Osteoblastic differentiation and potent osteogenicity of three-dimensional hBMSC-BCP particle constructs

Journal of Tissue Engineering and Regenerative Medicine

Volumn 8, Issue 5, 2014, Pages 364-376

  Cordonnier, Thomas ^a,c   Langonné, Alain ^b,c   Corre, Pierre ^a,d   Renaud, Audrey ^a   Sensebé, Luc ^b,c   Rosset, Philippe ^c   Layrolle, Pierre ^a   Sohier, Jérôme ^a  

^a UNIVERSITÉ DE NANTES   (France)

^b ETABLISSEMENT FRANÇAIS DU SANG   (France)

^c UNIVERSITÉ DE TOURS   (France)

^d HÔTEL DIEU   (France)

Author keywords

Biphasic calcium phosphate; Bone tissue engineering; Glass beads; Human bone marrow stromal cells; Osteoblastic differentiation; Osteogenicity in nude mice; Three dimensional constructs

Indexed keywords

CALCIUM PHOSPHATE; CELL ENGINEERING; CELL PROLIFERATION; DEGREES OF FREEDOM (MECHANICS); GLASS; GRANULAR MATERIALS; MAMMALS; SCAFFOLDS (BIOLOGY);

BIPHASIC CALCIUM PHOSPHATES; BONE TISSUE ENGINEERING; GLASS BEAD; HUMAN BONE MARROW STROMAL CELLS; IN-VITRO; NUDE MICE; OSTEOBLASTIC DIFFERENTIATION; OSTEOGENICITY; OSTEOGENICITY IN NUDE MOUSE; THREE DIMENSIONAL CONSTRUCT;

BONE;

BONE MORPHOGENETIC PROTEIN 2; BROMSULFOPHTHALEIN; CALCIUM PHOSPHATE; TRANSCRIPTION FACTOR RUNX2; HYDROXYAPATITE; HYDROXYAPATITE-BETA TRICALCIUM PHOSPHATE; MESSENGER RNA; MICROSPHERE;

ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INFRARED SPECTROSCOPY; MONONUCLEAR CELL; OSSIFICATION; OSTEOBLAST; OSTEOPROGENITOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; STROMA CELL; TISSUE ENGINEERING; UPREGULATION; X RAY DIFFRACTION; AGED; ANIMAL; BONE DEVELOPMENT; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; FEMALE; GENETICS; IMPLANT; MALE; MESENCHYMAL STROMA CELL; METABOLISM; MIDDLE AGED; MOUSE; NUDE MOUSE; TISSUE SCAFFOLD; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; FEMALE; HUMANS; HYDROXYAPATITES; IMPLANTS, EXPERIMENTAL; MALE; MESENCHYMAL STROMAL CELLS; MICE; MICE, NUDE; MICROSPHERES; MIDDLE AGED; OSTEOBLASTS; OSTEOGENESIS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; TISSUE SCAFFOLDS;

EID: 84898473285     PISSN: 19326254     EISSN: 19327005     Source Type: Journal    
DOI: 10.1002/term.1529     Document Type: Article

References (62)

