Tissue engineering of a vascularized bone graft of critical size with an osteogenic and angiogenic factor-based in vivo bioreactor

Tissue Engineering - Part A

Volumn 20, Issue 23-24, 2014, Pages 3189-3197

  Liu, Yanming ^a,b   Möller, Björn ^b   Wiltfang, Joerg ^b   Warnke, Patrick H ^c   Terheyden, Hendrik ^b,d  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^c GRIFFITH UNIVERSITY   (Australia)

^d Rotes Kreuz Krankenhaus   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCONVERSION; BIOREACTORS; FLUORESCENCE; HISTOLOGY; MAMMALS; RECOMBINANT PROTEINS; TISSUE;

ANGIOGENIC FACTOR; BIOACTIVE FACTOR; COMPOSITE SCAFFOLDS; FLUORESCENCE LABELING; HISTOMORPHOMETRY; HUMAN BONE MORPHOGENETIC PROTEIN; SYNERGIC EFFECTS; VASCULAR ENDOTHELIAL GROWTH;

SCAFFOLDS (BIOLOGY);

FLUORESCENT DYE; RECOMBINANT OSTEOGENIC PROTEIN 1; RECOMBINANT VASCULOTROPIN; TITANIUM; ANGIOGENIC FACTOR; BMP7 PROTEIN, HUMAN; OSTEOGENIC PROTEIN 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOREACTOR; BONE DENSITY; BONE DEVELOPMENT; BONE GRAFT; BONE IMPLANT; CONTROLLED STUDY; EXPERIMENTAL PIG; FLUORESCENCE MICROSCOPY; IMPLANTATION; IN VIVO STUDY; LATISSIMUS DORSI MUSCLE; MICROSCOPY; MORPHOMETRICS; NONHUMAN; OSSIFICATION; TISSUE ENGINEERING; TISSUE SCAFFOLD; TRABECULAR BONE; VASCULARIZED BONE GRAFT; ANIMAL; BONE TRANSPLANTATION; BOVINE; CHEMISTRY; DRUG EFFECTS; FEMALE; HUMAN; PIG; PROCEDURES;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; BIOREACTORS; BONE MORPHOGENETIC PROTEIN 7; BONE TRANSPLANTATION; CATTLE; FEMALE; HUMANS; MICROSCOPY, FLUORESCENCE; OSTEOGENESIS; SWINE; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84915753212     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2013.0653     Document Type: Article

References (44)

