Research progress of tissue engineering technology in promoting revascularization of necrotic femoral bone tissue_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

LIN Miaoyuan ¹ , YANG Jibin ¹ , YAN Wenqiang ² , HU Ning ³ , LIU Ziming ² ,  ZHANG Li ¹ ,  LI Yuwan ²

1. Affiliated Hospital of Zunyi Medical University, Zunyi Guizhou, 563000, P.R.China;
2. Department of Sports Medicine, Peking University Third Hospital, Institute of Sports Medicine of Peking University, Beijing Key Laboratory of Sports Injuries, Beijing, 100191, P.R.China;
3. Department of Joint Surgery, the First Affiliated Hospital of Chongqing Medical University, Chongqing, 400019, P.R.China;

Corresponding author：

ZHANG Li, Email: zhli8523@163.com; LI Yuwan, Email: docliyuwan@163.com

Keywords：

Osteonecrosis of the femoral head; vascularization; tissue engineering; three-dimensional printing technology; drug delivery system

DOI：

10.7507/1002-1892.202105047

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the research progress of tissue engineering technology to promote bone tissue revascularization in osteonecrosis of the femoral head (ONFH).Methods The relevant domestic and foreign literature in recent years was extensively reviewed. The mechanism of femoral head vascularization and the application progress of tissue engineering technology in the promotion of ONFH bone tissue revascularization were summarized.Results Rebuilding or improving the blood supply of the femoral head is the key to the treatment of ONFH. Tissue engineering is a hot spot in current research. It mainly focuses on the three elements of seed cells, scaffold materials, and angiogenic growth factors, combined with three-dimensional printing technology and drug delivery systems to promote the revascularization of the femoral bone tissue.Conclusion The strategy of revascularization of the femoral head can improve the local blood supply and delay or even reverse the progression of ONFH disease.

Citation： LIN Miaoyuan, YANG Jibin, YAN Wenqiang, HU Ning, LIU Ziming, ZHANG Li, LI Yuwan. Research progress of tissue engineering technology in promoting revascularization of necrotic femoral bone tissue. Chinese Journal of Reparative and Reconstructive Surgery, 2021, 35(11): 1479-1485. doi: 10.7507/1002-1892.202105047 Copy

