In vitro and in vivo evaluation of differentially demineralized cancellous bone scaffolds combined with human bone marrow stromal cells for tissue engineering

Biomaterials

Volumn 26, Issue 16, 2005, Pages 3173-3185

  Mauney, Joshua R ^a   Jaquiéry, Claude ^b   Volloch, Vladimir ^a   Heberer, Michael ^b   Martin, Ivan ^b   Kaplan, David L ^a  

^a TUFTS UNIVERSITY   (United States)

^b UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

Bone tissue engineering; Demineralization; Mesenchymal stem cell

Indexed keywords

BONE MARROW STROMAL CELL (BMSC); BONE MATRIX;

CELLS; ORGANIC ACIDS; TISSUE;

BONE;

ALKALINE PHOSPHATASE; BIOMATERIAL; CELL MARKER; MESSENGER RNA; OSTEOPONTIN; SIALOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEMINERALIZATION; BONE DEVELOPMENT; BONE MARROW CELL; BONE MATRIX; BONE MINERALIZATION; CANCELLOUS BONE; CATTLE; CELL CONTACT; CELL CULTURE; CELL DIFFERENTIATION; CLINICAL OBSERVATION; COCULTURE; CONTROLLED STUDY; DONOR; ENZYME ACTIVITY; EVALUATION; EX VIVO STUDY; EXPOSURE; GENE EXPRESSION; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMPLANTATION; IN VITRO STUDY; IN VIVO STUDY; MORPHOMETRICS; MOUSE; NONHUMAN; NUDE MOUSE; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; RNA ANALYSIS; SAMPLE; SOLUBILITY; STATISTICAL SIGNIFICANCE; STROMA CELL; TISSUE ENGINEERING;

ALKALINE PHOSPHATASE; ANIMALS; BIOCOMPATIBLE MATERIALS; BONE AND BONES; BONE MARROW CELLS; BONE TRANSPLANTATION; CALCIUM; CATTLE; CELL DIFFERENTIATION; CELL TRANSPLANTATION; COCULTURE TECHNIQUES; DNA, COMPLEMENTARY; MESODERM; MICE; MICE, NUDE; OSTEOBLASTS; OSTEOPONTIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; RNA, MESSENGER; SIALOGLYCOPROTEINS; STROMAL CELLS; TIME FACTORS; TISSUE ENGINEERING;

BOVINAE;

EID: 10644267768     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2004.08.020     Document Type: Article

References (76)

