Probing the osteoinductive effect of calcium phosphate by using an in vitro biomimetic model

Tissue Engineering - Part A

Volumn 17, Issue 7-8, 2011, Pages 1083-1097

  Chai, Yoke Chin ^a,b   Roberts, Scott J ^a   Schrooten, Jan ^a   Luyten, Frank P ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF MALAYA   (Malaysia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MATERIALS; BIOMIMETICS; BONE; CALCIUM PHOSPHATE; CELL PROLIFERATION; GENE EXPRESSION; PHOSPHATES;

BIOMIMETIC MODEL; BONE ENGINEERING; BONE FORMATION; BONE MORPHOGENETIC PROTEIN-2; BONE MORPHOGENETIC PROTEINS; CELL-CYCLE PROGRESSION; IN-VITRO; IN-VIVO; OSTEOGENIC; OSTEOINDUCTION; OSTEOINDUCTIVE EFFECTS; OSTEOINDUCTIVITY; TIME-DEPENDENT;

CALCIUM;

BIOMATERIAL; BMP2 PROTEIN, HUMAN; BONE MORPHOGENETIC PROTEIN 2; CALCIUM PHOSPHATE; OSTEOCALCIN; OSTEOPONTIN; TRANSCRIPTION FACTOR RUNX2;

ARTICLE; CELL CULTURE; CELL CYCLE; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION; GENETICS; HUMAN; PERIOSTEUM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

BIOCOMPATIBLE MATERIALS; BONE MORPHOGENETIC PROTEIN 2; CALCIUM PHOSPHATES; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; CORE BINDING FACTOR ALPHA 1 SUBUNIT; GENE EXPRESSION; HUMANS; OSTEOCALCIN; OSTEOPONTIN; PERIOSTEUM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 79952937413     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2010.0160     Document Type: Article

References (78)

