The role of osteoclasts in bone tissue engineering

Journal of Tissue Engineering and Regenerative Medicine

Volumn 9, Issue 10, 2015, Pages 1133-1149

  Detsch, Rainer ^a   Boccaccini, Aldo R ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Bioactive glasses; Bone resorption; Bone tissue engineering; Calcium phosphates; Osteoclasts; Scaffolds

Indexed keywords

BONE; CALCIUM PHOSPHATE; SCAFFOLDS (BIOLOGY);

BONE REGENERATION; BONE RESORPTION; BONE SUBSTITUTE MATERIALS; BONE TISSUE ENGINEERING; DISEASED TISSUES; OSTEOCLAST; OSTEOCLAST CELLS; PERFORMANCE; REGENERATIVE MEDICINE; SYNTHETIC BONE;

BIOACTIVE GLASS;

BIOCERAMICS; BIOMATERIAL; BIOPOLYMER; CALCIUM PHOSPHATE; HYDROXYAPATITE; BONE PROSTHESIS;

ANGIOGENESIS; BONE GRAFT; BONE MINERALIZATION; BONE REGENERATION; BONE REMODELING; CELL DIFFERENTIATION; CELL SPREADING; CHEMICAL COMPOSITION; COCULTURE; HUMAN; MESENCHYMAL STEM CELL; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOCLAST ACTIVITY; OSTEOCLASTOGENESIS; OSTEOLYSIS; OSTEOPOROSIS; OSTEOPROGENITOR CELL; PRIORITY JOURNAL; REVIEW; TISSUE ENGINEERING; TISSUE SCAFFOLD; BONE; BONE PROSTHESIS; CYTOLOGY; SCANNING ELECTRON MICROSCOPY;

BIOCOMPATIBLE MATERIALS; BONE AND BONES; BONE REMODELING; BONE SUBSTITUTES; HUMANS; MICROSCOPY, ELECTRON, SCANNING; OSTEOCLASTS; TISSUE ENGINEERING;

EID: 84944511113     PISSN: 19326254     EISSN: 19327005     Source Type: Journal    
DOI: 10.1002/term.1851     Document Type: Review

References (173)

1. Anderegg F, Geblinger D, Horvath P, et al. 2011; Substrate adhesion regulates sealing zone architecture and dynamics in cultured osteoclasts. PLoS One 6: 1-10.
2. Anderson JM. 2000; Multinucleated giant cells. Curr Opin Hematol 7: 40-47.
3. Anselme K, Bigerelle M, Noel B, et al. 2000; Qualitative and quantitative study of human osteoblast adhesion on materials with various surface roughnesses. J Biomed Mater Res 49: 155-166.
4. Bar-Shavit Z. 2007; The osteoclast a multinucleated, hematopoietic-origin, bone-resorbing osteoimmune cell. J Cell Biochem 102: 1130-1139.
5. Baron R, Neff L, Phuc Tran V, et al. 1986; Kinetic and cytochemical identification of osteoclast precursors and their differentiation into multinucleated osteoclasts. Am J Pathol 122: 363-378.
6. 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 kDa lysosomal membrane protein at the osteoclast ruffled border. J Cell Biol 101: 2210-2222.
7. Bassett JHD, Williams GR. 2003; The molecular actions of thyroid hormone in bone. Trends Endocrinol Metab 14: 356-364.
8. Bielby RC, Boccaccini AR, Polak JM, et al. 2004; In vitro differentiation and in vivo mineralization of osteogenic cells derived from human embryonic stem cells. Tissue Eng 10: 1518-1525.
9. Blair HC. 1998; How the osteoclast degrades bone. Bioessays 20: 837-846.
10. Blair HC, Teitelbaum SL, Ghiselli R, et al. 1989, Osteoclastic bone resorption by a polarized vacuolar proton pump. Science 245: 855-857.
11. Blottière HM, Daculsi G, Anegon I, et al. 1995; Utilization of activated U937 monocytic cells as a model to evaluate biocompatibility and biodegradation of synthetic calcium phosphate. Biomaterials 16: 497-503.
12. Bosetti M, Cannas M. 2005; The effect of bioactive glasses on bone marrow stromal cells differentiation. Biomaterials 26: 3873-3879.
13. Boyde A, Ali NN, Jones SJ. 1984; Resorption of dentine by isolated osteoclasts in vitro. Br Dent J 156: 216-220.
14. Brinkmann J, Hefti T, Schlottig F, et al. 2012; Response of osteoclasts to titanium surfaces with increasing surface roughness: an in vitro study. Biointerphases 7: 34.
