Application of cell sheet technology in bone and cartilage tissue engineering_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

ZHI Zhenya , XING Fei , CHEN Long , LI Lang , LONG Ye ,  XIANG Zhou

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

Corresponding author：

XIANG Zhou, Email: xiangzhou15@hotmail.com

Keywords：

Cell sheet technology; bone tissue engineering; cartilage tissue engineering

DOI：

10.7507/1002-1892.201707027

Video：

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Objective To review the progress of cell sheet technology and its application in bone and cartilage engineering. Methods The recent literature concerning the cell sheet technology used in treatment of bone and cartilage defects was extensively reviewed and summarized. Results Cell sheet built through many different ways can protect extracellular matrix from proteolytic enzymes. As a three-dimensional structure, cell sheet can repair bone and cartilige defects via folding, wrapping scaffold, or be created by the layering of individual cell sheets. Conclusion The cell sheet technology would have a very broad prospects in bone and cartilage tissue engineering in future.

Citation： ZHI Zhenya, XING Fei, CHEN Long, LI Lang, LONG Ye, XIANG Zhou. Application of cell sheet technology in bone and cartilage tissue engineering. Chinese Journal of Reparative and Reconstructive Surgery, 2018, 32(2): 237-241. doi: 10.7507/1002-1892.201707027 Copy

