Biomineralized hydroxyapatite nanoclay composite scaffolds with polycaprolactone for stem cell-based bone tissue engineering

Journal of Biomedical Materials Research - Part A

Volumn 103, Issue 6, 2015, Pages 2077-2101

  Ambre, Avinash H ^a   Katti, Dinesh R ^a   Katti, Kalpana S ^a  

^a North Dakota State University   (United States)

Author keywords

biomineralization; bone tissue engineering; hydroxyapatite composite; mesenchymal stem cell; nanoclay

Indexed keywords

AMINO ACIDS; BIOLOGICAL MATERIALS; BIOMINERALIZATION; BONE; CELL CULTURE; CELL ENGINEERING; CELLS; CYTOLOGY; FLOWCHARTING; HYDROXYAPATITE; MOBILE SECURITY; NANOCOMPOSITES; NANOSTRUCTURED MATERIALS; POLYCAPROLACTONE; STEM CELLS; TISSUE; TISSUE ENGINEERING;

BONE TISSUE ENGINEERING; HIERARCHICAL ORGANIZATIONS; HUMAN MESENCHYMAL STEM CELLS (HMSCS); HYDROXYAPATITE COMPOSITE; MESENCHYMAL STEM CELL; NANO CLAYS; NANOMECHANICAL PROPERTY; OSTEOGENIC SUPPLEMENTS;

SCAFFOLDS (BIOLOGY);

ALKALINE PHOSPHATASE; HYDROXYAPATITE; MOLECULAR SCAFFOLD; NANOCLAY COMPOSITE; NANOCOMPOSITE; NANOFILM; POLYCAPROLACTONE; UNCLASSIFIED DRUG; ALUMINUM SILICATE; CLAY; NANOPARTICLE; POLYESTER;

ARTICLE; ATOMIC FORCE MICROSCOPY; BIODEGRADATION; BIOMINERALIZATION; BONE REGENERATION; BONE TISSUE; CELL ADHESION; CELL DIFFERENTIATION; CELL VIABILITY; CLAY; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFRARED SPECTROSCOPY; MATERIALS TESTING; MESENCHYMAL STEM CELL; MOLECULAR MECHANICS; MORPHOLOGY; MTT ASSAY; NANOFABRICATION; OSSIFICATION; PHASE CONTRAST MICROSCOPY; POROSITY; SCANNING ELECTRON MICROSCOPY; TISSUE ENGINEERING; YOUNG MODULUS; BONE; BONE MINERALIZATION; CELL CULTURE; CELL SURVIVAL; CHEMISTRY; COMPRESSIVE STRENGTH; CYTOLOGY; DRUG EFFECTS; MESENCHYMAL STROMA CELL; METABOLISM; PHYSIOLOGY; PROCEDURES; STAINING; TISSUE SCAFFOLD; ULTRASTRUCTURE;

ALKALINE PHOSPHATASE; ALUMINUM SILICATES; BONE AND BONES; CALCIFICATION, PHYSIOLOGIC; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; COMPRESSIVE STRENGTH; DURAPATITE; EXTRACELLULAR MATRIX; HUMANS; MESENCHYMAL STROMAL CELLS; NANOPARTICLES; POLYESTERS; POROSITY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; STAINING AND LABELING; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84928542882     PISSN: 15493296     EISSN: 15524965     Source Type: Journal    
DOI: 10.1002/jbm.a.35342     Document Type: Article

References (119)