15. Bruder SP, Fink DJ, Caplan AI. 1994; Mesenchymal stem cells in bone development, bone repair, and skeletal regeneration therapy. J Cell Biochem 56: 283-294.
16. Bruder SP, Jaiswal N, Ricalton NS, et al. 1998; Mesenchymal stem cells in osteobiology and applied bone regeneration. Clin Orthop Rel Res 5: S247-256.
17. Bucholz RW. 2002; Nonallograft osteoconductive bone graft substitutes. Clin Orthop Relat Res 395: 44-52.
18. Cacciotti I, Lehmann G, Camaioni A, et al. 2013. AP40 bioactive glass ceramic by sol-gel synthesis: in vitro dissolution and cell-mediated bioresorption. J Biomed Mater Res 49: 155-166.
19. Capuccini C, Torricelli P, Sima F, et al. 2008; Strontium-substituted hydroxyapatite coatings synthesized by pulsed-laser deposition: in vitro osteoblast and osteoclast response. Acta Biomater 4: 1885-1893.
20. Chamberlain G, Fox J, Ashton B, et al. 2007; Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25: 2739-2749.
21. Chambers TJ. 2010; The birth of the osteoclast. Ann NY Acad Sci 1192: 19-26.
22. Chen D, Zhao M, Mundy GR. 2004; Bone morphogenetic proteins. Growth Factors 22: 233-241.
23. Chen QZ, Thompson ID, Boccaccini AR. 2006; 45S5 Bioglass-derived glass-ceramic scaffolds for bone tissue engineering. Biomaterials 27: 2414-2425.
24. Cody JJ, Rivera AA, Liu J, et al. 2011; A simplified method for the generation of human osteoclasts in vitro. Int J Biochem Mol Biol 2: 183-189.
25. Connor JR, Dodds RA, James IE, et al. 1995; Human osteoclast and giant cell differentiation: the apparent switch from nonspecific esterase to tartrate resistant acid phosphatase activity coincides with the in situ expression of osteopontin mRNA. J Histochem Cytochem 43: 1193-1201.
26. Cool SM, Kenny B, Wu A, et al. 2007; Poly(3-hydroxybutyrate-co-3-hydroxyvalerate) composite biomaterials for bone tissue regeneration: in vitro performance assessed by osteoblast proliferation, osteoclast adhesion and resorption, and macrophage proinflammatory response. J Biomed Mater Res A 82: 599-610.
27. Costa-Rodrigues J, Fernandes A, Lopes MA, et al. 2012; Hydroxyapatite surface roughness: complex modulation of the osteoclastogenesis of human precursor cells. Acta Biomater 8: 1137-1145.
28. Costa DO, Prowse PDH, Chrones T, et al. 2013; The differential regulation of osteoblast and osteoclast activity by surface topography of hydroxyapatite coatings. Biomaterials 34: 7215-7216.
29. Deckers MML, Karperien M, Van Der Bent C, et al. 2000; Expression of vascular endothelial growth factors and their receptors during osteoblast differentiation. Endocrinology 141: 1667-1674.
30. Deisinger U. 2010; Generating porous ceramic scaffolds: processing and properties. Key Eng Mat 441: 155-179.
31. Deisinger U, Hamisch S, Schumacher M, et al. 2008. Fabrication of tailored hydroxyapatite scaffolds: comparison between a direct and an indirect rapid prototyping technique. Key Eng Mat 361-363 II: 915-918.
32. Delaissé JM, Andersen TL, Engsig MT, et al. 2003; Matrix metalloproteinases (MMP) and cathepsin K contribute differently to osteoclastic activities. Microsc Res Techn 61: 504-513.
33. Despang F, Bernhardt A, Lode A, et al. 2013; Synthesis and physicochemical, in vitro and in vivo evaluation of an anisotropic, nanocrystalline hydroxyapatite bisque scaffold with parallel-aligned pores mimicking the microstructure of cortical bone. J Tissue Eng Regen Med DOI: 10.1002/term.1729. [Epub ahead of print]
34. Detsch R. 2009. In vitro Untersuchungen zur Osteoklastogenese und Osteogenese auf Calciumphosphat-basierten Knochenersatzmaterialien: Einfluss von verschiedenen Materialparametern. Dissertation, University Bayreuth, ISBN-10: 3866647166.
