Bringing new life to damaged bone: The importance of angiogenesis in bone repair and regeneration

Bone

Volumn 70, Issue , 2015, Pages 19-27

  Stegen, Steve ^a   van Gastel, Nick ^a   Carmeliet, Geert ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Angiogenesis; Bone healing; Fracture; Hypoxia; Tissue engineering; VEGF

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ANGIOPOIETIN; BONE MORPHOGENETIC PROTEIN; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 18; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 9; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 3; GELATINASE B; GLUCOSE TRANSPORTER 1; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; LACTATE DEHYDROGENASE; MICRORNA; MICRORNA 101; MICRORNA 16; NOTCH RECEPTOR; PLACENTAL GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR; SOMATOMEDIN; TRANSCRIPTION FACTOR OSTERIX; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; VASCULOTROPIN RECEPTOR; OXYGEN;

ANGIOGENESIS; ARTICLE; BONE CELL; BONE DEFECT; BONE MINERALIZATION; BONE REGENERATION; BONE REMODELING; BONE TISSUE; CALLUS; CARDIOVASCULAR SYSTEM; CARTILAGE CELL; CELL JUNCTION; ENCHONDRAL OSSIFICATION; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FILOPODIUM; FRACTURE HEALING; HUMAN; HYPOXIA; MESENCHYMAL STEM CELL; NONHUMAN; OSTEOBLAST; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TISSUE ENGINEERING; WOUND HEALING; ANIMAL; BONE; CYTOLOGY; DRUG EFFECTS; PATHOLOGY; PATHOPHYSIOLOGY; STEM CELL; VASCULARIZATION;

ANIMALS; BONE AND BONES; BONE REGENERATION; FRACTURE HEALING; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; OXYGEN; STEM CELLS;

EID: 84918584689     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2014.09.017     Document Type: Article

References (122)

1. Gomez-Gaviro M.V., Lovell-Badge R., Fernandez-Aviles F., Lara-Pezzi E. The vascular stem cell niche. J Cardiovasc Transl Res 2012, 5:618-630.
2. Dickson K.F., Katzman S., Paiement G. The importance of the blood supply in the healing of tibial fractures. Contemp Orthop 1995, 30:489-493.
3. Adams R.H., Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 2007, 8:464-478.
4. Jain R.K. Molecular regulation of vessel maturation. Nat Med 2003, 9:685-693.
5. Jakobsson L., Franco C.A., Bentley K., Collins R.T., Ponsioen B., Aspalter I.M., et al. Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat Cell Biol 2010, 12:943-953.
6. Potente M., Gerhardt H., Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell 2011, 146:873-887.
7. Carmeliet P., Ferreira V., Breier G., Pollefeyt S., Kieckens L., Gertsenstein M., et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996, 380:435-439.
8. Ferrara N., Gerber H.P., LeCouter J. The biology of VEGF and its receptors. Nat Med 2003, 9:669-676.
9. Ferguson C., Alpern E., Miclau T., Helms J.A. Does adult fracture repair recapitulate embryonic skeletal formation?. Mech Dev 1999, 87:57-66.
10. Dimitriou R., Tsiridis E., Giannoudis P.V. Current concepts of molecular aspects of bone healing. Injury 2005, 36:1392-1404.
11. Glowacki J. Angiogenesis in fracture repair. Clin Orthop Relat Res 1998, S82-S89.
12. Hausman M.R., Schaffler M.B., Majeska R.J. Prevention of fracture healing in rats by an inhibitor of angiogenesis. Bone 2001, 29:560-564.
13. Josko J., Gwozdz B., Jedrzejowska-Szypulka H., Hendryk S. Vascular endothelial growth factor (VEGF) and its effect on angiogenesis. Med Sci Monit 2000, 6:1047-1052.
14. Bluteau G., Julien M., Magne D., Mallein-Gerin F., Weiss P., Daculsi G., et al. VEGF and VEGF receptors are differentially expressed in chondrocytes. Bone 2007, 40:568-576.