1. Langer R, Vacanti JP,. Tissue engineering. Science 1993; 260: 920-926.
2. Murugan R, Ramakrishna S,. Development of nanocomposites for bone grafting. Compos Sci Technol 2005; 65: 2385-2406.
3. Zhou H, Lee J,. Nanoscale hydroxyapatite particles for bone tissue engineering. Acta Biomaterialia 2011; 7: 2769-2781.
4. Bose S, Tarafder S,. Calcium phosphate ceramic systems in growth factor and drug delivery for bone tissue engineering: A review. Acta Biomaterialia 2012; 8: 1401-1421.
5. Vallet-Regi M,. Ceramics for medical applications. J Chem Soc Dalton Transact 2001; 2: 97-108.
6. LeGeros RZ,. Calcium phosphate-based osteoinductive materials. Chem Rev 2008; 108: 4742-4753.
7. Chai YC, Carlier A, Bolander J, Roberts SJ, Geris L, Schrooten J, Van Oosterwyck H, Luyten FP,. Current views on calcium phosphate osteogenicity and the translation into effective bone regeneration strategies. Acta Biomaterialia 2012; 8: 3876-3887.
8. Chan CK, Kumar TSS, Liao S, Murugan R, Ngiam M, Ramakrishman S,. Biomimetic nanocomposites for bone graft applications. Nanomedicine 2006; 1: 177-188.
9. Patel N, Best SM, Bonfield W, Gibson IR, Hing KA, Damien E, Revell PA,. A comparative study on the in vivo behavior of hydroxyapatite and silicon substituted hydroxyapatite granules. J Mater Sci Mater Med 2002; 13: 1199-1206.
10. Thian ES, Huang J, Best SM, Barber ZH, Brooks RA, Rushton N, Bonfield W,. The response of osteoblasts to nanocrystalline silicon-substituted hydroxyapatite thin films. Biomaterials 2006; 27: 2692-2698.
11. Botelho CM, Brooks RA, Best SM, Lopes MA, Santos JD, Rushton N, Bonfield W,. Human osteoblast response to silicon-substituted hydroxyapatite. J Biomed Mater Res Part A 2006; 79: 723-730.
12. Vallet-Regi M,. Revisiting ceramics for medical applications. Dalton Transact 2006: 5211-5220.
13. Roether JA, Gough JE, Boccaccini AR, Hench LL, Maquet V, Jérôme R,. Novel bioresorbable and bioactive composites based on bioactive glass and polylactide foams for bone tissue engineering. J Mater Sci Mater Med 2002; 13: 1207-1214.
14. Xynos ID, Edgar AJ, Buttery LDK, Hench LL, Polak JM,. Gene-expression profiling of human osteoblasts following treatment with the ionic products of Bioglass® 45S5 dissolution. J Biomed Mater Res 2001; 55: 151-157.
15. Xynos I, Edgar A, Buttery L, Hench L, Polak J,. Ionic products of bioactive glass dissolution increase proliferation of human osteoblasts and induce insulin-like growth factor II mRNA expression and protein synthesis. Biochem Biophys Res Commun 2000; 276: 461-465.
16. Han P, Wu C, Xiao Y,. The effect of silicate ions on proliferation, osteogenic differentiation and cell signalling pathways (WNT and SHH) of bone marrow stromal cells. Biomater Sci 2013; 1: 379-392.
17. Giannelis EP,. Polymer layered silicate nanocomposites. Adv Mater 1996; 8: 29-35.
18. Sinha Ray S, Okamoto M,. Polymer/layered silicate nanocomposites: A review from preparation to processing. Prog Polym Sci 2003; 28: 1539-1641.
19. Depan D, Kumar AP, Singh RP,. Cell proliferation and controlled drug release studies of nanohybrids based on chitosan-g-lactic acid and montmorillonite. Acta Biomaterialia 2009; 5: 93-100.
20. Katti KS, Katti DR, Dash R,. Synthesis and characterization of a novel chitosan/montmorillonite/hydroxyapatite nanocomposite for bone tissue engineering. Biomed Mater 2008; 3: 12.
21. Mieszawska AJ, Llamas JG, Vaiana CA, Kadakia MP, Naik RR, Kaplan DL,. Clay enriched silk biomaterials for bone formation. Acta Biomaterialia 2011; 7: 3036-3041.
