Interactions Between Inorganic and Organic Phases in Bone Tissue as a Source of Inspiration for Design of Novel Nanocomposites

Tissue Engineering - Part B: Reviews

Volumn 20, Issue 2, 2014, Pages 173-188

  Farbod, Kambiz ^a   Nejadnik, M Reza ^a   Jansen, John A ^a   Leeuwenburgh, Sander C G ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BONE; DESIGN; FUNCTIONAL GROUPS; MINERALS; NANOCOMPOSITES;

BONE MINERALIZATION; EXTRACELLULAR BONE MATRICES; EXTRACELLULAR MATRIX COMPONENTS; MINERAL FORMATION; NOVEL NANOCOMPOSITES; ORGANIC COMPONENTS; STRUCTURAL LEVELS; SYNTHETIC APPROACH;

TISSUE;

ALENDRONIC ACID; AMINO ACID; APATITE; BIOMATERIAL; BISPHOSPHONIC ACID DERIVATIVE; BONE SIALOPROTEIN; CALCIUM ION; CALCIUM PHOSPHATE; CARBOXYL GROUP; CATECHOL; COLLAGEN; COLLAGEN FIBRIL; ELASTIN; FIBRONECTIN; HYALURONIC ACID; HYDROXYL GROUP; INORGANIC COMPOUND; LAMININ; NANOCOMPOSITE; NANOCRYSTAL; ORGANIC COMPOUND; OSTEOCALCIN; OSTEOPONTIN; PHOSPHATE; PHOSPHONIC ACID DERIVATIVE; POLYETHYLENEIMINE; POLYMER; SULFATE; BIOMIMETIC MATERIAL;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BIOMINERALIZATION; BONE GRAFT; BONE MATRIX; BONE MINERAL; BONE MINERALIZATION; BONE TISSUE; COMPOSITE MATERIAL; CRYSTALLIZATION; EQUIPMENT DESIGN; EXTRACELLULAR MATRIX; HUMAN; HYDROGEL; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; TISSUE ENGINEERING; ANIMAL; BONE; CHEMISTRY; CYTOLOGY; PHASE TRANSITION; PHYSIOLOGY;

ANIMALS; BIOMIMETIC MATERIALS; BONE AND BONES; CALCIFICATION, PHYSIOLOGIC; HUMANS; INORGANIC CHEMICALS; NANOCOMPOSITES; ORGANIC CHEMICALS; PHASE TRANSITION;

EID: 84897051826     PISSN: 19373368     EISSN: 19373376     Source Type: Journal    
DOI: 10.1089/ten.teb.2013.0221     Document Type: Article

References (197)

1. Chan, C.K., Kumar, T.S., Liao, S., Murugan, R., Ngiam, M., and Ramakrishnan, S. Biomimetic nanocomposites for bone graft applications. Nanomedicine (Lond) 1, 177, 2006
2. Spicer, P.P., Kretlow, J.D., Young, S., Jansen, J.A., Kasper, F.K., and Mikos, A.G. Evaluation of bone regeneration using the rat critical size calvarial defect. Nat Protoc 7, 1918, 2012
3. Kretlow, J.D., and Mikos, A.G. Review: Mineralization of synthetic polymer scaffolds for bone tissue engineering. Tissue Eng 13, 927, 2007
4. Porter, J.R., Ruckh, T.T., and Popat, K.C. Bone tissue engineering: A review in bone biomimetics and drug delivery strategies. Biotechnol Prog 25, 1539, 2009
5. Silber, J.S., Anderson, D.G., Daffner, S.D., Brislin, B.T., Leland, J.M., Hilibrand, A.S., Vaccaro, A.R., and Albert, T.J. Donor site morbidity after anterior iliac crest bone harvest for single-level anterior cervical discectomy and fusion. Spine (Phila Pa 1976) 28, 134, 2003
6. Rogers, S.N., Lakshmiah, S.R., Narayan, B., Lowe, D., Brownson, P., Brown, J.S., and Vaughan, E.D. A comparison of the long-Term morbidity following deep circumflex iliac and fibula free flaps for reconstruction following head and neck cancer. Plast Reconstr Surg 112, 1517, 2003
7. Niinomi, M. Metallic biomaterials. J Artif Organs 11, 105, 2008
8. Habraken, W.J.E.M., Wolke, J.G.C., and Jansen, J.A. Ceramic composites as matrices and scaffolds for drug delivery in tissue engineering. Adv Drug Deliv Rev 59, 234, 2007
9. Kohane, D.S., and Langer, R. Polymeric biomaterials in tissue engineering. Pediatr Res 63, 487, 2008
10. Staiger, M.P., Pietak, A.M., Huadmai, J., and Dias, G. Magnesium and its alloys as orthopedic biomaterials: A review. Biomaterials 27, 1728, 2006
11. Kannan, M.B., and Raman, R.K. In vitro degradation and mechanical integrity of calcium-containing magnesium alloys in modified-simulated body fluid. Biomaterials 29, 2306, 2008
12. Wang, H., and Shi, Z. In vitro biodegradation behavior of magnesium and magnesium alloy. J Biomed Mater Res B Appl Biomater 98B, 203, 2011
13. Ebramzadeh, E., Normand, P.L., Sangiorgio, S.N., Lliná s, A., Gruen, T.A., McKellop, H.A., and Sarmiento, A. Longterm radiographic changes in cemented total hip arthroplasty with six designs of femoral components. Biomaterials 24, 3351, 2003
14. Antunes, R.A., and de Oliveira, M.C. Corrosion fatigue of biomedical metallic alloys: Mechanisms and mitigation. Acta Biomater 8, 937, 2012
15. Yamamoto, A., Honma, R., and Sumita, M. Cytotoxycity of metal salts and its compound effects. In: Ikada, Y., and Zhang, X., eds. Biomedical Materials Research in the Far East (II). Kyoto: Kobunshi Kankokai, Inc., 1996, pp. 89-90
16. Kikuchi, M., Itoh, S., Ichinose, S., Shinomiya, K., and Tanaka, J. Self-organization mechanism in a bone-like hydroxyapatite/ collagen nanocomposite synthesized in vitro and its biological reaction in vivo. Biomaterials 22, 1705, 2001
17. Wong, J.Y., and Bronzino, J.D. Biomaterials. New York: CRC Press, 2007
