Cell sources for bone tissue engineering: Insights from basic science

Tissue Engineering - Part B: Reviews

Volumn 17, Issue 6, 2011, Pages 449-457

  Colnot, Céline ^a  

^a HÔPITAL NECKER ENFANTS MALADES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; BASIC SCIENCE; BONE MARROW; BONE REGENERATION; BONE REPAIR; BONE TISSUE ENGINEERING; CELL SOURCES; CELL-BASED; CHONDROGENIC POTENTIAL; CORD BLOOD; DELIVERY METHODS; IN-VITRO; IN-VIVO; PLURIPOTENT STEM CELLS; REPAIR PROCESS; THERAPEUTIC EFFECTS;

BONE; REPAIR; STEM CELLS; TISSUE; TISSUE ENGINEERING;

CYTOLOGY;

ADIPOSE TISSUE; BONE DEVELOPMENT; BONE MARROW CELL; BONE REGENERATION; BONE REMODELING; BONE TISSUE; CELL DIFFERENTIATION; CELL TYPE; CHONDROGENESIS; EMBRYONIC STEM CELL; HUMAN; MUSCLE TISSUE; NONHUMAN; PERIOSTEUM; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW; TISSUE ENGINEERING; UMBILICAL CORD BLOOD;

ANIMALS; BONE AND BONES; BONE MARROW CELLS; HUMANS; TISSUE ENGINEERING; WOUND HEALING;

ANIMALIA;

EID: 81755161439     PISSN: 19373368     EISSN: 19373376     Source Type: Journal    
DOI: 10.1089/ten.teb.2011.0243     Document Type: Review

References (116)

1. Einhorn, T.A. Enhancement of fracture-healing. J Bone Joint Surg Am 77, 940, 1995.
2. Dickson, K., Katzman, S., Delgado, E., and Contreras., D. Delayed unions and nonunions of open tibial fractures. Correlation with arteriography results. Clin Orthop Relat Res 302, 189, 1994.
3. Kline, A.J., Gruen, G.S., Pape, H.C., Tarkin, I.S., Irrgang, J.J., and Wukich, D.K. Early complications following the operative treatment of pilon fractures with and without diabetes. Foot Ankle Int 30, 1042, 2009.
4. Griffin, X.L., Warner, F., and Costa, M. The role of electromagnetic stimulation in the management of established non-union of long bone fractures: what is the evidence? Injury 39, 419, 2008.
5. Schofer, M.D., Block, J.E., Aigner, J., and Schmelz, A. Improved healing response in delayed unions of the tibia with low-intensity pulsed ultrasound: results of a randomized sham-controlled trial. BMC Musculoskelet Disord 11, 229, 2010.
6. Gruber, R., Koch, H., Doll, B.A., Tegtmeier, F., Einhorn, T.A., and Hollinger, J.O. Fracture healing in the elderly patient. Exp Gerontol 41, 1080, 2006.
7. Urist, M.R. Bone: formation by autoinduction. Science 150, 893, 1965.
8. Luyten, F.P., Cunningham, N.S., Ma, S., Muthukumaran, N., Hammonds, R.G., Nevins, W.B., Woods, W.I., and Reddi, A.H. Purification and partial amino acid sequence of osteogenin, a protein initiating bone differentiation. J Biol Chem 264, 13377, 1989.
9. Axelrad, T.W., and Einhorn, T.A. Bone morphogenetic proteins in orthopaedic surgery. Cytokine Growth Factor Rev 20, 481, 2009.
10. Matsunaga, T., Shigetomi, M., Hashimoto, T., Suzuki, H., Gondo, T., Tanaka, H., Sugiyama, T., and Taguchi, T. Effects of bisphosphonate treatment on bone repair under immunosuppression using cyclosporine A in adult rats. Osteoporos Int 18, 1531, 2007.