1.	Li Y, Ma T, Kniss DA, et al. Effects of filtration seeding on cell density, spatial distribution, and proliferation in nonwoven fibrous matrices. Biotechnol Prog, 2001, 17(5): 935-944.
2.	Pouliot R, Larouche D, Auger FA, et al. Reconstructed human skin produced in vitro and grafted on athymic mice. Transplantation, 2002, 73(11): 1751-1757.
3.	Gomes JA, Geraldes Monteiro B, Melo GB, et al. Corneal reconstruction with tissue-engineered cell sheets composed of human immature dental pulp stem cells. Invest Ophthalmol Vis Sci, 2010, 51(3): 1408-1414.
4.	Yamato M, Utsumi M, Kushida A, et al. Thermo-responsive culture dishes allow the intact harvest of multilayered keratinocyte sheets without dispase by reducing temperature. Tissue Eng, 2001, 7(4): 473-480.
5.	Shiroyanagi Y, Yamato M, Yamazaki Y, et al. Transplantable urothelial cell sheets harvested noninvasively from temperature-responsive culture surfaces by reducing temperature. Tissue Eng, 2003, 9(5): 1005-1012.
6.	Hasegawa M, Yamato M, Kikuchi A, et al. Human periodontal ligament cell sheets can regenerate periodontal ligament tissue in an athymic rat model. Tissue Eng, 2005, 11(3-4): 469-478.
7.	Okano T, Yamada N, Sakai H, et al. A novel recovery system for cultured cells using plasma-treated polystyrene dishes grafted with poly (N-isopropylacrylamide). J Biomed Mater Res, 1993, 27(10): 1243-1251.
8.	Ito A, Ino K, Kobayashi T, et al. The effect of RGD peptide-conjugated magnetite cationic liposomes on cell growth and cell sheet harvesting. Biomaterials, 2005, 26(31): 6185-6193.
9.	Guillaume-Gentil O, Akiyama Y, Schuler M, et al. Polyelectrolyte coatings with a potential for electronic control and cell sheet engineering. Adv Mater, 2008, 20: 560-565.
10.	Zhou Y, Chen F, Ho ST, et al. Combined marrow stromal cell-sheet techniques and high-strength biodegradable composite scaffolds for engineered functional bone grafts. Biomaterials, 2007, 28(5): 814-824.
11.	Ohashi K, Yokoyama T, Yamato M, et al. Engineering functional two- and three-dimensional liver systems in vivo using hepatic tissue sheets. Nat Med, 2007, 13(7): 880-885.
12.	Akahane M, Shigematsu H, Tadokoro M, et al. Scaffold-free cell sheet injection results in bone formation. J Tissue Eng Regen Med, 2010, 4(5): 404-411.
13.	Nakano K, Murata K, Omokawa S, et al. Promotion of osteogenesis and angiogenesis in vascularized tissue-engineered bone using osteogenic matrix cell sheets. Plast Reconstr Surg, 2016, 137(5): 1476-1484.
14.	Desvarieux M, Demmer RT, Rundek T, et al. Relationship between periodontal disease, tooth loss, and carotid artery plaque: the Oral Infections and Vascular Disease Epidemiology Study (INVEST). Stroke, 2003, 34(9): 2120-2125.
15.	Zhang H, Liu S, Zhu B, et al. Composite cell sheet for periodontal regeneration: crosstalk between different types of MSCs in cell sheet facilitates complex periodontal-like tissue regeneration. Stem Cell Res Ther, 2016, 7(1): 168.
16.	Panduwawala CP, Zhan X, Dissanayaka WL, et al. In vivo periodontal tissue regeneration by periodontal ligament stem cells and endothelial cells in three-dimensional cell sheet constructs. J Periodontal Res, 2017, 52(3): 408-418.
17.	Wang ZS, Feng ZH, Wu GF, et al. The use of platelet-rich fibrin combined with periodontal ligament and jaw bone mesenchymal stem cell sheets for periodontal tissue engineering. Sci Rep, 2016, 6: 28126.
18.	Gao LN, An Y, Lei M, et al. The effect of the coumarin-like derivative osthole on the osteogenic properties of human periodontal ligament and jaw bone marrow mesenchymal stem cell sheets. Biomaterials, 2013, 34(38): 9937-9951.
19.	Qi Y, Niu L, Zhao T, et al. Combining mesenchymal stem cell sheets with platelet-rich plasma gel/calcium phosphate particles: a novel strategy to promote bone regeneration. Stem Cell Res Ther, 2015, 6: 256.
20.	Shimizu T, Akahane M, Morita Y, et al. The regeneration and augmentation of bone with injectable osteogenic cell sheet in a rat critical fracture healing model. Injury, 2015, 46(8): 1457-1464.
21.	Zhang C, Wong A, Zhang Y, et al. Non-viral oligonucleotide antimiR-138 delivery to mesenchymal stem cell sheets and the effect on osteogenesis. Biomaterials, 2014, 35(27): 7734-7749.
22.	Han J, Kai Z, Qiao C, et al. Efficiently engineered cell sheet using a complex of polyethylenimine-alginate nanocomposites plus bone morphogenetic protein 2 gene to promote new bone formation. Int J Nanomedicine, 2014, 9: 2179-2190.