18. Rezwan, K., Chen, Q.Z., Blaker, J.J., and Boccaccini, A.R. Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials 27, 3413, 2006
19. Choi, J., Harcup, J., Yee, A.F., Zhu, Q., and Laine, R.M. Organic/inorganic hybrid composites from cubic silsesquioxanes. J Am Chem Soc 123, 11420, 2001
20. Hsu, F.Y., Chueh, S.C., and Wang, Y.J. Microspheres of hydroxyapatite/reconstituted collagen as supports for osteoblast cell growth. Biomaterials 20, 1931, 1999
21. Sivakumar, M., and Panduranga Rao, K. Preparation, characterization and in vitro release of gentamicin from coralline hydroxyapatite-gelatin composite microspheres. Biomaterials 23, 3175, 2002
22. Cushnie, E.K., Khan, Y.M., and Laurencin, C.T. Amorphous hydroxyapatite-sintered polymeric scaffolds for bone tissue regeneration: Physical characterization studies. J Biomed Mater Res A 84, 54, 2008
23. Chesnutt, B.M., Yuan, Y., Buddington, K., Haggard, W.O., and Bumgardner, J.D. Composite chitosan/nano-hydroxyapatite scaffolds induce osteocalcin production by osteoblasts in vitro and support bone formation in vivo. Tissue Eng Part A 15, 2571, 2009
24. Lv, Q., Nair, L., and Laurencin, C.T. Fabrication, characterization, and in vitro evaluation of poly(lactic acid glycolic acid)/nano-hydroxyapatite composite microsphere-based scaffolds for bone tissue engineering in rotating bioreactors. J Biomed Mater Res A 91, 679, 2009
25. Leeuwenburgh, S.C., Jo, J., Wang, H., Yamamoto, M., Jansen, J.A., and Tabata, Y. Mineralization, biodegradation, and drug release behavior of gelatin/apatite composite microspheres for bone regeneration. Biomacromolecules 11, 2653, 2010
26. Wang, H., Leeuwenburgh, S.C.G., Li, Y., and Jansen, J.A. The use of micro-And nanospheres as functional components for bone tissue regeneration. Tissue Eng Part B Rev 18, 24, 2011
27. Wang, Y., Azaïs, T., Robin, M., Valle'e, A., Catania, C., Legriel, P., Pehau-Arnaudet, G., Babonneau, F., Giraud-Guille, M.M., and Nassif, N. The predominant role of collagen in the nucleation, growth, structure and orientation of bone apatite. Nat Mater 11, 724, 2012
28. Matthews, F.L., and Rawlings, R.D. Composite Materials: Engineering and Science. London: Chapman & Hall, 1994
29. Morgan, E.F., Barnes, G.L., and Einhorn, T.A. The bone organ system: Form and function. In: Marcus, R., Feldman, D., Nelson, D., and Rosen, C.J., eds. Fundamentals of Osteoporosis. San Diego, CA: Elsevier Academic Press, 2008, pp. 1-25
30. Labat-Robert, J., Bihari-Varga, M., and Robert, L. Extracellular matrix. FEBS Lett 268, 386, 1990
31. Schönherr, E., and Hausser, H.J. Extracellular matrix and cytokines: A functional unit. Dev Immunol 7, 89, 2000
32. Rosso, F., Giordano, A., Barbarisi, M., and Barbarisi, A. From cell-ECM interactions to tissue engineering. J Cell Physiol 199, 174, 2004
33. Pradhan, S., and Farach-Carson, M.C. Mining the extracellular matrix for tissue engineering applications. Regen Med 5, 961, 2010
34. Fujisawa, R., and Tamura, M. Acidic bone matrix proteins and their roles in calcification. Front Biosci 17, 1891, 2012
35. Edwards, G.M., Wilford, F.H., Liu, X., Hennighausen, L., Djiane, J., and Streuli, C.H. Regulation of mammary differentiation by extracellular matrix involves protein-Tyrosine phosphatases. J Biol Chem 273, 9495, 1998
36. Palmer, L.C., Newcomb, C.J., Kaltz, S.R., Spoerke, E.D., and Stupp, S.I. Biomimetic systems for hydroxyapatite mineralization inspired by bone and enamel. Chem Rev 108, 4754, 2008
37. Beniash, E. Biominerals-hierarchical nanocomposites: The example of bone. Wiley Interdiscip Rev Nanomed Nanobiotechnol 3, 47, 2011
38. Glimcher, M.J. Mechanism of calcification: Role of collagen fibrils and collagen-phosphoprotein complexes in vitro and in vivo. Anat Rec 224, 139, 1989
39. Nudelman, F., Pieterse, K., George, A., Bomans, P.H., Friedrich, H., Brylka, L.J., Hilbers, P.A., de With, G., and Sommerdijk, N.A. The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat Mater 9, 1004, 2010
40. Landis, W.J., Silver, F.H., and Freeman, J.W. Collagen as a scaffold for biomimetic mineralization of vertebrate tissues. J Mater Chem 16, 1495, 2006
41. Cölfen, H. Biomineralization: A crystal-clear view. Nat Mater 9, 960, 2010
42. Dai, L., Qi, Y.P., Niu, L.N., Liu, Y., Pucci, C.R., Looney, S.W., Ling, J.Q., Pashley, D.H., and Tay, F.R. Inorganic-organic nanocomposite assembly using collagen as a template and sodium tripolyphosphate as a biomimetic analog of matrix phosphoprotein. Cryst Growth Des 11, 3504, 2011
43. Oldberg, A., Franze'n, A., and Heinega° rd, D. The primary structure of a cell-binding bone sialoprotein. J Biol Chem 263, 19430, 1988
44. Hunter, G.K., and Goldberg, H.A. Nucleation of hydroxyapatite by bone sialoprotein. Proc Natl Acad Sci U S A 90, 8562, 1993
