Submicron-scale surface architecture of tricalcium phosphate directs osteogenesis in vitro and in vivo

European Cells and Materials

Volumn 27, Issue , 2014, Pages 281-297

  Davison, Noel L ^a,b   Luo, X ^a,b   Schoenmaker, T ^c   Everts, V ^c   Yuan, H ^a,b,d   Barrere de Groot F ^b   de Bruijn, J D ^a,b,e  

^a UNIVERSITY OF TWENTE   (Netherlands)

^b XPand Biotechnology BV   (Netherlands)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

^d SICHUAN UNIVERSITY   (China)

^e QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Calcium phosphate; Microstructure; Osteoclast; Osteogenesis; Topography

Indexed keywords

CALCIUM PHOSPHATE CERAMIC;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CHEMICAL STRUCTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENCHYMAL STEM CELL; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; SURFACE PROPERTY;

AGED; AGED, 80 AND OVER; ANIMALS; CALCIUM PHOSPHATES; DOGS; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MUSCLE, SKELETAL; OSTEOCLASTS; OSTEOGENESIS;

EID: 84898477835     PISSN: 14732262     EISSN: None     Source Type: Journal    
DOI: 10.22203/eCM.v027a20     Document Type: Article

References (69)

1. Akiyama N, Takemoto M, Fujibayashi S, Neo M, Hirano M, Nakamura T (2011) Difference between dogs and rats with regard to osteoclast-like cells in calcium-deficient hydroxyapatite-induced osteoinduction. J Biomed Mater Res A 96: 402-412.
2. Barradas AMC, Yuan H, van Blitterswijk CA, Habibovic P (2011) Osteoinductive biomaterials: current knowledge of properties, experimental models and biological mechanisms. Eur Cell Mater 21: 407-429.
3. Bergers G, Song S (2005) The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol 7: 452-464.
4. Blokhuis TJ, Termaat MF, den Boer FC, Patka P, Bakker FC, Haarman HJ (2000) Properties of calcium phosphate ceramics in relation to their in vivo behavior. J Trauma 48: 179-186.
5. Bohner M, Galea L, Doebelin N (2012) Calcium phosphate bone graft substitutes: Failures and hopes. J Eur Ceram Soc 32: 2663-2671.
6. Brinkmann J, Hefti T, Schlottig F, Spencer ND, Hall H (2012) Response of osteoclasts to titanium surfaces with increasing surface roughness: an et al. study. Biointerphases 7: 34.
7. Champagne CM, Takebe J, Offenbacher S, Cooper LF (2002) Macrophage cell lines produce osteoinductive signals that include bone morphogenetic protein-2. Bone 30: 26-31.
8. Costa-Rodrigues J, Fernandes A, Lopes MA, Fernandes MH (2012) Hydroxyapatite surface roughness: complex modulation of the osteoclastogenesis of human precursor cells. Acta Biomater 8: 1137-1145.
9. Dalby MJ, Riehle MO, Sutherland DS, Agheli H, Curtis ASG (2004) Changes in fibroblast morphology in response to nano-columns produced by colloidal lithography. Biomaterials 25: 5415-5422.
10. Dalby MJ, McCloy D, Robertson M, Agheli H, Sutherland D, Affrossman S, Oreffo ROC (2006) Osteoprogenitor response to semi-ordered and random nanotopographies. Biomaterials 27: 2980-2987.
11. Dalby MJ, Gadegaard N, Tare R, Andar A, Riehle MO, Herzyk P, Wilkinson CDW, Oreffo ROC (2007) The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater 6: 997-1003.
12. Davison N, Yuan H, de Bruijn JD, Barrere-de Groot F (2012) In vivo performance of microstructured calcium phosphate formulated in novel water-free carriers. Acta Biomater 8: 2759-2769.
13. Dorozhkin SV (2010) Bioceramics of calcium orthophosphates. Biomaterials 31: 1465-1485.