23.	Wang Z, Wu G, Wei M, et al. Improving the osteogenesis of human bone marrow mesenchymal stem cell sheets by microRNA-21-loaded chitosan/hyaluronic acid nanoparticles via reverse transfection. Int J Nanomedicine, 2016, 11: 2091-2105.
24.	Ren L, Ma D, Liu B, et al. Preparation of three-dimensional vascularized MSC cell sheet constructs for tissue regeneration. Biomed Res Int, 2014, 2014: 301279.
25.	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.
26.	Mendes LF, Pirraco RP, Szymczyk W, et al. Perivascular-like cells contribute to the stability of the vascular network of osteogenic tissue formed from cell sheet-based constructs. PLoS One, 2012, 7(7): e41051.
27.	Li G, Wang X, Cao J, et al. Coculture of peripheral blood CD34+ cell and mesenchymal stem cell sheets increase the formation of bone in calvarial critical-size defects in rabbits. Br J Oral Maxillofac Surg, 2014, 52(2): 134-139.
28.	Liu Y, Ming L, Luo H, et al. Integration of a calcined bovine bone and BMSC-sheet 3D scaffold and the promotion of bone regeneration in large defects. Biomaterials, 2013, 34(38): 9998-10006.
29.	Long T, Zhu Z, Awad HA, et al. The effect of mesenchymal stem cell sheets on structural allograft healing of critical-sized femoral defects in mice. Biomaterials, 2014, 35(9): 2752-2759.
30.	Kang Y, Ren L, Yang Y. Engineering vascularized bone grafts by integrating a biomimetic periosteum and β-TCP scaffold. ACS Appl Mater Interfaces, 2014, 6(12): 9622-9633.
31.	Xie Q, Wang Z, Huang Y, et al. Characterization of human ethmoid sinus mucosa derived mesenchymal stem cells (hESMSCs) and the application of hESMSCs cell sheets in bone regeneration. Biomaterials, 2015, 66: 67-82.
32.	Lynn AK, Brooks RA, Bonfield W, et al. Repair of defects in articular joints. Prospects for material-based solutions in tissue engineering. J Bone Joint Surg (Br), 2004, 86(8): 1093-1099.
33.	Zhou L, Ding R, Li B, et al. Cartilage engineering using chondrocyte cell sheets and its application in reconstruction of microtia. Int J Clin Exp Pathol, 2015, 8(1): 73-80.
34.	Gong YY, Xue JX, Zhang WJ, et al. A sandwich model for engineering cartilage with acellular cartilage sheets and chondrocytes. Biomaterials, 2011, 32(9): 2265-2273.
35.	Solorio LD, Vieregge EL, Dhami CD, et al. Engineered cartilage via self-assembled hMSC sheets with incorporated biodegradable gelatin microspheres releasing transforming growth factor-β1. J Control Release, 2012, 158(2): 224-232.
36.	Miyagi S, Tensho K, Wakitani S, et al. Construction of an osteochondral-like tissue graft combining β-tricalcium phosphate block and scaffold-free mesenchymal stem cell sheet. J Orthop Sci, 2013, 18(3): 471-477.
37.	Yano F, Hojo H, Ohba S, et al. Cell-sheet technology combined with a thienoindazole derivative small compound TD-198946 for cartilage regeneration. Biomaterials, 2013, 34(22): 5581-5587.
38.	Sato Y, Mera H, Takahashi D, et al. Synergistic effect of ascorbic acid and collagen addition on the increase in type 2 collagen accumulation in cartilage-like MSC sheet. Cytotechnology, 2017, 69(3): 405-416.
39.	Cui Y, Yao M, Liu Y, et al. Effects of cartilage-derived morphogenetic protein 1 (CDMP1) transgenic mesenchymal stem cell sheets in repairing rabbit cartilage defects. Genet Mol Res, 2016, 15(2). doi: 10.4238/gmr.15028058.
40.	Sato Y, Wakitani S, Takagi M. Xeno-free and shrinkage-free preparation of scaffold-free cartilage-like disc-shaped cell sheet using human bone marrow mesenchymal stem cells. J Biosci Bioeng, 2013, 116(6): 734-739.
41.	Maeda S, Fujitomo T, Okabe T, et al. Shrinkage-free preparation of scaffold-free cartilage-like disk-shaped cell sheet using human bone marrow mesenchymal stem cells. J Biosci Bioeng, 2011, 111(4): 489-492.
42.	Mouthuy PA, El‐Sherbini Y, Cui Z, et al. Layering PLGA‐based electrospun membranes and cell sheets for engineering cartilage-bone transition. J Tissue Eng Regen Med, 2016, 10(4): E263-274.
43.	Yokoyama M, Sato M, Umezawa A, et al. Assessment of the Safety of chondrocyte sheet implantation for cartilage regeneration. Tissue Eng Part C Methods, 2016, 22(1): 59-68.
44.	Takaku Y, Murai K, Ukai T, et al. In vivo cell tracking by bioluminescence imaging after transplantation of bioengineered cell sheets to the knee joint. Biomaterials, 2014, 35(7): 2199-2206.

