RESEARCH PROGRESS OF CO-CULTURE SYSTEM FOR CONSTRUCTING VASCULARIZED TISSUE ENGINEERED BONE_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

FUWeili ,  XIANGZhou

Department of Orthopedics, West China Hospital, Sichuan University, Chengdu Sichuan, 610041, P. R. China;

Corresponding author：

XIANGZhou, Email: xiangzhou15@hotmail.com

Keywords：

Vascularized tissue engineered bone; Endothelial progenitor cells; Mesenchymal stem cells; Co-culture system; Bone regeneration

DOI：

10.7507/1002-1892.20140039

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To review the research progress of the co-culture system for constructing vascularized tissue engineered bone. Methods The recent literature concerning the co-culture system for constructing vascularized tissue engineered bone was reviewed, including the selection of osteogenic and endothelial lineages, the design and surface modification of scaffolds, the models and dimensions of the co-culture system, the mechanism, the culture conditions, and their application progress. Results The construction of vascularized tissue engineered bone is the prerequisite for their survival and further clinical application in vivo. Mesenchymal stem cells (owning the excellent osteogenic potential) and endothelial progenitor cells (capable of directional differentiation into endothelial cell) are considered as attractive cell types for the co-culture system to construct vascularized tissue engineered bone. The culture conditions need to be further optimized. Furthermore, how to achieve the clinical goals of minimal invasion and autologous transplantation also need to be further studied. Conclusion The strategy of the co-culture system for constructing vascularized tissue engineered bone would have a very broad prospects for clinical application in future.