14. Eggli PS, Müller W, Schenk RK (1988) Porous hydroxyapatite and tricalcium phosphate cylinders with two different pore size ranges implanted in the cancellous bone of rabbits. A comparative histomorphometric and histologic study of bony ingrowth and implant substitution. Clin Orthop Relat Res 232: 127-138.
15. Famery R, Richard N, Boch P (1994) Preparation of α-and β-tricalcium phosphate ceramics, with and without magnesium addition. Ceram Int 20: 327-336.
16. Fellah BH, Josselin N, Chappard D, Weiss P, Layrolle P (2007) Inflammatory reaction in rats muscle after implantation of biphasic calcium phosphate micro particles. J Mater Sci Mater Med 18: 287-294.
17. Fellah BH, Delorme B, Sohier J, Magne D, Hardouin P, Layrolle P (2010) Macrophage and osteoblast responses to biphasic calcium phosphate microparticles. J Biomed Mater Res A 93: 1588-1595.
18. Fujibayashi S, Neo M, Kim HM, Kokubo T, Nakamura T (2004) Osteoinduction of porous bioactive titanium metal. Biomaterials 25: 443-450.
19. Fukuda A, Takemoto M, Saito T, Fujibayashi S, Neo M, Pattanayak DK, Matsushita T, Sasaki K, Nishida N, Kokubo T, Nakamura T (2011) Osteoinduction of porous Ti implants with a channel structure fabricated by selective laser melting. Acta Biomater 7: 2327-2336.
20. Fuller K, Ross JL, Szewczyk KA, Moss R, Chambers TJ (2010) Bone is not essential for osteoclast activation. PLoS One 5: e128.
21. Geblinger D, Addadi L, Geiger B (2010) Nano-topography sensing by osteoclasts. J Cell Sci 123: 1814-1814.
22. Glass GE, Chan JK, Freidin A, Feldmann M, Horwood NJ, Nanchahal J (2011) TNF-alpha promotes fracture repair by augmenting the recruitment and differentiation of muscle-derived stromal cells. Proc Natl Acad Sci USA 108: 1585-1590.
23. Guihard P, Danger Y, Brounais B, David E, Brion R, Delecrin J, Richards CD, Chevalier S, Rédini 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.
24. Habibovic P, Yuan H, van der Valk CM, Meijer G, van Blitterswijk CA, de Groot K (2005) 3D microenvironment as essential element for osteoinduction by biomaterials. Biomaterials 26: 3565-3575.
25. Habibovic P, Yuan H, van den Doel M, Sees TM, van Blitterswijk CA, de Groot K (2006) Relevance of osteoinductive biomaterials in critical-sized orthotopic defect. J Orthop Res 24: 867-876.
26. Handschel J, Wiesmann HP, Stratmann U, Kleinheinz J, Meyer U, Joos U (2002) TCP is hardly resorbed and not osteoconductive in a non-loading calvarial model. Biomaterials 23: 1689-1695.
27. Honda Y, Anada T, Kamakura S, Nakamura M, Sugawara S, Suzuki O (2006) Elevated extracellular calcium stimulates secretion of bone morphogenetic protein 2 by a macrophage cell line. Biochem Biophys Res Commun 345: 1155-1160.
28. Jansen IDC, Vermeer JAF, Bloemen V, Stap J, Everts V (2012) Osteoclast fusion and fission. Calcif Tissue Int 90: 515-522.
29. 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.
30. 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.
31. Kondo N, Ogose A, Tokunaga K, Umezu H, Arai K, Kudo N, Hoshino M, Inoue H, Irie H, Kuroda K, Mera H, Endo N (2006) Osteoinduction with highly purified beta-tricalcium phosphate in dog dorsal muscles and the proliferation of osteoclasts before heterotopic bone formation. Biomaterials 27: 4419-4427.
32. 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.
33. LeGeros RZ (2008) Calcium phosphate-based osteoinductive materials. Chem Rev 108: 4742-4753.
34. Ljusberg J, Ek-Rylander B, Andersson G (1999) Tartrate-resistant purple acid phosphatase is synthesized as a latent proenzyme and activated by cysteine proteinases. Biochem J 343: 63-69.