45. Hunter, G.K., and Goldberg, H.A. Modulation of crystal formation by bone phosphoproteins: Role of glutamic acidrich sequences in the nucleation of hydroxyapatite by bone sialoprotein. Biochem J 302 (Pt 1), 175, 1994
46. Ganss, B., Kim, R.H., and Sodek, J. Bone sialoprotein. Crit Rev Oral Biol Med 10, 79, 1999
47. Tye, C.E., Rattray, K.R., Warner, K.J., Gordon, J.A., Sodek, J., Hunter, G.K., and Goldberg, H.A. Delineation of the hydroxyapatite-nucleating domains of bone sialoprotein. J Biol Chem 278, 7949, 2003
48. Chen, J., Shapiro, H.S., and Sodek, J. Developmental expression of bone sialoprotein mrna in rat mineralized connective tissues. J Bone Miner Res 7, 987, 2009
49. Mazzali, M., Kipari, T., Ophascharoensuk, V., Wesson, J.A., Johnson, R., and Hughes, J. Osteopontin-A molecule for all seasons. QJM 95, 3, 2002
50. Christensen, B., Petersen, T.E., and Sørensen, E.S. Posttranslational modification and proteolytic processing of urinary osteopontin. Biochem J 411, 53, 2008
51. Gericke, A., Qin, C., Spevak, L., Fujimoto, Y., Butler, W.T., Sørensen, E.S., and Boskey, A.L. Importance of phosphorylation for osteopontin regulation of biomineralization. Calcif Tissue Int 77, 45, 2005
52. Oldberg, A., Franze'n, A., and Heinega rd, D. Cloning and sequence analysis of rat bone sialoprotein (osteopontin) cDNA reveals an Arg-Gly-Asp cell-binding sequence. Proc Natl Acad Sci U S A 83, 8819, 1986
53. Craig, A.M., Smith, J.H., and Denhardt, D.T. Osteopontin, a transformation-Associated cell adhesion phosphoprotein, is induced by 12-O-Tetradecanoylphorbol 13-Acetate in mouse epidermis. J Biol Chem 264, 9682, 1989
54. Fantner, G.E., Hassenkam, T., Kindt, J.H., Weaver, J.C., Birkedal, H., Pechenik, L., Cutroni, J.A., Cidade, G.A., Stucky, G.D., Morse, D.E., and Hansma, P.K. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nat Mater 4, 612, 2005
55. Fantner, G.E., Adams, J., Turner, P., Thurner, P.J., Fisher, L.W., and Hansma, P.K. Nanoscale ion mediated networks in bone: Osteopontin can repeatedly dissipate large amounts of energy. Nano Lett 7, 2491, 2007
56. Thurner, P.J., Lam, S., Weaver, J.C., Morse, D.E., and Hansma, P.K. Localization of phosphorylated serine, osteopontin, and bone sialoprotein on bone fracture surfaces. J Adhes 85, 526, 2009
57. Qin, C., Baba, O., and Butler, W. Post-Translational modifications of sibling proteins and their roles in osteogenesis and dentinogenesis. Crit Rev Oral Biol Med 15, 126, 2004
58. Canalis, E., and Lian, J.B. Effects of bone associated growth factors on DNA, collagen and osteocalcin synthesis in cultured fetal rat calvariae. Bone 9, 243, 1988
59. Boivin, G., Morel, G., Lian, J.B., Anthoine-Terrier, C., Dubois, P.M., and Meunier, P.J. Localization of endogenous osteocalcin in neonatal rat bone and its absence in articular cartilage: Effect of warfarin treatment. Virchows Arch A Pathol Anat Histopathol 417, 505, 1990
60. Weinreb, M., Shinar, D., and Rodan, G.A. Different pattern of alkaline phosphatase, osteopontin, and osteocalcin expression in developing rat bone visualized by in situ hybridization. J Bone Miner Res 5, 831, 1990
61. Ducy, P., Desbois, C., Boyce, B., Pinero, G., Story, B., Dunstan, C., Smith, E., Bonadio, J., Goldstein, S., Gundberg, C., Bradley, A., and Karsenty, G. Increased bone formation in osteocalcin-deficient mice. Nature 382, 448, 1996
62. Ingram, R.T., Park, Y.K., Clarke, B.L., and Fitzpatrick, L.A. Age-And gender-related changes in the distribution of osteocalcin in the extracellular matrix of normal male and female bone. Possible involvement of osteocalcin in bone remodeling. J Clin Invest 93, 989, 1994
63. Smith, C., Craig, O., Prigodich, R., Nielsen-Marsh, C., Jans, M., Vermeer, C., and Collins, M. Diagenesis and survival of osteocalcin in archaeological bone. J Archaeol Sci 32, 105, 2005
64. Eppell, S.J., Tong, W., Katz, J.L., Kuhn, L., and Glimcher, M.J. Shape and size of isolated bone mineralites measured using atomic force microscopy. J Orthop Res 19, 1027, 2001
65. Grabner, B., Landis, W.J., Roschger, P., Rinnerthaler, S., Peterlik, H., Klaushofer, K., and Fratzl, P. Age-And genotype-dependence of bone material properties in the osteogenesis imperfecta murine model (oim). Bone 29, 453, 2001
66. Olszta, M.J., Cheng, X., Jee, S.S., Kumar, R., Kim, Y.-Y., Kaufman, M.J., Douglas, E.P., and Gower, L.B. Bone structure and formation: A new perspective. Mater Sci Eng R Rep 58, 77, 2007
67. Boskey, A.L. Matrix proteins and mineralization: An overview. Connect Tissue Res 35, 357, 1996
68. Chai, Y.C., Carlier, A., Bolander, J., Roberts, S.J., Geris, L., Schrooten, J., Oosterwyck, H.V., and Luyten, F.P. Current views on calcium phosphate osteogenicity and the translation into effective bone regeneration strategies. Acta Biomater 8, 3876, 2012
