Interaction of bone morphogenetic proteins with cells of the osteoclast lineage: Review of the existing evidence

Osteoporosis International

Volumn 18, Issue 12, 2007, Pages 1565-1581

  Giannoudis, P V ^a,c   Kanakaris, N K ^a   Einhorn, T A ^b  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b BOSTON UNIVERSITY MEDICAL CENTER   (United States)

^c LEEDS TEACHING HOSPITALS NHS TRUST   (United Kingdom)

Author keywords

BMPs; Bone morphogenetic proteins; Bone resorption; Osteoclasts; Remodeling; Review

Indexed keywords

ACTIVIN; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; PHOSPHOTRANSFERASE; SMAD PROTEIN;

BONE CELL; BONE DEFECT; CELL ISOLATION; CELL LINEAGE; FRACTURE; GEL MOBILITY SHIFT ASSAY; HUMAN; LEUKAPHERESIS; MONOCYTE; MONONUCLEAR CELL; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW;

ANIMALS; BONE MORPHOGENETIC PROTEINS; BONE REGENERATION; BONE RESORPTION; HUMANS; MICE; MODELS, ANIMAL; OSTEOCLASTS; RATS;

EID: 35448929069     PISSN: 0937941X     EISSN: 14332965     Source Type: Journal    
DOI: 10.1007/s00198-007-0441-x     Document Type: Review

References (102)