35. Lu J, Descamps M, Dejou J, Koubi G, Hardouin P, Lemaitre J, Proust JP (2002) The biodegradation mechanism of calcium phosphate biomaterials in bone. J Biomed Mater Res 63: 408-412.
36. Makihira S, Mine Y, Kosaka E, Nikawa H (2007) Titanium surface roughness accelerates RANKL-dependent differentiation in the osteoclast precursor cell line, RAW264. 7. Dent Mater J 26: 739-745.
37. Marchisio M, Di Carmine M, Pagone R, Piattelli A, Miscia S (2005) Implant surface roughness influences osteoclast proliferation and differentiation. J Biomed Mater Res B Appl Biomater 75: 251-256.
38. McCullough KA, Waits CA, Garimella R, Tague SE, Sipe JB, Anderson HC (2007) Immunohistochemical localization of bone morphogenetic proteins (BMPs) 2, 4, 6, and 7 during induced heterotopic bone formation. J Orthop Res 25: 465-472.
39. Miyauchi A, Hruska K A, Greenfield EM, Duncan R, Alvarez J, Barattolo R, Colucci S, Zambonin-Zallone A, Teitelbaum SL, Teti A (1990) Osteoclast cytosolic calcium, regulated by voltage-gated calcium channels and extracellular calcium, controls podosome assembly and bone resorption. J Cell Biol 111: 2543-2552.
40. Monchau F, Lefèvre A, Descamps M, Belquin-myrdycz A, Laffargue P, Hildebrand HF (2002) In vitro studies of human and rat osteoclast activity on hydroxyapatite, beta-tricalcium phosphate, calcium carbonate. Biomol Eng 19: 143-152.
41. Nicolaidou V, Wong MM, Redpath AN, Ersek A, Baban DF, Williams LM, Cope AP, Horwood NJ (2012) Monocytes induce STAT3 activation in human mesenchymal stem cells to promote osteoblast formation. PLoS One 7: e398: e39871.
42. Le Nihouannen D, Daculsi G, Saffarzadeh A, Gauthier O, Delplace S, Pilet P, Layrolle P (2005) Ectopic bone formation by microporous calcium phosphate ceramic particles in sheep muscles. Bone 36: 1086-1093.
43. Omar OM, Granéli C, Ekström K, Karlsson C, Johansson A, Lausmaa J, Wexell CL, Thomsen P (2011) The stimulation of an osteogenic response by classical monocyte activation. Biomaterials 32: 8190-8204.
44. Osborn JF, Newesely H (1980) The material science of calcium phosphate ceramics. Biomaterials 1: 108-111.
45. 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.
46. Ripamonti U, Richter PW, Nilen RWN, Renton L (2008) The induction of bone formation by smart biphasic hydroxyapatite tricalcium phosphate biomimetic matrices in the non-human primate Papio ursinus. J Cell Mol Med 12: 2609-2621.
47. Ripamonti U, Klar RM, Renton LF, Ferretti C (2010) Synergistic induction of bone formation by hOP-1, hTGF-beta3 and inhibition by zoledronate in macroporous coral-derived hydroxyapatites. Biomaterials 31: 6400-6410.
48. Sato K, Wakamatsu E, Sato T, Honma T, Kotake H, Byers P (1986) Histomorphometric study of trabecular channels in normal iliac bone. Calcif Tissue Int 39: 2-7.
49. Sims NA, Gooi JH (2008) Bone remodeling: Multiple cellular interactions required for coupling of bone formation and resorption. Semin Cell Dev Biol 19: 444-451.
50. Stevens MM, George JH (2005) Exploring and engineering the cell surface interface. Science 310: 1135-1138.
51. Takebe J, Champagne CM, Offenbacher S, Ishibashi K, Cooper LF (2003) Titanium surface topography alters cell shape and modulates bone morphogenetic protein 2 expression in the J774A. 1 macrophage cell line. J Biomed Mater Res A 64: 207-216.
52. Takeshita S, Fumoto T, Matsuoka K, Park K, Aburatani H, Kato S, Ito M, Ikeda K (2013) Osteoclast-secreted CTHRC1 in the coupling of bone resorption to formation. J Clin Invest 123: 3914-3924.