35. Detsch R, Hagmeyer D, Neumann M, et al. 2010; The resorption of nanocrystalline calcium phosphates by osteoclast-like cells. Acta Biomater 6: 3223-3233.
36. Detsch R, Mayr H, Seitz D, et al. 2008a. Is hydroxyapatite ceramic included in the bone remodelling process? An in vitro study of resorption and formation processes. Key Eng Mater 361-363 II: 1123-1126.
37. Detsch R, Mayr H, Ziegler G. 2008b; Formation of osteoclast-like cells on HA and TCP ceramics. Acta Biomater 4: 139-148.
38. Detsch R, Monchau F, Mayr H, et al. 2005; Osteoclast generated resorption of synthetic bone substitute materials. In Ninth Meeting and Seminar on Ceramics, Cells and Tissues, Ravaglioli A, Krejewski A (eds). ISTEC-CNR: Faenza; 82-86.
39. Detsch R, Schaefer S, Deisinger U, et al. 2011; In vitro osteoclastic activity studies on surfaces of 3D printed calcium phosphate scaffolds. J Biomater Appl 26: 359-380.
40. Detsch R, Uhl F, Deisinger U, et al. 2008c; In vitro studies of cell growth on three differently fabricated hydroxyapatite ceramic scaffolds for bone tissue engineering. Key Eng Mater 361-363(II): 1181-1184.
41. Dimitriou R, Jones E, McGonagle D, et al. 2011; Bone regeneration: current concepts and future directions. BMC Med 9: 1-10.
42. Doi Y, Iwanaga H, Shibutani T, et al. 1999; Osteoclastic responses to various calcium phosphates in cell cultures. J Biomed Mater Res 47: 424-433.
43. Domaschke H, Gelinsky M, Burmeister B, et al. 2006; In vitro ossification and remodeling of mineralized collagen I scaffolds. Tissue Eng 12: 949-958.
44. Duplat D, Chabadel A, Gallet M, et al. 2007; The in vitro osteoclastic degradation of nacre. Biomaterials 28: 2155-2162.
45. Durrani S, Konoplyannikov M, Ashraf M, et al. 2010; Skeletal myoblasts for cardiac repair. Regen Med 5: 919-932.
46. Einhorn TA. 1998; The cell and molecular biology of fracture healing. Clin Orthop Rel Res 355 SUPPL: S7-21.
47. Faccio R, Grano M, Colucci S, et al. 1998; Activation of αvβ3 integrin on human osteoclast-like cells stimulates adhesion and migration in response to osteopontin. Biochem Biophys Res Commun 249: 522-525.
48. Faust J, Lacey DL, Hunt P, et al. 1999; Osteoclast markers accumulate on cells developing from human peripheral blood mononuclear precursors. J Cell Biochem 72: 67-80.
49. Fong D, Bisson M, Laberge G, et al. 2013; Bone morphogenetic protein-9 activates Smad and ERK pathways and supports human osteoclast function and survival in vitro. Cell Signal 25: 717-728.
50. Fu Q, Saiz E, Rahaman MN, et al. 2011; Bioactive glass scaffolds for bone tissue engineering: state of the art and future perspectives. Mater Sci Eng C 31: 1245-1256.
51. Gentleman E, Fredholm YC, Jell G, et al. 2010; The effects of strontium-substituted bioactive glasses on osteoblasts and osteoclasts in vitro. Biomaterials 31: 3949-3956.
52. Ghanaati S, Barbeck M, Detsch R, et al. 2012; The chemical composition of synthetic bone substitutes influences tissue reactions in vivo: histological and histomorphometrical analysis of the cellular inflammatory response to hydroxyapatite, β-tricalcium phosphate and biphasic calcium phosphate ceramics. Biomed Mater 7: 1-4.
53. Giannoudis PV, Dinopoulos H, Tsiridis E. 2005; Bone substitutes: an update. Injury 36(suppl 3): S20-27.
54. Goldberg SR, Georgiou J, Glogauer M, et al. 2012; A 3D scanning confocal imaging method measures pit volume and captures the role of Rac in osteoclast function. Bone 51: 145-152.
55. Goodwin HS, Bicknese AR, Chien SN, et al. 2001; Multilineage differentiation activity by cells isolated from umbilical cord blood: expression of bone, fat, and neural markers. Biol Blood Marrow Transpl 7: 581-588.
56. Grano M, Zigrino P, Colucci S, et al. 1994; Adhesion properties and integrin expression of cultured human osteoclast-like cells. Exp Cell Res 212: 209-218.