Citation： FUWeili, XIANGZhou. RESEARCH PROGRESS OF CO-CULTURE SYSTEM FOR CONSTRUCTING VASCULARIZED TISSUE ENGINEERED BONE. Chinese Journal of Reparative and Reconstructive Surgery, 2014, 28(2): 179-185. doi: 10.7507/1002-1892.20140039 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.	Woodruff MA,Lange C,Reichert J,et al.Bone tissue engineering:from bench to bedside.Mater Today,2012,15(10):430-435.
4.	Güven S,Mehrkens A,Saxer F,et al.Engineering of large osteogenic grafts with rapid engraftment capacity using mesenchymal and endothelial progenitors from human adipose tissue.Biomaterials,2011,32(25):5801-5809.
5.	Potier E,Ferreira E,Meunier A,et al.Prolonged hypoxia concomitant with serum deprivation induces massive human mesenchymal stem cell death.Tissue Eng,2007,13(6):1325-1331.
6.	Hsiong SX,Mooney DJ.Regeneration of vascularized bone.Periodontol 2000,2006,41:109-122.
7.	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.
8.	Das A,Botchwey E.Evaluation of Angiogenesis and Osteogenesis.Tissue Eng Part B Rev,2011,17(6):403-414.
9.	Traktuev DO,Prater DN,Merfeld-Clauss S,et al.Robust functional vascular network formation in vivo by cooperation of adipose progenitor and endothelial cells.Circ Res,2009,104(12):1410-1420.
10.	Lokmic Z,Mitchell GM.Engineering the microcirculation.Tissue Eng Part B Rev,2008,14(1):87-103.
11.	Janardhanan S,Wang MO,Fisher JP.Coculture strategies in bone tissue engineering:the impact of culture conditions on pluripotent stem cell populations.Tissue Eng Part B Rev,2012,18(4):312-321.
12.	Szpalski C,Barbaro M,Sagebin F,et al.Bone tissue engineering:current strategies and techniques-part Ⅱ:Cell types.Tissue Eng Part B Rev,2012,18(4):258-269.
13.	Seong JM,Kim BC,Park JH,et al.Stem cells in bone tissue engineering.Biomed Mater,2010,5(6):062001.
14.	Zhang F,Citra F,Wang DA.Prospects of induced pluripotent stem cell technology in regenerative medicine.Tissue Eng Part B Rev,2011,17(2):115-124.
15.	Walia B,Satija N,Tripathi RP,et al.Induced pluripotent stem cells:fundamentals and applications of the reprogramming process and its ramifications on regenerative medicine.Stem Cell Rev,2012,8(1):100-115.
16.	Fuchs S,Jiang X,Schmidt H,et al.Dynamic processes involved in the pre-vascularization of silk fibroin constructs for bone regeneration using outgrowth endothelial cells.Biomaterials,2009,30(7):1329-1338.
17.	Fuchs S,Hofmann A,Kirkpatrick C.Microvessel-like structures from outgrowth endothelial cells from human peripheral blood in 2-dimensional and 3-dimensional co-cultures with osteoblastic lineage cells.Tissue Eng,2007,13(10):2577-2588.
18.	Bianco P,Robey PG,Simmons PJ.Mesenchymal stem cells:revisiting history,concepts,and assays.Cell Stem Cell,2008,2(4):313-319.
19.	Bieback K,Kern S,Kocaomer A,et al.Comparing mesenchymal stromal cells from different human tissues:Bone marrow,adipose tissue and umbilical cord blood.Biomed Mater Eng,2008,18(1 Suppl):S71-76.
20.	Ksiazek K.A comprehensive review on mesenchymal stem cell growth and senescence.Rejuvenation Res,2009,12(2):105-116.
21.	Zhu H,Guo ZK,Jiang XX,et al.A protocol for isolation and culture of mesenchymal stem cells from mouse compact bone.Nat Protoc,2010,5(3):550-560.
22.	Filardo G,Madry H,Jelic M,et al.Mesenchymal stem cells for the treatment of cartilage lesions:from preclinical findings to clinical application in orthopaedics.Knee Surg Sports Traumatol Arthrosc,2013,21(8):1717-1729.
23.	Lei HL,Yu B,Huang Z,et al.Comparative analysis of mesenchymal stem cells from adult mouse adipose,muscle,and fetal muscle.Mol Biol Rep,2013,40(2):885-892.
24.	Tsai CC,Huang TF,Ma HL,et al.Isolation of mesenchymal stem cells from shoulder rotator cuff:a potential source for muscle and tendon repair.Cell Transplant,2013,22(3):413-422.
25.	Kisiel AH,McDuffee LA,Masaoud E,et al.Isolation,characterization,and in vitro proliferation of canine mesenchymal stem cells derived from bone marrow,adipose tissue,muscle,and periosteum.Am J Vet Res,2012,73(8):1305-1317.