1. Olsen BR, Reginato AM, Wang W (2000) Bone development. Annu Rev Cell Dev Biol 16:191-220
2. Einhorn TA, Lee CA (2001) Bone regeneration: new findings and potential clinical applications. J Am Acad Orthop Surg 9:157-165
3. Boskey AL, Posner AS (1984) Bone structure, composition, and mineralization. Orthop Clin North Am 15:597-612
4. Yoshikawa H, Takaoka K (1994) Bone remodelling and its regulators. Nippon Rinsho 52:2262-2267
5. Urist MR (1965) Bone: formation by autoinduction. Science 150:893-899
6. Urist MR, Strates BS (1971) Bone morphogenetic protein. J Dent Res 50:1392-1406
7. Wozney JM, Rosen V, Celeste AJ et al (1988) Novel regulators of bone formation: molecular clones and activities. Science 242:1528-1534
8. Wang EA, Rosen V, Cordes P et al (1988) Purification and characterization of other distinct bone-inducing factors. Proc Natl Acad Sci USA 85:9484-9488
9. Wang EA, Rosen V, D'Alessandro JS et al (1990) Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci USA 87:2220-2224
10. Ozkaynak E, Rueger DC, Drier EA et al (1990) OP-1 cDNA encodes an osteogenic protein in the TGF-beta family. Embo J 9:2085-2093
11. Bessho K, Kusumoto K, Fujimura K et al (1999) Comparison of recombinant and purified human bone morphogenetic protein. Br J Oral Maxillofac Surg 37:2-5
12. Sakou T (1998) Bone morphogenetic proteins: from basic studies to clinical approaches. Bone 22:591-603
13. Termaat MF, Den Boer FC, Bakker FC et al (2005) Bone morphogenetic proteins. Development and clinical efficacy in the treatment of fractures and bone defects. J Bone Joint Surg Am 87:1367-1378
14. Cheng H, Jiang W, Phillips FM et al (2003) Osteogenic activity of the fourteen types of human bone morphogenetic proteins (BMPs). J Bone Joint Surg Am 85-A:1544-1552
15. Jung RE, Glauser R, Scharer P et al (2003) Effect of rhBMP-2 on guided bone regeneration in humans. Clin Oral Implants Res 14:556-568
16. Geesink RG, Hoefnagels NH, Bulstra SK (1999) Osteogenic activity of OP-1 bone morphogenetic protein (BMP-7) in a human fibular defect. J Bone Joint Surg Br 81:710-718
17. Tsumaki N, Yoshikawa H (2005) The role of bone morphogenetic proteins in endochondral bone formation. Cytokine Growth Factor Rev 16:279-285
18. Yamaguchi A, Katagiri T, Ikeda T et al (1991) Recombinant human bone morphogenetic protein-2 stimulates osteoblastic maturation and inhibits myogenic differentiation in vitro. J Cell Biol 113:681-687
19. Harwood PJ, Giannoudis PV (2005) Application of bone morphogenetic proteins in orthopaedic practice: their efficacy and side effects. Expert Opin Drug Saf 4:75-89
20. Dimitriou R, Dahabreh Z, Katsoulis E et al (2005) Application of recombinant BMP-7 on persistent upper and lower limb non-unions. Injury 36(Suppl 4):S51-S59
21. Wong RK, Hagg EU, Rabie AB et al (2002) Bone induction in clinical orthodontics: a review. Int J Adult Orthodon Orthognath Surg 17:140-149
22. Trippel SB, Coutts RD, Einhorn TA et al (1996) Instructional course lectures, the American Academy of Orthopaedic Surgeons - growth factors as therapeutic agents. J Bone Joint Surg Am 78:1272-1286
23. Cook SD (1999) Preclinical and clinical evaluation of osteogenic protein-1 (BMP-7) in bony sites. Orthopedics 22:669-671
24. Kain MS, Einhorn TA (2005) Recombinant human bone morphogenetic proteins in the treatment of fractures. Foot Ankle Clin 10:639-650, viii
25. Meraw SJ, Reeve CM, Lohse CM et al (2000) Treatment of peri-implant defects with combination growth factor cement. J Periodontol 71:8-13
26. Cook SD, Barrack RL, Shimmin A et al (2001) The use of osteogenic protein-1 in reconstructive surgery of the hip. J Arthroplasty 16:88-94
27. Einhorn TA, Trippel SB (1997) Growth factor treatment of fractures. Instr Course Lect 46:483-486
28. Friedlaender GE, Perry CR, Cole JD et al (2001) Osteogenic protein-1 (bone morphogenetic protein-7) in the treatment of tibial nonunions. J Bone Joint Surg Am 83-A Suppl 1:S151-S158
29. Einhorn TA (2003) Clinical applications of recombinant human BMPs: early experience and future development. J Bone Joint Surg Am 85-A Suppl 3:82-88