15. Street J., Bao M., deGuzman L., Bunting S., Peale F.V., Ferrara N, et al. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci U S A 2002, 99:9656-9661.
16. Peng H., Wright V., Usas A., Gearhart B., Shen H.C., Cummins J., et al. Synergistic enhancement of bone formation and healing by stem cell-expressed VEGF and bone morphogenetic protein-4. J Clin Invest 2002, 110:751-759.
17. Bouletreau P.J., Warren S.M., Spector J.A., Peled Z.M., Gerrets R.P., Greenwald J.A., et al. Hypoxia and VEGF up-regulate BMP-2 mRNA and protein expression in microvascular endothelial cells: implications for fracture healing. Plast Reconstr Surg 2002, 109:2384-2397.
18. Zelzer E., McLean W., Ng Y.S., Fukai N., Reginato A.M., Lovejoy S., et al. Skeletal defects in VEGF(120/120) mice reveal multiple roles for VEGF in skeletogenesis. Development 2002, 129:1893-1904.
19. Midy V., Plouet J. Vasculotropin/vascular endothelial growth factor induces differentiation in cultured osteoblasts. Biochem Biophys Res Commun 1994, 199:380-386.
20. Deckers M.M., Karperien M., van der Bent C., Yamashita T., Papapoulos S.E., Lowik C.W. Expression of vascular endothelial growth factors and their receptors during osteoblast differentiation. Endocrinology 2000, 141:1667-1674.
21. Mayr-Wohlfart U., Waltenberger J., Hausser H., Kessler S., Gunther K.P., Dehio C., et al. Vascular endothelial growth factor stimulates chemotactic migration of primary human osteoblasts. Bone 2002, 30:472-477.
22. Harper J., Gerstenfeld L.C., Klagsbrun M. Neuropilin-1 expression in osteogenic cells: down-regulation during differentiation of osteoblasts into osteocytes. J Cell Biochem 2001, 81:82-92.
23. Jacobsen K.A., Al-Aql Z.S., Wan C., Fitch J.L., Stapleton S.N., Mason Z.D., et al. Bone formation during distraction osteogenesis is dependent on both VEGFR1 and VEGFR2 signaling. J Bone Miner Res Off J Am Soc Bone Miner Res 2008, 23:596-609.
24. Liu Y., Berendsen A.D., Jia S., Lotinun S., Baron R., Ferrara N., et al. Intracellular VEGF regulates the balance between osteoblast and adipocyte differentiation. J Clin Invest 2012, 122:3101-3113.
25. Dewerchin M., Carmeliet P. PlGF: a multitasking cytokine with disease-restricted activity. Cold Spring Harb Perspect Med 2012, 2.
26. Maes C., Coenegrachts L., Stockmans I., Daci E., Luttun A., Petryk A., et al. Placental growth factor mediates mesenchymal cell development, cartilage turnover, and bone remodeling during fracture repair. J Clin Invest 2006, 116:1230-1242.
27. Javerzat S., Auguste P., Bikfalvi A. The role of fibroblast growth factors in vascular development. Trends Mol Med 2002, 8:483-489.
28. Montero A., Okada Y., Tomita M., Ito M., Tsurukami H., Nakamura T., et al. Disruption of the fibroblast growth factor-2 gene results in decreased bone mass and bone formation. J Clin Invest 2000, 105:1085-1093.
29. Ohbayashi N., Shibayama M., Kurotaki Y., Imanishi M., Fujimori T., Itoh N., et al. FGF18 is required for normal cell proliferation and differentiation during osteogenesis and chondrogenesis. Genes Dev 2002, 16:870-879.
30. Liu Z., Lavine K.J., Hung I.H., Ornitz D.M. FGF18 is required for early chondrocyte proliferation, hypertrophy and vascular invasion of the growth plate. Dev Biol 2007, 302:80-91.
