RESEARCH PROGRESS OF ANGIOGENESIS IN VASCULARIZED TISSUE ENGINEERED BONE_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

DUANXin , LIWei ,  XIANGZhou

Department of Burn and Plastic Surgery, the First Affiliated Hospital of PLA General Hospital, Beijing, 100048, P. R. China;

Corresponding author：

XIANGZhou, Email: xiangzhou15@hotmail.com

Keywords：

Tissue engineered bone; Angiogenesis; Seed cells; Cytokine

DOI：

10.7507/1002-1892.20150050

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To review the research progress of the role of seed cells and related cytokines in angiogenesis of the vascularized tissue engineered bone. Methods The latest literature of tissue engineered bone angiogenesis was reviewed, including the common source of seed cells, biological characteristics, transformation mechanism, related cytokines, and signaling pathways in re-vascularization. Results Microsurgery technique, genetic technique, and co-culture system of vascularized tissue engineered bone have developed to a new level. Moreover, both the induction of introduced pluripotent stem cells and vascular endothelial growth factor-angiopoietins 1 transfected mesenchymal stem cells and endothelial progenitor cells have some advantages for bone regeneration and vascularization. However, all the techniques were not used in clinical practice. Conclusion Using techniques of genetically modified seed cells, related cytokines, and scaffolds may have bright prospects for building vascularized tissue engineered bone.

Citation： DUANXin, LIWei, XIANGZhou. RESEARCH PROGRESS OF ANGIOGENESIS IN VASCULARIZED TISSUE ENGINEERED BONE. Chinese Journal of Reparative and Reconstructive Surgery, 2015, 29(2): 239-244. doi: 10.7507/1002-1892.20150050 Copy