22. Ambre AH, Katti DR, Katti KS,. Nanoclays mediate stem cell differentiation and mineralized ECM formation on biopolymer scaffolds. J Biomed Mater Res Part A 2013; 101: 2644-2660.
23. Gaharwar AK, Mihaila SM, Swami A, Patel A, Sant S, Reis RL, Marques AP, Gomes ME, Khademhosseini A,. Bioactive silicate nanoplatelets for osteogenic differentiation of human mesenchymal stem cells. Adv Mater 2013; 25: 3329-3336.
24. Goldberg M, Langer R, Jia XQ,. Nanostructured materials for applications in drug delivery and tissue engineering. J Biomater Sci-Polym Ed 2007; 18: 241-268.
25. Christenson EM, Anseth KS, van den Beucken L, Chan CK, Ercan B, Jansen JA, Laurencin CT, Li WJ, Murugan R, Nair LS, Ramakrishna S, Tuan RS, Webster TJ, Mikos AG., Nanobiomaterial applications in orthopedics. J Orthopaedic Res 2007; 25: 11-22.
26. Stevens MM, George JH,. Exploring and engineering the cell surface interface. Science 2005; 310: 1135-1138.
27. Okada A, Kawasumi M, Usuki A, Kojima Y, Kurauchi T, Kamigaito O,. Synthesis and properties of nylon-6/clay hybrids. In: Schaefer DW, Mark JE, editors. Polymer Based Molecular Composites. MRS SymposiumProceedings 1990; 171: 45-50.
28. Chen GX, Hao GJ, Guo TY, Song MD, Zhang BH,. Structure and mechanical properties of poly(3-hydroxybutyrateco-3-hydroxyvalerate) (PHBV)/clay nanocomposites. J Mater Sci Lett 2002; 21: 1587-1589.
29. Pramanik M, Srivastava SK, Samantaray BK, Bhowmick AK,. Rubber-clay nanocomposite by solution blending. J Appl Polym Sci 2003; 87: 2216-2220.
30. Messersmith PB, Giannelis EP,. Synthesis and barrier properties of poly(ε-caprolactone)-layered silicate nanocomposites. J Polym Sci Part A: Polym Chem 1995; 33: 1047-1057.
31. Yano K, Usuki A, Okada A, Kurauchi T, Kamigaito O,. Synthesis and properties of polyimide-clay hybrid. J Polym Sci Part A: Polym Chem 1993; 31: 2493-2498.
32. Bharadwaj RK,. Modeling the barrier properties of polymer-layered silicate nanocomposites. Macromolecules 2001; 34: 9189-9192.
33. Gilman JW,. Flammability and thermal stability studies of polymer layered-silicate (clay) nanocomposites. Appl Clay Sci 1999; 15: 31-49.
34. Gilman JW, Jackson CL, Morgan ABRH,. Flammability properties of polymer-layered-silicate nanocomposites. Polypropylene and polystyrene nanocomposites. Chem Mater 2000; 12: 1866-1873.
35. Sikdar D, Pradhan SM, Katti DR, Katti KS, Mohanty B,. Altered phase model for polymer clay nanocomposites. Langmuir 2008; 24: 5599-5607.
36. Sikdar D, Katti DR, Katti KS,. The role of interfacial interactions on the crystallinity and nanomechanical properties of clay-polymer nanocomposites: A molecular dynamics study. J Appl Polym Sci 2008; 107: 3137-3148.
37. Sikdar D, Katti D, Katti K, Mohanty, Bedabibhas. Influence of backbone chain length and functional groups of organic modifiers on crystallinity and nanomechanical properties of intercalated clay-polycaprolactam nanocomposites. Int J Nanotechnol 2009; 6: 468-492.
38. Carretero MI,. Clay minerals and their beneficial effects upon human health. A review. Appl Clay Sci 2002; 21: 155-163.
39. Viseras C, Aguzzi C, Cerezo P, Lopez-Galindo A,. Uses of clay minerals in semisolid health care and therapeutic products. Appl Clay Sci 2007; 36: 37-50.
40. Forni F, Iannuccelli V, Coppi G, Bernabei MT,. Effect of montmorillonite on drug release from polymeric matrices. Archiv der Pharmazie 1989; 322: 789-793.
41. Wen-Fu Lee, Yao-Tsung Fu,. Effect of montmorillonite on the swelling behavior and drug-release behavior of nanocomposite hydrogels. J Appl Polym Sci 2003; 89: 3652-3660.