69. Stubbs, J.T., Mintz, K.P., Eanes, E.D., Torchia, D.A., and Fisher, L.W. Characterization of native and recombinant bone sialoprotein: Delineation of the mineral-binding and cell adhesion domains and structural analysis of the RGD domain. J Bone Miner Res 12, 1210, 1997
70. He, G., Ramachandran, A., Dahl, T., George, S., Schultz, D., Cookson, D., Veis, A., and George, A. Phosphorylation of phosphophoryn is crucial for its function as a mediator of biomineralization. J Biol Chem 280, 33109, 2005
71. Monfoulet, L., Malaval, L., Aubin, J.E., Rittling, S.R., Gadeau, A.P., Fricain, J.C., and Chassande, O. Bone sialoprotein, but not osteopontin, deficiency impairs the mineralization of regenerating bone during cortical defect healing. Bone 46, 447, 2010
72. Meyer, U., Meyer, T., Vosshans, J., and Joos, U. Decreased expression of osteocalcin and osteonectin in relation to high strains and decreased mineralization in mandibular distraction osteogenesis. J Craniomaxillofac Surg 27, 222, 1999
73. Hoang, Q.Q., Sicheri, F., Howard, A.J., and Yang, D.S. Bone recognition mechanism of porcine osteocalcin from crystal structure. Nature 425, 977, 2003
74. Roach, H.I. Why does bone matrix contain non-collagenous proteins?The possible roles of osteocalcin, osteonectin, osteopontin and bone sialoprotein in bone mineralization and resorption. Cell Biol Int 18, 617, 1994
75. Rosenthal, A.K., Gohr, C.M., Uzuki, M., and Masuda, I. Osteopontin promotes pathologic mineralization in articular cartilage. Matrix Biol 26, 96, 2007
76. Elangovan, S., Margolis, H.C., Oppenheim, F.G., and Beniash, E. Conformational changes in salivary proline-rich protein 1 upon adsorption to calcium phosphate crystals. Langmuir 23, 11200, 2007
77. Orgel, J.P., Irving, T.C., Miller, A., and Wess, T.J. Microfibrillar structure of type I collagen in situ. Proc Natl Acad Sci U S A 103, 9001, 2006
78. Minary-Jolandan, M., and Yu, M.F. Nanomechanical heterogeneity in the gap and overlap regions of type I collagen fibrils with implications for bone heterogeneity. Biomacromolecules 10, 2565, 2009
79. Veis, A. Mineralization in organic matrix frameworks. Rev Miner Geochem 54, 249, 2003
80. Dahl, T., Sabsay, B., and Veis, A. Type I collagen-phosphophoryn interactions: Specificity of the monomer-monomer binding. J Struct Biol 123, 162, 1998
81. Beniash, E., Traub, W., Veis, A., and Weiner, S. A transmission electron microscope study using vitrified ice sections of predentin: Structural changes in the dentin collagenous matrix prior to mineralization. J Struct Biol 132, 212, 2000
82. He, G., and George, A. Dentin matrix protein 1 immobilized on type I collagen fibrils facilitates apatite deposition in vitro. J Biol Chem 279, 11649, 2004
83. Plate, U., Arnold, S., Reimer, L., Höhling, H.J., and Boyde, A. Investigation of the early mineralisation on collagen in dentine of rat incisors by quantitative electron spectroscopic diffraction (ESD). Cell Tissue Res 278, 543, 1994
84. Arnold, S., Plate, U., Wiesmann, H.P., Stratmann, U., Kohl, H., and Höhling, H.J. Quantitative electron spectroscopic diffraction analyses of the crystal formation in dentine. J Microsc 195, 58, 1999
85. Toroian, D., Lim, J.E., and Price, P.A. The size exclusion characteristics of type I collagen: Implications for the role of noncollagenous bone constituents in mineralization. J Biol Chem 282, 22437, 2007
86. He, G., Gajjeraman, S., Schultz, D., Cookson, D., Qin, C., Butler, W.T., Hao, J., and George, A. Spatially and temporally controlled biomineralization is facilitated by interaction between self-Assembled dentin matrix protein 1 and calcium phosphate nuclei in solution. Biochem 44, 16140, 2005
87. George, A., and Veis, A. Phosphorylated proteins and control over apatite nucleation, crystal growth and inhibition. Chem Rev 108, 4670, 2008
88. Gower, L.B. Biomimetic model systems for investigating the amorphous precursor pathway and its role in biomineralization. Chem Rev 108, 4551, 2008
89. Gebauer, D., Völkel, A., and Cölfen, H. Stable prenucleation calcium carbonate clusters. Science 322, 1819, 2008
90. Pouget, E.M., Bomans, P.H., Goos, J.A., Frederik, P.M., de With, G., and Sommerdijk, N.A. The initial stages of template-controlled CaCO3 formation revealed by cryo-TEM. Science 323, 1455, 2009
91. Dey, A., Bomans, P.H., Müller, F.A., Will, J., Frederik, P.M., de With, G., and Sommerdijk, N.A. The role of prenucleation clusters in surface-induced calcium phosphate crystallization. Nat Mater 9, 1010, 2010
92. Habraken, W.J., Tao, J., Brylka, L.J., Friedrich, H., Bertinetti, L., Schenk, A.S., Verch, A., Dmitrovic, V., Bomans, P.H., Frederik, P.M., Laven, J., van der Schoot, P., Aichmayer, B., de With, G., DeYoreo, J.J., and Sommerdijk, N.A. Ion-Association complexes unite classical and non-classical theories for the biomimetic nucleation of calcium phosphate. Nat Commun 4, 1507, 2013