1.	王义生, 李劲峰. 股骨头坏死发病机制的研究现状与展望. 中华实验外科杂志, 2020, 37(6): 1001-1010.
2.	Dailiana ZH, Stefanou N, Khaldi L, et al. Vascular endothelial growth factor for the treatment of femoral head osteonecrosis: An experimental study in canines. World J Orthop, 2018, 9(9): 120-129.
3.	张根生, 刘瑞宇, 党晓谦, 等. miR-27a 过表达的血管内皮细胞来源外泌体改善股骨头坏死实验研究. 中国修复重建外科杂志, 2021, 35(3): 356-365.
4.	Kusumbe AP, Ramasamy SK, Adams RH. Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature, 2014, 507(7492): 323-328.
5.	Todorova D, Simoncini S, Lacroix R, et al. Extracellular vesicles in angiogenesis. Circ Res, 2017, 120(10): 1658-1673.
6.	Ramasamy SK, Kusumbe AP, Wang L, et al. Endothelial Notch activity promotes angiogenesis and osteogenesis in bone. Nature, 2014, 507(7492): 376-380.
7.	Gao F, Mao T, Zhang Q, et al. H subtype vascular endothelial cells in human femoral head: an experimental verification. Ann Palliat Med, 2020, 9(4): 1497-1505.
8.	Xu Y, Jiang Y, Wang Y, et al. LINC00473 rescues human bone marrow mesenchymal stem cells from apoptosis induced by dexamethasone through the PEBP1-mediated Akt/Bad/Bcl-2 signaling pathway. Int J Mol Med, 2021, 47(1): 171-182.
9.	Yuan K, Shamskhou EA, Orcholski ME, et al. Loss of endothelium-derived Wnt5a is associated with reduced pericyte recruitment and small vessel loss in pulmonary arterial hypertension. Circulation, 2019, 139(14): 1710-1724.
10.	Song HG, Rumma RT, Ozaki CK, et al. Vascular tissue engineering: progress, challenges, and clinical promise. Cell Stem Cell, 2018, 22(3): 340-354.
11.	王新刚, 封占增, 郭明峰, 等. 组织工程促血管化策略的研究进展. 中华烧伤杂志, 2012, 28(5): 374-377.
12.	Melchiorri AJ, Nguyen BN, Fisher JP. Mesenchymal stem cells: roles and relationships in vascularization. Tissue Eng Part B Rev, 2014, 20(3): 218-228.
13.	Wang C, Li Y, Yang M, et al. Efficient differentiation of bone marrow mesenchymal stem cells into endothelial cells in vitro. Eur J Vasc Endovasc Surg, 2018, 55(2): 257-265.
14.	Abudusaimi A, Aihemaitijiang Y, Wang YH, et al. Adipose-derived stem cells enhance bone regeneration in vascular necrosis of the femoral head in the rabbit. J Int Med Res, 2011, 39(5): 1852-1860.
15.	Pak J. Autologous adipose tissue-derived stem cells induce persistent bone-like tissue in osteonecrotic femoral heads. Pain Physician, 2012, 15(1): 75-85.
16.	Chen C, Qu Z, Yin X, et al. Efficacy of umbilical cord-derived mesenchymal stem cell-based therapy for osteonecrosis of the femoral head: A three-year follow-up study. Mol Med Rep, 2016, 14(5): 4209-4215.
17.	Yue J, Yu H, Liu P, et al. Preliminary study of icariin indicating prevention of steroid-induced osteonecrosis of femoral head by regulating abnormal expression of miRNA-335 and protecting the functions of bone microvascular endothelial cells in rats. Gene, 2021, 766: 145128. doi: 10.1016/j.gene.2020.145128.
18.	冯勇. 内皮祖细胞在股骨头坏死发病机制及治疗中的作用研究. 武汉: 华中科技大学, 2010.
19.	Zigdon-Giladi H, Bick T, Lewinson D, et al. Co-transplantation of endothelial progenitor cells and mesenchymal stem cells promote neovascularization and bone regeneration. Clin Implant Dent Relat Res, 2015, 17(2): 353-359.
20.	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.
21.	Jin H, Xu T, Chen Q, et al. The fate and distribution of autologous bone marrow mesenchymal stem cells with intra-arterial infusion in osteonecrosis of the femoral head in dogs. Stem Cells Int, 2016, 2016: 8616143. doi: 10.1155/2016/8616143.
22.	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, 64: 173-182.
23.	Zhang H, Zhou Y, Zhang W, et al. Construction of vascularized tissue-engineered bone with a double-cell sheet complex. Acta Biomater, 2018, 77: 212-227.
24.	Gong M, Yu B, Wang J, et al. Mesenchymal stem cells release exosomes that transfer miRNAs to endothelial cells and promote angiogenesis. Oncotarget, 2017, 8(28): 45200-45212.
25.	Song H, Li X, Zhao Z, et al. Reversal of osteoporotic activity by endothelial cell-secreted bone targeting and biocompatible exosomes. Nano Lett, 2019, 19(5): 3040-3048.
26.	Liu X, Li Q, Niu X, et al. Exosomes secreted from human-induced pluripotent stem cell-derived mesenchymal stem cells prevent osteonecrosis of the femoral head by promoting angiogenesis. Int J Biol Sci, 2017, 13(2): 232-244.
27.	Yin S, Zhang W, Zhang Z, et al. Recent advances in scaffold design and material for vascularized tissue-engineered bone regeneration. Adv Healthc Mater, 2019, 8(10): e1801433. doi: 10.1002/adhm.201801433.
28.	Liu X, Jakus AE, Kural M, et al. Vascularization of natural and synthetic bone scaffolds. Cell Transplant, 2018, 27(8): 1269-1280.
