Osteoclast-derived coupling factors in bone remodeling

Calcified Tissue International

Volumn 94, Issue 1, 2014, Pages 88-97

  Henriksen, Kim ^a   Karsdal, Morten A ^a   John Martin, T ^b  

^a NORDIC BIOSCIENCE A S   (Denmark)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Bone turnover; Osteoblast; Osteoclast; Osteoprotegerin; RANK; RANKL; Remodeling

Indexed keywords

EPHRIN; SEMAPHORIN;

ARTICLE; BONE MASS; BONE MATRIX; BONE REMODELING; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINEAGE; COUPLING FACTOR; HUMAN; IN VITRO STUDY; NERVE FIBER; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; OSTEOCLASTOGENESIS; PRIORITY JOURNAL; TARGET CELL;

ANIMALS; BONE REMODELING; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; OSTEOBLASTS; OSTEOCLASTS; OSTEOGENESIS;

EID: 84893736988     PISSN: 0171967X     EISSN: 14320827     Source Type: Journal    
DOI: 10.1007/s00223-013-9741-7     Document Type: Article

References (89)

1. Hattner R, Epker BN, Frost HM (1965) Suggested sequential mode of control of changes in cell behaviour in adult bone remodelling. Nature 206:489-490
2. Ford JK, Young RW (1963) Cell proliferation and displacement in the adrenal cortex of young rats injected with tritiated thymidine. Anat Rec 146:125-137
3. Harris WH, Heaney RP (1969) Skeletal renewal and metabolic bone disease. N Engl J Med 280:303-311
4. Parfitt AM (1982) The coupling of bone formation to bone resorption: a critical analysis of the concept and of its relevance to the pathogenesis of osteoporosis. Metab Bone Dis Relat Res 4:1-6
5. Rodan GA, Martin TJ (1981) Role of osteoblasts in hormonal control of bone resorption - a hypothesis. Calcif Tissue Int 33:349-351
6. Chambers TJ (1985) The pathobiology of the osteoclast. J Clin Pathol 38:241-252
7. Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, Burgess T, Elliott R, Colombero A, Elliott G, Scully S, Hsu H, Sullivan J, Hawkins N, Davy E, Capparelli C, Eli A, Qian YX, Kaufman S, Sarosi I, Shalhoub V, Senaldi G, Guo J, Delaney J, Boyle WJ (1998) Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93:165-176
8. Simonet WS, Lacey DL, Dunstan CR, Kelley M, Chang MS, Luthy R, Nguyen HQ, Wooden S, Bennett L, Boone T, Shimamoto G, DeRose M, Elliott R, Colombero A, Tan HL, Trail G, Sullivan J, Davy E, Bucay N, Renshaw-Gegg L, Hughes TM, Hill D, Pattison W, Campbell P, Sander S, Van G, Tarpley J, Derby P, Lee R, Boyle WJ (1997) Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell 89:309-319
9. Yasuda H, Shima N, Nakagawa N, Mochizuki SI, Yano K, Fujise N, Sato Y, Goto M, Yamaguchi K, Kuriyama M, Kanno T, Murakami A, Tsuda E, Morinaga T, Higashio K (1998) Identity of osteoclastogenesis inhibitory factor (OCIF) and osteoprotegerin (OPG): a mechanism by which OPG/OCIF inhibits osteoclastogenesis in vitro. Endocrinology 139:1329-1337
10. Boyle WJ, Simonet WS, Lacey DL (2003) Osteoclast differentiation and activation. Nature 423:337-342
11. Henriksen K, Bollerslev J, Everts V, Karsdal MA (2011) Osteoclast activity and subtypes as a function of physiology and pathology - implications for future treatments of osteoporosis. Endocr Rev 32:31-63