31. Schmid G.J., Kobayashi C., Sandell L.J., Ornitz D.M. Fibroblast growth factor expression during skeletal fracture healing in mice. Dev Dyn 2009, 238:766-774.
32. Behr B., Leucht P., Longaker M.T., Quarto N. Fgf-9 is required for angiogenesis and osteogenesis in long bone repair. Proc Natl Acad Sci U S A 2010, 107:11853-11858.
33. Jacob A.L., Smith C., Partanen J., Ornitz D.M. Fibroblast growth factor receptor 1 signaling in the osteo-chondrogenic cell lineage regulates sequential steps of osteoblast maturation. Dev Biol 2006, 296:315-328.
34. Shimoaka T., Ogasawara T., Yonamine A., Chikazu D., Kawano H., Nakamura K., et al. Regulation of osteoblast, chondrocyte, and osteoclast functions by fibroblast growth factor (FGF)-18 in comparison with FGF-2 and FGF-10. J Biol Chem 2002, 277:7493-7500.
35. Chikazu D., Katagiri M., Ogasawara T., Ogata N., Shimoaka T., Takato T., et al. Regulation of osteoclast differentiation by fibroblast growth factor 2: stimulation of receptor activator of nuclear factor kappaB ligand/osteoclast differentiation factor expression in osteoblasts and inhibition of macrophage colony-stimulating factor function in osteoclast precursors. J Bone Miner Res 2001, 16:2074-2081.
36. Holmbeck K., Bianco P., Caterina J., Yamada S., Kromer M., Kuznetsov S.A., et al. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 1999, 99:81-92.
37. Zhou Z., Apte S.S., Soininen R., Cao R., Baaklini G.Y., Rauser R.W., et al. Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc Natl Acad Sci U S A 2000, 97:4052-4057.
38. Vu T.H., Shipley J.M., Bergers G., Berger J.E., Helms J.A., Hanahan D., et al. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 1998, 93:411-422.
39. Colnot C., Thompson Z., Miclau T., Werb Z., Helms J.A. Altered fracture repair in the absence of MMP9. Development 2003, 130:4123-4133.
40. Kim J.M., Shin H.I., Cha S.S., Lee C.S., Hong B.S., Lim S., et al. DJ-1 promotes angiogenesis and osteogenesis by activating FGF receptor-1 signaling. Nat Commun 2012, 3:1296.
41. Bernstein E., Kim S.Y., Carmell M.A., Murchison E.P., Alcorn H., Li M.Z., et al. Dicer is essential for mouse development. Nat Genet 2003, 35:215-217.
42. Liu B., Peng X.C., Zheng X.L., Wang J., Qin Y.W. MiR-126 restoration down-regulate VEGF and inhibit the growth of lung cancer cell lines in vitro and in vivo. Lung Cancer 2009, 66:169-175.
43. McArthur K., Feng B., Wu Y., Chen S., Chakrabarti S. MicroRNA-200b regulates vascular endothelial growth factor-mediated alterations in diabetic retinopathy. Diabetes 2011, 60:1314-1323.
44. Dong S., Yang B., Guo H., Kang F. MicroRNAs regulate osteogenesis and chondrogenesis. Biochem Biophys Res Commun 2012, 418:587-591.
45. Wang X., Guo B., Li Q., Peng J., Yang Z., Wang A., et al. miR-214 targets ATF4 to inhibit bone formation. Nat Med 2013, 19:93-100.
46. Sugatani T., Vacher J., Hruska K.A. A microRNA expression signature of osteoclastogenesis. Blood 2011, 117:3648-3657.
47. Murata K., Ito H., Yoshitomi H., Yamamoto K., Fukuda A., Yoshikawa J., et al. Inhibition of miR-92a enhances fracture healing via promoting angiogenesis in a model of stabilized fracture in young mice. J Bone Miner Res 2014, 29:316-326.
