthritis in DBA/1 mice. A comparative study using anti-TNF alpha, anti-IL-1 alpha/beta, and IL-1Ra. Arthritis Rheum 39 5 (1996) 797-809
69. Maini R.N., Breedveld F.C., Kalden J.R., et al. Sustained improvement over two years in physical function, structural damage, and signs and symptoms among patients with rheumatoid arthritis treated with infliximab and methotrexate. Arthritis Rheum 50 4 (2004) 1051-1065
70. Pincus T, Yazici Y, Sokka T, et al. Methotrexate as the "anchor drug" for the treatment of early rheumatoid arthritis. Clin Exp Rheumatol 2003;21(5)(Suppl 31)S179-85.
71. Seitz M., Zwicker M., and Loetscher P. Effects of methotrexate on differentiation of monocytes and production of cytokine inhibitors by monocytes. Arthritis Rheum 41 11 (1998) 2032-2038
72. Li P., Schwarz E.M., O'Keefe R.J., et al. RANK signaling is not required for TNFalpha-mediated increase in CD11(hi) osteoclast precursors but is essential for mature osteoclast formation in TNFalpha-mediated inflammatory arthritis. J Bone Miner Res 19 2 (2004) 207-213
73. Goldring S.R. Bone and joint destruction in rheumatoid arthritis: what is really happening?. J Rheumatol Suppl 65 (2002) 44-48
74. Stanton H., Rogerson F.M., East C.J., et al. ADAMTS5 is the major aggrecanase in mouse cartilage in vivo and in vitro. Nature 434 7033 (2005) 648-652
75. Glasson S.S., Askew R., Sheppard B., et al. Deletion of active ADAMTS5 prevents cartilage degradation in a murine model of osteoarthritis. Nature 434 7033 (2005) 644-648
76. Tanaka S., Nakamura K., Takahasi N., et al. Role of RANKL in physiological and pathological bone resorption and therapeutics targeting the RANKL-RANK signaling system. Immunol Rev 208 (2005) 30-49
77. Bekker P.J., Holloway D.L., Rasmussen A.S., et al. A single-dose placebo-controlled study of AMG 162, a fully human monoclonal antibody to RANKL, in postmenopausal women. J Bone Miner Res 19 7 (2004) 1059-1066
78. McClung M.R., Lewiecki E.M., Cohen S.B., et al. Denosumab in postmenopausal women with low bone mineral density. N Engl J Med 354 8 (2006) 821-831
79. Juji T., Hertz M., Aoki K., et al. A novel therapeutic vaccine approach, targeting RANKL, prevents bone destruction in bone-related disorders. J Bone Miner Metab 20 5 (2002) 266-268
80. Russell R.G., and Rogers M.J. Bisphosphonates: from the laboratory to the clinic and back again. Bone 25 1 (1999) 97-106
81. Green J.R. Bisphosphonates: preclinical review. Oncologist 9 Suppl 4 (2004) 3-13
82. Osterman T., Kippo K., Lauren L., et al. Effect of clodronate on established collagen-induced arthritis in rats. Inflamm Res 44 6 (1995) 258-263
83. Osterman T., Kippo K., Lauren L., Pasanen I., Hannuniemi R., and Sellman R. A comparison of clodronate and indomethacin in the treatment of adjuvant arthritis. Inflamm Res 46 3 (1997) 79-85
84. Kinne R.W., Schmidt-Weber C.B., Hoppe R., et al. Long-term amelioration of rat adjuvant arthritis following systemic elimination of macrophages by clodronate-containing liposomes. Arthritis Rheum 38 12 (1995) 1777-1790
85. Kinne R.W., Schmidt C.B., Buchner E., et al. Treatment of rat arthritides with clodronate-containing liposomes. Scand J Rheumatol Suppl 101 (1995) 91-97
86. Romas E. Bone loss in inflammatory arthritis: mechanisms and therapeutic approaches with bisphosphonates. Best Pract Res Clin Rheumatol 19 6 (2005) 1065-1079
87. Jarrett S., Conaghan P.G., Sloan V.S., et al. Preliminary evidence for a structural benefit of the new bisphosphonate zoledronic acid in early rheumatoid arthritis. Arthritis Rheum 54 5 (2006) 1410-1414
88. Sharp J.T., Van Der Heijde D., Boers M., et al. Repair of erosions in rheumatoid arthritis does occur. Results from 2 studies by the OMERACT Subcommittee on Healing of Erosions. J Rheumatol 30 5 (2003) 1102-1107
89. Martin T.J., and Sims N.A. Osteoclast-derived activity in the coupling of bone formation to resorption. Trends Mol Med 11 2 (2005) 76-81
90. Gilbert L.C., Rubin J., and Nanes M.S. The p55 TNF receptor mediates TNF inhibition of osteoblast differentiation independently of apoptosis. Am J Physiol Endocrinol Metab 288 5 (2005) E1011-E1018
91. Gilbert L., He X., Farmer P., et al. Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/AML3/Pebp2alpha A) is inhibited by tumor necrosis factor-alpha. J Biol Chem 277 4 (2002) 2695-2701
92. Hodsman A.B., Bauer D.C., Dempster D.W., et al. Parathyroid hormone and teriparatide for the treatment of osteoporosis: a review of the evidence and suggested guidelines for its use. Endocr Rev 26 5 (2005) 688-703
93. Redlich K., Gortz B., Hayer S., et al. Repair of local bone erosions and reversal of systemic bone loss upon therapy with anti-tumor necrosis factor in combination with osteoprotegerin or parathyroid hormone in tumor necrosis factor-mediated arthritis. Am J Pathol 164 2 (2004) 543-555
94. Schett G., Middleton S., Bolon B., et al. Additive bone-protective effects of anabolic treatment when used in conjunction with RANKL and tumor necrosis factor inhibition in two rat arthritis models. Arthritis Rheum 52 5 (2005) 1604-1611
95. Sugiyama T., Tanaka H., and Kawai S. Effects of parathyroid hormone and alendronate alone or in combination in osteoporosis. N Engl J Med 350 2 (2004) 189-192 [author reply 189-92]
96. Higashida J., Wun T., Schmidt S., et al. Safety and efficacy of rituximab in patients with rheumatoid arthritis refractory to disease modifying antirheumatic drugs and anti-tumor necrosis factor-alpha treatment. J Rheumatol 32 11 (2005) 2109-2115
97. Genovese M.C., Becker J.C., Schiff M., et al. Abatacept for rheumatoid arthritis refractory to tumor necrosis factor alpha inhibition. N Engl J Med 353 11 (2005) 1114-1123
98. Goldring S.R., and Gravallese E.M. Bisphosphonates: environmental protection for the joint?. Arthritis Rheum 50 7 (2004) 2044-2047
99. Farrugia M.C., Summerlin D.J., Krowiak E., et al. Osteonecrosis of the mandible or maxilla associated with the use of new generation bisphosphonates. Laryngoscope 116 1 (2006) 115-120