1. Li Y, Ma T, Kniss DA, et al. Effects of filtration seeding on cell density, spatial distribution, and proliferation in nonwoven fibrous matrices. Biotechnol Prog, 2001, 17(5): 935-944.
2. Pouliot R, Larouche D, Auger FA, et al. Reconstructed human skin produced in vitro and grafted on athymic mice. Transplantation, 2002, 73(11): 1751-1757.
3. Gomes JA, Geraldes Monteiro B, Melo GB, et al. Corneal reconstruction with tissue-engineered cell sheets composed of human immature dental pulp stem cells. Invest Ophthalmol Vis Sci, 2010, 51(3): 1408-1414.
4. Yamato M, Utsumi M, Kushida A, et al. Thermo-responsive culture dishes allow the intact harvest of multilayered keratinocyte sheets without dispase by reducing temperature. Tissue Eng, 2001, 7(4): 473-480.
5. Shiroyanagi Y, Yamato M, Yamazaki Y, et al. Transplantable urothelial cell sheets harvested noninvasively from temperature-responsive culture surfaces by reducing temperature. Tissue Eng, 2003, 9(5): 1005-1012.
6. Hasegawa M, Yamato M, Kikuchi A, et al. Human periodontal ligament cell sheets can regenerate periodontal ligament tissue in an athymic rat model. Tissue Eng, 2005, 11(3-4): 469-478.
7. Okano T, Yamada N, Sakai H, et al. A novel recovery system for cultured cells using plasma-treated polystyrene dishes grafted with poly (N-isopropylacrylamide). J Biomed Mater Res, 1993, 27(10): 1243-1251.
8. Ito A, Ino K, Kobayashi T, et al. The effect of RGD peptide-conjugated magnetite cationic liposomes on cell growth and cell sheet harvesting. Biomaterials, 2005, 26(31): 6185-6193.
9. Guillaume-Gentil O, Akiyama Y, Schuler M, et al. Polyelectrolyte coatings with a potential for electronic control and cell sheet engineering. Adv Mater, 2008, 20: 560-565.
10. Zhou Y, Chen F, Ho ST, et al. Combined marrow stromal cell-sheet techniques and high-strength biodegradable composite scaffolds for engineered functional bone grafts. Biomaterials, 2007, 28(5): 814-824.
11. Ohashi K, Yokoyama T, Yamato M, et al. Engineering functional two- and three-dimensional liver systems in vivo using hepatic tissue sheets. Nat Med, 2007, 13(7): 880-885.
12. Akahane M, Shigematsu H, Tadokoro M, et al. Scaffold-free cell sheet injection results in bone formation. J Tissue Eng Regen Med, 2010, 4(5): 404-411.
13. Nakano K, Murata K, Omokawa S, et al. Promotion of osteogenesis and angiogenesis in vascularized tissue-engineered bone using osteogenic matrix cell sheets. Plast Reconstr Surg, 2016, 137(5): 1476-1484.
14. Desvarieux M, Demmer RT, Rundek T, et al. Relationship between periodontal disease, tooth loss, and carotid artery plaque: the Oral Infections and Vascular Disease Epidemiology Study (INVEST). Stroke, 2003, 34(9): 2120-2125.
15. Zhang H, Liu S, Zhu B, et al. Composite cell sheet for periodontal regeneration: crosstalk between different types of MSCs in cell sheet facilitates complex periodontal-like tissue regeneration. Stem Cell Res Ther, 2016, 7(1): 168.
16. Panduwawala CP, Zhan X, Dissanayaka WL, et al. In vivo periodontal tissue regeneration by periodontal ligament stem cells and endothelial cells in three-dimensional cell sheet constructs. J Periodontal Res, 2017, 52(3): 408-418.
17. Wang ZS, Feng ZH, Wu GF, et al. The use of platelet-rich fibrin combined with periodontal ligament and jaw bone mesenchymal stem cell sheets for periodontal tissue engineering. Sci Rep, 2016, 6: 28126.
18. Gao LN, An Y, Lei M, et al. The effect of the coumarin-like derivative osthole on the osteogenic properties of human periodontal ligament and jaw bone marrow mesenchymal stem cell sheets. Biomaterials, 2013, 34(38): 9937-9951.
19. Qi Y, Niu L, Zhao T, et al. Combining mesenchymal stem cell sheets with platelet-rich plasma gel/calcium phosphate particles: a novel strategy to promote bone regeneration. Stem Cell Res Ther, 2015, 6: 256.
20. Shimizu T, Akahane M, Morita Y, et al. The regeneration and augmentation of bone with injectable osteogenic cell sheet in a rat critical fracture healing model. Injury, 2015, 46(8): 1457-1464.
21. Zhang C, Wong A, Zhang Y, et al. Non-viral oligonucleotide antimiR-138 delivery to mesenchymal stem cell sheets and the effect on osteogenesis. Biomaterials, 2014, 35(27): 7734-7749.
22. Han J, Kai Z, Qiao C, et al. Efficiently engineered cell sheet using a complex of polyethylenimine-alginate nanocomposites plus bone morphogenetic protein 2 gene to promote new bone formation. Int J Nanomedicine, 2014, 9: 2179-2190.