11. Barnes, G.L., Kakar, S., Vora, S., Morgan, E.F., Gerstenfeld, L.C., and Einhorn, T.A. Stimulation of fracture-healing with systemic intermittent parathyroid hormone treatment. J Bone Joint Surg Am 90 Suppl 1, 120, 2008.
12. Aspenberg, P., Genant, H.K., Johansson, T., Nino, A.J., See, K., Krohn, K., Garcia-Hernandez, P.A., Recknor, C.P., Einhorn, T.A., Dalsky, G.P., Mitlak, B.H., Fierlinger, A., and Lakshmanan, M.C. Teriparatide for acceleration of fracture repair in humans: a prospective, randomized, double-blind study of 102 postmenopausal women with distal radial fractures. J Bone Miner Res 25, 404, 2010.
13. Einhorn, T.A. The Wnt signaling pathway as a potential target for therapies to enhance bone repair. Sci Transl Med 2, 42ps36, 2010.
14. Marsell, R., and Einhorn, T.A. Emerging bone healing therapies. J Orthop Trauma 24 Suppl 1, S4, 2010.
15. Pittenger, M.F., Mackay, A.M., Beck, S.C., Jaiswal, R.K., Douglas, R., Mosca, J.D., Moorman, M.A., Simonetti, D.W., Craig, S., and Marshak, D.R. Multilineage potential of adult human mesenchymal stem cells. Science, 284, 143, 1999.
16. Caplan, A.I. Mesenchymal stem cells. J Orthop Res 9, 641, 1991.
17. Friedenstein, A.J., Petrakova, K.V., Kurolesova, A.I., and Frolova, G.P. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 6, 230, 1968.
18. Bianco, P., and Robey, P.G. Stem cells in tissue engineering. Nature 414, 118, 2001.
19. Viateau, V., Guillemin, G., Bousson, V., Oudina, K., Hannouche, D., Sedel, L., Logeart-Avramoglou, D., and Petite, H. Long-bone critical-size defects treated with tissueengineered grafts: a study on sheep. J Orthop Res 25, 741, 2007.
20. Kuznetsov, S.A., Mankani, M.H., Gronthos, S., Satomura, K., Bianco, P., and Robey, P.G. Circulating skeletal stem cells. J Cell Biol 153, 1133, 2001.
21. Eghbali-Fatourechi, G.Z., Modder, U.I., Charatcharoenwitthaya, N., Sanyal, A., Undale, A.H., Clowes, J.A., Tarara, J.E., and Khosla, S. Characterization of circulating osteoblast lineage cells in humans. Bone 40, 1370, 2007.
22. Kumagai, K., Vasanji, A., Drazba, J.A., Butler, R.S., and Muschler, G.F. Circulating cells with osteogenic potential are physiologically mobilized into the fracture healing site in the parabiotic mice model. J Orthop Res 26, 165, 2008.
23. Wang, X.X., Allen, R.J., Jr., Tutela, J.P., Sailon, A., Allori, A.C., Davidson, E.H., Paek, G.K., Saadeh, P.B., McCarthy, J.G., and Warren, S.M. Progenitor cell mobilization enhances bone healing by means of improved neovascularization and osteogenesis. Plast Reconstr Surg 128, 395, 2011.
24. da Silva Meirelles, L., Caplan, A.I., and Nardi, N.B. In search of the in vivo identity of mesenchymal stem cells. Stem Cells 26, 2287, 2008.
25. Taguchi, K., Ogawa, R., Migita, M., Hanawa, H., Ito, H., and Orimo, H. The role of bone marrow-derived cells in bone fracture repair in a green fluorescent protein chimeric mouse model. Biochem Biophys Res Commun 331, 31, 2005.
26. Otsuru, S., Tamai, K., Yamazaki, T., Yoshikawa, H., and Kaneda, Y. Bone marrow-derived osteoblast progenitor cells in circulating blood contribute to ectopic bone formation in mice. Biochem Biophys Res Commun 354, 453, 2007.