12. Howard GA, Bottemiller BL, Turner RT, Rader JI, Baylink DJ (1981) Parathyroid hormone stimulates bone formation and resorption in organ culture: evidence for a coupling mechanism. Proc Natl Acad Sci USA 78:3204-3208
13. Tang Y, Wu X, Lei W, Pang L, Wan C, Shi Z, Zhao L, Nagy TR, Peng X, Hu J, Feng X, Van HW, Wan M, Cao X (2009) TGF-beta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nat Med 15:757-765
14. Xian L, Wu X, Pang L, Lou M, Rosen CJ, Qiu T, Crane J, Frassica F, Zhang L, Rodriguez JP, Xiaofeng J, Shoshana Y, Shouhong X, Argiris E, Mei W, Xu C (2012) Matrix IGF-1 maintains bone mass by activation of mTOR in mesenchymal stem cells. Nat Med 18:1095-1101
15. Segovia-Silvestre T, Neutzsky-Wulff AV, Sorensen MG, Christiansen C, Bollerslev J, Karsdal MA, Henriksen K (2009) Advances in osteoclast biology resulting from the study of osteopetrotic mutations. Hum Genet 124:561-577
16. Tolar J, Teitelbaum SL, Orchard PJ (2004) Osteopetrosis. N Engl J Med 351:2839-2849
17. Bollerslev J, Marks SC Jr, Pockwinse S, Kassem M, Brixen K, Steiniche T, Mosekilde L (1993) Ultrastructural investigations of bone resorptive cells in two types of autosomal dominant osteopetrosis. Bone 14:865-869
18. Del Fattore A, Peruzzi B, Rucci N, Recchia I, Cappariello A, Longo M, Fortunati D, Ballanti P, Iacobini M, Luciani M, Devito R, Pinto R, Caniglia M, Lanino E, Messina C, Cesaro S, Letizia C, Bianchini G, Fryssira H, Grabowski P, Shaw N, Bishop N, Hughes D, Kapur RP, Datta HK, Taranta A, Fornari R, Migliaccio S, Teti A (2006) Clinical, genetic, and cellular analysis of 49 osteopetrotic patients: implications for diagnosis and treatment. J Med Genet 43:315-325
19. Frattini A, Orchard PJ, Sobacchi C, Giliani S, Abinun M, Mattsson JP, Keeling DJ, Andersson AK, Wallbrandt P, Zecca L, Notarangelo LD, Vezzoni P, Villa A (2000) Defects in TCIRG1 subunit of the vacuolar proton pump are responsible for a subset of human autosomal recessive osteopetrosis. Nat Genet 25:343-346
20. +-ATPase cause infantile malignant osteopetrosis. Hum Mol Genet 9:2059-2063
21. Henriksen K, Andreassen KV, Thudium CS, Gudmann KN, Moscatelli I, Cruger-Hansen CE, Schulz AS, Dziegiel MH, Richter J, Karsdal MA, Neutzsky-Wulff AV (2012) A specific subtype of osteoclasts secretes factors inducing nodule formation by osteoblasts. Bone 51:353-361
22. Nielsen RH, Karsdal MA, Sorensen MG, Dziegiel MH, Henriksen K (2007) Dissolution of the inorganic phase of bone leading to release of calcium regulates osteoclast survival. Biochem Biophys Res Commun 360:834-839
23. Alatalo SL, Ivaska KK, Waguespack SG, Econs MJ, Vaananen HK, Halleen JM (2004) Osteoclast-derived serum tartrate-resistant acid phosphatase 5b in Albers-Schonberg disease (type II autosomal dominant osteopetrosis). Clin Chem 50:883-890
24. Karsdal MA, Neutzsky-Wulff AV, Dziegiel MH, Christiansen C, Henriksen K (2008) Osteoclasts secrete non-bone derived signals that induce bone formation. Biochem Biophys Res Commun 366:483-488
25. Pederson L, Ruan M, Westendorf JJ, Khosla S, Oursler MJ (2008) Regulation of bone formation by osteoclasts involves Wnt/BMP signaling and the chemokine sphingosine-1-phosphate. Proc Natl Acad Sci USA 105:20764-20769