93. Anderson, H.C. Molecular biology of matrix vesicles. Clin Orthop Relat Res, 266, 1995
94. Anderson, H.C., Garimella, R., and Tague, S.E. The role of matrix vesicles in growth plate development and biomineralization. Front Biosci 10, 822, 2005
95. Stewart, A.J., Roberts, S.J., Seawright, E., Davey, M.G., Fleming, R.H., and Farquharson, C. The presence of PHOSPHO1 in matrix vesicles and its developmental expression prior to skeletal mineralization. Bone 39, 1000, 2006
96. Golub, E.E. Role of matrix vesicles in biomineralization. Biochim Biophys Acta 1790, 1592, 2009
97. Anderson, H.C., Sipe, J.B., Hessle, L., Dhanyamraju, R., Atti, E., Camacho, N.P., and Milla'n, J.L. Impaired calcification around matrix vesicles of growth plate and bone in alkaline phosphatase-deficient mice. Am J Pathol 164, 841, 2004
98. Siffert, R.S. The role of alkaline phosphatase in osteogenesis. J Exp Med 93, 415, 1951
99. Golub, E.E., Harrison, G., Taylor, A.G., Camper, S., and Shapiro, I.M. The role of alkaline phosphatase in cartilage mineralization. Bone Miner 17, 273, 1992
100. Orimo, H. The mechanism of mineralization and the role of alkaline phosphatase in health and disease. J Nippon Med Sch 77, 4, 2010
101. Houston, B., Stewart, A.J., and Farquharson, C. PHOSPHO1-A novel phosphatase specifically expressed at sites of mineralisation in bone and cartilage. Bone 34, 629, 2004
102. Roberts, S., Narisawa, S., Harmey, D., Milla'n, J.L., and Farquharson, C. Functional involvement of PHOSPHO1 in matrix vesicle-mediated skeletal mineralization. J Bone Miner Res 22, 617, 2007
103. Šupová, M. Problem of hydroxyapatite dispersion in polymer matrices: A review. J Mater Sci Mater Med 20, 1201, 2009
104. Kickelbick, G. Concepts for the incorporation of inorganic building blocks into organic polymers on a nanoscale. Prog Polym Sci 28, 83, 2003
105. Holmes, R.L., Campbell, J.A., Burford, R.P., and Karatchevtseva, I. Pyrolysis behaviour of titanium dioxide-poly(vinyl pyrrolidone) composite materials. Polym Degrad Stab 94, 1882, 2009
106. Toworfe, G.K., Composto, R.J., Shapiro, I.M., and Ducheyne, P. Nucleation and growth of calcium phosphate on amine-, carboxyl-And hydroxyl-silane self-Assembled monolayers. Biomaterials 27, 631, 2006
107. Shen, J.W., Wu, T., Wang, Q., and Pan, H.H. Molecular simulation of protein adsorption and desorption on hydroxyapatite surfaces. Biomaterials 29, 513, 2008
108. Rees, S.G., Hughes Wassell, D.T., Waddington, R.J., and Embery, G. Interaction of bone proteoglycans and proteoglycan components with hydroxyapatite. Biochim Biophys Acta 1568, 118, 2001
109. Zhang, S., Gangal, G., and Uludaǧ, H. 'Magic bullets' for bone diseases: Progress in rational design of bone-seeking medicinal agents. Chem Soc Rev 36, 507, 2007
110. Tiselius, A., Hjerte'n, S., and Levin, O. Protein chromatography on calcium phosphate columns. Arch Biochem Biophys 65, 132, 1956
111. Gorbunoff, M.J. The interaction of proteins with hydroxyapatite. I. Role of protein charge and structure. Anal Biochem 136, 425, 1984
112. Gorbunoff, M.J. The interaction of proteins with hydroxyapatite. II. Role of acidic and basic groups. Anal Biochem 136, 433, 1984
113. Gorbunoff, M.J., and Timasheff, S.N. The interaction of proteins with hydroxyapatite. III. Mechanism. Anal Biochem 136, 440, 1984
114. Hlady, V., and Füredi-Milhofer, H. Adsorption of human serum albumin on precipitated hydroxyapatite. J Colloid Interface Sci 69, 460, 1979
115. Hauschka, P.V., and Carr, S.A. Calcium-dependent a-helical structure in osteocalcin. Biochemistry 21, 2538, 1982
116. Nieuw Amerongen, A.V., Oderkerk, C.H., and Veerman, E.C. Interaction of human salivary mucins with hydroxyapatite. J Biol Buccale 17, 85, 1989
117. Rathman, W.M., Van Zeyl, M.J., Van den Keybus, P.A., Bank, R.A., Veerman, E.C., and Nieuw Amerongen, A.V. Isolation and characterization of three non-mucinous human salivary proteins with affinity for hydroxyapatite. J Biol Buccale 17, 199, 1989
118. Robinson, C., Connell, S., Brookes, S.J., Kirkham, J., Shore, R.C., and Smith, D.A. Surface chemistry of enamel apatite during maturation in relation to pH: Implications for protein removal and crystal growth. Arch Oral Biol 50, 267, 2005
119. Rhee, S.H., Lee, J.D., and Tanaka, J. Nucleation of hydroxyapatite crystal through chemical interaction with collagen. J Am Ceram Soc 83, 2890, 2000
120. Chang, M.C. Organic-inorganic interaction between hydroxyapatite and gelatin with the aging of gelatin in aqueous phosphoric acid solution. J Mater Sci Mater Med 19, 3411, 2008
121. Chang, M.C., Ikoma, T., Kikuchi, M., and Tanaka, J. Preparation of a porous hydroxyapatite/collagen nanocomposite using glutaraldehyde as a crosslinkage agent. J Mater Sci Lett 20, 1199, 2001