1.	Reichert JC, Saifzadeh S, Wullschleger ME, et al. The challenge of establishing preclinical models for segmental bone defect research. Biomaterials, 2009, 30(12):2149-2163.
2.	Chimutengwende-Gordon M, Khan WS. Advances in the use of stem cells and tissue engineering applications in bone repair. Curr Stem Cell Res Ther, 2012, 7(2):122-126.
3.	Kanczler JM, Oreffo RO. Osteogenesis and angiogenesis:the potential for engineering bone. Eur Cell Mater, 2008, 15:100-114.
4.	Towler DA. The osteogenic-angiogenic interface:novel insights into the biology of bone formation and fracture repair. Curr Osteoporos Rep, 2008, 6(2):67-71.
5.	Nguyen LH, Annabi N, Nikkhah M, et al. Vascularized bone tissue engineering:approaches for potential improvement. Tissue Eng Part B Rev, 2012, 18(5):363-382.
6.	Santos MI, Reis RL. Vascularization in bone tissue engineering:physiology, current strategies, major hurdles and future challenges. Macromol Biosci, 2010, 10(1):12-27.
7.	Khan WS, Longo UG, Adesida A, et al. Stem cell and tissue engineering applications in orthopaedics and musculoskeletal medicine. Stem Cells Int, 2012, 3(3):403170.
8.	Manetti M, Guiducci S, Romano E, et al. Decreased expression of the endothelial cell-derived factor EGFL7 in systemic sclerosis:potential contribution to impaired angiogenesis and vasculogenesis. Arthritis Res Ther, 2013, 15(5):R165.
9.	Toh H, Cao M, Daniels E, et al. Expression of the growth factor progranulin in endothelial cells influences growth and development of blood vessels:a novel mouse model. PLoS One, 2013, 8(5):e64989.
10.	Herzog DP, Dohle E, Bischoff I, et al. Cell communication in a coculture system consisting of outgrowth endothelial cells and primary osteoblasts. Biomed Res Int, 2014, 4(4):320123.
11.	Liu X, Zhang G, Hou C, et al. Vascularized bone tissue formation induced by fiber-reinforced scaffolds cultured with osteoblasts and endothelial cells. Biomed Res Int, 2013, 12(12):854917.
12.	郝增涛, 冯卫, 郝廷, 等. BMSCs来源成骨细胞和内皮细胞复合壳聚糖-羟基磷灰石多孔支架构建血管化组织工程骨研究. 中国修复重建外科杂志, 2012, 26(4):489-494.
13.	Ren L, Kang Y, Browne C, et al. Fabrication, vascularization and osteogenic properties of a novel synthetic biomimetic induced membrane for the treatment of large bone defects. Bone, 2014, 7(64):173-182.
14.	Kaigler D, Pagni G, Park CH, et al. Stem cell therapy for craniofacial bone regeneration:a randomized, controlled feasibility trial. Cell Transplant, 2013, 22(5):767-777.
15.	Kaigler D, Avila G, Wisner-Lynch L, et al. Platelet-derived growth factor applications in periodontal and peri-implant bone regeneration. Expert Opin Biol Ther, 2011, 11(3):375-385.
16.	Kaigler D, Silva EA, Mooney DJ. Guided bone regeneration using injectable vascular endothelial growth factor delivery gel. J Periodontol, 2013, 84(2):230-238.
17.	Wenger A, Kowalewski N, Stahl A, et al. Development and characterization of a spheroidal coculture model of endothelial cells and fibroblasts for improving angiogenesis in tissue engineering. Cells Tissues Organs, 2005, 181(2):80-88.
18.	Matsumoto T, Kuroda R, Mifune Y, et al. Circulating endothelial/skeletal progenitor cells for bone regeneration and healing. Bone, 2008, 43(3):434-439.
19.	Seong JM, Kim BC, Park JH, et al. Stem cells in bone tissue engineering. Biomed Mater, 2010, 5(60):062001.
20.	Richardson MR, Yoder MC. Endothelial progenitor cells:quo vadis? J Mol Cell Cardiol, 2011, 50(2):266-272.
21.	Li Q, Wang Z. Influence of mesenchymal stem cells with endothelial progenitor cells in co-culture on osteogenesis and angiogenesis:an in vitro study. Arch Med Res, 2013, 44(7):504-513.
22.	Keramaris NC, Kaptanis S, Moss HL, et al. Endothelial progenitor cells (EPCs) and mesenchymal stem cells (MSCs) in bone healing. Curr Stem Cell Res Ther, 2012, 7(4):293-301.