26. Guerrini MM, Sobacchi C, Cassani B, Abinun M, Kilic SS, Pangrazio A, Moratto D, Mazzolari E, Clayton-Smith J, Orchard P, Coxon FP, Helfrich MH, Crockett JC, Mellis D, Vellodi A, Tezcan I, Notarangelo LD, Rogers MJ, Vezzoni P, Villa A, Frattini A (2008) Human osteoclast-poor osteopetrosis with hypogammaglobulinemia due to TNFRSF11A (RANK) mutations. Am J Hum Genet 83:64-76
27. Soriano P, Montgomery C, Geske R, Bradley A (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64:693-702
28. -/- mice. Bone 44:199-207
29. Chiusaroli R, Knobler H, Luxenburg C, Sanjay A, Granot-Attas S, Tiran Z, Miyazaki T, Harmelin A, Baron R, Elson A (2004) Tyrosine phosphatase epsilon is a positive regulator of osteoclast function in vitro and in vivo. Mol Biol Cell 15:234-244
30. 0 subunit d2-deficient mice exhibit impaired osteoclast fusion and increased bone formation. Nat Med 12:1403-1409
31. Grigoriadis AE, Wang ZQ, Cecchini MG, Hofstetter W, Felix R, Fleisch HA, Wagner EF (1994) c-Fos: a key regulator of osteoclast-macrophage lineage determination and bone remodeling. Science 266:443-448
32. Henriksen K, Flores C, Thomsen JS, Bruel AM, Thudium CS, Neutzsky-Wulff AV, Langenbach GE, Sims N, Askmyr M, Martin TJ, Everts V, Karsdal MA, Richter J (2011) Dissociation of bone resorption and bone formation in adult mice with a non-functional V-ATPase in osteoclasts leads to increased bone strength. PLoS One 6:e27482
33. Thudium CS, Flores C, Moscatelli I, Richter J, Karsdal MA, Henriksen K (2012) Investigation of the in vivo osteoclast dependent and independent bone formation. J Bone Miner Res 27 Suppl 1: Abstract #SU0263
34. Karsdal MA, Martin TJ, Bollerslev J, Christiansen C, Henriksen K (2007) Are nonresorbing osteoclasts sources of bone anabolic activity? J Bone Miner Res 22:487-494
35. Martin TJ, Sims NA (2005) Osteoclast-derived activity in the coupling of bone formation to resorption. Trends Mol Med 11:76-81
36. Hauge EM, Qvesel D, Eriksen EF, Mosekilde L, Melsen F (2001) Cancellous bone remodeling occurs in specialized compartments lined by cells expressing osteoblastic markers. J Bone Miner Res 16:1575-1582
37. Andersen TL, Sondergaard TE, Skorzynska KE, Gnaes-Hansen F, Plesner TL, Hauge EM, Plesner T, Delaisse JM (2009) A physical mechanism for coupling bone resorption and formation in adult human bone. Am J Pathol 174:239-247
38. Kristensen HB, Andersen TL, Marcussen N, Rolighed L, Delaisse JM (2013) Increased presence of capillaries next to remodeling sites in adult human cancellous bone. J Bone Miner Res 28:574-585
39. Jensen PR, Andersen TL, Soe K, Hauge EM, Bollerslev J, Amling M, Barvencik F, Delaisse JM (2012) Premature loss of bone remodeling compartment canopies is associated with deficient bone formation: a study of healthy individuals and patients with Cushing's syndrome. J Bone Miner Res 27:770-780
40. Sims NA (2009) gp130 signaling in bone cell biology: multiple roles revealed by analysis of genetically altered mice. Mol Cell Endocrinol 310:30-39
41. Sims NA, Jenkins BJ, Quinn JM, Nakamura A, Glatt M, Gillespie MT, Ernst M, Martin TJ (2004) Glycoprotein 130 regulates bone turnover and bone size by distinct downstream signaling pathways. J Clin Invest 113:379-389
