Engineering vascularized bone grafts by integrating a biomimetic periosteum and β-TCP scaffold

ACS Applied Materials and Interfaces

Volumn 6, Issue 12, 2014, Pages 9622-9633

  Kang, Yunqing ^a,b   Ren, Liling ^a,b   Yang, Yunzhi ^a,c  

^a STANFORD UNIVERSITY   (United States)

^b LANZHOU UNIVERSITY   (China)

^c Stanford University   (United States)

Author keywords

biomimetic periosteum; bone tissue engineering; cell sheet; osteogenesis; vascularization; TCP

Indexed keywords

BIOMATERIALS; BIOMIMETICS; BONE; COMPUTERIZED TOMOGRAPHY; CYTOLOGY; ENDOTHELIAL CELLS; GRAFTING (CHEMICAL); STEM CELLS;

BETA TRICALCIUM PHOSPHATE; BONE TISSUE ENGINEERING; CELL SHEET; HUMAN MESENCHYMAL STEM CELLS (HMSCS); OSTEOGENESIS; SPATIAL CONFIGURATION; VASCULAR ENDOTHELIAL CELLS; VASCULARIZATION;

SCAFFOLDS (BIOLOGY);

BETA-TRICALCIUM PHOSPHATE; CALCIUM PHOSPHATE; OSTEOCALCIN;

ANIMAL; BIOMIMETICS; BONE DEVELOPMENT; BONE REGENERATION; BONE TRANSPLANTATION; CHEMISTRY; HUMAN; MESENCHYMAL STROMA CELL; MOUSE; PERIOSTEUM; TISSUE ENGINEERING; TISSUE SCAFFOLD; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; BIOMIMETICS; BONE REGENERATION; BONE TRANSPLANTATION; CALCIUM PHOSPHATES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MESENCHYMAL STROMAL CELLS; MICE; OSTEOCALCIN; OSTEOGENESIS; PERIOSTEUM; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84903527579     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/am502056q     Document Type: Article

References (65)