1. Urist, M.R. Bone: formation by autoinduction. Science 150, 893, 1965.
2. Riley, E.H., Lane, J.M., Urist, M.R., Lyons, K.M., and Lieberman, J.R. Bone morphogenetic protein-2: biology and applications. Clin Orthop Relat Res (324), 39, 1996.
3. Poynton, A.R., and Lane, J.M. Safety profile for the clinical use of bone morphogenetic proteins in the spine. Spine (Phila Pa 1976) 27, S40, 2002.
4. Gautschi, O.P., Frey, S.P., and Zellweger, R. Bone morphogenetic proteins in clinical applications. ANZ J Surg 77, 626, 2007.
5. Reddi, A.H. Bone morphogenetic proteins, bone marrow stromal cells, and mesenchymal stem cells. Maureen Owen revisited. Clin Orthop Relat Res (313), 115, 1995.
6. Nasu, T., Takemoto, M., Akiyama, N., Fujibayashi, S., Neo, M., and Nakamura, T. EP4 agonist accelerates osteoinduction and degradation of beta-tricalcium phosphate by stimulating osteoclastogenesis. J Biomed Mater Res A 89, 601, 2009.
7. Paralkar, V.M., Borovecki, F., Ke, H.Z., Cameron, K.O., Lefker, B., Grasser, W.A., et al. An EP2 receptor-selective prostaglandin E2 agonist induces bone healing. Proc Natl Acad Sci USA 100, 6736, 2003.
8. Iwaniec, U.T., Trevisiol, C.H., Maddalozzo, G.F., Rosen, C.J., and Turner, R.T. Effects of low-dose parathyroid hormone on bone mass, turnover, and ectopic osteoinduction in a rat model for chronic alcohol abuse. Bone 42, 695, 2008.
9. Moxham, J.P. Oncostatin-M enhances osteoinduction in a rabbit critical calvarial defect model. Laryngoscope 117, 1790, 2007.
10. Anada, T., Kumagai, T., Honda, Y., Masuda, T., Kamijo, R., Kamakura, S., et al. Dose-dependent osteogenic effect of octacalcium phosphate on mouse bone marrow stromal cells. Tissue Eng Part A 14, 965, 2008.
11. Cordonnier, T., Layrolle, P., Gaillard, J., Langonne, A., Sensebe, L., Rosset, P., et al. 3D environment on human mesenchymal stem cells differentiation for bone tissue engineering. J Mater Sci Mater Med 21, 981, 2010.
12. Lin, L., Chow, K.L., and Leng, Y. Study of hydroxyapatite osteoinductivity with an osteogenic differentiation of mesenchymal stem cells. J Biomed Mater Res A 89, 326, 2009.
13. Sun, H., Ye, F., Wang, J., Shi, Y., Tu, Z., Bao, J., et al. The upregulation of osteoblast marker genes in mesenchymal stem cells prove the osteoinductivity of hydroxyapatite/ tricalcium phosphate biomaterial. Transplant Proc 40, 2645, 2008.
14. Zhang, Z., Kurita, H., Kobayashi, H., and Kurashina, K. Osteoinduction with HA/TCP ceramics of different composition and porous structure in rabbits. Oral Sci Int 2, 85, 2005.
15. Nakamura, T. Biomaterial osteoinduction. J Orthop Sci 12, 111, 2007.
16. Ripamonti, U. Osteoinduction in porous hydroxyapatite implanted in heterotopic sites of different animal models. Biomaterials 17, 31, 1996.
17. Ripamonti, U., Van den Heever, B., and Van Wyk, J. Expression of the osteogenic phenotype in porous hydroxyapatite implanted extraskeletally in baboons. Matrix 13, 491, 1993.
18. Ripamonti, U., Crooks, J., Khoali, L., and Roden, L. The induction of bone formation by coral-derived calcium carbonate/hydroxyapatite constructs. Biomaterials 30, 1428, 2009.
19. Ripamonti, U., Richter, P.W., Nilen, R.W., and Renton, L. 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, 2008.
20. Habibovic, P., Yuan, H., van der Valk, C.M., Meijer, G., van Blitterswijk, C.A., and de Groot, K. 3D microenvironment as essential element for osteoinduction by biomaterials. Biomaterials 26, 3565, 2005.
21. Honda, Y., Anada, T., Kamakura, S., Morimoto, S., Kuriyagawa, T., and Suzuki, O. The effect of microstructure of octacalcium phosphate on the bone regenerative property. Tissue Eng Part A 15, 1965, 2009.
22. Habibovic, P., and de Groot, K. Osteoinductive biomaterials-properties and relevance in bone repair. J Tissue Eng Regen Med 1, 25, 2007.