23.	Seebach C, Henrich D, Wilhelm K, et al. Endothelial progenitor cells improve directly and indirectly early vascularization of mesenchymal stem cell-driven bone regeneration in a critical bone defect in rats. Cell Transplant, 2012, 21(8):1667-1677.
24.	Seebach C, Henrich D, Kahling C, et al. Endothelial progenitor cells and mesenchymal stem cells seeded onto beta-TCP granules enhance early vascularization and bone healing in a critical-sized bone defect in rats. Tissue Eng Part A, 2010, 16(6):1961-1970.
25.	Takebe T, Zhang RR, Koike H, et al. Generation of a vascularized and functional human liver from an iPSC-derived organ bud transplant. Nat Protoc, 2014, 9(2):396-409.
26.	Takebe T, Sekine K, Enomura M, et al. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature, 2013, 499(7459):481-484.
27.	Takase O, Yoshikawa M, Idei M, et al. The role of NF-κB signaling in the maintenance of pluripotency of human induced pluripotent stem cells. PLoS One, 2013, 8(2):e56399.
28.	Ho R, Papp B, Hoffman JA, et al. Stage-specific regulation of reprogramming to induced pluripotent stem cells by Wnt signaling and T cell factor proteins. Cell Rep, 2013, 3(6):2113-2126.
29.	Gong H, Yan Y, Fang B, et al. Knockdown of nucleosome assembly protein 1-like 1 induces mesoderm formation and cardiomyogenesis via notch signaling in murine-induced pluripotent stem cells. Stem Cells, 2014, 32(7):1759-1773.
30.	Tan KS, Tamura K, Lai MI, et al. Molecular pathways governing development of vascular endothelial cells from ES/iPS cells. Stem Cell Rev, 2013, 9(5):586-598.
31.	Kane NM, Xiao Q, Baker AH, et al. Pluripotent stem cell differentiation into vascular cells:a novel technology with promises for vascular re(generation). Pharmacol Ther, 2011, 129(1):29-49.
32.	Zhang L, Xu Q. Stem/Progenitor cells in vascular regeneration. Arterioscler Thromb Vasc Biol, 2014, 34(6):1114-1119.
33.	Herzog DP, Dohle E, Bischoff I, et al. Cell communication in a coculture system consisting of outgrowth endothelial cells and primary osteoblasts. Biomed Res Int, 2014, 4(4):320123.
34.	Jabbarzadeh E, Starnes T, Khan YM, et al. Induction of angiogenesis in tissue-engineered scaffolds designed for bone repair:a combined gene therapy-cell transplantation approach. Proc Natl Acad Sci USA, 2008, 105(32):11099-11104.
35.	Saran U, Piperni SG, Chatterjee S. Role of angiogenesis in bone repair. Arch Biochem Biophys, 2014, 11(561):109-117.
36.	Bry M, Kivela R, Leppanen VM, et al. Vascular Endothelial Growth Factor-B in Physiology and Disease. Physiol Rev, 2014, 94(2):779-794.
37.	Alfaidy N, Hoffmann P, Boufettal H, et al. The Multiple Roles of EG-VEGF/PROK1 in Normal and Pathological Placental Angiogenesis. Biomed Res Int, 2014, 5(5):451906.
38.	Koç A, Finkenzeller G, Elçin AE, et al. Evaluation of adenoviral vascular endothelial growth factor-activated chitosan/hydroxyapatite scaffold for engineering vascularized bone tissue using human osteoblasts:In vitro and in vivo studies. J Biomater Appl, 2014, 29(5):748-760.
39.	Ferretti C, Vozzi G, Falconi M, et al. Role of IGF1 and IGF1/VEGF on human mesenchymal stromal cells in bone healing:two sources and two fates. Tissue Eng Part A, 2014, 20(17-18):2473-2482.
40.	Zhou Y, Guan X, Yu M, et al. Angiogenic/osteogenic response of BMMSCs on bone derived scaffold:effect of hypoxia and role of PI3K/Akt mediated VEGF/VEGFR pathway. Biotechnol J, 2014, 9(7):944-953.
41.	Herzog DP, Dohle E, Bischoff I, et al. Cell communication in a coculture system consisting of outgrowth endothelial cells and primary osteoblasts. Biomed Res Int, 2014, 4(4):320123.