42. Lin F-H, Chen C-H, Cheng WTK, Kuo T-F,. Modified montmorillonite as vector for gene delivery. Biomaterials 2006; 27: 3333-3338.
43. Takahashi T, Yamada Y, Kataoka K, Nagasaki Y,. Preparation of a novel PEG-clay hybrid as a DDS material: Dispersion stability and sustained release profiles. J Control Release 2005; 107: 408-416.
44. Wang X, Du Y, Luo J., Biopolymer/montmorillonite nanocomposite: Preparation, drug-controlled release property and cytotoxicity. Nanotechnology 2008; 19: 065707.
45. Sun B, Ranganathan B, Feng S-S,. Multifunctional poly(d,l-lactide-co-glycolide)/montmorillonite (PLGA/MMT) nanoparticles decorated by Trastuzumab for targeted chemotherapy of breast cancer. Biomaterials 2008; 29: 475-486.
46. Lin K-F, Hsu C-Y, Huang T-S, Chiu W-Y, Lee Y-H, Young T-H,. A novel method to prepare chitosan/montmorillonite nanocomposites. J Appl Polym Sci 2005; 98: 2042-2047.
47. Marras SI, Kladi KP, Tsivintzelis I, Zuburtikudis I, Panayiotou C,. Biodegradable polymer nanocomposites: The role of nanoclays on the thermomechanical characteristics and the electrospun fibrous structure. Acta Biomaterialia 2008; 4: 756-765.
48. Zheng JP, Wang CZ, Wang XX, Wang HY, Zhuang H, Yao KD,. Preparation of biomimetic three-dimensional gelatin/montmorillonite-chitosan scaffold for tissue engineering. React Funct Polym 2007; 67: 780-788.
49. Woodruff MA, Hutmacher DW,. The return of a forgotten polymer-Polycaprolactone in the 21st century. Prog Polym Sci 2010; 35: 1217-1256.
50. Shi Y, Hu G, Su J, Li W, Chen Q, Shou P, Xu C, Chen X, Huang Y, Zhu Z, Huang X, Han X, Xie N, Ren G., Mesenchymal stem cells: A new strategy for immunosuppression and tissue repair. Cell Res 2010; 20: 510-518.
51. Chen F, Tuan R,. Mesenchymal stem cells in arthritic diseases. Arthritis Res Therapy 2008; 10: 223.
52. Uccelli A, Pistoia V, Moretta L,. Mesenchymal stem cells: A new strategy for immunosuppression? Trends Immunol 2007; 28: 219-226.
53. Otto W, Wright N,. Mesenchymal stem cells: From experiment to clinic. Fibrogenesis Tissue Repair 2011; 4: 20.
54. Han Z, Jing Y, Zhang S, Liu Y, Shi Y, Wei L,. The role of immunosuppression of mesenchymal stem cells in tissue repair and tumor growth. Cell Biosci 2012; 2: 8.
55. Abumaree M, Jumah M, Pace R, Kalionis B,. Immunosuppressive properties of mesenchymal stem cells. Stem Cell Revi Rep 2012; 8: 375-392.
56. Ghannam S, Bouffi C, Djouad F, Jorgensen C, Noel D,. Immunosuppression by mesenchymal stem cells: mechanisms and clinical applications. Stem Cell Res Therapy 2010; 1: 2.
57. Maxson S, Lopez EA, Yoo D, Danilkovitch-Miagkova A, LeRoux MA,. Concise review: Role of mesenchymal stem cells in wound repair. Stem Cells Translational Med 2012; 1: 142-149.
58. Crha M, Necas A, Srnec R, Janovec J, Stehlik L, Rauser P, Urbanova L, Planka L, Jancar J, Amler E,. Mesenchymal stem cells in bone tissue regeneration and application to bone healing. Acta Veterinaria Brno 2009; 78: 635-642.
59. Katti KS, Ambre AH, Peterka N, Katti DR,. Use of unnatural amino acids for design of novel organomodified clays as components of nanocomposite biomaterials. Phil Transact Roy Soc A 2010; 368: 1963-1980.
60. Katti DR, Ghosh P, Schmidt S, Katti KS,. Mechanical properties of the sodium montmorillonite interlayer intercalated with amino acids. Biomacromolecules 2005; 6: 3276-3282.
61. Ambre AH, Katti KS, Katti DR,. Nanoclay based composite scaffolds for bone tissue engineering applications. J Nanotechnol Eng Med 2010; 1: 031013-9.