23. Wang Z, Wu G, Wei M, et al. Improving the osteogenesis of human bone marrow mesenchymal stem cell sheets by microRNA-21-loaded chitosan/hyaluronic acid nanoparticles via reverse transfection. Int J Nanomedicine, 2016, 11: 2091-2105.
24. Ren L, Ma D, Liu B, et al. Preparation of three-dimensional vascularized MSC cell sheet constructs for tissue regeneration. Biomed Res Int, 2014, 2014: 301279.
25. 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.
26. Mendes LF, Pirraco RP, Szymczyk W, et al. Perivascular-like cells contribute to the stability of the vascular network of osteogenic tissue formed from cell sheet-based constructs. PLoS One, 2012, 7(7): e41051.
27. Li G, Wang X, Cao J, et al. Coculture of peripheral blood CD34+ cell and mesenchymal stem cell sheets increase the formation of bone in calvarial critical-size defects in rabbits. Br J Oral Maxillofac Surg, 2014, 52(2): 134-139.
28. Liu Y, Ming L, Luo H, et al. Integration of a calcined bovine bone and BMSC-sheet 3D scaffold and the promotion of bone regeneration in large defects. Biomaterials, 2013, 34(38): 9998-10006.
29. Long T, Zhu Z, Awad HA, et al. The effect of mesenchymal stem cell sheets on structural allograft healing of critical-sized femoral defects in mice. Biomaterials, 2014, 35(9): 2752-2759.
30. Kang Y, Ren L, Yang Y. Engineering vascularized bone grafts by integrating a biomimetic periosteum and β-TCP scaffold. ACS Appl Mater Interfaces, 2014, 6(12): 9622-9633.
31. Xie Q, Wang Z, Huang Y, et al. Characterization of human ethmoid sinus mucosa derived mesenchymal stem cells (hESMSCs) and the application of hESMSCs cell sheets in bone regeneration. Biomaterials, 2015, 66: 67-82.
32. Lynn AK, Brooks RA, Bonfield W, et al. Repair of defects in articular joints. Prospects for material-based solutions in tissue engineering. J Bone Joint Surg (Br), 2004, 86(8): 1093-1099.
33. Zhou L, Ding R, Li B, et al. Cartilage engineering using chondrocyte cell sheets and its application in reconstruction of microtia. Int J Clin Exp Pathol, 2015, 8(1): 73-80.
34. Gong YY, Xue JX, Zhang WJ, et al. A sandwich model for engineering cartilage with acellular cartilage sheets and chondrocytes. Biomaterials, 2011, 32(9): 2265-2273.
35. Solorio LD, Vieregge EL, Dhami CD, et al. Engineered cartilage via self-assembled hMSC sheets with incorporated biodegradable gelatin microspheres releasing transforming growth factor-β1. J Control Release, 2012, 158(2): 224-232.
36. Miyagi S, Tensho K, Wakitani S, et al. Construction of an osteochondral-like tissue graft combining β-tricalcium phosphate block and scaffold-free mesenchymal stem cell sheet. J Orthop Sci, 2013, 18(3): 471-477.
37. Yano F, Hojo H, Ohba S, et al. Cell-sheet technology combined with a thienoindazole derivative small compound TD-198946 for cartilage regeneration. Biomaterials, 2013, 34(22): 5581-5587.
38. Sato Y, Mera H, Takahashi D, et al. Synergistic effect of ascorbic acid and collagen addition on the increase in type 2 collagen accumulation in cartilage-like MSC sheet. Cytotechnology, 2017, 69(3): 405-416.
39. Cui Y, Yao M, Liu Y, et al. Effects of cartilage-derived morphogenetic protein 1 (CDMP1) transgenic mesenchymal stem cell sheets in repairing rabbit cartilage defects. Genet Mol Res, 2016, 15(2). doi: 10.4238/gmr.15028058.
40. Sato Y, Wakitani S, Takagi M. Xeno-free and shrinkage-free preparation of scaffold-free cartilage-like disc-shaped cell sheet using human bone marrow mesenchymal stem cells. J Biosci Bioeng, 2013, 116(6): 734-739.
41. Maeda S, Fujitomo T, Okabe T, et al. Shrinkage-free preparation of scaffold-free cartilage-like disk-shaped cell sheet using human bone marrow mesenchymal stem cells. J Biosci Bioeng, 2011, 111(4): 489-492.
42. Mouthuy PA, El‐Sherbini Y, Cui Z, et al. Layering PLGA‐based electrospun membranes and cell sheets for engineering cartilage-bone transition. J Tissue Eng Regen Med, 2016, 10(4): E263-274.
43. Yokoyama M, Sato M, Umezawa A, et al. Assessment of the Safety of chondrocyte sheet implantation for cartilage regeneration. Tissue Eng Part C Methods, 2016, 22(1): 59-68.
44. Takaku Y, Murai K, Ukai T, et al. In vivo cell tracking by bioluminescence imaging after transplantation of bioengineered cell sheets to the knee joint. Biomaterials, 2014, 35(7): 2199-2206.

Chinese Journal of Reparative and Reconstructive Surgery

Application of cell sheet technology in bone and cartilage tissue engineering

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