1. Schimming, R.; Schmelzeisen, R. Tissue-Engineered Bone for Maxillary Sinus Augmentation J. Oral Maxillofac. Surg. 2004, 62, 724-729
2. Lattermann, C.; Romine, S. E. Osteochondral Allografts: State of the Art Clin. Sports Med. 2009, 28, 285-301
3. Gitelis, S.; Cole, B. J. The Use of Allografts in Orthopaedic Surgery Instr. Course Lect. 2002, 51, 507-520
4. Li, J.; Lin, Z.; Zheng, Q.; Guo, X.; Lan, S.; Liu, S.; Yang, S. Repair of Rabbit Radial Bone Defects Using True Bone Ceramics Combined with BMP-2-related Peptide and Type I Collagen Mater. Sci. Eng., C 2010, 30, 1272-1279
5. Lozano, D.; Trejo, C. G.; Gomez-Barrena, E.; Manzano, M.; Doadrio, J. C.; Salinas, A. J.; Vallet-Regi, M.; Garcia-Honduvilla, N.; Esbrit, P.; Bujan, J. Osteostatin Loaded onto Mesoporous Ceramics Improves the Early Phase of Bone Regeneration in a Rabbit Osteopenia Model Acta Biomater. 2012, 8, 2317-2323
6. Sprio, S.; Guicciardi, S.; Dapporto, M.; Melandri, C.; Tampieri, A. Synthesis and Mechanical Behavior of β-Tricalcium Phosphate/Titania Composites Addressed to Regeneration of Long Bone Segments J. Mech. Behav. Biomed. Mater. 2013, 17, 1-10
7. Miño-Fariña, N.; Muñoz-Guzón, F. M.; López-Peña, M.; González-Cantalapiedra, A. Application of Different Calcium Phosphate Ceramics for Bone Regeneration Bone 2011, 48, S168-S168
8. El-Ghannam, A. Bone Reconstruction: From Bioceramics to Tissue Engineering Expert. Rev. Med. Devices 2005, 2, 87-101
9. Akita, S.; Tamai, N.; Myoui, A.; Nishikawa, M.; Kaito, T.; Takaoka, K.; Yoshikawa, H. Capillary Vessel Network Integration by Inserting a Vascular Pedicle Enhances Bone Formation in Tissue-Engineered Bone Using Interconnected Porous Hydroxyapatite Ceramics Tissue Eng. 2004, 10, 789-795
10. Elcin, Y. M.; Dixit, V.; Gitnick, G. Extensive In Vivo Angiogenesis Following Controlled Release of Human Vascular Endothelial Cell Growth Factor: Implications for Tissue Engineering and Wound Healing Artif. Organs. 2001, 25, 558-565
11. Royce, P. M.; Kato, T.; Ohsaki, K.; Miura, A. The Enhancement of Cellular Infiltration and Vascularization of a Collagenous Dermal Implant in the Rat by Platelet-derived Growth Factor BB J. Dermatol. Sci. 1995, 10, 42-52
12. Chiu, L. L.; Radisic, M. Scaffolds with Covalently Immobilized VEGF and Angiopoietin-1 for Vascularization of Engineered Tissues Biomaterials 2010, 31, 226-241
13. Freeman, I.; Cohen, S. The Influence of the Sequential Delivery of Angiogenic Factors from Affinity-binding Alginate Scaffolds on Vascularization Biomaterials 2009, 30, 2122-2131
14. Geiger, F.; Lorenz, H.; Xu, W.; Szalay, K.; Kasten, P.; Claes, L.; Augat, P.; Richter, W. VEGF Producing Bone Marrow Stromal Cells (BMSC) Enhance Vascularization and Resorption of a Natural Coral Bone Substitute Bone 2007, 41, 516-522
15. Anderson, S. M.; Siegman, S. N.; Segura, T. The Effect of Vascular Endothelial Growth Factor (VEGF) Presentation within Fibrin Matrices on Endothelial Cell Branching Biomaterials 2011, 32, 7432-7443
16. Fuchs, S.; Ghanaati, S.; Orth, C.; Barbeck, M.; Kolbe, M.; Hofmann, A.; Eblenkamp, M.; Gomes, M.; Reis, R. L.; Kirkpatrick, C. J. Contribution of Outgrowth Endothelial Cells from Human Peripheral Blood on In Vivo Vascularization of Bone Tissue Engineered Constructs Based on Starch Polycaprolactone Scaffolds Biomaterials 2009, 30, 526-534
17. Kirkpatrick, C. J.; Fuchs, S.; Unger, R. E. Co-culture Systems for Vascularization - Learning from Nature Adv. Drug Delivery Rev. 2011, 63, 291-299