27. Colnot, C., Huang, S., and Helms, J. Analyzing the cellular contribution of bone marrow to fracture healing using bone marrow transplantation in mice. Biochem Biophys Res Commun 350, 557, 2006.
28. Simmons, P.J., Przepiorka, D., Thomas, E.D., and Torok-Storb, B. Host origin of marrow stromal cells following allogeneic bone marrow transplantation. Nature 328, 429, 1987.
29. Johansson, M., Jansson, L., Ehinger, M., Fasth, A., Karlsson, S., and Richter, J. Neonatal hematopoietic stem cell transplantation cures oc/oc mice from osteopetrosis. Exp Hematol 34, 242, 2006.
30. Xing, Z., Lu, C., Hu, D., Miclau, T., 3rd, and Marcucio, R.S. Rejuvenation of the inflammatory system stimulates fracture repair in aged mice. J Orthop Res 28, 1000, 2010.
31. Behonick, D.J., Xing, Z., Lieu, S., Buckley, J.M., Lotz, J.C., Marcucio, R.S., Werb, Z., Miclau, T., and Colnot, C. Role of matrix metalloproteinase 13 in both endochondral and intramembranous ossification during skeletal regeneration. PLoS ONE 2, e1150, 2007.
32. Caplan, A.I. New era of cell-based orthopedic therapies. Tissue Eng Part B Rev 15, 195, 2009.
33. Rieger, K., Marinets, O., Fietz, T., Korper, S., Sommer, D., Mucke, C., Reufi, B., Blau, W.I., Thiel, E., and Knauf, W.U. Mesenchymal stem cells remain of host origin even a long time after allogeneic peripheral blood stem cell or bone marrow transplantation. Exp Hematol 33, 605, 2005.
34. Dominici, M., Marino, R., Rasini, V., Spano, C., Paolucci, P., Conte, P., Hofmann, T.J., and Horwitz, E.M. Donor cellderived osteopoiesis originates from a self-renewing stem cell with a limited regenerative contribution after transplantation. Blood 111, 4386, 2008.
35. Granero-Molto, F., Weis, J.A., Miga, M.I., Landis, B., Myers, T.J., O'Rear, L., Longobardi, L., Jansen, E.D., Mortlock, D.P., and Spagnoli, A. Regenerative effects of transplanted mesenchymal stem cells in fracture healing. Stem Cells 27, 1887, 2009.
36. Friedenstein, A., and Kuralesova, A.I. Osteogenic precursor cells of bone marrow in radiation chimeras. Transplantation 12, 99, 1971.
37. Gronthos, S., Graves, S.E., Ohta, S., and Simmons, P.J. The STRO-1 + fraction of adult human bone marrow contains the osteogenic precursors. Blood 84, 4164, 1994.
38. Prockop, D.J. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276, 71, 1997.
39. Shirley, D., Marsh, D., Jordan, G., McQuaid, S., and Li, G. Systemic recruitment of osteoblastic cells in fracture healing. J Orthop Res 23, 1013, 2005.
40. Devine, M.J., Mierisch, C.M., Jang, E., Anderson, P.C., and Balian, G. Transplanted bone marrow cells localize to fracture callus in a mouse model. J Orthop Res 20, 1232, 2002.
41. Morikawa, S., Mabuchi, Y., Kubota, Y., Nagai, Y., Niibe, K., Hiratsu, E., Suzuki, S., Miyauchi-Hara, C., Nagoshi, N., Sunabori, T., Shimmura, S., Miyawaki, A., Nakagawa, T., Suda, T., Okano, H., and Matsuzaki, Y. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J Exp Med 206, 2483, 2009.
42. Koide, Y., Morikawa, S., Mabuchi, Y., Muguruma, Y., Hiratsu, E., Hasegawa, K., Kobayashi, M., Ando, K., Kinjo, K., Okano, H., and Matsuzaki, Y. Two distinct stem cell lineages in murine bone marrow. Stem Cells 25, 1213, 2007.