122. Chang, M.C., Ko, C.C., and Douglas, W.H. Preparation of hydroxyapatite-gelatin nanocomposite. Biomaterials 24, 2853, 2003
123. Chirila, T.V., Minamisawa, T., Keen, I., and Shiba, K. Effect of motif-programmed artificial proteins on the calcium uptake in a synthetic hydrogel. Macromol Biosci 9, 959, 2009
124. Shiba, K., and Minamisawa, T. A synthesis approach to understanding repeated peptides conserved in mineralization proteins. Biomacromolecules 8, 2659, 2007
125. Tsuji, T., Onuma, K., Yamamoto, A., Iijima, M., and Shiba, K. Direct transformation from amorphous to crystalline calcium phosphate facilitated by motif-programmed artificial proteins. Proc Natl Acad Sci U S A 105, 16866, 2008
126. Wheeler, A.P., George, J.W., and Evans, C.A. Control of calcium carbonate nucleation and crystal growth by soluble matrx of oyster shell. Science 212, 1397, 1981
127. Jee, S.S., Culver, L., Li, Y., Douglas, E.P., and Gower, L.B. Biomimetic mineralization of collagen via an enzyme-Aided PILP process. J Cryst Growth 312, 1249, 2010
128. Jee, S.S., Thula, T.T., and Gower, L.B. Development of bone-like composites via the polymer-induced liquidprecursor (PILP) process. Part 1: Influence of polymer molecular weight. Acta Biomater 6, 3676, 2010
129. Delaittre, G., Greiner, A.M., Pauloehrl, T., Bastmeyer, M., and Barner-Kowollik, C. Chemical approaches to synthetic polymer surface biofunctionalization for targeted cell adhesion using small binding motifs. Soft Matter 8, 7323, 2012
130. Hynes, R.O. The extracellular matrix: Not just pretty fibrils. Science 326, 1216, 2009
131. Pozzi, A., and Zent, R. Integrins: Sensors of extracellular matrix and modulators of cell function. Nephron Exp Nephrol 94, e77, 2003
132. Ruoslahti, E. RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol 12, 697, 1996
133. Schwartz, M.A. Integrin signaling revisited. Trends Cell Biol 11, 466, 2001
134. Hersel, U., Dahmen, C., and Kessler, H. RGD modified polymers: Biomaterials for stimulated cell adhesion and beyond. Biomaterials 24, 4385, 2003
135. Ito, Y., Kajihara, M., and Imanishi, Y. Materials for enhancing cell adhesion by immobilization of cell-Adhesive peptide. J Biomed Mater Res 25, 1325, 1991
136. Hlady, V.V., and Buijs, J. Protein adsorption on solid surfaces. Curr Opin Biotechnol 7, 72, 1996
137. Iuliano, D.J., Saavedra, S.S., and Truskey, G.A. Effect of the conformation and orientation of adsorbed fibronectin on endothelial cell spreading and the strength of adhesion. J Biomed Mater Res 27, 1103, 1993
138. Lhoest, J.B., Detrait, E., van den Bosch de Aguilar, P., and Bertrand, P. Fibronectin adsorption, conformation, and orientation on polystyrene substrates studied by radiolabeling, XPS, and ToF SIMS. J Biomed Mater Res 41, 95, 1998
139. Barker, T.H. The role of ECM proteins and protein fragments in guiding cell behavior in regenerative medicine. Biomaterials 32, 4211, 2011
140. Bellis, S.L. Advantages of RGD peptides for directing cell association with biomaterials. Biomaterials 32, 4205, 2011
141. Collier, J.H., and Segura, T. Evolving the use of peptides as components of biomaterials. Biomaterials 32, 4198, 2011
142. Lucchese, G., Stufano, A., Trost, B., Kusalik, A., and Kanduc, D. Peptidology: Short amino acid modules in cell biology and immunology. Amino Acids 33, 703, 2007
143. Ratcliffe, A. Difficulties in the translation of functionalized biomaterials into regenerative medicine clinical products. Biomaterials 32, 4215, 2011
144. Williams, D.F. The role of short synthetic adhesion peptides in regenerative medicine; the debate. Biomaterials 32, 4195, 2011
145. Itoh, D., Yoneda, S., Kuroda, S., Kondo, H., Umezawa, A., Ohya, K., Ohyama, T., and Kasugai, S. Enhancement of osteogenesis on hydroxyapatite surface coated with synthetic peptide (EEEEEEEPRGDT) in vitro. J Biomed Mater Res 62, 292, 2002
146. Fujisawa, R., Wada, Y., Nodasaka, Y., and Kuboki, Y. Acidic amino acid-rich sequences as binding sites of osteonectin to hydroxyapatite crystals. Biochim Biophys Acta 1292, 53, 1996
147. Kasugai, S., Fujisawa, R., Waki, Y., Miyamoto, K., and Ohya, K. Selective drug delivery system to bone: Small peptide (Asp)6 conjugation. J Bone Miner Res 15, 936, 2000
148. Sarvestani, A.S., He, X., and Jabbari, E. Effect of osteonectin-derived peptide on the viscoelasticity of hydrogel/ apatite nanocomposite scaffolds. Biopolymers 85, 370, 2007
149. Sarvestani, A.S., He, X., and Jabbari, E. Osteonectin-derived peptide increases the modulus of a bone-mimetic nanocomposite. Eur Biophys J 37, 229, 2008
150. Culpepper, B.K., Phipps, M.C., Bonvallet, P.P., and Bellis, S.L. Enhancement of peptide coupling to hydroxyapatite and implant osseointegration through collagen mimetic peptide modified with a polyglutamate domain. Biomaterials 31, 9586, 2010