23. Habibovic, P., Kruyt, M.C., Juhl, M.V., Clyens, S., Martinetti, R., Dolcini, L., et al. Comparative in vivo study of six hydroxyapatite-based bone graft substitutes. J Orthop Res 26, 1363, 2008.
24. Habibovic, P., Sees, T.M., van den Doel, M.A., van Blitterswijk, C.A., and de Groot, K. Osteoinduction by biomaterials-physicochemical and structural influences. J Biomed Mater Res A 77, 747, 2006.
25. Muller, P., Bulnheim, U., Diener, A., Luthen, F., Teller, M., Klinkenberg, E.D., et al. Calcium phosphate surfaces promote osteogenic differentiation of mesenchymal stem cells. J Cell Mol Med 12, 281, 2008.
26. Biggs, M.J., Richards, R.G., Gadegaard, N., McMurray, R.J., Affrossman, S., Wilkinson, C.D., et al. Interactions with nanoscale topography: adhesion quantification and signal transduction in cells of osteogenic and multipotent lineage. J Biomed Mater Res A 91, 195, 2009.
27. Biggs, M.J., Richards, R.G., McFarlane, S., Wilkinson, C.D., Oreffo, R.O., and Dalby, M.J. Adhesion formation of primary human osteoblasts and the functional response of mesenchymal stem cells to 330nm deep microgrooves. J R Soc Interface 5, 1231, 2008.
28. Barrere, F., van der Valk, C.M., Dalmeijer, R.A., Meijer, G., van Blitterswijk, C.A., de Groot, K., et al. Osteogenecity of octacalcium phosphate coatings applied on porous metal implants. J Biomed Mater Res A 66, 779, 2003.
29. Fan, H., Ikoma, T., Tanaka, J., and Zhang, X. Surface structural biomimetics and the osteoinduction of calcium phosphate biomaterials. J Nanosci Nanotechnol 7, 808, 2007.
30. Heliotis, M., Ripamonti, U., Ferretti, C., Kerawala, C., Mantalaris, A., and Tsiridis, E. The basic science of bone induction. Br J Oral Maxillofac Surg 47, 511, 2009.
31. Li, X., van Blitterswijk, C.A., Feng, Q., Cui, F., and Watari, F. The effect of calcium phosphate microstructure on bonerelated cells in vitro. Biomaterials 29, 3306, 2008.
32. Yuan, H., Van Den Doel, M., Li, S., Van Blitterswijk, C.A., De Groot, K., and De Bruijn, J.D. A comparison of the osteoinductive potential of two calcium phosphate ceramics implanted intramuscularly in goats. J Mater Sci Mater Med 13, 1271, 2002.
33. Yuan, H., van Blitterswijk, C.A., de Groot, K., and de Bruijn, J.D. A comparison of bone formation in biphasic calcium phosphate (BCP) and hydroxyapatite (HA) implanted in muscle and bone of dogs at different time periods. J Biomed Mater Res A 78, 139, 2006.
34. Yuan, H., van Blitterswijk, C.A., de Groot, K., and de Bruijn, J.D. Cross-species comparison of ectopic bone formation in biphasic calcium phosphate (BCP) and hydroxyapatite (HA) scaffolds. Tissue Eng 12, 1607, 2006.
35. Arinzeh, T.L., Tran, T., McAlary, J., and Daculsi, G. A comparative study of biphasic calcium phosphate ceramics for human mesenchymal stem-cell-induced bone formation. Biomaterials 26, 3631, 2005.
36. Yao, J., Li, X., Bao, C., Zhang, C., Chen, Z., Fan, H., et al. Ectopic bone formation in adipose-derived stromal cellseeded osteoinductive calcium phosphate scaffolds. J Biomater Appl 24, 607, 2010.
37. Fujibayashi, S., Neo, M., Kim, H.M., Kokubo, T., and Nakamura, T. Osteoinduction of porous bioactive titanium metal. Biomaterials 25, 443, 2004.
38. Lui, P.P., Chan, L.S., Cheuk, Y.C., Lee, Y.W., and Chan, K.M. Expression of bone morphogenetic protein-2 in the chondrogenic and ossifying sites of calcific tendinopathy and traumatic tendon injury rat models. J Orthop Surg Res 4, 27, 2009.
39. Li, X., Yang, H.Y., and Giachelli, C.M. BMP-2 promotes phosphate uptake, phenotypic modulation, and calcification of human vascular smooth muscle cells. Atherosclerosis 199, 271, 2008.
40. Winter, G.D. Heterotopic bone induced by synthetic sponge implants. Isr J Med Sci 7, 433, 1971.