42. Guihard P, Danger Y, Brounais B, David E, Brion R, Delecrin J, Richards CD, Chevalier S, Redini F, Heymann D, Gascan H, Blanchard F (2012) Induction of osteogenesis in mesenchymal stem cells by activated monocytes/macrophages depends on oncostatin M signaling. Stem Cells 30:762-772
43. Del Fattore A, Fornari R, Van Wesenbeeck L, de Freitas F, Timmermans JP, Peruzzi B, Cappariello A, Rucci N, Spera G, Helfrich MH, Van Hul W, Migliaccio S, Teti A (2008) A new heterozygous mutation (R714C) of the osteopetrosis gene, pleckstrin homolog domain containing family M (with run domain) member 1 (PLEKHM1), impairs vesicular acidification and increases TRAP secretion in osteoclasts. J Bone Miner Res 23:380-391
44. Hayman AR, Jones SJ, Boyde A, Foster D, Colledge WH, Carlton MB, Evans MJ, Cox TM (1996) Mice lacking tartrate-resistant acid phosphatase (Acp 5) have disrupted endochondral ossification and mild osteopetrosis. Development 122:3151-3162
45. Roberts HC, Knott L, Avery NC, Cox TM, Evans MJ, Hayman AR (2007) Altered collagen in tartrate-resistant acid phosphatase (TRAP)-deficient mice: a role for TRAP in bone collagen metabolism. Calcif Tissue Int 80:400-410
46. Baron R, Rawadi G (2007) Targeting the Wnt/beta-catenin pathway to regulate bone formation in the adult skeleton. Endocrinology 148:2635-2643
47. Vukicevic S, Grgurevic L (2009) BMP-6 and mesenchymal stem cell differentiation. Cytokine Growth Factor Rev 20:441-448
48. Quint P, Ruan M, Pederson L, Kassem M, Westendorf JJ, Khosla S, Oursler MJ (2013) Sphingosine 1 phosphate (S1P) receptors 1 and 2 coordinately induce osteoblast migration through S1P activation of complementary kinase pathways. J Biol Chem 288:5398-5406
49. Ryu J, Kim HJ, Chang EJ, Huang H, Banno Y, Kim HH (2006) Sphingosine 1-phosphate as a regulator of osteoclast differentiation and osteoclast-osteoblast coupling. EMBO J 25:5840-5851
50. Ishii M, Egen JG, Klauschen F, Meier-Schellersheim M, Saeki Y, Vacher J, Proia RL, Germain RN (2009) Sphingosine-1-phosphate mobilizes osteoclast precursors and regulates bone homeostasis. Nature 458:524-528
51. Kim BJ, Lee YS, Lee SY, Park SY, Dieplinger H, Ryu SH, Yea K, Choi S, Lee SH, Koh JM, Kim GS (2012) Afamin secreted from nonresorbing osteoclasts acts as a chemokine for preosteoblasts via the Akt-signaling pathway. Bone 51:431-440
52. Kreja L, Brenner RE, Tautzenberger A, Liedert A, Friemert B, Ehrnthaller C, Huber-Lang M, Ignatius A (2010) Non-resorbing osteoclasts induce migration and osteogenic differentiation of mesenchymal stem cells. J Cell Biochem 109:347-355
53. Sanchez-Fernandez MA, Gallois A, Riedl T, Jurdic P, Hoflack B (2008) Osteoclasts control osteoblast chemotaxis via PDGF-BB/PDGF receptor beta signaling. PLoS One 3:e3537
54. Kubota K, Sakikawa C, Katsumata M, Nakamura T, Wakabayashi K (2002) Platelet-derived growth factor BB secreted from osteoclasts acts as an osteoblastogenesis inhibitory factor. J Bone Miner Res 17:257-265
55. Furuya Y, Inagaki A, Khan M, Mori K, Penninger JM, Nakamura M, Udagawa N, Aoki K, Ohya K, Uchida K, Yasuda H (2013) Stimulation of bone formation in cortical bone of mice treated with a receptor activator of nuclear factor-kappaB ligand (RANKL) binding peptide that possesses osteoclastogenesis inhibitory activity. J Biol Chem 288:5562-5571
