The osteoclast, bone remodelling and treatment of metabolic bone disease

European Journal of Clinical Investigation

Volumn 42, Issue 12, 2012, Pages 1332-1341

  Boyce, Brendan F ^a   Rosenberg, Elizabeth ^b   de Papp, Anne E ^b   Duong, Le T ^b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b MERCK RESEARCH LABORATORIES   (United States)

Author keywords

Bone formation; Bone remodelling; Bone resorption; Coupling; Osteoclast

Indexed keywords

ALENDRONIC ACID; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 6; CELL SURFACE PROTEIN; COLONY STIMULATING FACTOR 1; IBANDRONIC ACID; INTERLEUKIN 1; NEUROPILIN 1; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PARATHYROID HORMONE; RISEDRONIC ACID; SELECTIVE ESTROGEN RECEPTOR MODULATOR; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; TRANSCRIPTION FACTOR AP 1; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; ZOLEDRONIC ACID;

APOPTOSIS; BONE REMODELING; CELL DIFFERENTIATION; CELL FUNCTION; CELL SURVIVAL; CYTOKINE RESPONSE; ENDOCYTOSIS; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; MENOPAUSE; METABOLIC BONE DISEASE; OSSIFICATION; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; OSTEOMYELITIS; OSTEOPOROSIS; PERIODONTITIS; PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REVIEW; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION;

BONE DENSITY CONSERVATION AGENTS; BONE DISEASES, METABOLIC; BONE REMODELING; BONE RESORPTION; DRUG DESIGN; HUMANS; MACROPHAGE COLONY-STIMULATING FACTOR; OSTEOBLASTS; OSTEOCLASTS; RANK LIGAND;

EID: 84869863662     PISSN: 00142972     EISSN: 13652362     Source Type: Journal    
DOI: 10.1111/j.1365-2362.2012.02717.x     Document Type: Review

References (73)