57. 2O at 5°C, 15°C, 25°C and 37°C. J Res Natl Bur Stand Sect A Phys Chem 78A: 667-674.
58. Gross KA, Muller D, Lucas H, et al. 2012; Osteoclast resorption of thermal spray hydoxyapatite coatings is influenced by surface topography. Acta Biomater 8: 1948-1956.
59. Habermann B, Eberhardt C, Feld M, et al. 2007; Tartrate-resistant acid phosphatase 5b (TRAP 5b) as a marker of osteoclast activity in the early phase after cementless total hip replacement. Acta Orthopaed 78: 221-225.
60. Halleen JM, Alatalo SL, Suominen H, et al. 2000; Tartrate-resistant acid phosphatase 5b a novel serum marker of bone resorption. J Bone Miner Res 15: 1337-1345.
61. Han D, Zhang Q. 2006; An essential requirement for osteoclasts in refined bone-like tissue reconstruction in vitro. Med Hypoth 67: 75-78.
62. Hench LL. 1998; Bioceramics. J Am Ceram Soc 81: 1705-1727.
63. Hill PA, Reynolds JJ, Meikle MC. 1995; Osteoblasts mediate insulin-like growth factor-I and -II stimulation of osteoclast formation and function. Endocrinology 136: 124-131.
64. Holliday LS, Welgus HG, Fliszar CJ, et al. 1997; Initiation of osteoclast bone resorption by interstitial collagenase. J Biol Chem 272: 22053-22058.
65. Hoppe A, Güldal NS, Boccaccini AR. 2011; A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics. Biomaterials 32: 2757-2774.
66. Hou WS, Li Z, Gordon RE, et al. 2001; Cathepsin K is a critical protease in synovial fibroblast-mediated collagen degradation. Am J Pathol 159: 2167-2177.
67. Hsu CW, Olabisi RM, Olmsted-Davis EA, et al. 2011; Cathepsin K-sensitive poly(ethylene glycol) hydrogels for degradation in response to bone resorption. J Biomed Mater Res A 98A: 53-62.
68. Hutmacher DW, Schantz T, Zein I, et al. 2001; Mechanical properties and cell cultural response of polycaprolactone scaffolds designed and fabricated via fused deposition modeling. J Biomed Mater Res 55: 203-216.
69. Ishii M, Saeki Y. 2008; Osteoclast cell fusion: Mechanisms and molecules. Mod Rheumatol 18: 220-227.
70. Janning C, Willbold E, Vogt C, et al. 2010; Magnesium hydroxide temporarily enhancing osteoblast activity and decreasing the osteoclast number in peri-implant bone remodelling. Acta Biomater 6: 1861-1868.
71. Jimi E, Nakamura I, Amano H, et al. 1996; Osteoclast function is activated by osteoblastic cells through a mechanism involving cell-to-cell contact. Endocrinology 137: 2187-2190.
72. Jones GL, Motta A, Marshall MJ, et al. 2009; Osteoblast:osteoclast co-cultures on silk fibroin, chitosan and PLLA films. Biomaterials 30: 5376-5384.
73. Jones SJ, Arora M, Boyde A. 1995; The rate of osteoclastic destruction of calcified tissues is inversely proportional to mineral density. Calcif Tissue Int 56: 554-558.
74. Juhasz JA, Best SM. 2012; Bioactive ceramics: Processing, structures and properties. J Mater Sci 47: 610-624.
75. Kadow-Romacker A, Greiner S, Schmidmaier G, et al. 2013; Effect of β-tricalcium phosphate coated with zoledronic acid on human osteoblasts and human osteoclasts in vitro. J Biomater Applic 27: 577-585.
76. Kakudo S, Miyazawa K, Kameda T, et al. 1996; Isolation of highly enriched rabbit osteoclasts from collagen gels a new assay system for bone-resorbing activity of mature osteoclasts. J Bone Miner Metab 14: 129-136.
77. Kanatani M, Sugimoto T, Kano J, et al. 2003; Effect of high phosphate concentration on osteoclast differentiation as well as bone-resorbing activity. J Cell Physiol 196: 180-189.
78. Karpov M, Laczka M, Leboy PS, et al. 2008; Sol-gel bioactive glasses support both osteoblast and osteoclast formation from human bone marrow cells. J Biomed Mater Res A 84: 718-726.
79. Karsdal MA, Neutzsky-Wulff AV, Dziegiel MH, et al. 2008; Osteoclasts secrete non-bone derived signals that induce bone formation. Biochem Biophys Res Commun 366: 483-488.