1. J.B. Mulliken, J. Glowacki, L.B. Kaban, J. Folkman, and J.E. Murray Use of demineralized allogeneic bone implants for the correction of maxillocraniofacial deformities Ann Surg 194 1981 366 372
2. J. Upton, M. Boyajian, J.B. Mulliken, and J. Glowacki The use of demineralized xenogeneic bone implants to correct phalangeal defects a case report J Hand Surg [Am] 9 1984 388 391
3. N. Kubler, C. Michel, J. Zoller, J. Bill, J. Muhling, and J. Reuther Repair of human skull defects using osteoinductive bone alloimplants J Craniomaxillofac Surg 23 1995 337 346
4. R. Rosenthal, J. Folkman, and J. Glowacki Demineralized bone implants for nonunion fractures, bone cysts, and fibrous lesions Clin Orthop 364 1999 61 69
5. T.M. Chen, and H.J. Wang Cranioplasty using allogeneic perforated demineralized bone matrix with autogenous bone paste Ann Plast Surg 49 2002 272 279
6. P.A. Fugazzotto GBR using bovine bone matrix and resorbable and nonresorbable membranes. Part 1 histologic results Int J Periodontics Restorative Dent 23 2003 361 369
7. E.S. Tadjoedin, G.L. de Lange, A.L. Bronckers, D.M. Lyaruu, and E.H. Burger Deproteinized cancellous bovine bone (Bio-Oss) as bone substitute for sinus floor elevation. A retrospective, histomorphometrical study of five cases J Clin Periodontol 30 2003 261 270
8. P. Valentini, and D.J. Abensur Maxillary sinus grafting with anorganic bovine bone a clinical report of long-term results Int J Oral Maxillofac Implants 18 2003 556 560
9. O.A. Trentz, S.P. Hoerstrup, L.K. Sun, L. Bestmann, A. Platz, and O.L. Trentz Osteoblasts response to allogenic and xenogenic solvent dehydrated cancellous bone in vitro Biomaterials 24 2003 3417 3426
10. M.R. Urist Bone formation by autoinduction Science 150 1965 893 899
11. M.R. Urist, R.F. DeLange, and G.A. Finerman Bone cell differentiation and growth factors Science 220 1983 680 686
12. N.K. Harakas Demineralized bone-matrix-induced osteogenesis Clin Orthop 188 1984 239 251
13. E. Solheim Osteoinduction by demineralized bone Int Orthop 22 1998 335 342
14. J. Wang, R. Yang, L.C. Gerstenfeld, and M.J. Glimcher Characterization of demineralized bone matrix-induced osteogenesis in rat calvarial bone defects. Part III. Gene and protein expression Calcif Tissue Int 67 2000 314 320
15. G.T. Syftestad, J.T. Triffitt, M.R. Urist, and A.I. Caplan An osteo-inductive bone matrix extract stimulates the in vitro conversion of mesenchyme into chondrocytes Calcif Tissue Int 36 1984 625 627
16. P.A. Lucas, C. Laurencin, G.T. Syftestad, A. Domb, V.M. Goldberg, A.I. Caplan, and R. Langer Ectopic induction of cartilage and bone by water-soluble proteins from bovine bone using a polyanhydride delivery vehicle J Biomed Mater Res 24 1990 901 911
17. H.F. Swoboda, F.M. Wimmer, K. Pfeiffer, and K.H. Schmidt Ectopic bone induction by partially purified bone extract alone or attached to biomaterials Biomater Artif Cells Artif Organs 18 1990 383 401
18. Y. Ogawa, D.K. Schmidt, R.M. Nathan, R.M. Armstrong, K.L. Miller, S.J. Sawamura, J.M. Ziman, K.L. Erickson, E.R. de Leon, and D.M. Rosen Bovine bone activin enhances bone morphogenetic protein-induced ectopic bone formation J Biol Chem 267 1992 14233 14237
19. R. Katoh, and M.R. Urist Surface adhesion and attachment factors in bone morphogenetic protein-induced chondrogenesis in vitro Clin Orthop 295 1993 295 304
20. Y. Yoshimura, A. Hirano, M. Nishida, J. Kawada, Y. Horisaka, Y. Okamoto, N. Matsumoto, K. Yamashita, and T. Takagi Purification of water-soluble bone-inductive protein from bovine demineralized bone matrix Biol Pharm Bull 16 1993 444 447
21. J. Becerra, J.A. Andrades, D.C. Ertl, N. Sorgente, and M.E. Nimni Demineralized bone matrix mediates differentiation of bone marrow stromal cells in vitro effect of age of cell donor J Bone Miner Res 11 1996 1703 1714