26.	De Bari C,Dell'Accio F,Tylzanowski P,et al.Multipotent mesenchymal stem cells from adult human synovial membrane.Arthritis Rheum,2001,44(8):1928-1942.
27.	Fu WL,Zhang JY,Fu X,et al.Comparative study of the biological characteristics of mesenchymal stem cells from bone marrow and peripheral blood of rats.Tissue Eng Part A,2012,18(17-18):1793-1803.
28.	Valenzuela CD,Allori AC,Reformat DD,et al.Characterization of adipose-derived mesenchymal stem cell combinations for vascularized bone engineering.Tissue Eng Part A,2013,19(11-12):1373-1385.
29.	Guillotin B,Bareille R,Bourget C,et al.Interaction between human umbilical vein endothelial cells and human osteoprogenitors triggers pleiotropic effect that may support osteoblastic function.Bone,2008,42(6):1080-1091.
30.	Grellier M,Bordenave L,Amedee J.Cell-to-cell communication between osteogenic and endothelial lineages:implications for tissue engineering.Trends Biotechnol,2009,27(10):562-571.
31.	Unger RE,Sartoris A,Peters K,et al.Tissue-like self-assembly in cocultures of endothelial cells and osteoblasts and the formation of microcapillary-like structures on three-dimensional porous biomaterials.Biomaterials,2007,28(27):3965-3976.
32.	Rouwkema J,Westerweel PE,de Boer J,et al.The use of endothelial progenitor cells for prevascularized bone tissue engineering.Tissue Engi Part A,2009,15(8):2015-2027.
33.	Hung SC,Pochampally RR,Chen SC,et al.Angiogenic effects of human multipotent stromal cell conditioned medium activate the PI3K-Akt pathway in hypoxic endothelial cells to inhibit apoptosis,increase survival,and stimulate angiogenesis.Stem Cells,2007,25(9):2363-2370.
34.	Matsumoto T,Kuroda R,Mifune Y,et al.Circulating endothelial/skeletal progenitor cells for bone regeneration and healing.Bone,2008,43(3):434-439.
35.	Richardson MR,Yoder MC.Endothelial progenitor cells:quo vadis? J Mol Cell Cardiol,2011,50(2):266-272.
36.	Lin RZ,Dreyzin A,Aamodt K,et al.Functional endothelial progenitor cells from cryopreserved umbilical cord blood.Cell transplantation,2011,20(4):515-522.
37.	Chen JK,Deng YP,Jiang GJ,et al.Establishment of tube formation assay of bone marrow-derived endothelial progenitor cells.CNS Neurosci Ther,2013,19(7):533-535.
38.	Xue S,Zhang HT,Zhang P,et al.Functional endothelial progenitor cells derived from adipose tissue show beneficial effect on cell therapy of traumatic brain injury.Neurosci Lett,2010,473(3):186-191.
39.	Amini AR,Laurencin CT,Nukavarapu SP.Differential analysis of peripheral blood-and bone marrow-derived endothelial progenitor cells for enhanced vascularization in bone tissue engineering.J Orthop Res,2012,30(9):1507-1515.
40.	Dariima T,Jin GZ,Lee EJ,et al.Cooperation between osteoblastic cells and endothelial cells enhances their phenotypic responses and improves osteoblast function.Biotechnol Lett,2013,35(7):1135-1143.
41.	Thein-Han W,Xu HH.Prevascularization of a gas-foaming macroporous calcium phosphate cement scaffold via coculture of human umbilical vein endothelial cells and osteoblasts.Tissue Eng Part A,2013,19(15-16):1675-1685.
42.	Lee JH,Kim SW,Kim UK,et al.Generation of osteogenic construct using periosteal-derived osteoblasts and polydioxanone/pluronic F127 scaffold with periosteal-derived CD146 positive endothelial-like cells.J Biomed Mater Res Part A,2013,101(1):942-953.
43.	Shah AR,Shah SR,Oh S,et al.Migration of co-cultured endothelial cells and osteoblasts in composite hydroxyapatite/polylactic acid scaffolds.Ann Biomed Eng,2011,39(10):2501-2509.
44.	Dissanayaka WL,Zhan X,Zhang CF,et al.Coculture of dental pulp stem cells with endothelial cells enhances osteo-/odontogenic and angiogenic potential in vitro.J Endodont,2012,38(4):454-463.
45.	Correia C,Grayson WL,Park M,et al.In vitro model of vascularized bone:synergizing vascular development and osteogenesis.PLoS One,2011,6(12):e28352.