80. Khademhosseini A, Langer R, Borenstein J, et al. 2006; Microscale technologies for tissue engineering and biology. Proc Natl Acad Sci U S A 103: 2480-2487.
81. Kneser U, Schaefer DJ, Polykandriotis E, et al. 2006; Tissue engineering of bone: the reconstructive surgeon's point of view. J Cell Mol Med 10: 7-19.
82. Kölliker A. 1873; Die normale Resorption des Knochengewebes und ihre Bedeutung für die Entstehung der typischen Knochenformen. FCW Vogel: Leipzig; 86.
83. Komarova SV, Smith RJ, Dixon SJ, et al. 2003; Mathematical model predicts a critical role for osteoclast autocrine regulation in the control of bone remodeling. Bone 33: 206-215.
84. Kong YY, Penninger JM. 2000; Molecular control of bone remodeling and osteoporosis. Exp Gerontol 35: 947-956.
85. Krast M, Gorny G, Sells Galvin RJ, et al. 2004; Roles of stromal cell RANKL, OPG, and M-CSF expression in biphasic TGF-β regulation of osteoclast differentiation. J Cell Physiol 200: 99-106.
86. Lakkakorpi P, Tuukkanen J, Hentunen T, et al. 1989; Organization of osteoclast microfilaments during the attachment to bone surface in vitro. J Bone Miner Res 4: 817-825.
87. Lakkakorpi PT, Vaananen HK. 1991; Kinetics of the osteoclast cytoskeleton during the resorption cycle in vitro. J Bone Miner Res 6: 817-826.
88. Laurencin C, Khan Y, El-Amin SF. 2006; Bone graft substitutes. Expert Rev Med Devices 3: 49-57.
89. Le Nihouannen D, Hacking SA, Gbureck U, et al. 2008; The use of RANKL-coated brushite cement to stimulate bone remodelling. Biomaterials 29: 3253-3259.
90. Lees RL, Sabharwal VK, Heersche JNM. 2001; Resorptive state and cell size influence intracellular pH regulation in rabbit osteoclasts cultured on collagen-hydroxyapatite films. Bone 28: 187-194.
91. Leeuwenburgh S, Layrolle P, Barre F, et al. 2001; Osteoclastic resorption of biomimetic calcium phosphate coatings in vitro. J Biomed Mater Res 56: 208-215.
92. 2+. Exp Cell Res 242: 128-137.
93. Lehmann G, Cacciotti I, Palmero P, et al. 2012; Differentiation of osteoblast and osteoclast precursors on pure and silicon-substituted synthesized hydroxyapatites. Biomed Mater (Bristol) 7: 1-13.
94. Lincks J, Boyan BD, Blanchard CR, et al. 1998; Response of MG63 osteoblast-like cells to titanium and titanium alloy is dependent on surface roughness and composition. Biomaterials 19: 2219-2232.
95. Mabilleau G, Pascaretti-Grizon F, Baslé MF, et al. 2012; Depth and volume of resorption induced by osteoclasts generated in the presence of RANKL, TNF-α/IL-1 or LIGHT. Cytokine 57: 294-299.
96. Macneill SR, Cobb CM, Rapley JW, et al. 1999; In vivo comparison of synthetic osseous graft materials. A preliminary study. J Clin Periodontol 26: 239-245.
97. Majore I, Moretti P, Stahl F, et al. 2011; Growth and differentiation properties of mesenchymal stromal cell populations derived from whole human umbilical cord. Stem Cell Rev Rep 7: 17-31.
98. Mano JF, Silva GA, Azevedo HS, et al. 2007; Natural origin biodegradable systems in tissue engineering and regenerative medicine: present status and some moving trends. J R Soc Interface 4: 999-1030.
99. Martin TJ, Sims NA. 2005; Osteoclast-derived activity in the coupling of bone formation to resorption. Trends Mol Med 11: 76-81.
100. Mauney JR, Volloch V, Kaplan DL. 2005; Role of adult mesenchymal stem cells in bone tissue-engineering applications: current status and future prospects. Tissue Eng 11: 787-802.
101. Mayr H, Schlüfter S, Detsch R, et al. 2008. Influence of phase composition on degradation and resorption of biphasic calcium phosphate ceramics. Key Eng Mat 361-363 II: 1043-1046.
102. Midha S, Van Den Bergh W, Kim TB, et al. 2013; Bioactive glass foam scaffolds are remodelled by osteoclasts and support the formation of mineralized matrix and vascular networks in vitro. Adv Healthcare Mater 2: 490-499.