56. Aoki K, Saito H, Itzstein C, Ishiguro M, Shibata T, Blanque R, Mian AH, Takahashi M, Suzuki Y, Yoshimatsu M, Yamaguchi A, Deprez P, Mollat P, Murali R, Ohya K, Horne WC, Baron R (2006) A TNF receptor loop peptide mimic blocks RANK ligand-induced signaling, bone resorption, and bone loss. J Clin Invest 116:1525-1534
57. Hu Y, Chan E, Wang SX, Li B (2003) Activation of p38 mitogen-activated protein kinase is required for osteoblast differentiation. Endocrinology 144:2068-2074
58. Baron R, Neff L, Louvard D, Courtoy PJ (1985) Cell-mediated extracellular acidification and bone resorption: evidence for a low pH in resorbing lacunae and localization of a 100-kD lysosomal membrane protein at the osteoclast ruffled border. J Cell Biol 101:2210-2222
59. Gowen M, Lazner F, Dodds R, Kapadia R, Feild J, Tavaria M, Bertoncello I, Drake F, Zavarselk S, Tellis I, Hertzog P, Debouck C, Kola I (1999) Cathepsin K knockout mice develop osteopetrosis due to a deficit in matrix degradation but not demineralization. J Bone Miner Res 14:1654-1663
60. Saftig P, Hunziker E, Wehmeyer O, Jones S, Boyde A, Rommerskirch W, Moritz JD, Schu P, von Figura K (1998) Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice. Proc Natl Acad Sci USA 95:13453-13458
61. Lotinun S, Kiviranta R, Matsubara T, Alzate JA, Neff L, Luth A, Koskivirta I, Kleuser B, Vacher J, Vuorio E, Horne WC, Baron R (2013) Osteoclast-specific cathepsin K deletion stimulates S1P-dependent bone formation. J Clin Invest 123:666-681
62. Fuller K, Lawrence KM, Ross JL, Grabowska UB, Shiroo M, Samuelsson B, Chambers TJ (2008) Cathepsin K inhibitors prevent matrix-derived growth factor degradation by human osteoclasts. Bone 42:200-211
63. Karsdal MA, Henriksen K, Sorensen MG, Gram J, Schaller S, Dziegiel MH, Heegaard AM, Christophersen P, Martin TJ, Christiansen C, Bollerslev J (2005) Acidification of the osteoclastic resorption compartment provides insight into the coupling of bone formation to bone resorption. Am J Pathol 166:467-476
64. Allan EH, Hausler KD, Wei T, Gooi JH, Quinn JM, Crimeen-Irwin B, Pompolo S, Sims NA, Gillespie MT, Onyia JE, Martin TJ (2008) EphrinB2 regulation by PTH and PTHrP revealed by molecular profiling in differentiating osteoblasts. J Bone Miner Res 23:1170-1181
65. Cheng S, Zhao SL, Nelson B, Kesavan C, Qin X, Wergedal J, Mohan S, Xing W (2012) Targeted disruption of ephrin B1 in cells of myeloid lineage increases osteoclast differentiation and bone resorption in mice. PLoS One 7:e32887
66. Irie N, Takada Y, Watanabe Y, Matsuzaki Y, Naruse C, Asano M, Iwakura Y, Suda T, Matsuo K (2009) Bidirectional signaling through ephrinA2-EphA2 enhances osteoclastogenesis and suppresses osteoblastogenesis. J Biol Chem 284:14637-14644
67. 3-induced gene in osteoblasts that promotes osteoclastogenesis and induces osteopenia in mice. Mol Endocrinol 22:1370-1381
68. Takegahara N, Takamatsu H, Toyofuku T, Tsujimura T, Okuno T, Yukawa K, Mizui M, Yamamoto M, Prasad DV, Suzuki K, Ishii M, Terai K, Moriya M, Nakatsuji Y, Sakoda S, Sato S, Akira S, Takeda K, Inui M, Takai T, Ikawa M, Okabe M, Kumanogoh A, Kikutani H (2006) Plexin-A1 and its interaction with DAP12 in immune responses and bone homeostasis. Nat Cell Biol 8:615-622