42.	Fagiani E, Christofori G. Angiopoietins in angiogenesis. Cancer Lett, 2013, 328(1):18-26.
43.	Hall K, Ran S. Regulation of tumor angiogenesis by the local environment. Front Biosci, 2010, 15(15):195-212.
44.	Hou H, Zhang X, Tang T, et al. Enhancement of bone formation by genetically engineered bone marrow stromal cells expressing BMP-2, VEGF and angiopoietin-1. Biotechnol Lett, 2009, 31(8):1183-1189.
45.	Nakasa T, Ishida O, Sunagawa T, et al. Feasibility of prefabricated vascularized bone graft using the combination of FGF-2 and vascular bundle implantation within hydroxyapatite for osteointegration. J Biomed Mater Res A, 2008, 85(4):1090-1095.
46.	Gavalas NG, Liontos M, Trachana SP, et al. Angiogenesis-related pathways in the pathogenesis of ovarian cancer. Int J Mol Sci, 2013, 14(8):15885-15909.
47.	Munoz-Chapuli R. Evolution of angiogenesis. Int J Dev Biol, 2011, 55(4-5):345-351.
48.	Gothard D, Smith EL, Kanczler JM, et al. Tissue engineered bone using select growth factors:A comprehensive review of animal studies and clinical translation studies in man. Eur Cell Mater, 2014, 10(28):166-208.
49.	Okada M, Yano K, Namikawa T, et al. Bone morphogenetic protein-2 retained in synthetic polymer/beta-tricalcium phosphate composite promotes hypertrophy of a vascularized long bone graft in rabbits. Plast Reconstr Surg, 2011, 127(1):98-106.
50.	Yang P, Huang X, Shen J, et al. Development of a new pre-vascularized tissue-engineered construct using pre-differentiated rADSCs, arteriovenous vascular bundle and porous nano-hydroxyapatide-polyamide 66 scaffold. BMC Musculoskelet Disord, 2013, 14(14):318.
51.	Cui Q, Dighe AS, Irvine JN. Combined angiogenic and osteogenic factor delivery for bone regenerative engineering. Curr Pharm Des, 2013, 19(19):3374-3383.
52.	Guerrero J, Catros S, Derkaoui SM, et al. Cell interactions between human progenitor-derived endothelial cells and human mesenchymal stem cells in a three-dimensional macroporous polysaccharide-based scaffold promote osteogenesis. Acta Biomater, 2013, 9(9):8200-8213.
53.	Liu Y, Teoh SH, Chong MS, et al. Contrasting effects of vasculogenic induction upon biaxial bioreactor stimulation of mesenchymal stem cells and endothelial progenitor cells cocultures in three-dimensional scaffolds under in vitro and in vivo paradigms for vascularized bone tissue engineering. Tissue Eng Part A, 2013, 19(7-8):893-904.
54.	Kim J, Kim HN, Lim KT, et al. Synergistic effects of nanotopography and co-culture with endothelial cells on osteogenesis of mesenchymal stem cells. Biomaterials, 2013, 34(30):7257-7268.
55.	Zheng L, Yang J, Fan H, et al. Material-induced chondrogenic differentiation of mesenchymal stem cells is material-dependent. Exp Ther Med, 2014, 7(5):1147-1150.
56.	Jung O, Hanken H, Smeets R, et al. Osteogenic Differentiation of Mesenchymal Stem Cells in Fibrin-Hydroxyapatite Matrix in a 3-Dimensional Mesh Scaffold. In Vivo, 2014, 28(4):477-482.
57.	Klopper J, Lindenmaier W, Fiedler U, et al. High efficient adenoviral-mediated VEGF and Ang-1 gene delivery into osteogenically differentiated human mesenchymal stem cells. Microvasc Res, 2008, 75(1):83-90.
58.	Chong AK, Ang AD, Goh JC, et al. Bone marrow-derived mesenchymal stem cells influence early tendon-healing in a rabbit achilles tendon model. J Bone Joint Surg (Am), 2007, 89(1):74-81.
59.	Ren W, Zhang R, Wu B, et al. Effects of SU5416 and a vascular endothelial growth factor neutralizing antibody on wear debris-induced inflammatory osteolysis in a mouse model. J Inflamm Res, 2011, 3(4):29-38.
60.	Viateau V, Bensidhoum M, Pélissier P, et al. Use of the induced membrane technique for bone tissue engineering purposes:animal studies. Orthop Clin North Am, 2010, 41(1):49-56.