46.	Kang Y,Kim S,Fahrenholtz M,et al.Osteogenic and angiogenic potentials of monocultured and co-cultured human-bone-marrow-derived mesenchymal stem cells and human-umbilical-vein endothelial cells on three-dimensional porous beta-tricalcium phosphate scaffold.Acta biomaterialia,2013,9(1):4906-4915.
47.	Grellier M,Granja PL,Fricain JC,et al.The effect of the co-immobilization of human osteoprogenitors and endothelial cells within alginate microspheres on mineralization in a bone defect.Biomaterials,2009,30(19):3271-3278.
48.	Kim JY,Jin GZ,Park IS,et al.Evaluation of solid free-form fabrication-based scaffolds seeded with osteoblasts and human umbilical vein endothelial cells for use in vivo osteogenesis.Tissue Eng Part A,2010,16(7):2229-2236.
49.	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.
50.	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.
51.	Duttenhoefer F,Egli S,Benneker LM,et al.Coculture of endothelial progenitor cells (EPC) and coculture of endothelial progenitor cells (EPC) and mesenchymal stem cells (MSC) in polyurethane scaffolds (PU) promotes simultaneously implant neo-vascularization and bone neo-formation.J Tissue Eng Regen M,2012,6(Suppl 1):310-311.
52.	Szpalski C,Wetterau M,Barr J,et al.Bone tissue engineering:current strategies and techniques-part I:Scaffolds.Tissue Eng Part B Rev,2012,18(4):246-257.
53.	Hofmann A,Ritz U,Verrier S,et al.The effect of human osteoblasts on proliferation and neo-vessel formation of human umbilical vein endothelial cells in a long-term 3D co-culture on polyurethane scaffolds.Biomaterials,2008,29(31):4217-4226.
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.	Hu X,Neoh KG,Zhang JY,et al.Immobilization strategy for optimizing VEGF's concurrent bioactivity towards endothelial cells and osteoblasts on implant surfaces.Biomaterials,2012,33(32):8082-8093.
56.	Ma J,van den Beucken JJJ,Yang F,et al.Coculture of osteoblasts and endothelial cells:optimization of culture medium and cell ratio.Tissue Eng Part C Methods,2011,17(3):349-357.
57.	Kolbe M,Xiang Z,Dohle E,et al.Paracrine effects influenced by cell culture medium and consequences on microvessel-like structures in cocultures of mesenchymal stem cells and outgrowth endothelial Cells.Tissue Eng Part A,2011,17(17-18):2199-2212.
58.	Cenni E,Perut F,Baldini N.In vitro models for the evaluation of angiogenic potential in bone engineering.Acta pharmacologica Sinica,2011,32(1):21-30.
59.	Villars F,Guillotin B,Amedee T,et al.Effect of HUVEC on human osteoprogenitor cell differentiation needs heterotypic gap junction communication.AmJ Physiol Cell Physiol,2002,282(4):C775-785.
60.	Rouwkema J,de Boer J,Van Blitterswijk CA.Endothelial cells assemble into a 3-dimensional prevascular network in a bone tissue engineering construct.Tissue Eng,2006,12(9):2685-2693.
61.	Clarkin CE,Emery RJ,Pitsillides AA,et al.Evaluation of VEGF-mediated signaling in primary human cells reveals a paracrine action for VEGF in osteoblast-mediated crosstalk to endothelial cells.J Cell Physiol,2008,214(2):537-544.
62.	Kanczler JM,Oreffo RO.Osteogenesis and angiogenesis:the potential for engineering bone.Eur Cells Mater,2008,15:100-114.
63.	Li HY,Daculsi R,Grellier M,et al.Role of neural-cadherin in early osteoblastic differentiation of human bone marrow stromal cells cocultured with human umbilical vein endothelial cells.Am J Physiol Cell Physiol,2010,299(2):C422-430.
64.	Hager S,Lampert FM,Orimo H,et al.Up-regulation of alkaline phosphatase expression in human primary osteoblasts by cocultivation with primary endothelial cells is mediated by p38 mitogen-activated protein kinase-dependent mRNA stabilization.Tissue Eng Part A,2009,15(11):3437-3447.
65.	Dohle E,Fuchs S,Kolbe M,et al.Sonic hedgehog promotes angiogenesis and osteogenesis in a coculture system consisting of primary osteoblasts and outgrowth endothelial cells.Tissue Eng Part A,2010,16(4):1235-1237.