1. Arinzeh TL, Tran T, McAlary J, et al. 2005; A comparative study of biphasic calcium phosphate ceramics for human mesenchymal stem cell-induced bone formation. Biomaterials 26(17): 3631-3638.
2. Borden M, El-Amin SF, Attawia M, et al. 2003; Structural and human cellular assessment of a novel microsphere-based tissue engineered scaffold for bone repair. Biomaterials 24(4): 597-609.
3. Brown KL, Cruess RL. 1982; Bone and cartilage transplantation in orthopaedic surgery. A review. J Bone Joint Surg Am 64(2): 270-279.
4. Bruder SP, Jaiswal N, Ricalton NS, et al. 1998; Mesenchymal stem cells in osteobiology and applied bone regeneration. Clin Orthop Relat Res 355(suppl): S247-256.
5. Burchardt H. 1987; Biology of bone transplantation. Orthop Clin North Am 18(2): 187-196.
6. Chen D, Harris MA, Rossini G, et al. 1997; Bone morphogenetic protein 2 (BMP-2) enhances BMP-3, BMP-4, and bone cell differentiation marker gene expression during the induction of mineralized bone matrix formation in cultures of fetal rat calvarial osteoblasts. Calcif Tissue Int 60(3): 283-290.
7. Clarke B. 2008; Normal bone anatomy and physiology. Clin J Am Soc Nephrol 3(suppl 3): S131-139.
8. Cool SM, Nurcombe V. 2005; Substrate induction of osteogenesis from marrow-derived mesenchymal precursors. Stem Cells Dev 14(6): 632-642.
9. Cordonnier T, Langonne A, Sohier J, et al. 2011; Consistent osteoblastic differentiation of human mesenchymal stem cells with bone morphogenetic protein 4 and low serum. Tissue Eng Part C Methods 17(3): 249-259.
10. Cordonnier T, Layrolle P, Gaillard J, et al. 2010; 3D environment on human mesenchymal stem cells differentiation for bone tissue engineering. J Mater Sci Mater Med 21(3): 981-987.
11. Daculsi G, LeGeros RZ, Heughebaert M, et al. 1990; Formation of carbonate-apatite crystals after implantation of calcium phosphate ceramics. Calcif Tissue Int 46(1): 20-27.
12. Daculsi G, LeGeros RZ, Nery E, et al. 1989; Transformation of biphasic calcium phosphate ceramics in vivo: ultrastructural and physicochemical characterization. J Biomed Mater Res 23(8): 883-894.
13. Damien CJ, Parsons JR. 1991; Bone graft and bone graft substitutes: a review of current technology and applications. J Appl Biomater 2(3): 187-208.
14. de Groot K. 1980; Bioceramics consisting of calcium phosphate salts. Biomaterials 1(1): 47-50.
15. Delorme B, Charbord P. 2007; Culture and characterization of human bone marrow mesenchymal stem cells. Methods Mol Med 140: 67-81.
16. Derubeis AR, Cancedda R. 2004; Bone marrow stromal cells (BMSCs) in bone engineering: limitations and recent advances. Ann Biomed Eng 32(1): 160-165.
17. Fellah BH, Weiss P, Gauthier O, et al. 2006; Bone repair using a new injectable self-crosslinkable bone substitute. J Orthop Res 24(4): 628-635.
18. Fischer EM, Layrolle P, van Blitterswijk CA, et al. 2003; Bone formation by mesenchymal progenitor cells cultured on dense and microporous hydroxyapatite particles. Tissue Eng 9(6): 1179-1188.
19. Friedenstein AJ, Gorskaja JF, Kulagina NN. 1976; Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 4(5): 267-274.
20. Habibovic P, de Groot K. 2007; Osteoinductive biomaterials - properties and relevance in bone repair. J Tissue Eng Regen Med 1(1): 25-32.
21. Helm GA, Dayoub H, Jane JA Jr. 2001; Bone graft substitutes for the promotion of spinal arthrodesis. Neurosurg Focus 10(4): E4.
22. Heughebaert M, LeGeros RZ, Gineste M, et al. 1988; Physicochemical characterization of deposits associated with HA ceramics implanted in nonosseous sites. J Biomed Mater Res 22(suppl 3): 257-268.
23. Hollinger JO, Battistone GC. 1986; Biodegradable bone repair materials. Synthetic polymers and ceramics. Clin Orthop Relat Res 207: 290-305.
24. Ito Y, Tanaka N, Fujimoto Y, et al. 2004; Bone formation using novel interconnected porous calcium hydroxyapatite ceramic hybridized with cultured marrow stromal stem cells derived from Green rat. J Biomed Mater Res A 69(3): 454-461.
25. Javed A, Afzal F, Bae JS, et al. 2009; Specific residues of RUNX2 are obligatory for formation of BMP2-induced RUNX2-SMAD complex to promote osteoblast differentiation. Cells Tissues Organs 189(1-4): 133-137.
26. Johnson KD, Frierson KE, Keller TS, et al. 1996; Porous ceramics as bone graft substitutes in long bone defects: a biomechanical, histological, and radiographic analysis. J Orthop Res 14(3): 351-369.
27. Jung GY, Park YJ, Han JS. 2010; Effects of HA released calcium ion on osteoblast differentiation. J Mater Sci Mater Med 21(5): 1649-1654.
28. Keselowsky BG, Collard DM, Garcia AJ, et al. 2004; Surface chemistry modulates focal adhesion composition and signaling through changes in integrin binding. Biomaterials 25(28): 5947-5954.
29. Keselowsky BG, Collard DM, Garcia AJ. 2005; Integrin binding specificity regulates biomaterial surface chemistry effects on cell differentiation. Proc Natl Acad Sci USA 102(17): 5953-5957.
30. Klein C, de Groot K, Chen W, et al. 1994; Osseous substance formation induced in porous calcium phosphate ceramics in soft tissues. Biomaterials 15(1): 31-34.
31. Krebsbach PH, Kuznetsov SA, Satomura K, et al. 1997; Bone formation in vivo: comparison of osteogenesis by transplanted mouse and human marrow stromal fibroblasts. Transplantation 63(8): 1059-1069.