1. Reichert JC, Saifzadeh S, Wullschleger ME, et al. The challenge of establishing preclinical models for segmental bone defect research. Biomaterials, 2009, 30(12):2149-2163.
2. Chimutengwende-Gordon M, Khan WS. Advances in the use of stem cells and tissue engineering applications in bone repair. Curr Stem Cell Res Ther, 2012, 7(2):122-126.
3. Kanczler JM, Oreffo RO. Osteogenesis and angiogenesis:the potential for engineering bone. Eur Cell Mater, 2008, 15:100-114.
4. Towler DA. The osteogenic-angiogenic interface:novel insights into the biology of bone formation and fracture repair. Curr Osteoporos Rep, 2008, 6(2):67-71.
5. Nguyen LH, Annabi N, Nikkhah M, et al. Vascularized bone tissue engineering:approaches for potential improvement. Tissue Eng Part B Rev, 2012, 18(5):363-382.
6. Santos MI, Reis RL. Vascularization in bone tissue engineering:physiology, current strategies, major hurdles and future challenges. Macromol Biosci, 2010, 10(1):12-27.
7. Khan WS, Longo UG, Adesida A, et al. Stem cell and tissue engineering applications in orthopaedics and musculoskeletal medicine. Stem Cells Int, 2012, 3(3):403170.
8. Manetti M, Guiducci S, Romano E, et al. Decreased expression of the endothelial cell-derived factor EGFL7 in systemic sclerosis:potential contribution to impaired angiogenesis and vasculogenesis. Arthritis Res Ther, 2013, 15(5):R165.
9. Toh H, Cao M, Daniels E, et al. Expression of the growth factor progranulin in endothelial cells influences growth and development of blood vessels:a novel mouse model. PLoS One, 2013, 8(5):e64989.
10. Herzog DP, Dohle E, Bischoff I, et al. Cell communication in a coculture system consisting of outgrowth endothelial cells and primary osteoblasts. Biomed Res Int, 2014, 4(4):320123.
11. Liu X, Zhang G, Hou C, et al. Vascularized bone tissue formation induced by fiber-reinforced scaffolds cultured with osteoblasts and endothelial cells. Biomed Res Int, 2013, 12(12):854917.
12. 郝增涛, 冯卫, 郝廷, 等. BMSCs来源成骨细胞和内皮细胞复合壳聚糖-羟基磷灰石多孔支架构建血管化组织工程骨研究. 中国修复重建外科杂志, 2012, 26(4):489-494.
13. Ren L, Kang Y, Browne C, et al. Fabrication, vascularization and osteogenic properties of a novel synthetic biomimetic induced membrane for the treatment of large bone defects. Bone, 2014, 7(64):173-182.
14. Kaigler D, Pagni G, Park CH, et al. Stem cell therapy for craniofacial bone regeneration:a randomized, controlled feasibility trial. Cell Transplant, 2013, 22(5):767-777.
15. Kaigler D, Avila G, Wisner-Lynch L, et al. Platelet-derived growth factor applications in periodontal and peri-implant bone regeneration. Expert Opin Biol Ther, 2011, 11(3):375-385.
16. Kaigler D, Silva EA, Mooney DJ. Guided bone regeneration using injectable vascular endothelial growth factor delivery gel. J Periodontol, 2013, 84(2):230-238.
17. Wenger A, Kowalewski N, Stahl A, et al. Development and characterization of a spheroidal coculture model of endothelial cells and fibroblasts for improving angiogenesis in tissue engineering. Cells Tissues Organs, 2005, 181(2):80-88.
18. Matsumoto T, Kuroda R, Mifune Y, et al. Circulating endothelial/skeletal progenitor cells for bone regeneration and healing. Bone, 2008, 43(3):434-439.
19. Seong JM, Kim BC, Park JH, et al. Stem cells in bone tissue engineering. Biomed Mater, 2010, 5(60):062001.
20. Richardson MR, Yoder MC. Endothelial progenitor cells:quo vadis? J Mol Cell Cardiol, 2011, 50(2):266-272.
21. Li Q, Wang Z. Influence of mesenchymal stem cells with endothelial progenitor cells in co-culture on osteogenesis and angiogenesis:an in vitro study. Arch Med Res, 2013, 44(7):504-513.
22. Keramaris NC, Kaptanis S, Moss HL, et al. Endothelial progenitor cells (EPCs) and mesenchymal stem cells (MSCs) in bone healing. Curr Stem Cell Res Ther, 2012, 7(4):293-301.