18. Novosel, E. C.; Kleinhans, C.; Kluger, P. J. Vascularization is the Key Challenge in Tissue Engineering Adv. Drug Delivery Rev. 2011, 63, 300-311
19. Kang, Y.; Kim, S.; Fahrenholtz, M.; Khademhosseini, A.; Yang, Y. 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 β-Tricalcium Phosphate Scaffold Acta Biomater. 2013, 9, 4906-4915
20. Wang, L.; Fan, H.; Zhang, Z. Y.; Lou, A. J.; Pei, G. X.; Jiang, S.; Mu, T. W.; Qin, J. J.; Chen, S. Y.; Jin, D. Osteogenesis and Angiogenesis of Tissue-Engineered Bone Constructed by Prevascularized β-Tricalcium Phosphate Scaffold and Mesenchymal Stem Cells Biomaterials 2010, 31, 9452-9461
21. Kokemueller, H.; Spalthoff, S.; Nolff, M.; Tavassol, F.; Essig, H.; Stuehmer, C.; Bormann, K. H.; Rücker, M.; Gellrich, N. C. Prefabrication of Vascularized Bioartificial Bone Grafts In Vivo for Segmental Mandibular Reconstruction: Experimental Pilot Study in Sheep and First Clinical Application Int. J. Oral Maxillofac. Surg. 2010, 39, 379-387
22. Altun, B. U. Periosteum: Resorption or Formation Area? Turk. Jem. 2008, 12, 28-31
23. Knothe Tate, M. L. "Whither Flows the Fluid in Bone?" An Osteocyte's Perspective J. Biomech. 2003, 36, 1409-1424
24. Tami, A. E.; Schaffler, M. B.; Knothe Tate, M. L. Probing the Tissue to Subcellular Level Structure Underlying Bone's Molecular Sieving Function Biorheology 2003, 40, 577-590
25. Evans, S. F.; Parent, J. B.; Lasko, C. E.; Zhen, X.; Knothe, U. R.; Lemaire, T.; Knothe Tate, M. L. Periosteum, Bone's "Smart" Bounding Membrane, Exhibits Direction-Ddependent Permeability J. Bone Miner. Res. 2013, 28, 608-617
26. Song, H. R.; Puri, A.; Lee, J. H.; Park, H. B.; Ra, D. K.; Kim, G. S.; Yeon, S. C. Spontaneous Bone Regeneration in Surgically Induced Bone Defects in Young Rabbits J. Pediatr. Orthop. B 2002, 11, 343-349
27. Chen, X.; Aledia, A. S.; Ghajar, C. M.; Griffith, C. K.; Putnam, A. J.; Hughes, C. C.; George, S. C. Prevascularization of a Fibrin-based Ttissue Construct Accelerates the Formation of Functional Anastomosis with Host Vasculature Tissue Eng., Part A 2009, 15, 1363-1371
28. Runyan, C. M.; Jones, D. C.; Bove, K. E.; Maercks, R. A.; Simpson, D. S.; Taylor, J. A. Porcine Allograft Mandible Revitalization Using Autologous Adipose-derived Stem Cells, Bone Morphogenetic Protein-2, and Periosteum Plast. Reconstr. Surg. 2010, 125, 1372-1382
29. Canalis, R. F.; Burstein, F. D. Osteogenesis in Vascularized Periosteum. Interactions with Underlying Bone Arch. Otolaryngol. 1985, 111, 511-516
30. Maercks, R. A.; Runyan, C. M.; Jones, D. C.; Taylor, J. A. The Vastus Intermedius Periosteal (VIP) Flap: A Novel Flap for Osteoinduction J. Reconstr. Microsurg. 2010, 26, 335-340
31. Iorio, M. L.; Masden, D. L.; Higgins, J. P. The Limits of Medial Femoral Condyle Corticoperiosteal Flaps J. Hand Surg. Am. 2011, 36, 1592-1596
32. Gallay, S. H.; Miura, Y.; Commisso, C. N.; Fitzsimmons, J. S.; O'Driscoll, S. W. Relationship of Donor Site to Chondrogenic Potential of Periosteum In Vitro J. Orthop. Res. 1994, 12, 515-525
33. Zhao, L.; Zhao, J.; Wang, S.; Wang, J.; Liu, J. Comparative Study Between Tissue-Engineered Periosteum and Structural Allograft in Rabbit Critical-Sized Radial Defect Model J. Biomed. Mater. Res., Part B 2011, 97, 1-9