48. Brighton C.T., Krebs A.G. Oxygen tension of healing fractures in the rabbit. J Bone Joint Surg Am 1972, 54:323-332.
49. Semenza G.L. Hypoxia-inducible factors in physiology and medicine. Cell 2012, 148:399-408.
50. Komatsu D.E., Hadjiargyrou M. Activation of the transcription factor HIF-1 and its target genes, VEGF, HO-1, iNOS, during fracture repair. Bone 2004, 34:680-688.
51. Maes C., Carmeliet G., Schipani E. Hypoxia-driven pathways in bone development, regeneration and disease. Nat Rev Rheumatol 2012, 8:358-366.
52. Wan C., Gilbert S.R., Wang Y., Cao X., Shen X., Ramaswamy G., et al. Activation of the hypoxia-inducible factor-1alpha pathway accelerates bone regeneration. Proc Natl Acad Sci U S A 2008, 105:686-691.
53. Shen X., Wan C., Ramaswamy G., Mavalli M., Wang Y., Duvall C.L., et al. Prolyl hydroxylase inhibitors increase neoangiogenesis and callus formation following femur fracture in mice. J Orthop Res 2009, 27:1298-1305.
54. Colnot C. Cellular and molecular interactions regulating skeletogenesis. J Cell Biochem 2005, 95:688-697.
55. Crisan M., Yap S., Casteilla L., Chen C.W., Corselli M., Park T.S., et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008, 3:301-313.
56. Sacchetti B., Funari A., Michienzi S., Di C.S., Piersanti S., Saggio I., et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 2007, 131:324-336.
57. Mendez-Ferrer S., Michurina T.V., Ferraro F., Mazloom A.R., Macarthur B.D., Lira S.A., et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 2010, 466:829-834.
58. Park D., Spencer J.A., Koh B.I., Kobayashi T., Fujisaki J., Clemens T.L., et al. Endogenous bone marrow MSCs are dynamic, fate-restricted participants in bone maintenance and regeneration. Cell Stem Cell 2012, 10:259-272.
59. Murray I.R., West C.C., Hardy W.R., James A.W., Park T.S., Nguyen A., et al. Natural history of mesenchymal stem cells, from vessel walls to culture vessels. Cell Mol Life Sci 2013, 51:1353-1374.
60. Zannettino A.C., Paton S., Arthur A., Khor F., Itescu S., Gimble J.M., et al. Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 2008, 214:413-421.
61. Ozerdem U., Grako K.A., Dahlin-Huppe K., Monosov E., Stallcup W.B. NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Dev Dyn 2001, 222:218-227.
62. Skalli O., Pelte M.F., Peclet M.C., Gabbiani G., Gugliotta P., Bussolati G., et al. Alpha-smooth muscle actin, a differentiation marker of smooth muscle cells, is present in microfilamentous bundles of pericytes. J Histochem Cytochem 1989, 37:315-321.
63. Kunisaki Y., Bruns I., Scheiermann C., Ahmed J., Pinho S., Zhang D., et al. Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 2013, 502:637-643.
64. Dellavalle A., Maroli G., Covarello D., Azzoni E., Innocenzi A., Perani L., et al. Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat Commun 2011, 2:499.
65. Krautler N.J., Kana V., Kranich J., Tian Y., Perera D., Lemm D., et al. Follicular dendritic cells emerge from ubiquitous perivascular precursors. Cell 2012, 150:194-206.
66. Diaz-Flores L., Gutierrez R., Lopez-Alonso A., Gonzalez R., Varela H. Pericytes as a supplementary source of osteoblasts in periosteal osteogenesis. Clin Orthop Relat Res 1992, 280-286.
67. Grcevic D., Pejda S., Matthews B.G., Repic D., Wang L., Li H., et al. In vivo fate mapping identifies mesenchymal progenitor cells. Stem Cells 2012, 30:187-196.
68. Zhang X., Xie C., Lin A.S., Ito H., Awad H., Lieberman J.R., et al. Periosteal progenitor cell fate in segmental cortical bone graft transplantations: implications for functional tissue engineering. J Bone Miner Res 2005, 20:2124-2137.