1. Seeman E. Bone modeling and remodeling. Crit Rev Eukaryot Gene Expr 2009;19:219-33.
2. Eriksen EF. Cellular mechanisms of bone remodeling. Rev Endocr Metab Disord 2010;11:219-27.
3. Cummings SR, Melton LJ. Epidemiology and outcomes of osteoporotic fractures. Lancet 2002;359:1761-7.
4. Del Fattore A, Cappariello A, Teti A. Genetics, pathogenesis and complications of osteopetrosis. Bone 2008;42:19-29.
5. Heaney RP. Is the paradigm shifting? Bone 2003;33:457-65.
6. Henriksen K, Bollerslev J, Everts V, Karsdal MA. Osteoclast activity and subtypes as a function of physiology and pathology - implications for future treatments of osteoporosis. Endocr Rev 2011;32:31-63.
7. Muto A, Mizoguchi T, Udagawa N, Ito S, Kawahara I, Abiko Y et al. Lineage-committed osteoclast precursors circulate in blood and settle down into bone. J Bone Miner Res 2011;26:2978-90.
8. Boyce BF, Xing L. Functions of RANKL/RANK/OPG in bone modeling and remodeling. Arch Biochem Biophys 2008;473:139-46.
9. Vaananen K. Mechanism of osteoclast mediated bone resorption - rationale for the design of new therapeutics. Adv Drug Deliv Rev 2005;57:959-71.
10. Mellis D, Itzstein C, Helfrich MH, Crockett JC. The skeleton: a multi-functional complex organ: the role of key signalling pathways in osteoclast differentiation and in bone resorption. J Endocrinol 2011;211:131-43.
11. Maeda K, Kobayashi Y, Udagawa N, Uehara S, Ishihara A, Mizoguchi T et al. Wnt5a-Ror2 signaling between osteoblast-lineage cells and osteoclast precursors enhances osteoclastogenesis. Nat Med 2012;18:405-12.
12. Hayashi M, Nakashima T, Taniguchi M, Kodama T, Kumanogoh A, Takayanagi H. Osteoprotection by semaphorin 3A. Nature 2012;485:69-74.
13. Yao Z, Xing L, Boyce BF. NF-kappaB p100 limits TNF-induced bone resorption in mice by a TRAF3-dependent mechanism. J Clin Invest 2009;119:3024-34.
14. Boyce BF, Yao Z, Xing L. Osteoclasts have multiple roles in bone in addition to bone resorption. Crit Rev Eukaryot Gene Expr 2009;19:171-80.
15. Takayanagi H. Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems. Nat Rev Immunol 2007;7:292-304.
16. Barrow AD, Raynal N, Andersen TL, Slatter DA, Bihan D, Pugh N et al. OSCAR is a collagen receptor that costimulates osteoclastogenesis in DAP12-deficient humans and mice. J Clin Invest 2011;121:3505-16.
17. Okamoto K, Takayanagi H. Regulation of bone by the adaptive immune system in arthritis. Arthritis Res Ther 2011;13:219.
18. Manabe N, Kawaguchi H, Chikuda H, Miyaura C, Inada M, Nagai R et al. Connection between B lymphocyte and osteoclast differentiation pathways. J Immunol 2001;167:2625-31.
19. Weitzmann MN, Cenci S, Haug J, Brown C, DiPersio J, Pacifici R. B lymphocytes inhibit human osteoclastogenesis by secretion of TGFbeta. J Cell Biochem 2000;78:318-24.
20. Bonewald LF. The amazing osteocyte. J Bone Miner Res 2011;26:229-38.
21. Tatsumi S, Ishii K, Amizuka N, Li M, Kobayashi T, Kohno K. Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab 2007;5:464-75.
22. Nakashima T, Hayashi M, Fukunaga T, Kurata K, Oh-Hora M, Feng JQ. Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat Med 2011;17:1231-4.
23. Xiong J, Onal M, Jilka RL, Weinstein RS, Manolagas SC, O'Brien CA. Matrix-embedded cells control osteoclast formation. Nat Med 2011;17:1235-41.
24. Ishii M, Egen JG, Klauschen F, Meier-Schellersheim M, Saeki Y, Vacher J et al. Sphingosine-1-phosphate mobilizes osteoclast precursors and regulates bone homeostasis. Nature 2009;458:524-8.
25. Ishii M, Kikuta J, Shimazu Y, Meier-Schellersheim M, Germain RN. Chemorepulsion by blood S1P regulates osteoclast precursor mobilization and bone remodeling in vivo. J Exp Med 2010;207:2793-8.
26. Kikuta J, Iwai K, Saeki Y, Ishii M. S1P-targeted therapy for elderly rheumatoid arthritis patients with osteoporosis. Rheumatol Int 2011;31:967-9.
27. Teitelbaum SL. Osteoclasts and integrins. Ann N Y Acad Sci 2006;1068:95-9.
28. Boyce BF, Yoneda T, Lowe C, Soriano P, Mundy GR. Requirement of pp60c-src expression for osteoclasts to form ruffled borders and resorb bone in mice. J Clin Invest 1992;90:1622-7.
29. Segovia-Silvestre T, Neutzsky-Wulff AV, Sorensen MG, Christiansen C, Bollerslev J, Karsdal MA et al. Advances in osteoclast biology resulting from the study of osteopetrotic mutations. Hum Genet 2009;124:561-77.