32. Kuznetsov SA, Huang KE, Marshall GW, et al. 2008; Long-term stable canine mandibular augmentation using autologous bone marrow stromal cells and hydroxyapatite/tricalcium phosphate. Biomaterials 29(31): 4211-4216.
33. Langer R, Vacanti JP. 1993; Tissue engineering. Science 260(5110): 920-926.
34. LeGeros RZ. 2002; Properties of osteoconductive biomaterials: calcium phosphates. Clin Orthop Relat Res 395: 81-98.
35. Li Z, Zhou Z, Yellowley CE, et al. 1999; Inhibiting gap junctional intercellular communication alters expression of differentiation markers in osteoblastic cells. Bone 25(6): 661-666.
36. Liu G, Hu YY, Zhao JN, et al. 2004a; Effect of type I collagen on the adhesion, proliferation, and osteoblastic gene expression of bone marrow-derived mesenchymal stem cells. Chin J Traumatol 7(6): 358-362.
37. Liu Y, Hunziker EB, Layrolle P, et al. 2004b; Bone morphogenetic protein 2 incorporated into biomimetic coatings retains its biological activity. Tissue Eng 10(1-2): 101-108.
38. Liu Y, Layrolle P, de Bruijn J, et al. 2001; Biomimetic coprecipitation of calcium phosphate and bovine serum albumin on titanium alloy. J Biomed Mater Res 57(3): 327-335.
39. -ΔΔCt method. Methods 25(4): 402-408.
40. Mankani MH, Kuznetsov SA, Marshall GW, et al. 2008; Creation of new bone by the percutaneous injection of human bone marrow stromal cell and HA/TCP suspensions. Tissue Eng Part A 14(12): 1949-1958.
41. Nair MB, Suresh Babu S, Varma HK, et al. 2008; A triphasic ceramic-coated porous hydroxyapatite for tissue engineering application. Acta Biomater 4(1): 173-181.
42. Okamoto M, Dohi Y, Ohgushi H, et al. 2006; Influence of the porosity of hydroxyapatite ceramics on in vitro and in vivo bone formation by cultured rat bone marrow stromal cells. J Mater Sci Mater Med 17(4): 327-336.
43. Oklund SA, Prolo DJ, Gutierrez RV, et al. 1986; Quantitative comparisons of healing in cranial fresh autografts, frozen autografts and processed autografts, and allografts in canine skull defects. Clin Orthop Relat Res 205: 269-291.
44. Palomares KT, Gleason RE, Mason ZD, et al. 2009; Mechanical stimulation alters tissue differentiation and molecular expression during bone healing. J Orthop Res 27(9): 1123-1132.
45. Park SH, O'Connor K, McKellop H, et al. 1998; The influence of active shear or compressive motion on fracture-healing. J Bone Joint Surg Am 80(6): 868-878.
46. Petite H, Viateau V, Bensaid W, et al. 2000; Tissue-engineered bone regeneration. Nat Biotechnol 18(9): 959-963.
47. Pittenger MF, Mackay AM, Beck SC, et al. 1999; Multilineage potential of adult human mesenchymal stem cells. Science 284(5411): 143-147.
48. Prockop DJ. 1997; Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276(5309): 71-74.
49. Reed JS. 1995; Principles of Ceramics Processing, 2nd edn. Wiley Interscience: New York.
50. Ripamonti U. 1996; Osteoinduction in porous hydroxyapatite implanted in heterotopic sites of different animal models. Biomaterials 17(1): 31-35.
51. Rohanizadeh R, Padrines M, Bouler JM, et al. 1998; Apatite precipitation after incubation of biphasic calcium-phosphate ceramic in various solutions: influence of seed species and proteins. J Biomed Mater Res 42(4): 530-539.
52. Schiller PC, D'Ippolito G, Balkan W, et al. 2001; Gap-junctional communication is required for the maturation process of osteoblastic cells in culture. Bone 28(4): 362-369.
53. Shimazaki K, Mooney V. 1985; Comparative study of porous hydroxyapatite and tricalcium phosphate as bone substitute. J Orthop Res 3(3): 301-310.
54. Shirakawa K, Maeda S, Gotoh T, et al. 2006; CCAAT/enhancer-binding protein homologous protein (CHOP) regulates osteoblast differentiation. Mol Cell Biol 26(16): 6105-6116.
55. Sun H, Ye F, Wang J, et al. 2008; The upregulation of osteoblast marker genes in mesenchymal stem cells prove the osteoinductivity of hydroxyapatite/tricalcium phosphate biomaterial. Transpl Proc 40(8): 2645-2648.
56. Urist MR, Strates BS. 1970; Bone formation in implants of partially and wholly demineralized bone matrix. Including observations on acetone-fixed intra- and extracellular proteins. Clin Orthop Relat Res 71: 271-278.
57. Vaccaro AR. 2002; The role of the osteoconductive scaffold in synthetic bone graft. Orthopedics 25(suppl 5): s571-578.
58. Valarmathi MT, Yost MJ, Goodwin RL, et al. 2008; A three-dimensional tubular scaffold that modulates the osteogenic and vasculogenic differentiation of rat bone marrow stromal cells. Tissue Eng Part A 14(4): 491-504.
59. van der Lubbe HB, Klein CP, de Groot K. 1988; A simple method for preparing thin (10μm) histological sections of undecalcified plastic embedded bone with implants. Stain Technol 63(3): 171-176.
60. Yamasaki H, Sakai H. 1992; Osteogenic response to porous hydroxyapatite ceramics under the skin of dogs. Biomaterials 13(5): 308-312.
61. Yuan H, Zou P, Yang Z, et al. 1998; Bone morphogenetic protein and ceramic-induced osteogenesis. J Mater Sci Mater Med 9(12): 717-721.
62. Zannettino AC, Paton S, Itescu S, et al. 2010; Comparative assessment of the osteoconductive properties of different biomaterials in vivo seeded with human or ovine mesenchymal stem/stromal cells. Tissue Eng Part A 16(12): 3579-3587.