34. Schonmeyr, B.; Clavin, N.; Avraham, T.; Longo, V.; Mehrara, B. J. Synthesis of a Tissue-Engineered Periosteum with Acellular Dermal Matrix and Cultured Mesenchymal Stem Cells Tissue Eng., Part A 2009, 15, 1833-1841
35. Long, T.; Zhu, Z.; Awad, H. A.; Schwarz, E. M.; Hilton, M. J.; Dong, Y. The Effect of Mesenchymal Stem Cell Sheets on Structural Allograft Healing of Critical Sized Femoral Defects in Mice Biomaterials 2014, 35, 2752-2759
36. Shi, X.; Chen, S.; Zhao, Y.; Lai, C.; Wu, H. Enhanced Osteogenesis by a Biomimic Pseudo-periosteum-Involved Tissue Engineering Strategy Adv. Healthcare Mater. 2013, 2, 1229-1235
37. Hoffman, M. D.; Xie, C.; Zhang, X.; Benoit, D. S. The Effect of Mesenchymal Stem Cells Delivered via Hydrogel-based Tissue Engineered Periosteum on Bone Allograft Healing Biomaterials 2013, 34, 8887-8898
38. Xie, C.; Reynolds, D.; Awad, H.; Rubery, P. T.; Pelled, G.; Gazit, D.; Guldberg, R. E.; Schwarz, E. M.; O'Keefe, R. J.; Zhang, X. Structural Bone Allograft Combined with Genetically Engineered Mesenchymal Stem Cells as a Novel Platform for Bone Tissue Engineering Tissue Eng. 2007, 13, 435-445
39. Zhang, X.; Xie, C.; Lin, A. S.; Ito, H.; Awad, H.; Lieberman, J. R.; Rubery, P. T.; Schwarz, E. M.; O'Keefe, R. J.; Guldberg, R. E. Periosteal Progenitor Cell Fate in Segmental Cortical Bone Graft Transplantations: Implications for Functional Tissue Engineering J. Bone Miner. Res. 2005, 20, 2124-2137
40. Nehls, V.; Denzer, K.; Drenckhahn, D. Pericyte Involvement in Capillary Sprouting During Angiogenesis In Situ Cell Tissue Res. 1992, 270, 469-474
41. Adams, R. H.; Alitalo, K. Molecular Regulation of Angiogenesis and Lymphangiogenesis Nat. Rev. Mol. Cell Biol. 2007, 8, 464-478
42. Liu, Y.; Kim, J. H.; Young, D.; Kim, S.; Nishimoto, S. K.; Yang, Y. Novel Template-Casting Technique for Fabricating β-Tricalcium Phosphate Scaffolds with High Interconnectivity and Mechanical Strength and In Vitro Cell Responses J. Biomed. Mater. Res., Part A 2010, 92, 997-1006
43. Kang, Y.; Kim, S.; Khademhosseini, A.; Yang, Y. Creation of Bony Microenvironment with CaP and Cell-Derived ECM to Enhance Human Bone-Marrow MSC Behavior and Delivery of BMP-2 Biomaterials 2011, 32, 6119-6130
44. Kang, Y.; Scully, A.; Young, D. A.; Kim, S.; Tsao, H.; Sen, M.; Yang, Y. Enhanced Mechanical Performance and Biological Evaluation of a PLGA Coated Beta-TCP Composite Scaffold for Load-Bearing Applications Eur. Polym. J. 2011, 47, 1569-1577
45. Kang, Y.; Kim, S.; Bishop, J.; Khademhosseini, A.; Yang, Y. The Osteogenic Differentiation of Human Bone Marrow MSCs on HUVEC-Derived ECM and β-TCP Scaffold Biomaterials 2012, 33, 6998-7007
46. Bauer, S. M.; Bauer, R. J.; Liu, Z. J.; Chen, H.; Goldstein, L.; Velazquez, O. C. Vascular Endothelial Growth Factor-C Promotes Vasculogenesis, Angiogenesis, and Collagen Constriction in Three-Dimensional Collagen Gels J. Vasc. Surg. 2005, 41, 699-707
47. Eppley, B. L. Experimental Assessment of the Revascularization of Acellular Human Dermis for Soft-Tissue Augmentation Plast. Reconstr. Surg. 2001, 107, 757-762
48. Ma, D.; Yao, H.; Tian, W.; Chen, F.; Liu, Y.; Mao, T.; Ren, L. Enhancing Bone Formation by Transplantation of a Scaffold-free Tissue-Engineered Periosteum in a Rabbit Model Clin. Oral Implants Res. 2011, 22, 1193-1199
49. Ma, D.; Zhong, C.; Yao, H.; Liu, Y.; Chen, F.; Li, J.; Zhao, J.; Mao, T.; Ren, L. Engineering Injectable Bone Using Bone Marrow Stromal Cell Aggregates Stem Cells Dev. 2011, 20, 989-999