103. Miyamoto A, Kunisada T, Hemmi H, et al. 1998; Establishment and characterization of an immortal macrophage-like cell line inducible to differentiate to osteoclasts. Biochem Biophys Res Commun 242: 703-709.
104. Mladenović Ž, Johansson A, Willman B, et al. 2014; Soluble silica inhibits osteoclast formation and bone resorption in vitro. Acta Biomater 10: 406-418.
105. Monchau F, Lefèvre A, Descamps M, et al. 2002; In vitro studies of human and rat osteoclast activity on hydroxyapatite, β-tricalcium phosphate, calcium carbonate. Biomol Eng 19: 143-152.
106. Moore WR, Graves SE, Bain GI. 2001; Synthetic bone graft substitutes. ANZ J Surg 71: 354-361.
107. Mouriño V, Boccaccini AR. 2010; Bone tissue engineering therapeutics: controlled drug delivery in three-dimensional scaffolds. J R Soc Interface 7: 209-227.
108. Nakagawa K, Abukawa H, Shin MY, et al. 2004; Osteoclastogenesis on tissue-engineered bone. Tissue Eng 10: 93-100.
109. Olsen BR, Reginato AM, Wang W. 2000. Bone development. Annu Rev Cell Dev Biol 16: 191-220.
110. Oonishi H, Kushitani S, Yasukawa E, et al. 1997; Particulate bioglass compared with hydroxyapatite as a bone graft substitute. Clin Orthop Rel Res 334: 316-325.
111. Panetta NJ, Gupta DM, Longaker MT. 2010; Bone regeneration and repair. Curr Stem Cell Res Ther 5: 122-128.
112. Papadimitropoulos A, Scherberich A, Güven S, et al. 2011; A 3D in vitro bone organ model using human progenitor cells. Eur Cells Mater 21: 445-458, discussion 458.
113. Pascaretti-Grizon F, Mabilleau G, Basle M, et al. 2011; Measurement by vertical scanning profilometry of resorption volume and lacunae depth caused by osteoclasts on dentine slices. J Microsc 241: 147-152.
114. Perrotti V, Nicholls BM, Horton MA, et al. 2009; Human osteoclast formation and activity on a xenogenous bone mineral. J Biomed Mater Res A 90: 238-246.
115. Petite H, Viateau V, Bensaïd W, et al. 2000; Tissue-engineered bone regeneration. Nat Biotechnol 18: 959-963.
116. Pierce AM, Lindskog S, Hammarström L. 1991; Osteoclasts: structure and function. Electron Microsc Rev 4: 1-45.
117. Pirraco RP, Marques AP, Reis RL. 2010; Cell interactions in bone tissue engineering. J Cell Mol Med 14: 93-102.
118. Pivonka P, Komarova SV. 2010; Mathematical modeling in bone biology: From intracellular signaling to tissue mechanics. Bone 47: 181-189.
119. Redey SA, Razzouk S, Rey C, et al. 1999; Osteoclast adhesion and activity on synthetic hydroxyapatite, carbonated hydroxyapatite, and natural calcium carbonate: relationship to surface energies. J Biomed Mater Res 45: 140-147.
120. Rezwan K, Chen QZ, Blaker JJ, et al. 2006; Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials 27: 3413-3431.
121. Ringe J, Kaps C, Burmester GR, et al. 2002; Stem cells for regenerative medicine: advances in the engineering of tissues and organs. Naturwissenschaften 89: 338-351.
122. Roldán JC, Detsch R, Schaefer S, et al. 2010; Bone formation and degradation of a highly porous biphasic calcium phosphate ceramic in presence of BMP-7, VEGF and mesenchymal stem cells in an ectopic mouse model. J Craniomaxillofac Surg 38: 423-430.
123. Roldán JC, Klünter T, Schulz P, et al. 2011; Effect of BMP-7 on degradation and resorption of different calcium phosphate ceramics as well as on bone formation in an ectopic Minipig model. Int J Oral Maxillofac Surg 40: e15-16.
124. Roodman GD. 1996; Advances in bone biology: the osteoclast. Endocr Rev 17: 308-332.
125. Roy M, Bose S. 2012; Osteoclastogenesis and osteoclastic resorption of tricalcium phosphate: effect of strontium and magnesium doping. J Biomed Mater Res A 100A: 2450-2461.
126. Salgado AJ, Coutinho OP, Reis RL. 2004; Bone tissue engineering: state of the art and future trends. Macromol Biosci 4: 743-765.