30. Kornak U, Kasper D, Bosl MR, Kaiser E, Schweizer M, Schulz A et al. Loss of the ClC-7 chloride channel leads to osteopetrosis in mice and man. Cell 2001;104:205-15.
31. Lecaille F, Bromme D, Lalmanach G. Biochemical properties and regulation of cathepsin K activity. Biochimie 2008;90:208-26.
32. Li CY, Jepsen KJ, Majeska RJ, Zhang J, Ni R, Gelb BD et al. Mice lacking cathepsin K maintain bone remodeling but develop bone fragility despite high bone mass. J Bone Miner Res 2006;21:865-75.
33. Gowen M, Lazner F, Dodds R, Kapadia R, Feild J, Tavaria M et al. Cathepsin K knockout mice develop osteopetrosis due to a deficit in matrix degradation but not demineralization. J Bone Miner Res 1999;14:1654-63.
34. Pennypacker B, Shea M, Liu Q, Masarachia P, Saftig P, Rodan S et al. Bone density, strength, and formation in adult cathepsin K (-/-) mice. Bone 2009;44:199-207.
35. Delaisse JM, Andersen TL, Engsig MT, Henriksen K, Troen T, Blavier L. Matrix metalloproteinases (MMP) and cathepsin K contribute differently to osteoclastic activities. Microsc Res Tech 2003;61:504-13.
36. Kiviranta R, Morko J, Alatalo SL, NicAmhlaoibh R, Risteli J, Laitala-Leinonen T et al. Impaired bone resorption in cathepsin K-deficient mice is partially compensated for by enhanced osteoclastogenesis and increased expression of other proteases via an increased RANKL/OPG ratio. Bone 2005;36:159-72.
37. Boyce BF, Xing L, Jilka RL, Bellido T, Weinstein RS, Parfitt AM et al. Apoptosis in bone cells. Bilezikian JP, Raisz LG, Rodan GA, editors. Principles of Bone Biology. San Diego, CA: Academic Press; 2002: pp 151-68.
38. Lorget F, Kamel S, Mentaverri R, Wattel A, Naassila M, Maamer M et al. High extracellular calcium concentrations directly stimulate osteoclast apoptosis. Biochem Biophys Res Commun 2000;268:899-903.
39. Hughes DE, Dai A, Tiffee JC, Li HH, Mundy GR, Boyce BF. Estrogen promotes apoptosis of murine osteoclasts mediated by TGF-beta. Nat Med 1996;2:1132-6.
40. Hughes DE, Wright KR, Uy HL, Sasaki A, Yoneda T, Roodman GD et al. Bisphosphonates promote apoptosis in murine osteoclasts in vitro and in vivo. J Bone Miner Res 1995;10:1478-87.
41. Everts V, Delaisse JM, Korper W, Jansen DC, Tigchelaar-Gutter W, Saftig P et al. The bone lining cell: its role in cleaning Howship's lacunae and initiating bone formation. J Bone Miner Res 2002;17:77-90.
42. Karsdal MA, Martin TJ, Bollerslev J, Christiansen C, Henriksen K. Are nonresorbing osteoclasts sources of bone anabolic activity? J Bone Miner Res 2007;22:487-94.
43. Martin TJ, Sims NA. Osteoclast-derived activity in the coupling of bone formation to resorption. Trends Mol Med 2005;11:76-81.
44. Fuller K, Lawrence KM, Ross JL, Grabowska UB, Shiroo M, Samuelsson B et al. Cathepsin K inhibitors prevent matrix-derived growth factor degradation by human osteoclasts. Bone 2008;42:200-11.
45. Tang Y, Wu X, Lei W, Pang L, Wan C, Shi Z et al. TGF-beta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nat Med 2009;15:757-65.
46. Karsdal MA, Neutzsky-Wulff AV, Dziegiel MH, Christiansen C, Henriksen K. Osteoclasts secrete non-bone derived signals that induce bone formation. Biochem Biophys Res Commun 2008;366:483-8.
47. Kreja L, Brenner RE, Tautzenberger A, Liedert A, Friemert B, Ehrnthaller C et al. Non-resorbing osteoclasts induce migration and osteogenic differentiation of mesenchymal stem cells. J Cell Biochem 2010;109:347-55.
48. Pederson L, Ruan M, Westendorf JJ, Khosla S, Oursler MJ. Regulation of bone formation by osteoclasts involves Wnt/BMP signaling and the chemokine sphingosine-1-phosphate. Proc Natl Acad Sci USA 2008;105:20764-9.
49. Lee SH, Rho J, Jeong D, Sul JY, Kim T, Kim N et al. v-ATPase V0 subunit d2-deficient mice exhibit impaired osteoclast fusion and increased bone formation. Nat Med 2006;12:1403-9.
50. Pasquale EB. Eph-ephrin bidirectional signaling in physiology and disease. Cell 2008;133:38-52.
51. Zhao C, Irie N, Takada Y, Shimoda K, Miyamoto T, Nishiwaki T et al. Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis. Cell Metab 2006;4:111-21.
52. Negishi-Koga T, Shinohara M, Komatsu N, Bito H, Kodama T, Friedel RH et al. Suppression of bone formation by osteoclastic expression of semaphorin 4D. Nat Med 2011;17:1473-80.
53. Rogers MJ, Crockett JC, Coxon FP, Monkkonen J. Biochemical and molecular mechanisms of action of bisphosphonates. Bone 2011;49:34-41.