23. Seebach C, Henrich D, Wilhelm K, et al. Endothelial progenitor cells improve directly and indirectly early vascularization of mesenchymal stem cell-driven bone regeneration in a critical bone defect in rats. Cell Transplant, 2012, 21(8):1667-1677.
24. Seebach C, Henrich D, Kahling C, et al. Endothelial progenitor cells and mesenchymal stem cells seeded onto beta-TCP granules enhance early vascularization and bone healing in a critical-sized bone defect in rats. Tissue Eng Part A, 2010, 16(6):1961-1970.
25. Takebe T, Zhang RR, Koike H, et al. Generation of a vascularized and functional human liver from an iPSC-derived organ bud transplant. Nat Protoc, 2014, 9(2):396-409.
26. Takebe T, Sekine K, Enomura M, et al. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature, 2013, 499(7459):481-484.
27. Takase O, Yoshikawa M, Idei M, et al. The role of NF-κB signaling in the maintenance of pluripotency of human induced pluripotent stem cells. PLoS One, 2013, 8(2):e56399.
28. Ho R, Papp B, Hoffman JA, et al. Stage-specific regulation of reprogramming to induced pluripotent stem cells by Wnt signaling and T cell factor proteins. Cell Rep, 2013, 3(6):2113-2126.
29. Gong H, Yan Y, Fang B, et al. Knockdown of nucleosome assembly protein 1-like 1 induces mesoderm formation and cardiomyogenesis via notch signaling in murine-induced pluripotent stem cells. Stem Cells, 2014, 32(7):1759-1773.
30. Tan KS, Tamura K, Lai MI, et al. Molecular pathways governing development of vascular endothelial cells from ES/iPS cells. Stem Cell Rev, 2013, 9(5):586-598.
31. Kane NM, Xiao Q, Baker AH, et al. Pluripotent stem cell differentiation into vascular cells:a novel technology with promises for vascular re(generation). Pharmacol Ther, 2011, 129(1):29-49.
32. Zhang L, Xu Q. Stem/Progenitor cells in vascular regeneration. Arterioscler Thromb Vasc Biol, 2014, 34(6):1114-1119.
33. Herzog DP, Dohle E, Bischoff I, et al. Cell communication in a coculture system consisting of outgrowth endothelial cells and primary osteoblasts. Biomed Res Int, 2014, 4(4):320123.
34. Jabbarzadeh E, Starnes T, Khan YM, et al. Induction of angiogenesis in tissue-engineered scaffolds designed for bone repair:a combined gene therapy-cell transplantation approach. Proc Natl Acad Sci USA, 2008, 105(32):11099-11104.
35. Saran U, Piperni SG, Chatterjee S. Role of angiogenesis in bone repair. Arch Biochem Biophys, 2014, 11(561):109-117.
36. Bry M, Kivela R, Leppanen VM, et al. Vascular Endothelial Growth Factor-B in Physiology and Disease. Physiol Rev, 2014, 94(2):779-794.
37. Alfaidy N, Hoffmann P, Boufettal H, et al. The Multiple Roles of EG-VEGF/PROK1 in Normal and Pathological Placental Angiogenesis. Biomed Res Int, 2014, 5(5):451906.
38. Koç A, Finkenzeller G, Elçin AE, et al. Evaluation of adenoviral vascular endothelial growth factor-activated chitosan/hydroxyapatite scaffold for engineering vascularized bone tissue using human osteoblasts:In vitro and in vivo studies. J Biomater Appl, 2014, 29(5):748-760.
39. Ferretti C, Vozzi G, Falconi M, et al. Role of IGF1 and IGF1/VEGF on human mesenchymal stromal cells in bone healing:two sources and two fates. Tissue Eng Part A, 2014, 20(17-18):2473-2482.
40. Zhou Y, Guan X, Yu M, et al. Angiogenic/osteogenic response of BMMSCs on bone derived scaffold:effect of hypoxia and role of PI3K/Akt mediated VEGF/VEGFR pathway. Biotechnol J, 2014, 9(7):944-953.
41. Herzog DP, Dohle E, Bischoff I, et al. Cell communication in a coculture system consisting of outgrowth endothelial cells and primary osteoblasts. Biomed Res Int, 2014, 4(4):320123.
42. Fagiani E, Christofori G. Angiopoietins in angiogenesis. Cancer Lett, 2013, 328(1):18-26.
43. Hall K, Ran S. Regulation of tumor angiogenesis by the local environment. Front Biosci, 2010, 15(15):195-212.