43. Sengers, B.G., Dawson, J.I., and Oreffo, R.O. Characterisation of human bone marrow stromal cell heterogeneity for skeletal regeneration strategies using a two-stage colony assay and computational modelling. Bone 46, 496, 2010.
44. Muschler, G.F., Boehm, C., and Easley, K. Aspiration to obtain osteoblast progenitor cells from human bone marrow: the influence of aspiration volume. J Bone Joint Surg Am 79, 1699, 1997.
45. Sacchetti, B., Funari, A., Michienzi, S., Di Cesare, S., Piersanti, S., Saggio, I., Tagliafico, E., Ferrari, S., Robey, P.G., Riminucci, M., and Bianco, P. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 131, 324, 2007.
46. Kawanami, A., Matsushita, T., Chan, Y.Y., and Murakami, S. Mice expressing GFP and CreER in osteochondro progenitor cells in the periosteum. Biochem Biophys Res Commun 386, 477, 2009.
47. Colnot, C. Skeletal cell fate decisions within periosteum and bone marrow during bone regeneration. J Bone Miner Res 24, 274, 2009.
48. Zhang, X., Xie, C., Lin, A.S., Ito, H., Awad, H., Lieberman, J.R., Rubery, P.T., Schwarz, E.M., O'Keefe, R.J., and Guldberg, R.E. Periosteal progenitor cell fate in segmental cortical bone graft transplantations: implications for functional tissue engineering. J Bone Miner Res 20, 2124, 2005.
49. Xie, C., Ming, X., Wang, Q., Schwarz, E.M., Guldberg, R.E., O'Keefe, R.J., and Zhang, X. COX-2 from the injury milieu is critical for the initiation of periosteal progenitor cell mediated bone healing. Bone 43, 1075, 2008.
50. Wang, Q., Huang, C., Xue, M., and Zhang, X. Expression of endogenous BMP-2 in periosteal progenitor cells is essential for bone healing. Bone 48, 524, 2011.
51. Yu, Y.Y., Lieu, S., Lu, C., and Colnot, C. Bone morphogenetic protein 2 stimulates endochondral ossification by regulating periosteal cell fate during bone repair. Bone 47, 65, 2010.
52. Utvag, S.E., Grundnes, O., and Reikeraos, O. Effects of periosteal stripping on healing of segmental fractures in rats. J Orthop Trauma 10, 279, 1996.
53. Ozaki, A., Tsunoda, M., Kinoshita, S., and Saura, R. Role of fracture hematoma and periosteum during fracture healing in rats: interaction of fracture hematoma and the periosteum in the initial step of the healing process. J Orthop Sci 5, 64, 2000.
54. Guichet, J.M., Braillon, P., Bodenreider, O., and Lascombes, P. Periosteum and bone marrow in bone lengthening: a DEXA quantitative evaluation in rabbits. Acta Orthop Scand 69, 527, 1998.
55. Iwasaki, M., Le, A.X., and Helms, J.A. Expression of Indian hedgehog, bone morphogenetic protein 6 and gli during skeletal morphogenesis. Mech Dev 69, 197, 1997.
56. Brighton, C.T., and Hunt, R.M. Early histologic and ultrastructural changes in microvessels of periosteal callus. J Orthop Trauma 11, 244, 1997.
57. Maes, C., Kobayashi, T., Selig, M.K., Torrekens, S., Roth, S.I., Mackem, S., Carmeliet, G., and Kronenberg, H.M. Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev Cell 19, 329, 2010.
58. Ito, H., Koefoed, M., Tiyapatanaputi, P., Gromov, K., Goater, J.J., Carmouche, J., Zhang, X., Rubery, P.T., Rabinowitz, J., Samulski, R.J., Nakamura, T., Soballe, K., O'Keefe, R.J., Boyce, B.F., and Schwarz, E.M. Remodeling of cortical bone allografts mediated by adherent rAAV-RANKL and VEGF gene therapy. Nat Med 11, 291, 2005.