62. Ambre A, Katti KS, Katti DR,. In situ mineralized hydroxyapatite on amino acid modified nanoclays as novel bone biomaterials. Mater Sci Eng C 2011; 31: 1017-1029.
63. Verma D, Katti KS, Katti DR., Osteoblast adhesion, proliferation and growth on polyelectrolyte complex-hydroxyapatite nanocomposites. Phil Transact Roy Soc A Mathematical Phys Eng Sci 2010; 368: 2083.
64. Khanna R, Katti KS, Katti DR,. Bone nodules on chitosan-polygalacturonic acid-hydroxyapatite nanocomposite films mimic hierarchy of natural bone. Acta Biomaterialia 2011; 7: 1173-1183.
65. Mikos AG, Lyman MD, Freed LE, Langer R,. Wetting of poly(l-lactic acid) and poly(dl-lactic-co-glycolic acid) foams for tissue culture. Biomaterials 1994; 15: 55-58.
66. Mikos AG, Sarakinos G, Lyman MD, Ingber DE, Vacanti JP, Langer R,. Prevascularization of porous biodegradable polymers. Biotechnol Bioeng 1993; 42: 716-723.
67. Chong EJ, Phan TT, Lim IJ, Zhang YZ, Bay BH, Ramakrishna S, Lim CT,. Evaluation of electrospun PCL/gelatin nanofibrous scaffold for wound healing and layered dermal reconstitution. Acta Biomaterialia 2007; 3: 321-330.
68. Xu CY, Inai R, Kotaki M, Ramakrishna S,. Aligned biodegradable nanofibrous structure: A potential scaffold for blood vessel engineering. Biomaterials 2004; 25: 877-886.
69. Plaisant M, Giorgetti-Peraldi S, Gabrielson M, Loubat A, Dani C, Peraldi P,. Inhibition of hedgehog signaling decreases proliferation and clonogenicity of human mesenchymal stem cells. PLoS One 2011; 6: e16798.
70. Oliver WC, Pharr GM,. An improved technique for determining hardness and elastic modulus using load and displacement. J Mater Res 1992; 7: 1664-1683.
71. Hassenkam T, Fantner GE, Cutroni JA, Weaver JC, Morse DE, Hansma PK,. High-resolution AFM imaging of intact and fractured trabecular bone. Bone 2004; 35: 4-10.
72. Woodward SC, Brewer PS, Moatamed F, Schindler A, Pitt CG,. The intracellular degradation of poly(ε-caprolactone). J Biomed Mater Res 1985; 19: 437-444.
73. Raghavan D, Egwim K,. Degradation of polyester film in alkali solution. J Appl Polym Sci 2000; 78: 2454-2463.
74. Htay AS, Teoh SH, Hutmacher DW,. Development of perforated microthin poly(ε-caprolactone) films as matrices for membrane tissue engineering. J Biomater Sci Polym Ed 2004; 15: 683-700.
75. Karageorgiou V, Kaplan D,. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 2005; 26: 5474-5491.
76. Simon JL, Roy TD, Parsons JR, Rekow ED, Thompson VP, Kemnitzer J, Ricci JL,. Engineered cellular response to scaffold architecture in a rabbit trephine defect. J Biomed Mater Res Part A 2003; 66: 275-282.
77. Scaglione S, Giannoni P, Bianchini P, Sandri M, Marotta R, Firpo G, Valbusa U, Tampieri A, Diaspro A, Bianco P, Quarto R., Order versus disorder: In vivo bone formation within osteoconductive scaffolds. Sci Rep 2012; 2.
78. Graziano A, d'Aquino R, Cusella-De Angelis MG, Laino G, Piattelli A, Pacifici M, De Rosa A, Papaccio G,. Concave pit-containing scaffold surfaces improve stem cell-derived osteoblast performance and lead to significant bone tissue formation. PLoS One 2007; 2: e496.
79. Yuan H, Kurashina K, de Bruijn JD, Li Y, de Groot K, Zhang X,. A preliminary study on osteoinduction of two kinds of calcium phosphate ceramics. Biomaterials 1999; 20: 1799-1806.
80. Zhang Q, Luo H, Zhang Y, Zhou Y, Ye Z, Tan W, Lang M,. Fabrication of three-dimensional poly(ε-caprolactone) scaffolds with hierarchical pore structures for tissue engineering. Mater Sci Eng C 2013; 33: 2094-2103.