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. Woodruff MA,Lange C,Reichert J,et al.Bone tissue engineering:from bench to bedside.Mater Today,2012,15(10):430-435.
4. Güven S,Mehrkens A,Saxer F,et al.Engineering of large osteogenic grafts with rapid engraftment capacity using mesenchymal and endothelial progenitors from human adipose tissue.Biomaterials,2011,32(25):5801-5809.
5. Potier E,Ferreira E,Meunier A,et al.Prolonged hypoxia concomitant with serum deprivation induces massive human mesenchymal stem cell death.Tissue Eng,2007,13(6):1325-1331.
6. Hsiong SX,Mooney DJ.Regeneration of vascularized bone.Periodontol 2000,2006,41:109-122.
7. 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.
8. Das A,Botchwey E.Evaluation of Angiogenesis and Osteogenesis.Tissue Eng Part B Rev,2011,17(6):403-414.
9. Traktuev DO,Prater DN,Merfeld-Clauss S,et al.Robust functional vascular network formation in vivo by cooperation of adipose progenitor and endothelial cells.Circ Res,2009,104(12):1410-1420.
10. Lokmic Z,Mitchell GM.Engineering the microcirculation.Tissue Eng Part B Rev,2008,14(1):87-103.
11. Janardhanan S,Wang MO,Fisher JP.Coculture strategies in bone tissue engineering:the impact of culture conditions on pluripotent stem cell populations.Tissue Eng Part B Rev,2012,18(4):312-321.
12. Szpalski C,Barbaro M,Sagebin F,et al.Bone tissue engineering:current strategies and techniques-part Ⅱ:Cell types.Tissue Eng Part B Rev,2012,18(4):258-269.
13. Seong JM,Kim BC,Park JH,et al.Stem cells in bone tissue engineering.Biomed Mater,2010,5(6):062001.
14. Zhang F,Citra F,Wang DA.Prospects of induced pluripotent stem cell technology in regenerative medicine.Tissue Eng Part B Rev,2011,17(2):115-124.
15. Walia B,Satija N,Tripathi RP,et al.Induced pluripotent stem cells:fundamentals and applications of the reprogramming process and its ramifications on regenerative medicine.Stem Cell Rev,2012,8(1):100-115.
16. Fuchs S,Jiang X,Schmidt H,et al.Dynamic processes involved in the pre-vascularization of silk fibroin constructs for bone regeneration using outgrowth endothelial cells.Biomaterials,2009,30(7):1329-1338.
17. Fuchs S,Hofmann A,Kirkpatrick C.Microvessel-like structures from outgrowth endothelial cells from human peripheral blood in 2-dimensional and 3-dimensional co-cultures with osteoblastic lineage cells.Tissue Eng,2007,13(10):2577-2588.
18. Bianco P,Robey PG,Simmons PJ.Mesenchymal stem cells:revisiting history,concepts,and assays.Cell Stem Cell,2008,2(4):313-319.
19. Bieback K,Kern S,Kocaomer A,et al.Comparing mesenchymal stromal cells from different human tissues:Bone marrow,adipose tissue and umbilical cord blood.Biomed Mater Eng,2008,18(1 Suppl):S71-76.
20. Ksiazek K.A comprehensive review on mesenchymal stem cell growth and senescence.Rejuvenation Res,2009,12(2):105-116.
21. Zhu H,Guo ZK,Jiang XX,et al.A protocol for isolation and culture of mesenchymal stem cells from mouse compact bone.Nat Protoc,2010,5(3):550-560.
22. Filardo G,Madry H,Jelic M,et al.Mesenchymal stem cells for the treatment of cartilage lesions:from preclinical findings to clinical application in orthopaedics.Knee Surg Sports Traumatol Arthrosc,2013,21(8):1717-1729.
23. Lei HL,Yu B,Huang Z,et al.Comparative analysis of mesenchymal stem cells from adult mouse adipose,muscle,and fetal muscle.Mol Biol Rep,2013,40(2):885-892.
24. Tsai CC,Huang TF,Ma HL,et al.Isolation of mesenchymal stem cells from shoulder rotator cuff:a potential source for muscle and tendon repair.Cell Transplant,2013,22(3):413-422.
25. Kisiel AH,McDuffee LA,Masaoud E,et al.Isolation,characterization,and in vitro proliferation of canine mesenchymal stem cells derived from bone marrow,adipose tissue,muscle,and periosteum.Am J Vet Res,2012,73(8):1305-1317.
26. De Bari C,Dell'Accio F,Tylzanowski P,et al.Multipotent mesenchymal stem cells from adult human synovial membrane.Arthritis Rheum,2001,44(8):1928-1942.