29.	Maruyama M, Nabeshima A, Pan CC, et al. The effects of a functionally-graded scaffold and bone marrow-derived mononuclear cells on steroid-induced femoral head osteonecrosis. Biomaterials, 2018, 187: 39-46.
30.	Wang P, Li G, Qin W, et al. Repair of osteonecrosis of the femoral head: 3D printed cervi cornus colla deproteinized bone scaffolds. Orthopade, 2019, 48(3): 213-223.
31.	Samara S, Dailiana Z, Varitimidis S, et al. Bone morphogenetic proteins (BMPs) expression in the femoral heads of patients with avascular necrosis. Mol Biol Rep, 2013, 40(7): 4465-4472.
32.	Wang P, Shi B, Gao ZH, et al. Effect of colla cornus cervi combined with LV-mediated BMP7 transfected BMSCs on ANFH in rats. Acta Pol Pharm, 2016, 73(6): 1521-1530.
33.	Wu J, Yao L, Wang B, et al. Tao-Hong-Si-Wu decoction ameliorates steroid-induced avascular necrosis of the femoral head by regulating the HIF-1α pathway and cell apoptosis. Biosci Trends, 2016, 10(5): 410-417.
34.	Song Y, Du Z, Ren M, et al. Association of gene variants of transcription factors PPARγ, RUNX2, Osterix genes and COL2A1, IGFBP3 genes with the development of osteonecrosis of the femoral head in Chinese population. Bone, 2017, 101: 104-112.
35.	Wang J, Liu H, Zhang Q. IGF-1 polymorphisms modulate the susceptibility to osteonecrosis of the femoral head among Chinese Han population. Medicine (Baltimore), 2019, 98(23): e15921. doi: 10.1097/MD.0000000000015921.
36.	Kuroda Y, Asada R, So K, et al. A pilot study of regenerative therapy using controlled release of recombinant human fibroblast growth factor for patients with pre-collapse osteonecrosis of the femoral head. Int Orthop, 2016, 40(8): 1747-1754.
37.	Peng W, Zhang J, Zhang F, et al. Expression of osteoprotegerin and receptor activator for the nuclear factor-κB ligand in XACB/LV-bFGF/MSCs transplantation for repair of rabbit femoral head defect necrosis. J Cell Biochem, 2018. doi: 10.1002/jcb.27201.
38.	Zhang XL, Wang YM, Chu K, et al. The application of PRP combined with TCP in repairing avascular necrosis of the femoral head after femoral neck fracture in rabbit. Eur Rev Med Pharmacol Sci, 2018, 22(4): 903-909.
39.	Tong S, Yin J, Liu J. Platelet-rich plasma has beneficial effects in mice with osteonecrosis of the femoral head by promoting angiogenesis. Exp Ther Med, 2018, 15(2): 1781-1788.
40.	Zhang XL, Shi KQ, Jia PT, et al. Effects of platelet-rich plasma on angiogenesis and osteogenesis-associated factors in rabbits with avascular necrosis of the femoral head. Eur Rev Med Pharmacol Sci, 2018, 22(7): 2143-2152.
41.	Wang CK, Ho ML, Wang GJ, et al. Controlled-release of rhBMP-2 carriers in the regeneration of osteonecrotic bone. Biomaterials, 2009, 30(25): 4178-4186.
42.	Liao H, Zhong Z, Liu Z, et al. Bone mesenchymal stem cells co-expressing VEGF and BMP-6 genes to combat avascular necrosis of the femoral head. Exp Ther Med, 2018, 15(1): 954-962.
43.	Ma XW, Cui DP, Zhao DW. Vascular endothelial growth factor/bone morphogenetic protein-2 bone marrow combined modification of the mesenchymal stem cells to repair the avascular necrosis of the femoral head. Int J Clin Exp Med, 2015, 8(9): 15528-15534.
44.	Matai I, Kaur G, Seyedsalehi A, et al. Progress in 3D bioprinting technology for tissue/organ regenerative engineering. Biomaterials, 2020, 226: 119536. doi: 10.1016/j.biomaterials.2019.119536.
45.	Fielding G, Bose S. SiO₂ and ZnO dopants in three-dimensionally printed tricalcium phosphate bone tissue engineering scaffolds enhance osteogenesis and angiogenesis in vivo. Acta Biomater, 2013, 9(11): 9137-9148.
46.	Byambaa B, Annabi N, Yue K, et al. Bioprinted osteogenic and vasculogenic patterns for engineering 3D bone tissue. Adv Healthc Mater, 2017, 6(16). doi: 10.1002/adhm.201700015.
47.	Wan Z, Zhang P, Liu Y, et al. Four-dimensional bioprinting: Current developments and applications in bone tissue engineering. Acta Biomater, 2020, 101: 26-42.
48.	Wang C, Xu H, Liu C, et al. CaO₂/gelatin oxygen slow-releasing microspheres facilitate tissue engineering efficiency for the osteonecrosis of femoral head by enhancing the angiogenesis and survival of grafted bone marrow mesenchymal stem cells. Biomater Sci, 2021, 9(8): 3005-3018.
49.	Piuzzi NS, Chahla J, Schrock JB, et al. Evidence for the use of cell-based therapy for the treatment of osteonecrosis of the femoral head: a systematic review of the literature. J Arthroplasty, 2017, 32(5): 1698-1708.