151. Culpepper, B.K., Bonvallet, P.P., Reddy, M.S., Ponnazhagan, S., and Bellis, S.L. Polyglutamate directed coupling of bioactive peptides for the delivery of osteoinductive signals on allograft bone. Biomaterials 34, 1506, 2013
152. Murphy, M.B., Hartgerink, J.D., Goepferich, A., and Mikos, A.G. Synthesis and in vitro hydroxyapatite binding of peptides conjugated to calcium-binding moieties. Biomacromolecules 8, 2237, 2007
153. Yang, X., Xie, B., Wang, L., Qin, Y., Henneman, Z.J., and Nancollas, G.H. Influence of magnesium ions and amino acids on the nucleation and growth of hydroxyapatite. Cryst Eng Comm 13, 1153, 2011
154. Bleek, K., and Taubert, A. New developments in polymercontrolled, bioinspired calcium phosphate mineralization from aqueous solution. Acta Biomater 9, 6283, 2013
155. Palazzo, B., Walsh, D., Iafisco, M., Foresti, E., Bertinetti, L., Martra, G., Bianchi, C.L., Cappelletti, G., and Roveri, N. Amino acid synergetic effect on structure, morphology and surface properties of biomimetic apatite nanocrystals. Acta Biomater 5, 1241, 2009
156. Boanini, E., Torricelli, P., Gazzano, M., Giardino, R., and Bigi, A. Nanocomposites of hydroxyapatite with aspartic acid and glutamic acid and their interaction with osteoblast-like cells. Biomaterials 27, 4428, 2006
157. Furuichi, K., Oaki, Y., Ichimiya, H., Komotori, J., and Imai, H. Preparation of hierarchically organized calcium phosphate-organic polymer composites by calcification of hydrogel. Sci Technol Adv Mater 7, 219, 2006
158. Imai, H., Tatara, S., Furuichi, K., and Oaki, Y. Formation of calcium phosphate having a hierarchically laminated architecture through periodic precipitation in organic gel. Chem Commun (Camb) 15, 1952, 2003
159. Gkioni, K., Leeuwenburgh, S.C., Douglas, T.E., Mikos, A.G., and Jansen, J.A. Mineralization of hydrogels for bone regeneration. Tissue Eng Part B Rev 16, 577, 2010
160. Hu, Y.Y., Rawal, A., and Schmidt-Rohr, K. Strongly bound citrate stabilizes the apatite nanocrystals in bone. Proc Natl Acad Sci U S A 107, 22425, 2010
161. Hu, Y.Y., Liu, X.P., Ma, X., Rawal, A., Prozorov, T., Akinc, M., Mallapragada, S.K., and Schmidt-Rohr, K. Biomimetic self-Assembling copolymer-hydroxyapatite nanocomposites with the nanocrystal size controlled by citrate. Chem Mater 23, 2481, 2011
162. Lo'pez-Macipe, A., Go'mez-Morales, J., and Rodri'guez-Clemente, R. Nanosized hydroxyapatite precipitation from homogeneous calcium/citrate/ phosphate solutions using microwave and conventional heating. Adv Mater 10, 49, 1998
163. Martins, M.A., Santos, C., Almeida, M.M., and Costa, M.E. Hydroxyapatite micro-And nanoparticles: Nucleation and growth mechanisms in the presence of citrate species. J Colloid Interface Sci 318, 210, 2008
164. Sun, T., Hayakawa, K., Bateman, K.S., and Fraser, M.E. Identification of the citrate-binding site of human ATPcitrate lyase using X-ray crystallography. J Biol Chem 285, 27418, 2010
165. Leeuwenburgh, S.C., Ana, I.D., and Jansen, J.A. Sodium citrate as an effective dispersant for the synthesis of inorganic-organic composites with a nanodispersed mineral phase. Acta Biomater 6, 836, 2010
166. Phadke, A., Zhang, C., Hwang, Y., Vecchio, K., and Varghese, S. Templated mineralization of synthetic hydrogels for bone-like composite materials: Role of matrix hydrophobicity. Biomacromolecules 11, 2060, 2010
167. Badiger, M., Lele, A., Bhalerao, V., Varghese, S., and Mashelkar, R. Molecular tailoring of thermoreversible copolymer gels: Some new mechanistic insights. J Chem Phys 109, 1175, 1998
168. Varghese, S., Lele, A.K., Srinivas, D., and Mashelkar, R.A. Role of hydrophobicity on structure of polymer-metal complexes. J Phys Chem B 105, 5368, 2001
169. Song, J., Saiz, E., and Bertozzi, C.R. A new approach to mineralization of biocompatible hydrogel scaffolds: An efficient process toward 3-dimensional bonelike composites. J Am Chem Soc 125, 1236, 2003
170. Bigi, A., Boanini, E., Panzavolta, S., and Roveri, N. Biomimetic growth of hydroxyapatite on gelatin films doped with sodium polyacrylate. Biomacromolecules 1, 752, 2000
171. Cha, C., Kim, E.S., Kim, I.W., and Kong, H. Integrative design of a poly(ethylene glycol)-poly(propylene glycol)-Alginate hydrogel to control three dimensional biomineralization. Biomaterials 32, 2695, 2011
172. Suzuki, S., Whittaker, M.R., Grøndahl, L., Monteiro, M.J., and Wentrup-Byrne, E. Synthesis of soluble phosphate polymers by RAFT and their in vitro mineralization. Biomacromolecules 7, 3178, 2006
173. Chirila, T.V., Zainuddin, Hill, D.J., Whittaker, A.K., and Kemp, A. Effect of phosphate functional groups on the calcification capacity of acrylic hydrogels. Acta Biomater 3, 95, 2007