22. M. Zhang, R.M. Powers Jr., and L. Wolfinbarger Jr. Effect(s) of the demineralization process on the osteoinductivity of demineralized bone matrix J Periodontol 68 1997 1085 1092
23. K.U. Lewandrowski, W.W. Tomford, A. Yeadon, T.F. Deutsch, H.J. Mankin, and H.K. Uhthoff Flexural rigidity in partially demineralized diaphyseal bone grafts Clin Orthop 317 1995 254 262
24. S. Berven, B.K. Tay, F.S. Kleinstueck, and D.S. Bradford Clinical applications of bone graft substitutes in spine surgery consideration of mineralized and demineralized preparations and growth factor supplementation Eur Spine J 10 Suppl 2 2001 S169 S177
25. B.T. Rougraff, and T.J. Kling Treatment of active unicameral bone cysts with percutaneous injection of demineralized bone matrix and autogenous bone marrow J Bone Joint Surg Am 84 2002 921 929
26. J.J. Tiedeman, J.F. Connolly, B.S. Strates, and L. Lippiello Treatment of nonunion by percutaneous injection of bone marrow and demineralized bone matrix An experimental study in dogs. Clin Orthop 268 1991 294 302
27. P. Bianco, and P. Gehron Robey Marrow stromal stem cells J Clin Invest 105 2000 1663 1668
28. M. Owen, and A.J. Friedenstein Stromal stem cells marrow-derived osteogenic precursors Ciba Found Symp 136 1988 42 60
29. J.N. Beresford Osteogenic stem cells and the stromal system of bone and marrow Clin Orthop 240 1989 270 280
30. E. Kon, A. Muraglia, A. Corsi, P. Bianco, M. Marcacci, I. Martin, A. Boyde, I. Ruspantini, P. Chistolini, M. Rocca, R. Giardino, R. Cancedda, and R. Quarto Autologous bone marrow stromal cells loaded onto porous hydroxyapatite ceramic accelerate bone repair in critical-size defects of sheep long bones J Biomed Mater Res 49 2000 328 337
31. H. Petite, V. Viateau, W. Bensaid, A. Meunier, C. de Pollak, M. Bourguignon, K. Oudina, L. Sedel, and G. Guillemin Tissue-engineered bone regeneration Nat Biotechnol 18 2000 959 963
32. Q. Shang, Z. Wang, W. Liu, Y. Shi, L. Cui, and Y. Cao Tissue-engineered bone repair of sheep cranial defects with autologous bone marrow stromal cells J Craniofac Surg 12 2001 586 595
33. J.A. Andrades, J.A. Santamaria, M.E. Nimni, and J. Becerra Selection and amplification of a bone marrow cell population and its induction to the chondro-osteogenic lineage by rhOP-1 an in vitro and in vivo study Int J Dev Biol 45 2001 689 693
34. J.R. Mauney, J. Blumberg, M. Pirun, V. Volloch, G. Vunjak-Novakovic, and D.L. Kaplan Osteogenic differentiation of human bone marrow stromal cells on partially demineralized bone scaffolds in vitro Tissue Eng 10 2004 81 92
35. J.R. Mauney, S. Sjostrom, J. Blumberg, R. Horan, J.P. O'Leary, G. Vunjak-Novakovic, V. Volloch, and D.L. Kaplan Mechanical stimulation promotes osteogenic differentiation of human bone marrow stromal cells on 3-D partially demineralized bone scaffolds in vitro Calcif Tissue Int 74 2004 458 468
36. S.P. Bruder, N. Jaiswal, and S.E. Haynesworth Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation J Cell Biochem 64 1997 278 294
37. R.O. Oreffo, S. Bord, and J.T. Triffitt Skeletal progenitor cells and ageing human populations Clin Sci 94 1998 549 555
38. D.G. Phinney, G. Kopen, W. Righter, S. Webster, N. Tremain, and D.J. Prockop Donor variation in the growth properties and osteogenic potential of human marrow stromal cells J Cell Biochem 75 1999 424 436
39. O. Frank, M. Heim, M. Jakob, A. Barbero, D. Schafer, I. Bendik, W. Dick, M. Heberer, and I. Martin Real-time quantitative RT-PCR analysis of human bone marrow stromal cells during osteogenic differentiation in vitro J Cell Biochem 85 2002 737 746
40. S.C. Mendes, J.M. Tibbe, M. Veenhof, K. Bakker, S. Both, P.P. Platenburg, F.C. Oner, J.D. De Bruijn, and C.A. Van Blitterswijk Bone tissue-engineered implants using human bone marrow stromal cells effect of culture conditions and donor age Tissue Eng 8 2002 911 920