1. 王义生, 李劲峰. 股骨头坏死发病机制的研究现状与展望. 中华实验外科杂志, 2020, 37(6): 1001-1010.
2. Dailiana ZH, Stefanou N, Khaldi L, et al. Vascular endothelial growth factor for the treatment of femoral head osteonecrosis: An experimental study in canines. World J Orthop, 2018, 9(9): 120-129.
3. 张根生, 刘瑞宇, 党晓谦, 等. miR-27a 过表达的血管内皮细胞来源外泌体改善股骨头坏死实验研究. 中国修复重建外科杂志, 2021, 35(3): 356-365.
4. Kusumbe AP, Ramasamy SK, Adams RH. Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature, 2014, 507(7492): 323-328.
5. Todorova D, Simoncini S, Lacroix R, et al. Extracellular vesicles in angiogenesis. Circ Res, 2017, 120(10): 1658-1673.
6. Ramasamy SK, Kusumbe AP, Wang L, et al. Endothelial Notch activity promotes angiogenesis and osteogenesis in bone. Nature, 2014, 507(7492): 376-380.
7. Gao F, Mao T, Zhang Q, et al. H subtype vascular endothelial cells in human femoral head: an experimental verification. Ann Palliat Med, 2020, 9(4): 1497-1505.
8. Xu Y, Jiang Y, Wang Y, et al. LINC00473 rescues human bone marrow mesenchymal stem cells from apoptosis induced by dexamethasone through the PEBP1-mediated Akt/Bad/Bcl-2 signaling pathway. Int J Mol Med, 2021, 47(1): 171-182.
9. Yuan K, Shamskhou EA, Orcholski ME, et al. Loss of endothelium-derived Wnt5a is associated with reduced pericyte recruitment and small vessel loss in pulmonary arterial hypertension. Circulation, 2019, 139(14): 1710-1724.
10. Song HG, Rumma RT, Ozaki CK, et al. Vascular tissue engineering: progress, challenges, and clinical promise. Cell Stem Cell, 2018, 22(3): 340-354.
11. 王新刚, 封占增, 郭明峰, 等. 组织工程促血管化策略的研究进展. 中华烧伤杂志, 2012, 28(5): 374-377.
12. Melchiorri AJ, Nguyen BN, Fisher JP. Mesenchymal stem cells: roles and relationships in vascularization. Tissue Eng Part B Rev, 2014, 20(3): 218-228.
13. Wang C, Li Y, Yang M, et al. Efficient differentiation of bone marrow mesenchymal stem cells into endothelial cells in vitro. Eur J Vasc Endovasc Surg, 2018, 55(2): 257-265.
14. Abudusaimi A, Aihemaitijiang Y, Wang YH, et al. Adipose-derived stem cells enhance bone regeneration in vascular necrosis of the femoral head in the rabbit. J Int Med Res, 2011, 39(5): 1852-1860.
15. Pak J. Autologous adipose tissue-derived stem cells induce persistent bone-like tissue in osteonecrotic femoral heads. Pain Physician, 2012, 15(1): 75-85.
16. Chen C, Qu Z, Yin X, et al. Efficacy of umbilical cord-derived mesenchymal stem cell-based therapy for osteonecrosis of the femoral head: A three-year follow-up study. Mol Med Rep, 2016, 14(5): 4209-4215.
17. Yue J, Yu H, Liu P, et al. Preliminary study of icariin indicating prevention of steroid-induced osteonecrosis of femoral head by regulating abnormal expression of miRNA-335 and protecting the functions of bone microvascular endothelial cells in rats. Gene, 2021, 766: 145128. doi: 10.1016/j.gene.2020.145128.
18. 冯勇. 内皮祖细胞在股骨头坏死发病机制及治疗中的作用研究. 武汉: 华中科技大学, 2010.
19. Zigdon-Giladi H, Bick T, Lewinson D, et al. Co-transplantation of endothelial progenitor cells and mesenchymal stem cells promote neovascularization and bone regeneration. Clin Implant Dent Relat Res, 2015, 17(2): 353-359.