127. Salo J, Lehenkari P, Mulari M, et al. 1997; Removal of osteoclast bone resorption products by transcytosis. Science 276: 270-273.
128. Salo J, Metsikkö K, Palokangas H, et al. 1996; Bone-resorbing osteoclasts reveal a dynamic division of basal plasma membrane into two different domains. J Cell Sci 109: 301-307.
129. Sapp JP. 1976; An ultrastructural study of nuclear and centriolar configurations in multinucleated giant cells. Lab Invest 34: 109-114.
130. Schaefer S, Detsch R, Uhl F, et al. 2011; How degradation of calcium phosphate bone substitute materials is influenced by phase composition and porosity. Adv Eng Mater 13: 342-350.
131. Seitz H, Deisinger U, Leukers B, et al. 2009; Different calcium phosphate granules for 3D printing of bone tissue engineering scaffolds. Adv Eng Mater 11: B41-46.
132. i signaling expressed by GCT23 osteoclast-like cells. Proc Assoc Am Physic 111: 70-81.
133. Severson AR. 1983; Differentiation of mononuclear cells into multinucleated osteoclast-like cells. Exp Cell Biol 51: 267-274.
134. Shafieyan Y, Tiedemann K, Goulet A, et al. 2012; Monocyte proliferation and differentiation to osteoclasts is affected by density of collagen covalently bound to a poly(dimethyl siloxane) culture surface. J Biomed Mater Res A 100A: 1573-1581.
135. Shimizu H, Sakamoto S, Sakamoto M, et al. 1989; The effect of substrate composition and condition on resorption by isolated osteoclasts. Bone Miner 6: 261-275.
136. Silver IA, Murrills RJ, Etherington DJ. 1988; Microelectrode studies on the acid microenvironment beneath adherent macrophages and osteoclasts. Exp Cell Res 175: 266-276.
137. Song G. 2007; Control of biodegradation of biocompatable magnesium alloys. Corros Sci 49: 1696-1701.
138. Stenbeck G. 2002; Formation and function of the ruffled border in osteoclasts. Semin Cell Dev Biol 13: 285-292.
139. Stolzing A, Jones E, McGonagle D, et al. 2008; Age-related changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies. Mech Ageing Dev 129: 163-173.
140. Susa M, Luong-Nguyen NH, Cappellen D, et al. 2004; Human primary osteoclasts: in vitro generation and applications as pharmacological and clinical assay. J Transl Med 2: 1-2.
141. Takahashi N, Udagawa N, Suda T. 1999; A new member of tumor necrosis factor ligand family, ODF/OPGL/TRANCE/RANKL, regulates osteoclast differentiation and function. Biochem Biophys Res Commun 256: 449-455.
142. Taylor JC, Cuff SE, Leger JPL, et al. 2002; In vitro osteoclast resorption of bone substitute biomaterials used for implant site augmentation a pilot study. Int J Oral Maxillofac Implants 17: 321-330.
143. Theler JM. 2011; Bone tissue substitutes and replacements. Curr Opin Otolaryngol Head Neck Surg 19: 317-322.
144. Torres AL, Santos SG, Oliveira MI, et al. 2013; Fibrinogen promotes resorption of chitosan by human osteoclasts. Acta Biomater 9: 6553-6562.
145. Tortelli F, Pujic N, Liu Y, et al. 2009; Osteoblast and osteoclast differentiation in an in vitro three-dimensional model of bone. Tissue Eng A 15: 2373-2383.
146. Trebec-Reynolds DP, Voronov I, Heersche JNM, et al. 2010; VEGF-A expression in osteoclasts is regulated by NF-κB induction of HIF-1α. J Cell Biochem 110: 343-351.
147. Unger RE, Ghanaati S, Orth C, et al. 2010; The rapid anastomosis between prevascularized networks on silk fibroin scaffolds generated in vitro with cocultures of human microvascular endothelial and osteoblast cells and the host vasculature. Biomaterials 31: 6959-6967.
148. Vaahtio M, Peltola T, Hentunen T, et al. 2006; The properties of biomimetically processed calcium phosphate on bioactive ceramics and their response on bone cells. J Mater Sci Mater Med 17: 1113-1125.
149. Väänänen HK, Laitala-Leinonen T. 2008; Osteoclast lineage and function. Arch Biochem Biophys 473: 132-138.
150. Väänänen HK, Zhao H, Mulari M, et al. 2000; The cell biology of osteoclast function. J Cell Sci 113: 377-381.
151. Väänänen K. 2005; Mechanism of osteoclast mediated bone resorption - rationale for the design of new therapeutics. Adv Drug Deliv Rev 57: 959-971.