69. van Gastel N., Torrekens S., Roberts S.J., Moermans K., Schrooten J., Carmeliet P., et al. Engineering vascularized bone: osteogenic and proangiogenic potential of murine periosteal cells. Stem Cells 2012, 30:2460-2471.
70. Dickson K., Katzman S., Delgado E., Contreras D. Delayed unions and nonunions of open tibial fractures. Correlation with arteriography results. Clin Orthop Relat Res 1994, 189-193.
71. Lammens J., Laumen A., Delport H., Vanlauwe J. The Pentaconcept in skeletal tissue engineering. A combined approach for the repair of bone defects. Acta Orthop Belg 2012, 78:569-573.
72. Giannoudis P.V., Einhorn T.A., Schmidmaier G., Marsh D. The diamond concept-open questions. Injury 2008, 39(Suppl. 2):S5-S8.
73. Giannoni P., Scaglione S., Daga A., Ilengo C., Cilli M., Quarto R. Short-time survival and engraftment of bone marrow stromal cells in an ectopic model of bone regeneration. Tissue Eng Part A 2010, 16:489-499.
74. Muschler G.F., Nakamoto C., Griffith L.G. Engineering principles of clinical cell-based tissue engineering. J Bone Joint Surg Am 2004, 86-A:1541-1558.
75. Santos M.I., Reis R.L. Vascularization in bone tissue engineering: physiology, current strategies, major hurdles and future challenges. Macromol Biosci 2010, 10:12-27.
76. Nomi M., Atala A., Coppi P.D., Soker S. Principals of neovascularization for tissue engineering. Mol Aspects Med 2002, 23:463-483.
77. Takeshita S., Zheng L.P., Brogi E., Kearney M., Pu L.Q., Bunting S., et al. Therapeutic angiogenesis. A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hind limb model. J Clin Invest 1994, 93:662-670.
78. Maes C., Goossens S., Bartunkova S., Drogat B., Coenegrachts L., Stockmans I., et al. Increased skeletal VEGF enhances beta-catenin activity and results in excessively ossified bones. EMBO J 2010, 29:424-441.
79. Chen R.R., Silva E.A., Yuen W.W., Mooney D.J. Spatio-temporal VEGF and PDGF delivery patterns blood vessel formation and maturation. Pharm Res 2007, 24:258-264.
80. Zisch A.H., Lutolf M.P., Hubbell J.A. Biopolymeric delivery matrices for angiogenic growth factors. Cardiovasc Pathol 2003, 12:295-310.
81. Pieper J.S., Hafmans T., van Wachem P.B., van Luyn M.J., Brouwer L.A., Veerkamp J.H., et al. Loading of collagen-heparan sulfate matrices with bFGF promotes angiogenesis and tissue generation in rats. J Biomed Mater Res 2002, 62:185-194.
82. Kaigler D., Wang Z., Horger K., Mooney D.J., Krebsbach P.H. VEGF scaffolds enhance angiogenesis and bone regeneration in irradiated osseous defects. J Bone Miner Res 2006, 21:735-744.
83. Murphy W.L., Simmons C.A., Kaigler D., Mooney D.J. Bone regeneration via a mineral substrate and induced angiogenesis. J Dent Res 2004, 83:204-210.
84. Rabie A.B., Dai J., Xu R. Recombinant AAV-mediated VEGF gene therapy induces mandibular condylar growth. Gene Ther 2007, 14:972-980.
85. Huang Y.C., Kaigler D., Rice K.G., Krebsbach P.H., Mooney D.J. Combined angiogenic and osteogenic factor delivery enhances bone marrow stromal cell-driven bone regeneration. J Bone Miner Res 2005, 20:848-857.
86. Li G., Corsi-Payne K., Zheng B., Usas A., Peng H., Huard J. The dose of growth factors influences the synergistic effect of vascular endothelial growth factor on bone morphogenetic protein 4-induced ectopic bone formation. Tissue Eng Part A 2009, 15:2123-2133.