41. M. Hosny, C. Arcidi, and M. Sharawy Effects of preservation on the osteoinductive capacity of demineralized bone powder allografts J Oral Maxillofac Surg 45 1987 1051 1054
42. M. Yazdi, S. Bernick, W.J. Paule, and M.E. Nimni Postmortem degradation of demineralized bone matrix osteoinductive potential Effect of time and storage temperature. Clin Orthop 262 1991 281 285
43. K.K. Hallfeldt, H. Stutzle, M. Puhlmann, S. Kessler, and L. Schweiberer Sterilization of partially demineralized bone matrix the effects of different sterilization techniques on osteogenetic properties J Surg Res 59 1995 614 620
44. G. Vunjak-Novakovic, B. Obradovic, I. Martin, P.M. Bursac, R. Langer, and L.E. Freed Dynamic cell seeding of polymer scaffolds for cartilage tissue engineering Biotechnol Prog 14 1998 193 202
45. S.L. Voytik-Harbin, A.O. Brightman, B. Waisner, C.H. Lamar, and S.F. Badylak Application and evaluation of the alamarBlue assay for cell growth and survival of fibroblasts In Vitro Cell Dev Biol Anim 34 1998 239 246
46. A. Sabokbar, P.J. Millett, B. Myer, and N. Rushton A rapid, quantitative assay for measuring alkaline phosphatase activity in osteoblastic cells in vitro Bone Miner 27 1994 57 67
47. P. Chomczynski, and N. Sacchi Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction Anal Biochem 162 1987 156 159
48. I. Martin, M. Jakob, D. Schafer, W. Dick, G. Spagnoli, and M. Heberer Quantitative analysis of gene expression in human articular cartilage from normal and osteoarthritis joints Osteoarthr Cartilage 9 2001 112 118
49. J.E. Aubin, F. Liu, L. Malaval, and A.K. Gupta Osteoblast and chondroblast differentiation Bone 17 1995 77S 83S
50. M.R. Forwood, M.B. Bennett, A.R. Blowers, and R.L. Nadorfi Modification of the in vivo four-point loading model for studying mechanically induced bone adaptation Bone 23 1998 307 310
51. M. Wozniak, A. Fausto, C.P. Carron, D.M. Meyer, and K.A. Hruska Mechanically strained cells of the osteoblast lineage organize their extracellular matrix through unique sites of alphavbeta3-integrin expression J Bone Miner Res 15 2000 1731 1745
52. L.F. Cooper, C.T. Harris, S.P. Bruder, R. Kowalski, and S. Kadiyala Incipient analysis of mesenchymal stem-cell-derived osteogenesis J Dent Res 80 2001 314 320
53. S. Wakitani, T. Goto, S.J. Pineda, R.G. Young, J.M. Mansour, A.I. Caplan, and V.M. Goldberg Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage J Bone Jt Surg 76 1994 579 592
54. K. Satomura, P. Krebsbach, P. Bianco, and P. Gehron Robey Osteogenic imprinting upstream of marrow stromal cell differentiation J Cell Biochem 78 2000 391 403
55. B. Seshi, S. Kumar, and D. Sellers Human bone marrow stromal cell coexpression of markers specific for multiple mesenchymal cell lineages Blood Cells Mol Dis 26 2000 234 246
56. J. Chen, K. Singh, B.B. Mukherjee, and J. Sodek Developmental expression of osteopontin (OPN) mRNA in rat tissues evidence for a role for OPN in bone formation and resorption Matrix 13 1993 113 123
57. D.D. Marucci, Y. Yu, J. McTavish, S. Fiona Bonar, M.D. Poole, and W.R. Walsh Matrix metalloproteinases and their inhibitors in bone remodelling following distraction osteogenesis of the sheep mandible J Craniomaxillofac Surg 30 2002 208 212
58. J.M. Delaisse, T.L. Andersen, M.T. Engsig, K. Henriksen, T. Troen, and L. Blavier Matrix metalloproteinases (MMP) and cathepsin K contribute differently to osteoclastic activities Microsc Res Tech 61 2003 504 513
59. S. Cheifetz, I.W. Li, C.A. McCulloch, K. Sampath, and J. Sodek Influence of osteogenic protein-1 (OP-1;BMP-7) and transforming growth factor-beta 1 on bone formation in vitro Connect Tissue Res 35 1996 71 78