27. Fu WL,Zhang JY,Fu X,et al.Comparative study of the biological characteristics of mesenchymal stem cells from bone marrow and peripheral blood of rats.Tissue Eng Part A,2012,18(17-18):1793-1803.
28. Valenzuela CD,Allori AC,Reformat DD,et al.Characterization of adipose-derived mesenchymal stem cell combinations for vascularized bone engineering.Tissue Eng Part A,2013,19(11-12):1373-1385.
29. Guillotin B,Bareille R,Bourget C,et al.Interaction between human umbilical vein endothelial cells and human osteoprogenitors triggers pleiotropic effect that may support osteoblastic function.Bone,2008,42(6):1080-1091.
30. Grellier M,Bordenave L,Amedee J.Cell-to-cell communication between osteogenic and endothelial lineages:implications for tissue engineering.Trends Biotechnol,2009,27(10):562-571.
31. Unger RE,Sartoris A,Peters K,et al.Tissue-like self-assembly in cocultures of endothelial cells and osteoblasts and the formation of microcapillary-like structures on three-dimensional porous biomaterials.Biomaterials,2007,28(27):3965-3976.
32. Rouwkema J,Westerweel PE,de Boer J,et al.The use of endothelial progenitor cells for prevascularized bone tissue engineering.Tissue Engi Part A,2009,15(8):2015-2027.
33. Hung SC,Pochampally RR,Chen SC,et al.Angiogenic effects of human multipotent stromal cell conditioned medium activate the PI3K-Akt pathway in hypoxic endothelial cells to inhibit apoptosis,increase survival,and stimulate angiogenesis.Stem Cells,2007,25(9):2363-2370.
34. Matsumoto T,Kuroda R,Mifune Y,et al.Circulating endothelial/skeletal progenitor cells for bone regeneration and healing.Bone,2008,43(3):434-439.
35. Richardson MR,Yoder MC.Endothelial progenitor cells:quo vadis? J Mol Cell Cardiol,2011,50(2):266-272.
36. Lin RZ,Dreyzin A,Aamodt K,et al.Functional endothelial progenitor cells from cryopreserved umbilical cord blood.Cell transplantation,2011,20(4):515-522.
37. Chen JK,Deng YP,Jiang GJ,et al.Establishment of tube formation assay of bone marrow-derived endothelial progenitor cells.CNS Neurosci Ther,2013,19(7):533-535.
38. Xue S,Zhang HT,Zhang P,et al.Functional endothelial progenitor cells derived from adipose tissue show beneficial effect on cell therapy of traumatic brain injury.Neurosci Lett,2010,473(3):186-191.
39. Amini AR,Laurencin CT,Nukavarapu SP.Differential analysis of peripheral blood-and bone marrow-derived endothelial progenitor cells for enhanced vascularization in bone tissue engineering.J Orthop Res,2012,30(9):1507-1515.
40. Dariima T,Jin GZ,Lee EJ,et al.Cooperation between osteoblastic cells and endothelial cells enhances their phenotypic responses and improves osteoblast function.Biotechnol Lett,2013,35(7):1135-1143.
41. Thein-Han W,Xu HH.Prevascularization of a gas-foaming macroporous calcium phosphate cement scaffold via coculture of human umbilical vein endothelial cells and osteoblasts.Tissue Eng Part A,2013,19(15-16):1675-1685.
42. Lee JH,Kim SW,Kim UK,et al.Generation of osteogenic construct using periosteal-derived osteoblasts and polydioxanone/pluronic F127 scaffold with periosteal-derived CD146 positive endothelial-like cells.J Biomed Mater Res Part A,2013,101(1):942-953.
43. Shah AR,Shah SR,Oh S,et al.Migration of co-cultured endothelial cells and osteoblasts in composite hydroxyapatite/polylactic acid scaffolds.Ann Biomed Eng,2011,39(10):2501-2509.
44. Dissanayaka WL,Zhan X,Zhang CF,et al.Coculture of dental pulp stem cells with endothelial cells enhances osteo-/odontogenic and angiogenic potential in vitro.J Endodont,2012,38(4):454-463.
45. Correia C,Grayson WL,Park M,et al.In vitro model of vascularized bone:synergizing vascular development and osteogenesis.PLoS One,2011,6(12):e28352.
46. Kang Y,Kim S,Fahrenholtz M,et al.Osteogenic and angiogenic potentials of monocultured and co-cultured human-bone-marrow-derived mesenchymal stem cells and human-umbilical-vein endothelial cells on three-dimensional porous beta-tricalcium phosphate scaffold.Acta biomaterialia,2013,9(1):4906-4915.