87. Kim S., von Recum H. Endothelial stem cells and precursors for tissue engineering: cell source, differentiation, selection, and application. Tissue Eng Part B Rev 2008, 14:133-147.
88. Sumpio B.E., Riley J.T., Dardik A. Cells in focus: endothelial cell. Int J Biochem Cell Biol 2002, 34:1508-1512.
89. Garlanda C., Dejana E. Heterogeneity of endothelial cells. Specific markers. Arterioscler Thromb Vasc Biol 1997, 17:1193-1202.
90. Chi J.T., Chang H.Y., Haraldsen G., Jahnsen F.L., Troyanskaya O.G., Chang D.S., et al. Endothelial cell diversity revealed by global expression profiling. Proc Natl Acad Sci U S A 2003, 100:10623-10628.
91. Luttun A., Carmeliet G., Carmeliet P. Vascular progenitors: from biology to treatment. Trends Cardiovasc Med 2002, 12:88-96.
92. Hristov M., Erl W., Weber P.C. Endothelial progenitor cells: isolation and characterization. Trends Cardiovasc Med 2003, 13:201-206.
93. Veleva A.N., Heath D.E., Cooper S.L., Patterson C. Selective endothelial cell attachment to peptide-modified terpolymers. Biomaterials 2008, 29:3656-3661.
94. Fuchs S., Hermanns M.I., Kirkpatrick C.J. Retention of a differentiated endothelial phenotype by outgrowth endothelial cells isolated from human peripheral blood and expanded in long-term cultures. Cell Tissue Res 2006, 326:79-92.
95. Ghanaati S., Fuchs S., Webber M.J., Orth C., Barbeck M., Gomes M.E., et al. Rapid vascularization of starch-poly(caprolactone) in vivo by outgrowth endothelial cells in co-culture with primary osteoblasts. J Tissue Eng Regen Med 2011, 5:e136-e143.
96. Yoon C.H., Hur J., Park K.W., Kim J.H., Lee C.S., Oh I.Y., et al. Synergistic neovascularization by mixed transplantation of early endothelial progenitor cells and late outgrowth endothelial cells: the role of angiogenic cytokines and matrix metalloproteinases. Circulation 2005, 112:1618-1627.
97. Wu H.C., Wang T.W., Kang P.L., Tsuang Y.H., Sun J.S., Lin F.H. Coculture of endothelial and smooth muscle cells on a collagen membrane in the development of a small-diameter vascular graft. Biomaterials 2007, 28:1385-1392.
98. Melero-Martin J.M., De Obaldia M.E., Kang S.Y., Khan Z.A., Yuan L., Oettgen P., et al. Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ Res 2008, 103:194-202.
99. Narayan D., Venkatraman S.S. Effect of pore size and interpore distance on endothelial cell growth on polymers. J Biomed Mater Res A 2008, 87:710-718.
100. Karageorgiou V., Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 2005, 26:5474-5491.
101. Bonfield W. Designing porous scaffolds for tissue engineering. Philos Trans R Soc A Math Phys Eng Sci 2006, 364:227-232.
102. Tsuda Y., Shimizu T., Yamato M., Kikuchi A., Sasagawa T., Sekiya S., et al. Cellular control of tissue architectures using a three-dimensional tissue fabrication technique. Biomaterials 2007, 28:4939-4946.
103. Moroni L., de Wijn J.R., van Blitterswijk C.A. 3D fiber-deposited scaffolds for tissue engineering: influence of pores geometry and architecture on dynamic mechanical properties. Biomaterials 2006, 27:974-985.
104. Santos M.I., Unger R.E., Sousa R.A., Reis R.L., Kirkpatrick C.J. Crosstalk between osteoblasts and endothelial cells co-cultured on a polycaprolactone-starch scaffold and the in vitro development of vascularization. Biomaterials 2009, 30:4407-4415.
105. Unger R.E., Ghanaati S., Orth C., Sartoris A., Barbeck M., Halstenberg S., et al. The rapid anastomosis between prevascularized networks on silk fibroin scaffolds generated in vitro with cocultures of human microvascular endothelial and osteoblast cells and the host vasculature. Biomaterials 2010, 31:6959-6967.