50. Ma, D.; Ren, L.; Chen, F.; Liu, Y.; Zhang, J.; Xue, Z.; Mao, T. Reconstruction of Rabbit Critical-size Calvarial Defects Using Autologous Bone Marrow Stromal Cell Sheets Ann. Plast. Surg. 2010, 65, 259-265
51. Ren, L.; Kang, Y. Q.; Browne, C.; Bishop, J.; Yang, Y. Fabrication, Vascularization, and Osteogenic Properties of a Novel Synthetic Biomimetic Induced Membrane for the Treatment of Large Bone Defects Bone 2014, 64, 173-182
52. Ma, D.; Ren, L.; Yao, H.; Tian, W.; Chen, F.; Zhang, J.; Liu, Y.; Mao, T. Locally Injection of Cell Sheet Fragments Enhances New Bone Formation in Mandibular Distraction Osteogenesis: A Rabbit Model J. Orthop. Res. 2013, 31, 1082-1088
53. Yuan, Q.; Kubo, T.; Doi, K.; Morita, K.; Takeshita, R.; Katoh, S.; Shiba, T.; Gong, P.; Akagawa, Y. Effect of Combined Application of bFGF and Inorganic Polyphosphate on Bioactivities of Osteoblasts and Bone Regeneration Acta Biomater. 2009, 5, 1716-1724
54. Elloumi-Hannachi, I.; Yamato, M.; Okano, T. Cell Sheet Engineering: A Unique Nanotechnology for Scaffold-free Tissue Reconstruction with Clinical Applications in Regenerative Medicine J. Int. Med. 2010, 267, 54-70
55. Chalupowicz, D. G.; Chowdhury, Z. A.; Bach, T. L.; Barsigian, C.; Martinez, J. Fibrin II Induces Endothelial Cell Capillary Tube Formation J. Cell. Biol. 1995, 130, 207-215
56. Soucy, P. A.; Romer, L. H. Endothelial Cell Adhesion, Signaling, and Morphogenesis in Fibroblast-Derived Matrix Matrix Biol. 2009, 28, 273-283
57. Mendes, L. F.; Pirraco, R. P.; Szymczyk, W.; Frias, A. M.; Santos, T. C.; Reis, R. L.; Marques, A. P. Perivascular-like Cells Contribute to the Stability of the Vascular Network of Osteogenic Tissue Formed from Cell Sheet-based Constructs PLoS One 2012, 7, 1-12
58. Blocki, A.; Wang, Y.; Koch, M.; Peh, P.; Beyer, S.; Law, P.; Hui, J.; Raghunath, M. Not All MSCs can Act as Pericytes: Functional In Vitro Assays to Distinguish Pericytes from other Mesenchymal Stem Cells in Angiogenesis Stem Cells Dev. 2013, 22, 2347-2355
59. Yachouh, J.; Breton, P.; Roux, J. P.; Goudot, P. Osteogenic Capacity of Vascularized Periosteum: An Experimental Study on Mandibular Irradiated Bone in Rabbits J. Plast. Reconstr. Aesthet. Surg. 2010, 63, 2160-2167
60. Sun, M. H.; Leung, K. S.; Zheng, Y. P.; Huang, Y. P.; Wang, L. K.; Qin, L.; Leung, A. H.; Chow, S. K.; Cheung, W. H. Three-Dimensional High Frequency Power Doppler Ultrasonography for the Assessment of Microvasculature during Fracture Healing in a Rat Model J. Orthop. Res. 2012, 30, 137-143
61. Kollmann, C.; Turetschek, K.; Mostbeck, G. Amplitude-coded Colour Doppler Sonography: Physical Principles and Technique Eur. Radiol. 1998, 8, 649-656
62. Risselada, M.; Kramer, M.; Saunders, J. H.; Verleyen, P.; Van Bree, H. Power Doppler Assessment of the Neovascularization during Uncomplicated Fracture Healing of Long Bones in Dogs and Cats Vet. Radiol. Ultrasound 2006, 47, 301-306
63. Raines, A. L.; S, M.; Thacker, K. Angiogenesis in Hyaluronan Treated Bone Repair. 56th Annual Meeting of the Orthopaedic Research Society 2010, March, New Orleans.
64. Bottinelli, O.; Calliada, F.; Campani, R. Bone Callus: Possible Assessment with Color Doppler Ultrasonography. Normal Bone Healing Process Radiol. Med. 1996, 91, 537-541
65. Barros, J. W.; Barbieri, C. H.; Fernandes, C. D. Scintigraphic Evaluation of Tibial Shaft Fracture Healing Injury 2000, 31, 51-54 and Skin Diseases Research