59. Bi, Y., Ehirchiou, D., Kilts, T.M., Inkson, C.A., Embree, M.C., Sonoyama, W., Li, L., Leet, A.I., Seo, B.M., Zhang, L., Shi, S., and Young, M.F. Identification of tendon stem/progenitor cells and the role of the extracellular matrix in their niche. Nat Med 13, 1219, 2007.
60. Lee, J.Y., Qu-Petersen, Z., Cao, B.H., Kimura, S., Jankowski, R., Cummins, J., Usas, A., Gates, C., Robbins, P., Wernig, A., and Huard, J. Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J Cell Biol 150, 1085, 2000.
61. Zheng, B., Cao, B., Li, G., and Huard, J. Mouse adiposederived stem cells undergo multilineage differentiation in vitro but primarily osteogenic and chondrogenic differentiation in vivo. Tissue Eng 12, 1891, 2006.
62. Kahle, M., Wiesmann, H.P., Berr, K., Depprich, R.A., Kubler, N.R., Naujoks, C., Cohnen, M., Ommerborn, M.A., Meyer, U., and Handschel, J. Embryonic stem cells induce ectopic bone formation in rats. Biomed Mater Eng 20, 371, 2010.
63. Gruenloh, W., Kambal, A., Sondergaard, C., McGee, J., Nacey, C., Kalomoiris, S., Pepper, K., Olson, S., Fierro, F., and Nolta, J.A. Characterization and in vivo testing of mesenchymal stem cells derived from human embryonic stem cells. Tissue Eng Part A 17, 1517, 2011.
64. Illich, D.J., Demir, N., Stojkovic, M., Scheer, M., Rothamel, D., Neugebauer, J., Hescheler, J., and Zoller, J.E. Induced pluripotent stem (iPS) cells and lineage reprogramming: prospects for bone regeneration. Stem Cells 29, 555, 2011.
65. Kuznetsov, S.A., Cherman, N., and Robey, P.G. In vivo bone formation by progeny of human embryonic stem cells. Stem Cells Dev 20, 269, 2011.
66. Bonnarens, F., and Einhorn, T.A. Production of a standard closed fracture in laboratory animal bone. J Orthop Res 2, 97, 1984.
67. Thompson, Z., Miclau, T., Hu, D., and Helms, J.A. A model for intramembranous ossification during fracture healing. J Orthop Res 20, 1091, 2002.
68. Choi, P., Ogilvie, C., Thompson, Z., Miclau, T., and Helms, J.A. Cellular and molecular characterization of a murine non-union model. J Orthop Res 22, 1100, 2004.
69. Burastero, G., Scarfi, S., Ferraris, C., Fresia, C., Sessarego, N., Fruscione, F., Monetti, F., Scarfo, F., Schupbach, P., Podesta, M., Grappiolo, G., and Zocchi, E. The association of human mesenchymal stem cells with BMP-7 improves bone regeneration of critical-size segmental bone defects in athymic rats. Bone 47, 117, 2010.
70. Lieberman, J.R., Daluiski, A., Stevenson, S., Wu, L., McAllister, P., Lee, Y.P., Kabo, J.M., Finerman, G.A., Berk, A.J., and Witte, O.N. The effect of regional gene therapy with bone morphogenetic protein-2-producing bonemarrow cells on the repair of segmental femoral defects in rats. J Bone Joint Surg Am 81, 905, 1999.
71. Colnot, C., Romero, D.M., Huang, S., and Helms, J.A. Mechanisms of action of demineralized bonematrix in the repair of cortical bone defects. Clin Orthop Relat Res 435, 69, 2005.