106. Einhorn T. Mechanisms of fracture healing. Hosp Pract 1991, 26(Suppl. 1):41-45.
107. Dimitriou R., Jones E., McGonagle D., Giannoudis P.V. Bone regeneration: current concepts and future directions. BMC Med 2011, 9:66.
108. Kasama T., Isozaki T., Odai T., Matsunawa M., Wakabayashi K., Takeuchi H.T., et al. Expression of angiopoietin-1 in osteoblasts and its inhibition by tumor necrosis factor-alpha and interferon-gamma. Transl Res 2007, 149:265-273.
109. Suzuki T., Miyamoto T., Fujita N., Ninomiya K., Iwasaki R., Toyama Y., et al. Osteoblast-specific angiopoietin 1 overexpression increases bone mass. Biochem Biophys Res Commun 2007, 362:1019-1025.
110. Marie P.J. Fibroblast growth factor signaling controlling bone formation: an update. Gene 2012, 498:1-4.
111. Saadeh P.B., Mehrara B.J., Steinbrech D.S., Spector J.A., Greenwald J.A., Chin G.S., et al. Mechanisms of fibroblast growth factor-2 modulation of vascular endothelial growth factor expression by osteoblastic cells. Endocrinology 2000, 141:2075-2083.
112. Wan M., Cao X. BMP signaling in skeletal development. Biochem Biophys Res Commun 2005, 328:651-657.
113. Deckers M.M., van Bezooijen R.L., van der Horst G., Hoogendam J., van der Bent C., Papapoulos S.E., et al. Bone morphogenetic proteins stimulate angiogenesis through osteoblast-derived vascular endothelial growth factor A. Endocrinology 2002, 143:1545-1553.
114. Minuto F., Palermo C., Arvigo M., Barreca A.M. The IGF system and bone. J Endocrinol Invest 2005, 28:8-10.
115. Hansson H.A., Brandsten C., Lossing C., Petruson K. Transient expression of insulin-like growth factor I immunoreactivity by vascular cells during angiogenesis. Exp Mol Pathol 1989, 50:125-138.
116. Goad D.L., Rubin J., Wang H., Tashjian A.H., Patterson C. Enhanced expression of vascular endothelial growth factor in human SaOS-2 osteoblast-like cells and murine osteoblasts induced by insulin-like growth factor I. Endocrinology 1996, 137:2262-2268.
117. Colciago A., Celotti F., Casati L., Giancola R., Castano S.M., Antonini G., et al. In vitro effects of PDGF isoforms (AA, BB, AB and CC) on migration and proliferation of SaOS-2 osteoblasts and on migration of human osteoblasts. Int J Biomed Sci 2009, 5:380-389.
118. Caplan A.I., Correa D. PDGF in bone formation and regeneration: new insights into a novel mechanism involving MSCs. J Orthop Res 2011, 29:1795-1803.
119. Bouletreau P.J., Warren S.M., Spector J.A., Steinbrech D.S., Mehrara B.J., Longaker M.T. Factors in the fracture microenvironment induce primary osteoblast angiogenic cytokine production. Plast Reconstr Surg 2002, 110:139-148.
120. Chen G., Deng C., Li Y.P. TGF-beta and BMP signaling in osteoblast differentiation and bone formation. Int J Biol Sci 2012, 8:272-288.
121. Yang E.Y., Moses H.L. Transforming growth factor beta 1-induced changes in cell migration, proliferation, and angiogenesis in the chicken chorioallantoic membrane. J Cell Biol 1990, 111:731-741.
122. Saadeh P.B., Mehrara B.J., Steinbrech D.S., Dudziak M.E., Greenwald J.A., Luchs J.S., et al. Transforming growth factor-beta1 modulates the expression of vascular endothelial growth factor by osteoblasts. Am J Physiol 1999, 277:C628-C637.