41. Eyckmans, J., Roberts, S.J., Schrooten, J., and Luyten, F.P. A clinically relevant model of osteoinduction: a process requiring calcium phosphate and BMP/Wnt signaling. J Cell Mol Med 14, 1845, 2010.
42. Honda, Y., Anada, T., Kamakura, S., Nakamura, M., Sugawara, S., and Suzuki, O. Elevated extracellular calcium stimulates secretion of bone morphogenetic protein 2 by a macrophage cell line. Biochem Biophys Res Commun 345, 1155, 2006.
43. Braet, F., De Zanger, R., and Wisse, E. Drying cells for SEM, AFM and TEM by hexamethyldisilazane: a study on hepatic endothelial cells. J Microsc 186, 84, 1997.
44. Dvorak, M.M., Siddiqua, A., Ward, D.T., Carter, D.H., Dallas, S.L., Nemeth, E.F., et al. Physiological changes in extracellular calcium concentration directly control osteoblast function in the absence of calciotropic hormones. Proc Natl Acad Sci USA 101, 5140, 2004.
45. Maeno, S., Niki, Y., Matsumoto, H., Morioka, H., Yatabe, T., Funayama, A., et al. The effect of calcium ion concentration on osteoblast viability, proliferation and differentiation in monolayer and 3D culture. Biomaterials 26, 4847, 2005.
46. Liu, Y.K., Lu, Q.Z., Pei, R., Ji, H.J., Zhou, G.S., Zhao, X.L., et al. The effect of extracellular calcium and inorganic phosphate on the growth and osteogenic differentiation of mesenchymal stem cells in vitro: implication for bone tissue engineering. Biomed Mater 4, 1, 2009.
47. McCullen, S., Zhan, J., Onorato, M., Bernacki, S., and Loboa, E. Effect of varied ionic calcium on human adipose-derived stem cell mineralization. Tissue Eng Part A 16, 1971, 2010.
48. Matsumoto, T., Nakamura, S., Sasaki, J.-I., Egusa, H., Lee, K.Y.Y., Nakano, T., et al. Effect of calcium ion concentrations on osteogenic differentiation and hematopoietic stem cell niche-related protein expressions in osteoblasts. Tissue Eng Part A 16, 2467, 2010.
49. De Bari, C., Dell'Accio, F., Vanlauwe, J., Eyckmans, J., Khan, I.M., Archer, C.W., et al. Mesenchymal multipotency of adult human periosteal cells demonstrated by single-cell lineage analysis. Arthritis Rheum 54, 1209, 2006.
50. Hutmacher, D.W., and Sittinger, M. Periosteal cells in bone tissue engineering. Tissue Eng 9, S-45, 2003.
51. Eyckmans, J., and Luyten, F.P. Species specificity of ectopic bone formation using periosteum-derived mesenchymal progenitor cells. Tissue Eng 12, 2203, 2006.
52. Peterson, D.R., Heideger, W.J., and Beach, K.W. Calcium homeostasis: the effect of parathyroid hormone on bone membrane electrical potential difference. Calcif Tissue Int 37, 307, 1985.
53. Karner, E., Backesjo, C.-M., Cedervall, J., Sugars, R.V., Ahrlund-Richter, L., and Wendel, M. Dynamics of gene expression during bone matrix formation in osteogenic cultures derived from human embryonic stem cells in vitro. Biochim Biophys Acta 1790, 110, 2009.
54. Cohen, M.M., Jr. The new bone biology: pathologic, molecular, and clinical correlates. Am J Med Genet Part A 140A, 2646, 2006.
55. Zhang, C. Transcriptional regulation of bone formation by the osteoblast-specific transcription factor Osx. J Orthop Surg Res 5, 1, 2010.
56. Nayab, S.N., Jones, F.H., and Olsen, I. Modulation of the human bone cell cycle by calcium ion-implantation of titanium. Biomaterials 28, 38, 2007.
57. Rodrigues, M.A., Gomes, D.A., Leite, M.F., Grant, W., Zhang, L., Lam, W., et al. Nucleoplasmic calcium is required for cell proliferation. J Biol Chem 282, 17061, 2007.
58. Nayab, S.N., Jones, F.H., and Olsen, I. Effects of calcium ionimplantation of titanium on bone cell function in vitro. J Biomed Mater Res A 83, 296, 2007.
59. Zayzafoon, M. Calcium/calmodulin signaling controls osteoblast growth and differentiation. J Cell Biochem 97, 56, 2006.