30. Govender S, Csimma C, Genant HK et al (2002) Recombinant human bone morphogenetic protein-2 for treatment of open tibial fractures: a prospective, controlled, randomized study of four hundred and fifty patients. J Bone Joint Surg Am 84-A:2123-2134
31. Sakata H, Takagi K (1987) Effect of bone marrow mononuclear phagocytes on the bone matrix-induced bone formation in rats. Clin Orthop Relat Res 253-258
32. Tanaka S, Nakamura I, Inoue J et al (2003) Signal transduction pathways regulating osteoclast differentiation and function. J Bone Miner Metab 21:123-133
33. Serke S, Sauberlich S, Abe Y et al (1991) Analysis of CD34-positive hemopoietic progenitor cells from normal human adult peripheral blood: flow-cytometrical studies and in-vitro colony (CFU-GM, BFU-E) assays. Ann Hematol 62:45-53
34. Miyamoto T, Ohneda O, Arai F et al (2001) Bifurcation of osteoclasts and dendritic cells from common progenitors. Blood 98:2544-2554
35. Roodman GD (2006) Regulation of osteoclast differentiation. Ann N Y Acad Sci 1068:100-109
36. Dougall WC, Glaccum M, Charrier K et al (1999) RANK is essential for osteoclast and lymph node development. Genes Dev 13:2412-2424
37. Lacey DL, Timms E, Tan HL et al (1998) Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93:165-176
38. Otsuka E, Notoya M, Hagiwara H (2003) Treatment of myoblastic C2C12 cells with BMP-2 stimulates vitamin D-induced formation of osteoclasts. Calcif Tissue Int 73:72-77
39. Kanatani M, Sugimoto T, Kaji H et al (1995) Stimulatory effect of bone morphogenetic protein-2 on osteoclast-like cell formation and bone-resorbing activity. J Bone Miner Res 10:1681-1690
40. Manolagas SC, Jilka RL (1995) Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med 332:305-311
41. Choi SJ, Han JH, Roodman GD (2001) ADAM8: a novel osteoclast stimulating factor. J Bone Miner Res 16:814-822
42. Takahashi S, Reddy SV, Chirgwin JM et al (1994) Cloning and identification of annexin II as an autocrine/paracrine factor that increases osteoclast formation and bone resorption. J Biol Chem 269:28696-28701
43. Udagawa N (2002) Mechanisms involved in bone resorption. Biogerontology 3:79-83
44. Suda T, Takahashi N, Udagawa N et al (1999) Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr Rev 20:345-357
45. Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239-257
46. Wyllie AH, Kerr JF, Currie AR (1980) Cell death: the significance of apoptosis. Int Rev Cytol 68:251-306
47. Koide M, Murase Y, Yamato K et al (1999) Bone morphogenetic protein-2 enhances osteoclast formation mediated by interleukin-1alpha through upregulation of osteoclast differentiation factor and cyclooxygenase-2. Biochem Biophys Res Commun 259:97-102
48. Suda T, Jimi E, Nakamura I et al (1997) Role of 1 alpha,25- dihydroxyvitamin D3 in osteoclast differentiation and function. Methods Enzymol 282:223-235
49. Nicholson GC, Moseley JM, Sexton PM et al (1986) Abundant calcitonin receptors in isolated rat osteoclasts. Biochemical and autoradiographic characterization. J Clin Invest 78:355-360
50. Hattersley G, Chambers TJ (1989) Calcitonin receptors as markers for osteoclastic differentiation: correlation between generation of bone-resorptive cells and cells that express calcitonin receptors in mouse bone marrow cultures. Endocrinology 125:1606-1612
51. Takada Y, Kusuda M, Hiura K et al (1992) A simple method to assess osteoclast-mediated bone resorption using unfractionated bone cells. Bone Miner 17:347-359
52. Massague J (1996) TGFbeta signaling: receptors, transducers, and Mad proteins. Cell 85:947-950
53. Derynck R, Feng XH (1997) TGF-beta receptor signaling. Biochim Biophys Acta 1333:F105-F150
54. Chen D, Zhao M, Mundy G (2004) Bone Morphogenetic Proteins. Growth Factors 22:233-241
55. Lieberman JR, Daluiski A, Einhorn TA (2002) The role of growth factors in the repair of bone. Biology and clinical applications. J Bone Joint Surg Am 84-A:1032-1044
56. Massague J, Wotton D (2000) Transcriptional control by the TGF-beta/Smad signaling system. Embo J 19:1745-1754
57. Granjeiro JM, Oliveira RC, Bustos-Valenzuela JC et al (2005) Bone morphogenetic proteins: from structure to clinical use. Braz J Med Biol Res 38:1463-1473