20. 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.
21. Jin H, Xu T, Chen Q, et al. The fate and distribution of autologous bone marrow mesenchymal stem cells with intra-arterial infusion in osteonecrosis of the femoral head in dogs. Stem Cells Int, 2016, 2016: 8616143. doi: 10.1155/2016/8616143.
22. 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, 64: 173-182.
23. Zhang H, Zhou Y, Zhang W, et al. Construction of vascularized tissue-engineered bone with a double-cell sheet complex. Acta Biomater, 2018, 77: 212-227.
24. Gong M, Yu B, Wang J, et al. Mesenchymal stem cells release exosomes that transfer miRNAs to endothelial cells and promote angiogenesis. Oncotarget, 2017, 8(28): 45200-45212.
25. Song H, Li X, Zhao Z, et al. Reversal of osteoporotic activity by endothelial cell-secreted bone targeting and biocompatible exosomes. Nano Lett, 2019, 19(5): 3040-3048.
26. Liu X, Li Q, Niu X, et al. Exosomes secreted from human-induced pluripotent stem cell-derived mesenchymal stem cells prevent osteonecrosis of the femoral head by promoting angiogenesis. Int J Biol Sci, 2017, 13(2): 232-244.
27. Yin S, Zhang W, Zhang Z, et al. Recent advances in scaffold design and material for vascularized tissue-engineered bone regeneration. Adv Healthc Mater, 2019, 8(10): e1801433. doi: 10.1002/adhm.201801433.
28. Liu X, Jakus AE, Kural M, et al. Vascularization of natural and synthetic bone scaffolds. Cell Transplant, 2018, 27(8): 1269-1280.
29. Maruyama M, Nabeshima A, Pan CC, et al. The effects of a functionally-graded scaffold and bone marrow-derived mononuclear cells on steroid-induced femoral head osteonecrosis. Biomaterials, 2018, 187: 39-46.
30. Wang P, Li G, Qin W, et al. Repair of osteonecrosis of the femoral head: 3D printed cervi cornus colla deproteinized bone scaffolds. Orthopade, 2019, 48(3): 213-223.
31. Samara S, Dailiana Z, Varitimidis S, et al. Bone morphogenetic proteins (BMPs) expression in the femoral heads of patients with avascular necrosis. Mol Biol Rep, 2013, 40(7): 4465-4472.
32. Wang P, Shi B, Gao ZH, et al. Effect of colla cornus cervi combined with LV-mediated BMP7 transfected BMSCs on ANFH in rats. Acta Pol Pharm, 2016, 73(6): 1521-1530.
33. Wu J, Yao L, Wang B, et al. Tao-Hong-Si-Wu decoction ameliorates steroid-induced avascular necrosis of the femoral head by regulating the HIF-1α pathway and cell apoptosis. Biosci Trends, 2016, 10(5): 410-417.
34. Song Y, Du Z, Ren M, et al. Association of gene variants of transcription factors PPARγ, RUNX2, Osterix genes and COL2A1, IGFBP3 genes with the development of osteonecrosis of the femoral head in Chinese population. Bone, 2017, 101: 104-112.
35. Wang J, Liu H, Zhang Q. IGF-1 polymorphisms modulate the susceptibility to osteonecrosis of the femoral head among Chinese Han population. Medicine (Baltimore), 2019, 98(23): e15921. doi: 10.1097/MD.0000000000015921.
36. Kuroda Y, Asada R, So K, et al. A pilot study of regenerative therapy using controlled release of recombinant human fibroblast growth factor for patients with pre-collapse osteonecrosis of the femoral head. Int Orthop, 2016, 40(8): 1747-1754.