47. Grellier M,Granja PL,Fricain JC,et al.The effect of the co-immobilization of human osteoprogenitors and endothelial cells within alginate microspheres on mineralization in a bone defect.Biomaterials,2009,30(19):3271-3278.
48. Kim JY,Jin GZ,Park IS,et al.Evaluation of solid free-form fabrication-based scaffolds seeded with osteoblasts and human umbilical vein endothelial cells for use in vivo osteogenesis.Tissue Eng Part A,2010,16(7):2229-2236.
49. 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.
50. 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.
51. Duttenhoefer F,Egli S,Benneker LM,et al.Coculture of endothelial progenitor cells (EPC) and coculture of endothelial progenitor cells (EPC) and mesenchymal stem cells (MSC) in polyurethane scaffolds (PU) promotes simultaneously implant neo-vascularization and bone neo-formation.J Tissue Eng Regen M,2012,6(Suppl 1):310-311.
52. Szpalski C,Wetterau M,Barr J,et al.Bone tissue engineering:current strategies and techniques-part I:Scaffolds.Tissue Eng Part B Rev,2012,18(4):246-257.
53. Hofmann A,Ritz U,Verrier S,et al.The effect of human osteoblasts on proliferation and neo-vessel formation of human umbilical vein endothelial cells in a long-term 3D co-culture on polyurethane scaffolds.Biomaterials,2008,29(31):4217-4226.
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. Hu X,Neoh KG,Zhang JY,et al.Immobilization strategy for optimizing VEGF's concurrent bioactivity towards endothelial cells and osteoblasts on implant surfaces.Biomaterials,2012,33(32):8082-8093.
56. Ma J,van den Beucken JJJ,Yang F,et al.Coculture of osteoblasts and endothelial cells:optimization of culture medium and cell ratio.Tissue Eng Part C Methods,2011,17(3):349-357.
57. Kolbe M,Xiang Z,Dohle E,et al.Paracrine effects influenced by cell culture medium and consequences on microvessel-like structures in cocultures of mesenchymal stem cells and outgrowth endothelial Cells.Tissue Eng Part A,2011,17(17-18):2199-2212.
58. Cenni E,Perut F,Baldini N.In vitro models for the evaluation of angiogenic potential in bone engineering.Acta pharmacologica Sinica,2011,32(1):21-30.
59. Villars F,Guillotin B,Amedee T,et al.Effect of HUVEC on human osteoprogenitor cell differentiation needs heterotypic gap junction communication.AmJ Physiol Cell Physiol,2002,282(4):C775-785.
60. Rouwkema J,de Boer J,Van Blitterswijk CA.Endothelial cells assemble into a 3-dimensional prevascular network in a bone tissue engineering construct.Tissue Eng,2006,12(9):2685-2693.
61. Clarkin CE,Emery RJ,Pitsillides AA,et al.Evaluation of VEGF-mediated signaling in primary human cells reveals a paracrine action for VEGF in osteoblast-mediated crosstalk to endothelial cells.J Cell Physiol,2008,214(2):537-544.
62. Kanczler JM,Oreffo RO.Osteogenesis and angiogenesis:the potential for engineering bone.Eur Cells Mater,2008,15:100-114.
63. Li HY,Daculsi R,Grellier M,et al.Role of neural-cadherin in early osteoblastic differentiation of human bone marrow stromal cells cocultured with human umbilical vein endothelial cells.Am J Physiol Cell Physiol,2010,299(2):C422-430.
64. Hager S,Lampert FM,Orimo H,et al.Up-regulation of alkaline phosphatase expression in human primary osteoblasts by cocultivation with primary endothelial cells is mediated by p38 mitogen-activated protein kinase-dependent mRNA stabilization.Tissue Eng Part A,2009,15(11):3437-3447.
65. Dohle E,Fuchs S,Kolbe M,et al.Sonic hedgehog promotes angiogenesis and osteogenesis in a coculture system consisting of primary osteoblasts and outgrowth endothelial cells.Tissue Eng Part A,2010,16(4):1235-1237.

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RESEARCH PROGRESS OF SKELETAL MYOBLASTS FOR CARDIAC REPAIR

Chinese Journal of Reparative and Reconstructive Surgery

RESEARCH PROGRESS OF CO-CULTURE SYSTEM FOR CONSTRUCTING VASCULARIZED TISSUE ENGINEERED BONE

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