44. Hou H, Zhang X, Tang T, et al. Enhancement of bone formation by genetically engineered bone marrow stromal cells expressing BMP-2, VEGF and angiopoietin-1. Biotechnol Lett, 2009, 31(8):1183-1189.
45. Nakasa T, Ishida O, Sunagawa T, et al. Feasibility of prefabricated vascularized bone graft using the combination of FGF-2 and vascular bundle implantation within hydroxyapatite for osteointegration. J Biomed Mater Res A, 2008, 85(4):1090-1095.
46. Gavalas NG, Liontos M, Trachana SP, et al. Angiogenesis-related pathways in the pathogenesis of ovarian cancer. Int J Mol Sci, 2013, 14(8):15885-15909.
47. Munoz-Chapuli R. Evolution of angiogenesis. Int J Dev Biol, 2011, 55(4-5):345-351.
48. Gothard D, Smith EL, Kanczler JM, et al. Tissue engineered bone using select growth factors:A comprehensive review of animal studies and clinical translation studies in man. Eur Cell Mater, 2014, 10(28):166-208.
49. Okada M, Yano K, Namikawa T, et al. Bone morphogenetic protein-2 retained in synthetic polymer/beta-tricalcium phosphate composite promotes hypertrophy of a vascularized long bone graft in rabbits. Plast Reconstr Surg, 2011, 127(1):98-106.
50. Yang P, Huang X, Shen J, et al. Development of a new pre-vascularized tissue-engineered construct using pre-differentiated rADSCs, arteriovenous vascular bundle and porous nano-hydroxyapatide-polyamide 66 scaffold. BMC Musculoskelet Disord, 2013, 14(14):318.
51. Cui Q, Dighe AS, Irvine JN. Combined angiogenic and osteogenic factor delivery for bone regenerative engineering. Curr Pharm Des, 2013, 19(19):3374-3383.
52. Guerrero J, Catros S, Derkaoui SM, et al. Cell interactions between human progenitor-derived endothelial cells and human mesenchymal stem cells in a three-dimensional macroporous polysaccharide-based scaffold promote osteogenesis. Acta Biomater, 2013, 9(9):8200-8213.
53. Liu Y, Teoh SH, Chong MS, et al. Contrasting effects of vasculogenic induction upon biaxial bioreactor stimulation of mesenchymal stem cells and endothelial progenitor cells cocultures in three-dimensional scaffolds under in vitro and in vivo paradigms for vascularized bone tissue engineering. Tissue Eng Part A, 2013, 19(7-8):893-904.
54. Kim J, Kim HN, Lim KT, et al. Synergistic effects of nanotopography and co-culture with endothelial cells on osteogenesis of mesenchymal stem cells. Biomaterials, 2013, 34(30):7257-7268.
55. Zheng L, Yang J, Fan H, et al. Material-induced chondrogenic differentiation of mesenchymal stem cells is material-dependent. Exp Ther Med, 2014, 7(5):1147-1150.
56. Jung O, Hanken H, Smeets R, et al. Osteogenic Differentiation of Mesenchymal Stem Cells in Fibrin-Hydroxyapatite Matrix in a 3-Dimensional Mesh Scaffold. In Vivo, 2014, 28(4):477-482.
57. Klopper J, Lindenmaier W, Fiedler U, et al. High efficient adenoviral-mediated VEGF and Ang-1 gene delivery into osteogenically differentiated human mesenchymal stem cells. Microvasc Res, 2008, 75(1):83-90.
58. Chong AK, Ang AD, Goh JC, et al. Bone marrow-derived mesenchymal stem cells influence early tendon-healing in a rabbit achilles tendon model. J Bone Joint Surg (Am), 2007, 89(1):74-81.
59. Ren W, Zhang R, Wu B, et al. Effects of SU5416 and a vascular endothelial growth factor neutralizing antibody on wear debris-induced inflammatory osteolysis in a mouse model. J Inflamm Res, 2011, 3(4):29-38.
60. Viateau V, Bensidhoum M, Pélissier P, et al. Use of the induced membrane technique for bone tissue engineering purposes:animal studies. Orthop Clin North Am, 2010, 41(1):49-56.

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RESEARCH PROGRESS OF ANGIOGENESIS IN VASCULARIZED TISSUE ENGINEERED BONE

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