72. Peng, H., Wright, V., Usas, A., Gearhart, B., Shen, H.C., Cummins, J., and Huard, J. Synergistic enhancement of bone formation and healing by stem cell-expressed VEGF and bone morphogenetic protein-4. J Clin Invest 110, 751, 2002.
73. Muschler, G.F., Nitto, H., Boehm, C.A., and Easley, K.A. Age-and gender-related changes in the cellularity of human bone marrow and the prevalence of osteoblastic progenitors. J Orthop Res 19, 117, 2001.
74. Stolzing, A., Jones, E., McGonagle, D., and Scutt, A. Agerelated changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies. Mech Ageing Dev 129 163, 2008.
75. Sen, M.K., and Miclau, T. Autologous iliac crest bone graft: should it still be the gold standard for treating nonunions? Injury 38 Suppl 1, S75, 2007.
76. Zhang, X., Naik, A., Xie, C., Reynolds, D., Palmer, J., Lin, A., Awad, H., Guldberg, R., Schwarz, E., and O'Keefe, R. Periosteal stem cells are essential for bone revitalization and repair. J Musculoskelet Neuronal Interact 5, 360, 2005.
77. Leucht, P., Kim, J.B., Amasha, R., James, A.W., Girod, S., and Helms, J.A. Embryonic origin and Hox status determine progenitor cell fate during adult bone regeneration. Development 135, 2845, 2008.
78. Roberts, S.J., Geris, L., Kerckhofs, G., Desmet, E., Schrooten, J., and Luyten, F.P. The combined bone forming capacity of human periosteal derived cells and calcium phosphates. Biomaterials 32, 4393, 2011.
79. Xie, C., Reynolds, D., Awad, H., Rubery, P.T., Pelled, G., Gazit, D., Guldberg, R.E., Schwarz, E.M., O'Keefe, R.J., and Zhang, X. Structural bone allograft combined with genetically engineered mesenchymal stem cells as a novel platform for bone tissue engineering. Tissue Eng 13, 435, 2007.
80. Levi, B., and Longaker, M.T. Adipose derived stromal cells for skeletal regenerative medicine. Stem Cells 29, 576, 2011.
81. Li, H., Dai, K., Tang, T., Zhang, X., Yan, M., and Lou, J. Bone regeneration by implantation of adipose-derived stromal cells expressing BMP-2. Biochem Biophys Res Commun 356, 836, 2007.
82. Lee, J.Y., Musgrave, D., Pelinkovic, D., Fukushima, K., Cummins, J., Usas, A., Robbins, P., Fu, F.H., and Huard, J. Effect of bone morphogenetic protein-2-expressing musclederived cells on healing of critical-sized bone defects in mice. J Bone Joint Surg Am 83A, 1032, 2001.
83. Shen, H.C., Peng, H., Usas, A., Gearhart, B., Cummins, J., Fu, F.H., and Huard, J. Ex vivo gene therapy-induced endochondral bone formation: comparison of muscle-derived stem cells and different subpopulations of primary musclederived cells. Bone 34, 982, 2004.
84. Wright, V., Peng, H., Usas, A., Young, B., Gearhart, B., Cummins, J., and Huard, J. BMP4-expressing musclederived stem cells differentiate into osteogenic lineage and improve bone healing in immunocompetent mice. Mol Ther 6, 169, 2002.
85. Bianco, P., Robey, P.G., and Simmons, P.J. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell 2, 313, 2008.
86. Jones, E., and McGonagle, D. Human bone marrow mesenchymal stem cells in vivo. Rheumatology (Oxford) 47, 126, 2008.
87. Buchheiser, A., Liedtke, S., Looijenga, L.H., and Kogler, G. Cord blood for tissue regeneration. J Cell Biochem 108, 762, 2009.
88. Zhang, Z.Y., Teoh, S.H., Chong, M.S., Lee, E.S., Tan, L.G., Mattar, C.N., Fisk, N.M., Choolani, M., and Chan, J. Neovascularization and bone formation mediated by fetal mesenchymal stem cell tissue-engineered bone grafts in critical-size femoral defects. Biomaterials 31, 608, 2010.