58. Canalis E, Economides AN, Gazzerro E (2003) Bone morphogenetic proteins, their antagonists, and the skeleton. Endocr Rev 24:218-235
59. Kuriyama S, Lupo G, Ohta K et al (2006) Tsukushi controls ectodermal patterning and neural crest specification in Xenopus by direct regulation of BMP4 and X-delta-1 activity. Development 133:75-88
60. Yanagita M (2005) BMP antagonists: their roles in development and involvement in pathophysiology. Cytokine Growth Factor Rev 16:309-317
61. Cunningham NS, Paralkar V, Reddi AH (1992) Osteogenin and recombinant bone morphogenetic protein 2B are chemotactic for human monocytes and stimulate transforming growth factor beta 1 mRNA expression. Proc Natl Acad Sci US'A 89:11740-11744
62. Hentunen TA, Cunningham NS, Vuolteenaho O et al (1994) Osteoclast recruiting activity in bone matrix. Bone Miner 25:183-198
63. Nakase T, Nomura S, Yoshikawa H et al (1994) Transient and localized expression of bone morphogenetic protein 4 messenger RNA during fracture healing. J Bone Miner Res 9:651-659
64. Hentunen TA, Lakkakorpi PT, Tuukkanen J et al (1995) Effects of recombinant human osteogenic protein-1 on the differentiation of osteoclast-like cells and bone resorption. Biochem Biophys Res Commun 209:433-443
65. Hodges PT, Baehner FL, Masuhara K et al (1997) Immunolocalization of bone morphogenetic protein-4 and -6 in human growth plate. Trans Orthop Res Soc 22:615
66. Nishimura T, Simmons DJ, Mainous EG (1997) The origin of bone formed by heterotopic periosteal autografts. J Oral Maxillofac Surg 55:1265-1268
67. Helder MN, Karg H, Bervoets TJ et al (1998) Bone morphogenetic protein-7 (osteogenic protein-1, OP-1) and tooth development. J Dent Res 77:545-554
68. Hofbauer LC, Dunstan CR, Spelsberg TC et al (1998) Osteoprotegerin production by human osteoblast lineage cells is stimulated by vitamin D, bone morphogenetic protein-2, and cytokines. Biochem Biophys Res Commun 250:776-781
69. Onishi T, Ishidou Y, Nagamine T et al (1998) Distinct and overlapping patterns of localization of bone morphogenetic protein (BMP) family members and a BMP type II receptor during fracture healing in rats. Bone 22:605-612
70. Anderson H, Hodges P, Moylan P (1999) Bone morphogenetic protein expression by cells of human and rat growth plate, metaphysis and articular cartilage. J Bone Miner Res 14(Suppl 1):S530-S539
71. Abe E, Yamamoto M, Taguchi Y et al (2000) Essential requirement of BMPs-2/4 for both osteoblast and osteoclast formation in murine bone marrow cultures from adult mice: antagonism by noggin. J Bone Miner Res 15:663-673
72. Anderson HC, Hodges PT, Aguilera XM et al (2000) Bone morphogenetic protein (BMP) localization in developing human and rat growth plate, metaphysis, epiphysis, and articular cartilage. J Histochem Cytochem 48:1493-1502
73. Kaneko H, Arakawa T, Mano H et al (2000) Direct stimulation of osteoclastic bone resorption by bone morphogenetic protein (BMP)-2 and expression of BMP receptors in mature osteoclasts. Bone 27:479-486
74. Itoh K, Udagawa N, Katagiri T et al (2001) Bone morphogenetic protein 2 stimulates osteoclast differentiation and survival supported by receptor activator of nuclear factor-kappaB ligand. Endocrinology 142:3656-3662
75. Koseki T, Gao Y, Okahashi N et al (2002) Role of TGF-beta family in osteoclastogenesis induced by RANKL. Cell Signal 14:31-36
76. Irie K, Alpaslan C, Takahashi K et al (2003) Osteoclast differentiation in ectopic bone formation induced by recombinant human bone morphogenetic protein 2 (rhBMP-2). J Bone Miner Metab 21:363-369
77. Kusu N, Laurikkala J, Imanishi M et al (2003) Sclerostin is a novel secreted osteoclast-derived bone morphogenetic protein antagonist with unique ligand specificity. J Biol Chem 278:24113-24117
78. Mishina Y, Starbuck MW, Gentile MA et al (2004) Bone morphogenetic protein type IA receptor signaling regulates postnatal osteoblast function and bone remodeling. J Biol Chem 279:27560-27566
79. Saito A, Suzuki Y, Ogata S et al (2004) Prolonged ectopic calcification induced by BMP-2-derived synthetic peptide. J Biomed Mater Res A 70:115-121