54. Venken K, Boonen S, Bouillon R, Vanderschueren D. Gonadal steroids. Compston JE, Lian JB, editors. Primer on the Metabolic Bone Diseases and Disorders of Mineral Metabolism, 7th Edn. Washington, DC: American Society for Bone and Mineral Research; 2008: pp 117-22.
55. Yan MZ, Xu Y, Gong YX, Liu JM, Lu SY, Huang L et al. Raloxifene inhibits bone loss and improves bone strength through an Opg-independent mechanism. Endocrine 2010;37:55-61.
56. Cummings SR, San Martin J, McClung MR, Siris ES, Eastell R, Reid IR et al. Denosumab for prevention of fractures in postmenopausal women with osteoporosis. N Engl J Med 2009;361:756-65.
57. Boonen S, Rosenberg E, Claessens F, Vanderschueren D, Papapoulos S. Inhibition of Cathepsin K for Osteoporosis. Curr Osteoporos Rep 2012;10:73-9.
58. Eisman JA, Bone HG, Hosking DJ, McClung MR, Reid IR, Rizzoli R et al. Odanacatib in the treatment of postmenopausal women with low bone mineral density: three-year continued therapy and resolution of effect. J Bone Miner Res 2010;25:937-47.
59. Langdahl B, Binkley N, Bone H, Gilchrist N, Resch H, Portales JR, Denker A, Lombardi A, De Tilleghem CL, Dasilva C, Rosenberg E, Leung A. Odanacatib in the treatment of postmenopausal women with low bone mineral density: 5 years of continued therapy in a phase 2 study. J Bone Miner Res. July, 2012. doi: 10.1002/jbmr.1695. [Epub ahead of print].
60. Ochi Y, Yamada H, Mori H, Nakanishi Y, Nishikawa S, Kayasuga R et al. Effects of ONO-5334, a novel orally-active inhibitor of cathepsin K, on bone metabolism. Bone 2011;49:1351-6.
61. Eastell R, Nagase S, Ohyama M, Small M, Sawyer J, Boonen S et al. Safety and efficacy of the cathepsin K inhibitor ONO-5334 in postmenopausal osteoporosis: the OCEAN study. J Bone Miner Res 2011;26:1303-12.
62. Hannon RA, Clack G, Rimmer M, Swaisland A, Lockton JA, Finkelman RD et al. Effects of the Src kinase inhibitor saracatinib (AZD0530) on bone turnover in healthy men: a randomized, double-blind, placebo-controlled, multiple-ascending-dose phase I trial. J Bone Miner Res 2010;25:463-71.
63. Boyce BF, Xing L. Src inhibitors in the treatment of metastatic bone disease - rationale and clinical data. Clin Investig 2011;1:1695-706.
64. Marie PJ, Felsenberg D, Brandi ML. How strontium ranelate, via opposite effects on bone resorption and formation, prevents osteoporosis. Osteoporos Int 2011;22:1659-67.
65. Caudrillier A, Hurtel-Lemaire AS, Wattel A, Cournarie F, Godin C, Petit L et al. Strontium ranelate decreases receptor activator of nuclear factor-KappaB ligand-induced osteoclastic differentiation in vitro: involvement of the calcium-sensing receptor. Mol Pharmacol 2010;78:569-76.
66. Meunier PJ, Roux C, Seeman E, Ortolani S, Badurski JE, Spector TD et al. The effects of strontium ranelate on the risk of vertebral fracture in women with postmenopausal osteoporosis. N Engl J Med 2004;350:459-68.
67. Terauchi M, Li JY, Bedi B, Baek KH, Tawfeek H, Galley S et al. T lymphocytes amplify the anabolic activity of parathyroid hormone through Wnt10b signaling. Cell Metab 2009;10:229-40.
68. Luiz de Freitas PH, Li M, Ninomiya T, Nakamura M, Ubaidus S, Oda K et al. Intermittent PTH administration stimulates pre-osteoblastic proliferation without leading to enhanced bone formation in osteoclast-less c-fos(-/-) mice. J Bone Miner Res 2009;24:1586-97.
69. Black DM, Greenspan SL, Ensrud KE, Palermo L, McGowan JA, Lang TF et al. The effects of parathyroid hormone and alendronate alone or in combination in postmenopausal osteoporosis. N Engl J Med 2003;349:1207-15.
70. Cosman F, Nieves J, Woelfert L, Shen V, Lindsay R. Alendronate does not block the anabolic effect of PTH in postmenopausal osteoporotic women. J Bone Miner Res 1998;13:1051-5.
71. Horwitz MJ, Tedesco MB, Garcia-Ocana A, Sereika SM, Prebehala L, Bisello A et al. Parathyroid hormone-related protein for the treatment of postmenopausal osteoporosis: defining the maximal tolerable dose. J Clin Endocrinol Metab 2010;95:1279-87.
72. Papapoulos SE. Targeting sclerostin as potential treatment of osteoporosis. Ann Rheum Dis 2011;70(Suppl. 1):i119-22.
73. Padhi D, Jang G, Stouch B, Fang L, Posvar E. Single-dose, placebo-controlled, randomized study of AMG 785, a sclerostin monoclonal antibody. J Bone Miner Res 2011;26:19-26.