89. Arpornmaeklong, P., Brown, S.E., Wang, Z., and Krebsbach, P.H. Phenotypic characterization, osteoblastic differentiation, and bone regeneration capacity of human embryonic stem cell-derived mesenchymal stem cells. Stem Cells Dev 18, 955, 2009.
90. Duan, X., Tu, Q., Zhang, J., Ye, J., Sommer, C., Mostoslavsky, G., Kaplan, D., Yang, P., and Chen, J. Application of induced pluripotent stem (iPS) cells in periodontal tissue regeneration. J Cell Physiol 226 150, 2011.
91. Ye, J.H., Xu, Y.J., Gao, J., Yan, S.G., Zhao, J., Tu, Q., Zhang, J., Duan, X.J., Sommer, C.A., Mostoslavsky, G., Kaplan, D.L., Wu, Y.N., Zhang, C.P., Wang, L., and Chen, J. Critical-size calvarial bone defects healing in a mouse model with silk scaffolds and SATB2-modified iPSCs. Biomaterials 32, 5065, 2011.
92. Beyth, S., Borovsky, Z., Mevorach, D., Liebergall, M., Gazit, Z., Aslan, H., Galun, E., and Rachmilewitz, J. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 105, 2214, 2005.
93. Caplan, A.I. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 213, 341, 2007.
94. Calvi, L.M., Adams, G.B., Weibrecht, K.W., Weber, J.M., Olson, D.P., Knight, M.C., Martin, R.P., Schipani, E., Divieti, P., Bringhurst, F.R., Milner, L.A., Kronenberg, H.M., and Scadden, D.T. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425, 841, 2003.
95. Zhang, J., Niu, C., Ye, L., Huang, H., He, X., Tong, W.G., Ross, J., Haug, J., Johnson, T., Feng, J.Q., Harris, S., Wiedemann, L.M., Mishina, Y., and Li, L. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425, 836, 2003.
96. Kumar, S., and Ponnazhagan, S. Bone homing of mesenchymal stem cells by ectopic alpha 4 integrin expression. FASEB J 21, 3917, 2007.
97. Le Blanc, K., Gotherstrom, C., Ringden, O., Hassan, M., McMahon, R., Horwitz, E., Anneren, G., Axelsson, O., Nunn, J., Ewald, U., Norden-Lindeberg, S., Jansson, M., Dalton, A., Astrom, E., and Westgren, M. Fetal mesenchymal stem-cell engraftment in bone after in utero transplantation in a patient with severe osteogenesis imperfecta. Transplantation 79, 1607, 2005.
98. Guillot, P.V., Abass, O., Bassett, J.H., Shefelbine, S.J., Bou-Gharios, G., Chan, J., Kurata, H., Williams, G.R., Polak, J., and Fisk, N.M. Intrauterine transplantation of human fetal mesenchymal stem cells from first-trimester blood repairs bone and reduces fractures in osteogenesis imperfecta mice. Blood 111, 1717, 2008.
99. Tiedeman, J.J., Connolly, J.F., Strates, B.S., and Lippiello, L. Treatment of nonunion by percutaneous injection of bone marrow and demineralized bone matrix. An experimental study in dogs. Clin Orthop Relat Res 268, 294, 1991.
100. Healey, J.H., Zimmerman, P.A., McDonnell, J.M., and Lane, J.M. Percutaneous bone marrow grafting of delayed union and nonunion in cancer patients. Clin Orthop Relat Res 256, 280, 1990.
101. Garg, N.K., and Gaur, S. Percutaneous autogenous bonemarrow grafting in congenital tibial pseudarthrosis. J Bone Joint Surg Br 77, 830, 1995.
102. Hernigou, P., Poignard, A., Beaujean, F., and Rouard, H. Percutaneous autologous bone-marrow grafting for nonunions. Influence of the number and concentration of progenitor cells. J Bone Joint Surg Am 87, 1430, 2005.