60. A.G. Brownell, N. Gerth, and G.A. Finerman Isolation, partial purification and in vitro characterization of osteogenic inhibitory protein Connect Tissue Res 17 4 1988 261 275
61. H. Imabayashi, T. Mori, S. Gojo, T. Kiyono, T. Sugiyama, R. Irie, T. Isogai, J. Hata, Y. Toyama, and A. Umezawa Redifferentiation of dedifferentiated chondrocytes and chondrogenesis of human bone marrow stromal cells via chondrosphere formation with expression profiling by large-scale cDNA analysis Exp Cell Res 288 2003 35 50
62. S. Spinella-Jaegle, S. Roman-Roman, C. Faucheu, F.W. Dunn, S. Kawai, S. Gallea, V. Stiot, A.M. Blanchet, B. Courtois, R. Baron, and G. Rawadi Opposite effects of bone morphogenetic protein-2 and transforming growth factor-beta1 on osteoblast differentiation Bone 29 2001 323 330
63. M.E. Bahamonde, and K.M. Lyons BMP3 to be or not to be a BMP J Bone Jt Surg Am 83 2001 S56 62
64. C.S. Ranucci, and P.V. Moghe Polymer substrate topography actively regulates the multicellular organization and liver-specific functions of cultured hepatocytes Tissue Eng 5 1999 407 420
65. J. Camps, I. About, B. Thonneman, T.A. Mitsiadis, G. Schmaltz, and J.C. Franquin Two- versus three-dimensional in vitro differentiation of human pulp cells into odontoblastic cells Connect Tissue Res 43 2002 396 400
66. K.M. Yamada, R. Pankov, and E. Cukierman Dimensions and dynamics in integrin function Braz J Med Biol Res 36 2003 959 966
67. Z. Schwartz, T. Weesner, S. van Dijk, D.L. Cochran, J.T. Mellonig, C.H. Lohmann, D.L. Carnes, M. Goldstein, D.D. Dean, and B.D. Boyan Ability of deproteinized cancellous bovine bone to induce new bone formation J Periodontol 71 2000 1258 1269
68. Z. Artzi, N. Givol, M.D. Rohrer, C.E. Nemcovsky, H.S. Prasad, and H. Tal Qualitative and quantitative expression of bovine bone mineral in experimental bone defects. Part 2 Morphometric analysis J Periodontol 74 2003 1153 1160
69. Q. Zhang, O. Cornu, and C. Delloye Ethylene oxide does not extinguish the osteoinductive capacity of demineralized bone A reappraisal in rats. Acta Orthop Scand 68 1997 104 108
70. S.D. Ferreira, W.S. Dernell, B.E. Powers, R.A. Schochet, C.A. Kuntz, S.J. Withrow, and R.M. Wilkins Effect of gas-plasma sterilization on the osteoinductive capacity of demineralized bone matrix Clin Orthop 388 2001 233 239
71. K.M. Chow, and A.B. Rabie Vascular endothelial growth pattern of endochondral bone graft in the presence of demineralized intramembranous bone matrix - quantitative analysis Cleft Palate Craniofac J 37 2000 385 394
72. J.H. Lee, C.P. Cornelius, and N. Schwenzer Neo-osseous flaps using demineralized allogeneic bone in a rat model Ann Plast Surg 44 2000 195 204
73. E.H. Groeneveld, J.P. van den Bergh, P. Holzmann, C.M. ten Bruggenkate, D.B. Tuinzing, and E.H. Burger Mineralization processes in demineralized bone matrix grafts in human maxillary sinus floor elevations J Biomed Mater Res 48 1999 393 402
74. F. Brugnami, P.R. Then, H. Moroi, S. Kabani, and C.W. Leone GBR in human extraction sockets and ridge defects prior to implant placement clinical results and histologic evidence of osteoblastic and osteoclastic activities in DFDBA Int J Periodontics Restorative Dent 19 1999 259 267
75. V.I. Sikavitsas, G.N. Bancroft, H.L. Holtorf, J.A. Jansen, and A.G. Mikos Mineralized matrix deposition by marrow stromal osteoblasts in 3D perfusion culture increases with increasing fluid shear forces Proc Natl Acad Sci USA 100 2003 14683 14688
76. G.N. Bancroft, V.I. Sikavitsas, J. van den Dolder, T.L. Sheffield, C.G. Ambrose, J.A. Jansen, and A.G. Mikos Fluid flow increases mineralized matrix deposition in 3D perfusion culture of marrow stromal osteoblasts in a dose-dependent manner Proc Natl Acad Sci USA 99 2002 12600 12605