37. Peng W, Zhang J, Zhang F, et al. Expression of osteoprotegerin and receptor activator for the nuclear factor-κB ligand in XACB/LV-bFGF/MSCs transplantation for repair of rabbit femoral head defect necrosis. J Cell Biochem, 2018. doi: 10.1002/jcb.27201.
38. Zhang XL, Wang YM, Chu K, et al. The application of PRP combined with TCP in repairing avascular necrosis of the femoral head after femoral neck fracture in rabbit. Eur Rev Med Pharmacol Sci, 2018, 22(4): 903-909.
39. Tong S, Yin J, Liu J. Platelet-rich plasma has beneficial effects in mice with osteonecrosis of the femoral head by promoting angiogenesis. Exp Ther Med, 2018, 15(2): 1781-1788.
40. Zhang XL, Shi KQ, Jia PT, et al. Effects of platelet-rich plasma on angiogenesis and osteogenesis-associated factors in rabbits with avascular necrosis of the femoral head. Eur Rev Med Pharmacol Sci, 2018, 22(7): 2143-2152.
41. Wang CK, Ho ML, Wang GJ, et al. Controlled-release of rhBMP-2 carriers in the regeneration of osteonecrotic bone. Biomaterials, 2009, 30(25): 4178-4186.
42. Liao H, Zhong Z, Liu Z, et al. Bone mesenchymal stem cells co-expressing VEGF and BMP-6 genes to combat avascular necrosis of the femoral head. Exp Ther Med, 2018, 15(1): 954-962.
43. Ma XW, Cui DP, Zhao DW. Vascular endothelial growth factor/bone morphogenetic protein-2 bone marrow combined modification of the mesenchymal stem cells to repair the avascular necrosis of the femoral head. Int J Clin Exp Med, 2015, 8(9): 15528-15534.
44. Matai I, Kaur G, Seyedsalehi A, et al. Progress in 3D bioprinting technology for tissue/organ regenerative engineering. Biomaterials, 2020, 226: 119536. doi: 10.1016/j.biomaterials.2019.119536.
45. Fielding G, Bose S. SiO₂ and ZnO dopants in three-dimensionally printed tricalcium phosphate bone tissue engineering scaffolds enhance osteogenesis and angiogenesis in vivo. Acta Biomater, 2013, 9(11): 9137-9148.
46. Byambaa B, Annabi N, Yue K, et al. Bioprinted osteogenic and vasculogenic patterns for engineering 3D bone tissue. Adv Healthc Mater, 2017, 6(16). doi: 10.1002/adhm.201700015.
47. Wan Z, Zhang P, Liu Y, et al. Four-dimensional bioprinting: Current developments and applications in bone tissue engineering. Acta Biomater, 2020, 101: 26-42.
48. Wang C, Xu H, Liu C, et al. CaO₂/gelatin oxygen slow-releasing microspheres facilitate tissue engineering efficiency for the osteonecrosis of femoral head by enhancing the angiogenesis and survival of grafted bone marrow mesenchymal stem cells. Biomater Sci, 2021, 9(8): 3005-3018.
49. Piuzzi NS, Chahla J, Schrock JB, et al. Evidence for the use of cell-based therapy for the treatment of osteonecrosis of the femoral head: a systematic review of the literature. J Arthroplasty, 2017, 32(5): 1698-1708.

Chinese Journal of Reparative and Reconstructive Surgery

Research progress of tissue engineering technology in promoting revascularization of necrotic femoral bone tissue

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