174. Kim, C.W., Kim, S.E., Kim, Y.W., Lee, H.J., Choi, H.W., Chang, J.H., Choi, J., Kim, K.J., Shim, K.B., Jeong, Y.K., and Lee, S.C. Fabrication of hybrid composites based on biomineralization of phosphorylated poly(ethylene glycol) hydrogels. J Mater Res 24, 50, 2009
175. Song, J., Malathong, V., and Bertozzi, C.R. Mineralization of synthetic polymer scaffolds: A bottom-up approach for the development of artificial bone. J Am Chem Soc 127, 3366, 2005
176. Addison, W.N., Miller, S.J., Ramaswamy, J., Mansouri, A., Kohn, D.H., and McKee, M.D. Phosphorylation-dependent mineral-Type specificity for apatite-binding peptide sequences. Biomaterials 31, 9422, 2010
177. Sailaja, G.S., Ramesh, P., and Varma, H.K. Ultrastructural evaluation of in vitro mineralized calcium phosphate phase on surface phosphorylated poly(hydroxy ethyl methacrylate-co-methyl methacrylate). J Mater Sci Mater Med 21, 1183, 2010
178. Gu, L.S., Kim, J., Kim, Y.K., Liu, Y., Dickens, S.H., Pashley, D.H., Ling, J.Q., and Tay, F.R. A chemical phosphorylationinspired design for type I collagen biomimetic remineralization. Dent Mater 26, 1077, 2010
179. Gu, L.S., Kim, Y.K., Liu, Y., Takahashi, K., Arun, S., Wimmer, C.E., Osorio, R., Ling, J.Q., Looney, S.W., Pashley, D.H., and Tay, F.R. Immobilization of a phosphonated analog of matrix phosphoproteins within crosslinked collagen as a templating mechanism for biomimetic mineralization. Acta Biomater 7, 268, 2011
180. Ferna'ndez, D., Vega, D., and Goeta, A. The calcium-binding properties of pamidronate, a bone-resorption inhibitor. Acta Crystallogr C 58, m494, 2002
181. Ferna'ndez, D., Vega, D., and Goeta, A. Alendronate zwitterions bind to calcium cations arranged in columns. Acta Crystallogr C 59, m543, 2003
182. Yang, X., Akhtar, S., Rubino, S., Leifer, K., Hilborn, J., and Ossipov, D. Direct ''click'' synthesis of hybrid bisphosphonate-hyaluronic acid hydrogel in aqueous solution for biomineralization. Chem Mater 24, 1690, 2012
183. Radeva, T., and Petkanchin, I.I. Electric properties and conformation of polyethylenimine at the hematite-Aqueous solution interface. J Colloid Interface Sci 196, 87, 1997
184. Me'sza'ros, R., Thompson, L., Bos, M., and de Groot, P. Adsorption and electrokinetic properties of polyethylenimine on silica surfaces. Langmuir 18, 6164, 2002
185. Zhang, S., Wright, J.E., özber, N., and Uludaǧ, H. The interaction of cationic polymers and their bisphosphonate derivatives with hydroxyapatite. Macromol Biosci 7, 656, 2007
186. Wang, D., Miller, S., Sima, M., Kopečková, P., and Kopeček, J. Synthesis and evaluation of water-soluble polymeric bone-Targeted drug delivery systems. Bioconjug Chem 14, 853, 2003
187. Wang, D., Miller, S.C., Kopečková, P., and Kopeček, J. Bone-Targeting macromolecular therapeutics. Adv Drug Deliv Rev 57, 1049, 2005
188. Wang, G., Kucharski, C., Lin, X., and Uludaǧ, H. Bisphosphonate-coated BSA nanoparticles lack bone targeting after systemic administration. J Drug Target 18, 611, 2010
189. Wang, G., Mostafa, N.Z., Incani, V., Kucharski, C., and Uludaǧ, H. Bisphosphonate-decorated lipid nanoparticles designed as drug carriers for bone diseases. J Biomed Mater Res A 100, 684, 2012
190. Boanini, E., Gazzano, M., Rubini, K., and Bigi, A. Composite nanocrystals provide new insight on alendronate interaction with hydroxyapatite structure. Adv Mater 19, 2499, 2007
191. Jung, A., Bisaz, S., and Fleisch, H. The binding of pyrophosphate and two diphosphonates by hydroxyapatite crystals. Calcif Tissue Res 11, 269, 1973
192. Rogers, M.J., Watts, D.J., and Russell, R.G. Overview of bisphosphonates. Cancer 80, 1652, 1997
193. Hutchens, S.A., Benson, R.S., Evans, B.R., O'Neill, H.M., and Rawn, C.J. Biomimetic synthesis of calcium-deficient hydroxyapatite in a natural hydrogel. Biomaterials 27, 4661, 2006
194. Kawai, T., Ohtsuki, C., Kamitakahara, M., Hosoya, K., Tanihara, M., Miyazaki, T., Sakaguchi, Y., and Konagaya, S. In vitro apatite formation on polyamide containing carboxyl groups modified with silanol groups. J Mater Sci Mater Med 18, 1037, 2007
195. Ryu, J., Ku, S.H., Lee, H., and Park, C.B. Mussel-inspired polydopamine coating as a universal route to hydroxyapatite crystallization. Adv Funct Mater 20, 2132, 2010
196. Douglas, T., Wlodarczyk, M., Pamula, E., Declercq, H., de Mulder, E., Bucko, M., Balcaen, L., Vanhaecke, F., Cornelissen, R., Dubruel, P., Jansen, J., and Leeuwenburgh, S. Enzymatic mineralization of gellan gum hydrogel for bone tissue-engineering applications and its enhancement by polydopamine. J Tissue Eng Regen Med 2012 [Epub ahead of print]; DOI: 10.1002/term.1616
197. Chang, M.C. Modification of hydroxyapatite/gelatin nanocomposite with the addition of chondroitin sulfate. J Korean Ceram Soc 45, 573, 2008