81. Phadke A, Hwang Y, Kim SH, Kim SH, Yamaguchi T, Masuda K, Varghese S,. Effect of scaffold microarchitecture on osteogenic differentiation of human mesenchymal stem cells. Eur Cells Mater 2013; 25: 114-129.
82. Uebersax L, Hagenmuller H, Hofmann S, Gruenblatt E, Muller R, Vunjaknovakovic G, Kaplan D, Merkle HP, Meinel L,. Effect of scaffold design on bone morphology in vitro. Tissue Eng 2006; 12: 3417-3429.
83. Kim K, Yeatts A, Dean D, Fisher JP,. Stereolithographic bone scaffold design parameters: Osteogenic differentiation and signal expression. Tissue Eng Part B: Rev 2010; 16: 523-529.
84. Van Bael S, Chai YC, Truscello S, Moesen M, Kerckhofs G, Van Oosterwyck H, Kruth JP, Schrooten J,. The effect of pore geometry on the in vitro biological behavior of human periosteum-derived cells seeded on selective laser-melted Ti6Al4V bone scaffolds. Acta Biomaterialia 2012; 8: 2824-2834.
85. Ratner B,. Replacing and renewing: Synthetic materials, biomimetics, and tissue engineering in implant dentistry. J Dental Educ 2001; 65: 1340-1347.
86. Anderson JM, Rodriguez A, Chang DT,. Foreign body reaction to biomaterials. Seminars Immunol 2008; 20: 86-100.
87. Brown BN, Ratner BD, Goodman SB, Amar S, Badylak SF,. Macrophage polarization: An opportunity for improved outcomes in biomaterials and regenerative medicine. Biomaterials 2012; 33: 3792-3802.
88. Bryers JD, Giachelli CM, Ratner BD,. Engineering biomaterials to integrate and heal: The biocompatibility paradigm shifts. Biotechnol Bioeng 2012; 109: 1898-1911.
89. Garg K, Pullen NA, Oskeritzian CA, Ryan JJ, Bowlin GL,. Macrophage functional polarization (M1/M2) in response to varying fiber and pore dimensions of electrospun scaffolds. Biomaterials 2013; 34: 4439-4451.
90. Madden LR, Mortisen DJ, Sussman EM, Dupras SK, Fugate JA, Cuy JL, Hauch KD, Laflamme MA, Murry CE, Ratner BD,. Proangiogenic scaffolds as functional templates for cardiac tissue engineering. Proc Natl Acad Sciences 2010; 107: 15211-15216.
91. Bota PCS, Collie AMB, Puolakkainen P, Vernon RB, Sage EH, Ratner BD, Stayton PS,. Biomaterial topography alters healing in vivo and monocyte/macrophage activation in vitro. J Biomed Mater Res Part A 2010; 95: 649-657.
92. Tsuruga E, Takita H, Itoh H, Wakisaka Y, Kuboki Y,. Pore size of porous hydroxyapatite as the cell-substratum controls BMP-induced osteogenesis. J Biochem 1997; 121: 317-324.
93. Murphy CM, Haugh MG, O'Brien FJ,. The effect of mean pore size on cell attachment, proliferation and migration in collagen-glycosaminoglycan scaffolds for bone tissue engineering. Biomaterials 2010; 31: 461-466.
94. Tang G, Zhang H, Zhao Y, Zhang Y, Li X, Yuan X,. Preparation of PLGA scaffolds with graded pores by using a gelatin-microsphere template as porogen. J Biomater Sci Polym Ed 2012; 23: 2241-2257.
95. Wuchter P, Boda-Heggemann J, Straub B, Grund C, Kuhn C, Krause U, Seckinger A, Peitsch W, Spring H, Ho A, Franke W., Processus and recessus adhaerentes: Giant adherens cell junction systems connect and attract human mesenchymal stem cells. Cell Tissue Res 2007; 328: 499-514.
96. Anderson HC,. Molecular biology of matrix vesicles. Clinical orthopaedics and related research 1995; 314: 266-280.
97. Boonrungsiman S, Gentleman E, Carzaniga R, Evans ND, McComb DW, Porter AE, Stevens MM,. The role of intracellular calcium phosphate in osteoblast-mediated bone apatite formation. Proc Natl Acad Sci 2012.
98. Bruder SP, Caplan AI,. Cellular and molecular events during embryonic bone development. Connective Tissue Res 1989; 20: 65-71.