60. Sugimoto, T., Kanatani, M., Kano, J., Kobayashi, T., Yamaguchi, T., Fukase, M., et al. IGF-1 mediates the stimulatory effect of high calcium concentration on osteoblastic cell proliferation. Am J Physiol Endocrinol Metab 266, E709, 1994.
61. Kanatani, M., Sugimoto, T., Kano, J., and Chihara, K. IGF-1 mediates the stimulatory effect of high phosphate concentration on osteoblastic cell proliferation. J Cell Physiol 190, 306, 2002.
62. Meleti, Z., Shapiro, I.M., and Adams, C.S. Inorganic phosphate induces apoptosis of osteoblast-like cells in culture. Bone 27, 359, 2000.
63. Adams, C.S., Mansfield, K., Perlot, R.L., and Shapiro, I.M. Matrix regulation of skeletal cell apoptosis: role of calcium and phosphate ions. J Biol Chem 276, 20316, 2001.
64. Saunders, R., Szymczyk, K.H., Shapiro, I.M., and Adams, C.S. Matrix regulation of skeletal cell apoptosis III: mechanism of ion pair-induced apoptosis. J Cell Biochem 100, 703, 2007.
65. Beck, L., Leroy, C., Salaun, C., Margall-Ducos, G., Desdouets, C., and Friedlander, G. Identification of a novel function of PiT1 critical for cell proliferation and independent of its phosphate transport activity. J Biol Chem 284, 31363, 2009.
66. O'Neill, W.C. Pyrophosphate, alkaline phosphatase, and vascular calcification. Circ Res 99, e2, 2006. (Pubitemid 44297030)
67. Roach, H.I. Why does bone matrix contain non-collagenous proteins? The possible roles of osteocalcin, osteonectin, osteopontin and bone sialoprotein in bone mineralisation and resorption. Cell Biol Int 18, 617, 1994.
68. Nakamura, A., Dohi, Y., Akahane, M., Ohgushi, H., Nakajima, H., Funaoka, H., et al. Osteocalcin secretion as an early marker of in vitro osteogenic differentiation of rat mesenchymal stem cells. Tissue Eng Part C Methods 15, 169, 2009.
69. Boskey, A.L., Spevak, L., Paschalis, E., Doty, S.B., and McKee, M.D. Osteopontin deficiency increases mineral content and mineral crystallinity in mouse bone. Calcif Tissue Int 71, 145, 2002.
70. Ducy, P., Desbois, C., Boyce, B., Pinero, G., Story, B., Dunstan, C., et al. Increased bone formation in osteocalcindeficient mice. Nature 382, 448, 1996.
71. Fatherazi, S., Matsa-Dunn, D., Foster, B.L., Rutherford, R.B., Somerman, M.J., and Presland, R.B. Phosphate regulates osteopontin gene transcription. J Dent Res 88, 39, 2009.
72. Yoshiko, Y., Candeliere, G.A., Maeda, N., and Aubin, J.E. Osteoblast autonomous Pi regulation via Pit1 plays a role in bone mineralization. Mol Cell Biol 27, 4465, 2007.
73. Fujita, T., Izumo, N., Fukuyama, R., Meguro, T., Nakamuta, H., Kohno, T., et al. Phosphate provides an extracellular signal that drives nuclear export of Runx2/Cbfa1 in bone cells. Biochem Biophys Res Commun 280, 348, 2001.
74. Eyckmans, J., Roberts, S.J., Schrooten, J., and Luyten, F.P. A clinically relevant model of osteoinduction: a process requiring calcium phosphate and BMP/Wnt signaling. J Cell Mol Med 14, 1845, 2010.
75. Rashid, F., Shiba, H., Mizuno, N., Mouri, Y., Fujita, T., Shinohara, H., et al. The effect of extracellular calcium ion on gene expression of bone-related proteins in human pulp cells. J Endod 29, 104, 2003.
76. Nakade, O., Takahashi, K., Takuma, T., Aoki, T., and Kaku, T. Effect of extracellular calcium on the gene expression of bone morphogenetic protein-2 and -4 of normal human bone cells. J Bone Miner Metab 19, 13, 2001.
77. Peiris, D., Pacheco, I., Spencer, C., and MacLeod, R.J. The extracellular calcium-sensing receptor reciprocally regulates the secretion of BMP-2 and the BMP antagonist Noggin in colonic myofibroblasts. Am J Physiol Gastrointest Liver Physiol 292, G753, 2007.
78. Ripamonti, U. Soluble osteogenic molecular signals and the induction of bone formation. Biomaterials 27, 807, 2006.