80. Wise GE, Ding D, Yao S (2004) Regulation of secretion of osteoprotegerin in rat dental follicle cells. Eur J Oral Sci 112:439-444
81. Cowan CM, Aalami OO, Shi YY et al (2005) Bone morphogenetic protein 2 and retinoic acid accelerate in vivo bone formation, osteoclast recruitment, and bone turnover. Tissue Eng 11:645-658
82. Little DG, McDonald M, Bransford R et al (2005) Manipulation of the anabolic and catabolic responses with OP-1 and zoledronic acid in a rat critical defect model. J Bone Miner Res 20:2044-2052
83. Liu D, Yao S, Pan F et al (2005) Chronology and regulation of gene expression of RANKL in the rat dental follicle. Eur J Oral Sci 113:404-409
84. Takahashi D, Odajima T, Morita M et al (2005) Formation and resolution of ankylosis under application of recombinant human bone morphogenetic protein-2 (rhBMP-2) to class III furcation defects in cats. J Periodontal Res 40:299-305
85. Wildemann B, Kadow-Romacker A, Lubberstedt M et al (2005) Differences in the fusion and resorption activity of human osteoclasts after stimulation with different growth factors released from a polylactide carrier. Calcif Tissue Int 76:50-55
86. Feeley BT, Krenek L, Liu N et al (2006) Overexpression of noggin inhibits BMP-mediated growth of osteolytic prostate cancer lesions. Bone 38:154-166
87. Ghosh-Choudhury N, Singha PK, Woodruff K et al (2006) Concerted action of Smad and CREB-binding protein regulates bone morphogenetic protein-2-stimulated osteoblastic colony-stimulating factor-1 expression. J Biol Chem 281:20160-20170
88. Miyaji H, Sugaya T, Kato K et al (2006) Dentin resorption and cementum-like tissue formation by bone morphogenetic protein application. J Periodontal Res 41:311-315
89. Okamoto M, Murai J, Yoshikawa H et al (2006) Bone morphogenetic proteins in bone stimulate osteoclasts and osteoblasts during bone development. J Bone Miner Res 21:1022-1033
90. Wan C, He Q, Li G (2006) Osteoclastogenesis in the nonadherent cell population of human bone marrow is inhibited by rhBMP-2 alone or together with rhVEGF. J Orthop Res 24:29-36
91. Wutzl A, Brozek W, Lernbass I et al (2006) Bone morphogenetic proteins 5 and 6 stimulate osteoclast generation. J Biomed Mater Res A 77:75-83
92. Yamamoto Y, Udagawa N, Matsuura S et al (2006) Osteoblasts provide a suitable microenvironment for the action of receptor activator of nuclear factor-kappaB ligand. Endocrinology 147:3366-3374
93. Ellies DL, Viviano B, McCarthy J et al (2006) Bone density ligand, Sclerostin, directly interacts with LRP5 but not LRP5G171V to modulate Wnt activity. J Bone Miner Res 21:1738-1749
94. Poole KE, van Bezooijen RL, Loveridge N et al (2005) Sclerostin is a delayed secreted product of osteocytes that inhibits bone formation. Faseb J 19:1842-1844
95. van Bezooijen RL, Roelen BA, Visser A et al (2004) Sclerostin is an osteocyte-expressed negative regulator of bone formation, but not a classical BMP antagonist. J Exp Med 199:805-814
96. Laursen M, Hoy K, Hansen ES et al (1999) Recombinant bone morphogenetic protein-7 as an intracorporal bone growth stimulator in unstable thoracolumbar burst fractures in humans: preliminary results. Eur Spine J 8:485-490
97. Pradhan BB, Bae HW, Dawson EG et al (2006) Graft resorption with the use of bone morphogenetic protein: lessons from anterior lumbar interbody fusion using femoral ring allografts and recombinant human bone morphogenetic protein-2. Spine 31:E277-E284
98. Jeppsson C, Astrand J, Tagil M et al (2003) A combination of bisphosphonate and BMP additives in impacted bone allografts. Acta Orthop Scand 74:483-489
99. Dimitriou R, Tsiridis E, Giannoudis PV (2005) Current concepts of molecular aspects of bone healing. Injury 36:1392-1404
100. Poynton AR, Lane JM (2002) Safety profile for the clinical use of bone morphogenetic proteins in the spine. Spine 27:S40-S48
101. Hansen SM, Sasso RC (2006) Resorptive response of rhBMP2 simulating infection in an anterior lumbar interbody fusion with a femoral ring. J Spinal Disord Tech 19:130-134
102. Höstner J, Karrhölm J, Hultmark P (2000) Early failures after femoral revisions using milled allograft bone mixed with OP-1. Poster Presentation. In SOF 2000. pp 205-206