99. Khanna R, Katti K, Katti D,. Nanomechanics of surface modified nanohydroxyapatite particulates used in biomaterials. J Eng Mech 2009; 135: 468-478.
100. Discher DE, Janmey P, Wang Y-L,. Tissue cells feel and respond to the stiffness of their substrate. Science 2005; 310: 1139-1143.
101. Buxboim A, Ivanovska IL, Discher DE,. Matrix elasticity, cytoskeletal forces and physics of the nucleus: how deeply do cells 'feel' outside and in? J Cell Sci 2010; 123: 297-308.
102. Bellows CG, Aubin JE, Heersche JNM,. Initiation and progression of mineralization of bone nodules formed in vitro: The role of alkaline phosphatase and organic phosphate. Bone Mineral 1991; 14: 27-40.
103. Dorozhkin SV,. Calcium orthophosphates. J Mater Sci 2007; 42: 1061-1095.
104. Genge BR, Sauer GR, Wu LN, McLean FM, Wuthier RE,. Correlation between loss of alkaline phosphatase activity and accumulation of calcium during matrix vesicle-mediated mineralization. J Biol Chem 1988; 263: 18513-18519.
105. Malaval L, Liu F, Roche P, Aubin JE,. Kinetics of osteoprogenitor proliferation and osteoblast differentiation in vitro. J Cell Biochem 1999; 74: 616-627.
106. Turksen K, Aubin JE,. Positive and negative immunoselection for enrichment of two classes of osteoprogenitor cells. J Cell Biol 1991; 114: 373-384.
107. Hauschka PV, Lian JB, Cole DE, Gundberg CM,. Osteocalcin and matrix Gla protein: Vitamin K-dependent proteins in bone. Physiol Rev 1989; 69: 990-1047.
108. Kim E-K, Lim S, Park J-M, Seo JK, Kim JH, Kim KT, Ryu SH, Suh P-G,. Human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by AMP-activated protein kinase. J Cell Physiol 2012; 227: 1680-1687.
109. Fang M, Holl MMB,. Variation in type I collagen nanomorphology: The significance and origin. BoneKEy Reports Volume 2: International Bone and Mineral Society; 2013.
110. Curtis A, Wilkinson C,. Topographical control of cells. Biomaterials 1997; 18: 1573-1583.
111. Chen W, Villa-Diaz LG, Sun Y, Weng S, Kim JK, Lam RHW, Han L, Fan R, Krebsbach PH, Fu J,. Nanotopography influences adhesion, spreading, and self-renewal of human embryonic stem cells. ACS Nano 2012; 6: 4094-4103.
112. Meyle J, Gültig K, Brich M, Hämmerle H, Nisch W,. Contact guidance of fibroblasts on biomaterial surfaces. J Mater Sci Mater Med 1994; 5: 463-466.
113. Chen S, Jones JA, Xu Y, Low H-Y, Anderson JM, Leong KW,. Characterization of topographical effects on macrophage behavior in a foreign body response model. Biomaterials 2010; 31: 3479-3491.
114. Wang T, Wang H, Li H, Gan Z, Yan S,. Banded spherulitic structures of poly(ethylene adipate), poly(butylene succinate) and in their blends. Phys Chem Chem Phys 2009; 11: 1619-1627.
115. Yang P, Han Y,. Crystal growth transition from flat-on to edge-on induced by solvent evaporation in ultrathin films of polystyrene-b-poly(ethylene oxide). Langmuir 2009; 25: 9960-9968.
116. Sikdar D, Katti D, Katti K, Mohanty B,. Effect of organic modifiers on dynamic and static nanomechanical properties and crystallinity of intercalated clay-polycaprolactam nanocomposites. J Appl Polym Sci 2007; 105: 790-802.
117. Lam CXF, Savalani MM, Teoh S, Hutmacher DW., Dynamics of in vitro polymer degradation of polycaprolactone-based scaffolds: Accelerated versus simulated physiological conditions. Biomed Mater 2008; 3: 034108.
118. Coleman MM, Zarian J,. Fourier-transform infrared studies of polymer blends. II. Poly(ε-caprolactone)-poly(vinyl chloride) system. J Polym Sci Polym Phys Ed 1979; 17: 837-850.
119. Gibson LJ, Ashby MF,. Cellular Solids: Structure and Properties. New York: Cambridge University Press; 1999.