152. Vignery A. 2000; Osteoclasts and giant cells: Macrophage-macrophage fusion mechanism. Int J Exp Pathol 81: 291-304.
153. Vogel M, Voigt C, Gross UM, et al. 2001; In vivo comparison of bioactive glass particles in rabbits. Biomaterials 22: 357-362.
154. Wang W, Ferguson DJP, Quinn JMW, et al. 1997; Biomaterial particle phagocytosis by bone-resorbing osteoclasts. J Bone Joint Surg B 79: 849-856.
155. Wang X, Schröder HC, Diehl-Seifert B, et al. 2012; Dual effect of inorganic polymeric phosphate/polyphosphate on osteoblasts and osteoclasts in vitro. J Tissue Eng Regen Med 7: 767-776.
156. Warnke PH, Seitz H, Warnke F, et al. 2010; Ceramic scaffolds produced by computer-assisted 3D printing and sintering: characterization and biocompatibility investigations. J Biomed Mater Res B Appl Biomater 93: 212-217.
157. Webster TJ, Ergun C, Doremus RH, et al. 2001; Enhanced osteoclast-like cell functions on nanophase ceramics. Biomaterials 22: 1327-1333.
158. Wei S, Teitelbaum SL, Wang MWH, et al. 2001; Receptor activator of nuclear factor-κB ligand activates nuclear factor-κB in osteoclast precursors. Endocrinology 142: 1290-1295.
159. Weldon WFR. 1898; Scientific worthies XXXI. Albert Von Kölliker. Nature 58: 1-4.
160. Wilson A, Trumpp A. 2006; Bone-marrow haematopoietic stem-cell niches. Nat Rev Immunol 6: 93-106.
161. Wilson T, Parikka V, Holmbom J, et al. 2006; Intact surface of bioactive glass S53P4 is resistant to osteoclastic activity. J Biomed Mater Res A 77: 67-74.
162. Witte F, Hort N, Vogt C, et al. 2008; Degradable biomaterials based on magnesium corrosion. Curr Opin Solid State Mater Sci 12: 63-72.
163. Yamada S, Heymann D, Bouler JM, et al. 1997; Osteoclastic resorption of biphasic calcium phosphate ceramic in vitro. J Biomed Mater Res 37: 346-352.
164. Yamada S, Nakamura T, Kokubo T, et al. 1994; Osteoclastic resorption of apatite formed on apatite- and wollastonite-containing glass-ceramic by a simulated body fluid. J Biomed Mater Res 28: 1357-1363.
165. Yamagiwa H, Endo N. 2009; Bone fracture and the healing mechanisms. Histological aspect of fracture healing. Primary and secondary healing. Clin Calcium 19: 627-633.
166. Yang L, Perez-Amodio S, Barrère-De Groot FYF, et al. 2010; The effects of inorganic additives to calcium phosphate on in vitro behavior of osteoblasts and osteoclasts. Biomaterials 31: 2976-2989.
167. Yang Q, McHugh KP, Patntirapong S, et al. 2008; VEGF enhancement of osteoclast survival and bone resorption involves VEGF receptor-2 signaling and β3-integrin. Matrix Biol 27: 589-599.
168. Yao Z, Xing L, Qin C, et al. 2008; Osteoclast precursor interaction with bone matrix induces osteoclast formation directly by an interleukin-1-mediated autocrine mechanism. J Biol Chem 283: 9917-9924.
169. Zaidi M, Adebanjo OA, Moonga BS, et al. 1999; Emerging insights into the role of calcium ions in osteoclast regulation. J Bone Miner Res 14: 669-674.
170. Zhang Q, Guo R, Lu Y, et al. 2008; VEGF-C a lymphatic growth factor, is a RANKL target gene in osteoclasts that enhances osteoclastic bone resorption through an autocrine mechanism. J Biol Chem 283: 13491-13499.
171. Zhang Z, Egaña JT, Reckhenrich AK, et al. 2012; Cell-based resorption assays for bone graft substitutes. Acta Biomater 8: 13-19.
172. Zhao YM, Zhang YM, Zhao YT, et al. 2005. Osteoclast behaviour on synthetic bioglasses with different crystallinity in vitro. Biomaterialien 6: 281-286.
173. Zimmermann G, Moghaddam A. 2011; Allograft bone matrix versus synthetic bone graft substitutes. Injury 42: 1.