53. Tanaka T, Saito M, Chazono M, Kumagae Y, Kikuchi T, Kitasato S, Marumo K (2010) Effects of alendronate on bone formation and osteoclastic resorption after implantation of beta-tricalcium phosphate. J Biomed Mater Res A 93: 469-474.
54. Teitelbaum SL (2011) The osteoclast and its unique cytoskeleton. Ann NY Acad Sci 1240: 14-17.
55. Theiss F, Apelt D, Brand B, Kutter A, Zlinszky K, Bohner M, Matter S, Frei C, Auer JA, von Rechenberg B (2005) Biocompatibility and resorption of a brushite calcium phosphate cement. Biomaterials 26: 4383-4394.
56. Wenisch S, Stahl JP, Horas U, Heiss C, Kilian O, Trinkaus K, Hild A, Schnettler R (2003) In vivo mechanisms of hydroxyapatite ceramic degradation by osteoclasts: fine structural microscopy. J Biomed Mater Res A 67: 713-718.
57. Winkler T, Hoenig E, Gildenhaar R, Berger G, Fritsch D, Janssen R, Morlock MM, Schilling AF (2010) Volumetric analysis of osteoclastic bioresorption of calcium phosphate ceramics with different solubilities. Acta Biomater 6: 4127-4135.
58. Xia Z, Grover LM, Huang Y, Adamopoulos IE, Gbureck U, Triffitt JT, Shelton RM, Barralet JE (2006) In vitro biodegradation of three brushite calcium phosphate cements by a macrophage cell-line. Biomaterials 27: 4557-4565.
59. Yamada S, Heymann D, Bouler JM, Daculsi G (1997) Osteoclastic resorption of calcium phosphate ceramics with different hydroxyapatite/beta-tricalcium phosphate ratios. Biomaterials 18: 1037-1041.
60. Yuan H, Kurashina K, de Bruijn JD, Li Y, de Groot K, Zhang X (1999) A preliminary study on osteoinduction of two kinds of calcium phosphate ceramics. Biomaterials 20: 1799-1806.
61. Yuan H, De Bruijn JD, Li Y, Feng J, Yang Z, De Groot K, Zhang X (2001a) Bone formation induced by calcium phosphate ceramics in soft tissue of dogs: a comparative study between porous alpha-TCP and beta-TCP. J Mater Sci Mater Med 12: 7-13.
62. Yuan H, de Bruijn JD, Zhang X, van Blitterswijk CA, de Groot K (2001b) Bone induction by porous glass ceramic made from Bioglass (45S5). J Biomed Mater Res 58: 270-276.
63. Yuan H, Van Den Doel M, Li S, Van Blitterswijk CA, De Groot K, De Bruijn JD (2002) A comparison of the osteoinductive potential of two calcium phosphate ceramics implanted intramuscularly in goats. J Mater Sci Mater Med 13: 1271-1275.
64. Yuan H, Fernandes H, Habibovic P, de Boer J, Barradas AMC, de Ruiter A, Walsh WR, van Blitterswijk CA, de Bruijn JD (2010) Osteoinductive ceramics as a synthetic alternative to autologous bone grafting. Proc Natl Acad Sci USA 107: 13614-13619.
65. Zou W, Teitelbaum SL (2010) Integrins, growth factors, and the osteoclast cytoskeleton. Ann N Y Acad Sci 1192: 27-31.
66. Barradas AMC, Monticone V, Hulsman M, Danoux C, Fernandes H, Tahmasebi Birgani Z, Barrère-de Groot F, Yuan H, Reinders M, Habibovic P, van Blitterswijk C, de Boer J (2013) Molecular mechanisms of biomaterial-driven osteogenic differentiation in human mesenchymal stromal cells. Integr Biol 5: 920-931.
67. Lee SJ, Choi JS, Park KS, Khang G, Lee YM, Lee HB (2004) Response of MG63 osteoblast-like cells onto polycarbonate membrane surfaces with different micropore sizes. Biomaterials 25: 4699-4707.
68. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6: 483-495.
69. Schmidmaier G, Schwabe P, Wildemann B, Haas NP (2007) Use of bone morphogenetic proteins for treatment of non-unions and future perspectives. Injury 38 Suppl 4: S35-41.