69. Takyar FM, Tonna S, Ho PW, Crimeen-Irwin B, Baker EK, Martin TJ, Sims NA (2012) EphrinB2/EphB4 inhibition in the osteoblast lineage modifies the anabolic response to parathyroid hormone. J Bone Miner Res 28:912-925
70. Zhao C, Irie N, Takada Y, Shimoda K, Miyamoto T, Nishiwaki T, Suda T, Matsuo K (2006) Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis. Cell Metab 4:111-121
71. Gale NW, Holland SJ, Valenzuela DM, Flenniken A, Pan L, Ryan TE, Henkemeyer M, Strebhardt K, Hirai H, Wilkinson DG, Pawson T, Davis S, Yancopoulos GD (1996) Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 17:9-19
72. Pasquale EB (2005) Eph receptor signalling casts a wide net on cell behaviour. Nat Rev Mol Cell Biol 6:462-475
73. Murai KK, Pasquale EB (2003) "Eph"ective signaling: forward, reverse and crosstalk. J Cell Sci 116:2823-2832
74. Flanagan JG, Vanderhaeghen P (1998) The ephrins and Eph receptors in neural development. Annu Rev Neurosci 21:309-345
75. Boyce BF, Zuscik MJ, Xing L (2013) Genetics of bone biology and skeletal disease. Elsevier, London
76. Mundy GR, Elefteriou F (2006) Boning up on ephrin signaling. Cell 126:441-443
77. Xing W, Kim J, Wergedal J, Chen ST, Mohan S (2010) Ephrin B1 regulates bone marrow stromal cell differentiation and bone formation by influencing TAZ transactivation via complex formation with NHERF1. Mol Cell Biol 30:711-721
78. Compagni A, Logan M, Klein R, Adams RH (2003) Control of skeletal patterning by ephrinB1-EphB interactions. Dev Cell 5:217-230
79. Davy A, Aubin J, Soriano P (2004) Ephrin-B1 forward and reverse signaling are required during mouse development. Genes Dev 18:572-583
80. Ting MC, Wu NL, Roybal PG, Sun J, Liu L, Yen Y, Maxson RE Jr (2009) EphA4 as an effector of Twist1 in the guidance of osteogenic precursor cells during calvarial bone growth and in craniosynostosis. Development 136:855-864
81. Takahashi T, Fournier A, Nakamura F, Wang LH, Murakami Y, Kalb RG, Fujisawa H, Strittmatter SM (1999) Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 99:59-69
82. Tamagnone L, Artigiani S, Chen H, He Z, Ming GI, Song H, Chedotal A, Winberg ML, Goodman CS, Poo M, Tessier-Lavigne M, Comoglio PM (1999) Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99:71-80
83. Winberg ML, Noordermeer JN, Tamagnone L, Comoglio PM, Spriggs MK, Tessier-Lavigne M, Goodman CS (1998) Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 95:903-916
84. Negishi-Koga T, Shinohara M, Komatsu N, Bito H, Kodama T, Friedel RH, Takayanagi H (2011) Suppression of bone formation by osteoclastic expression of semaphorin 4D. Nat Med 17:1473-1480
85. Hayashi M, Nakashima T, Taniguchi M, Kodama T, Kumanogoh A, Takayanagi H (2012) Osteoprotection by semaphorin 3A. Nature 485:69-74
86. Aubin JE (1998) Advances in the osteoblast lineage. Biochem Cell Biol 76:899-910
87. Liu F, Malaval L, Aubin JE (1997) The mature osteoblast phenotype is characterized by extensive plasticity. Exp Cell Res 232:97-105
88. Manolagas SC (2000) Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 21:115-137
89. Martin TJ, Ng KW, Sims NA (2013) Basic principles of bone cell biology. In: Karsenty G (ed) Translational endocrinology of bone. Elsevier, London, pp 5-26