103. Nicodemus, G.D., and Bryant, S.J. Cell encapsulation in biodegradable hydrogels for tissue engineering applications. Tissue Eng Part B Rev 14, 149, 2008.
104. Ben-David, D., Kizhner, T.A., Kohler, T., Muller, R., Livne, E., and Srouji, S. Cell-scaffold transplant of hydrogel seeded with rat bone marrow progenitors for bone regeneration. J Craniomaxillofac Surg 39, 364, 2011.
105. Wang, G., Zheng, L., Zhao, H., Miao, J., Sun, C., Ren, N., Wang, J., Liu, H., and Tao, X. In vitro assessment of the differentiation potential of bone marrow-derived mesenchymal stem cells on genipin-chitosan conjugation scaffold with surface hydroxyapatite nanostructure for bone tissue engineering. Tissue Eng Part A 17, 1341, 2011.
106. Petite, H., Vandamme, K., Monfoulet, L., and Logeart-Avramoglou, D. Strategies for improving the efficacy of bioengineered bone constructs: a perspective. Osteoporos Int 22, 2017, 2011.
107. Deschepper, M., Oudina, K., David, B., Myrtil, V., Collet, C., Bensidhoum, M., Logeart-Avramoglou, D., and Petite, H. Survival and function of mesenchymal stem cells (MSCs) depend on glucose to overcome exposure to longterm, severe and continuous hypoxia. J Cell Mol Med 15, 1505, 2011.
108. Rauh, J., Milan, F., Gunther, K.P., and Stiehler, M. Bioreactor systems for bone tissue engineering. Tissue Eng Part B Rev 17, 263, 2011.
109. David, B., Bonnefont-Rousselot, D., Oudina, K., Degat, M.C., Deschepper, M., Viateau, V., Bensidhoum, M., Oddou, C., and Petite, H. A perfusion bioreactor for engineering bone constructs: an in vitro and in vivo study. Tissue Eng Part C Methods 17, 505, 2011.
110. Nakahara, H., Misawa, H., Hayashi, T., Kondo, E., Yuasa, T., Kubota, Y., Seita, M., Kawamoto, Hassan, W.A., Hassan, R.A., Javed, S.M., Tanaka, M., Endo, H., Noguchi, H., Matsumoto, S., Takata, K., Tashiro, Y., Nakaji, S., Ozaki, T., and Kobayashi, N. Bone repair by transplantation of hTERT-immortalized human mesenchymal stem cells in mice. Transplantation 88, 346, 2009.
111. Liu, Y., Wang, L., Fatahi, R., Kronenberg, M., Kalajzic, I., Rowe, D., Li, Y., and Maye, P. Isolation of murine bone marrow derived mesenchymal stem cells using Twist2 Cre transgenic mice. Bone 47, 916, 2011.
112. Zhou, J., Lin, H., Fang, T., Li, X., Dai, W., Uemura, T., and Dong, J. The repair of large segmental bone defects in the rabbit with vascularized tissue engineered bone. Biomaterials 31, 1171, 2010.
113. Kumar, S., Wan, C., Ramaswamy, G., Clemens, T.L., and Ponnazhagan, S. Mesenchymal stem cells expressing osteogenic and angiogenic factors synergistically enhance bone formation in a mouse model of segmental bone defect. Mol Ther 18, 1026, 2010.
114. Evans, C. Gene therapy for the regeneration of bone. Injury 42, 599, 2011.
115. Karp, J.M., and Leng Teo, G.S. Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 4, 206, 2009.
116. Villa, C., Erratico, S., Razini, P., Farini, A., Meregalli, M., Belicchi, M., and Torrente, Y. In vivo tracking of stem cell by nanotechnologies: future prospects for mouse to human translation. Tissue Eng Part B Rev 17, 1, 2011.