1. Smith, J.O., Aarvold, A., Tayton, E.R., Dunlop, D.G., and Oreffo, R.O. Skeletal tissue regeneration: current approaches, challenges, and novel reconstructive strategies for an aging population. Tissue Eng Part B Rev 17, 307, 2011.
2. Chen, J., Liu, Y., Ping, F., Zhao, S., Xu, X., and Yan, F. Two-step transport-disk distraction osteogenesis in reconstruction of mandibular defect involving body and ramus. Int J Oral Maxillofac Surg 39, 573, 2010.
3. Bak, M., Jacobson, A.S., Buchbinde, D., and Urken, M.L. Contemporary reconstruction of the mandible. Oral Oncol 46, 71, 2010.
4. Korompilias, A.V., Paschos, N.K., Lykissas, M.G., Kostas-Agnantis, I., Vekris, M.D., and Beris, A.E. Recent updates of surgical techniques and applications of free vascularized fibular graft in extremity and trunk reconstruction. Microsurgery 31, 171, 2011.
5. Gaskill, T.R., Urbaniak, J.R., and Aldridge, J.M., 3rd. Free vascularized fibular transfer for femoral head osteonecrosis: donor and graft site morbidity. J Bone Joint Surg Am 91, 1861, 2009.
6. Sieg, P., Taner, C., Hakim, S.G., and Jacobsen, H.C. Longterm evaluation of donor site morbidity after free fibula transfer. Br J Oral Maxillofac Surg 48, 267, 2010.
7. Langer, R., and Vacanti, J.P. Tissue engineering. Science 260, 920, 1993.
8. Lin, C.Y., Chang, Y.H., Lin, K.J., Yen, T.C., Tai, C.L., and Chen, C.Y. The healing of critical-sized femoral segmental bone defects in rabbits using baculovirus-engineered mesenchymal stem cells. Biomaterials 31, 3222, 2010.
9. Schneider, R.K., Puellen, A., Kramann, R., Raupach, K., Bornemann, J., and Knuechel, R. The osteogenic differentiation of adult bone marrow and perinatal umbilical mesenchymal stem cells and matrix remodelling in threedimensional collagen scaffolds. Biomaterials 31, 467, 2010.
10. Warnke, P.H., Springer, I.N., Acil, Y., Julga, G., Wiltfang, J., and Terheyden, H. The mechanical integrity of in vivo engineered heterotopic bone. Biomaterials 27, 1081, 2006.
11. Kanczler, J.M., and Oreffo, R.O. Osteogenesis and angiogenesis: the potential for engineering bone. Eur Cell Mater 15, 100, 2008.
12. Komaki, H., Tanaka, T., Chazono, M., and Kikuchi, T. Repair of segmental bone defects in rabbit tibiae using a complex of beta-tricalcium phosphate, type I collagen, and fibroblast growth factor-2. Biomaterials 27, 5118, 2006.
13. Axelrad, T.W., and Einhorn, T.A. Bone morphogenetic proteins in orthopaedic surgery. Cytokine Growth Factor Rev 20, 481, 2009.
14. Wozney, J.M. Overview of bone morphogenetic proteins. Spine 7, S2, 2002.
15. Nanno, K., Sugiyasu, K., Daimon, T., Yoshikawa, H., and Myoui, A. Synthetic alginate is a carrier of OP-1 for bone induction. Clin Orthop Relat Res 467, 3149, 2009.
16. Wang, E.A., Rosen, V., D'Alessandro, J.S., Bauduy, M., Cordes, P., and Harada, T. Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci USA 87, 2220, 1990.
17. Chen, D., Zhao, M., and Mundy, G.R. Bone morphogenetic proteins. Growth Factors 22, 233, 2004.
18. Terheyden, H., Knak, C., Jepsen, S., Palmie, S., and Rueger, D.R. Mandibular reconstruction with a prefabricated vascularized bone graft using recombinant human osteogenic protein-1: an experimental study in miniature pigs. Part I: prefabrication. Int J Oral Maxillofac Surg 30, 373, 2001.
19. Terheyden, H., Warnke, P., Dunsche, A., Jepsen, S., Brenner, W., and Palmie, S. Mandibular reconstruction with prefabricated vascularized bone grafts using recombinant human osteogenic protein-1: an experimental study in miniature pigs. Part II: transplantation. Int J Oral Maxillofac Surg 30, 469, 2001.
20. Terheyden, H., Menzel, C., Wang, H., Springer, I.N., Rueger, D.R., and Acil, Y. Prefabrication of vascularized bone grafts using recombinant human osteogenic protein-1-part 3: dosage of rhOP-1, the use of external and internal scaffolds. Int J Oral Maxillofac Surg 33, 164, 2004.
21. Warnke, P.H., Springer, I.N., Wiltfang, J., Acil, Y., Eufinger, H., and Terheyden, H. Growth and transplantation of a custom vascularised bone graft in a man. Lancet 364, 766, 2004.
22. Glowacki, J. Angiogenesis in fracture repair. Clin Orthop Relat Res 355, S82, 1998.
23. Collin-Osdoby, P. Role of vascular endothelial cells in bone biology. J Cell Biochem 55, 304, 1994.
24. Kurt, D., Hankenson, K.D., Dishowitz, M., Gray, C., and Schenker, M. Angiogenesis in bone regeneration. Injury 42, 556, 2011.
25. Zou, D., Zhang, Z., He, J., Zhang, K., Ye, D., and Han, W. Blood vessel formation in the tissue-engineered bone with the constitutively active form of HIF-1a mediated BMSCs. Biomaterials 33, 2097, 2012.
26. Guo, X., Zheng, Q., Kulbatski, I., Yuan, Q., Yang, S., and Shao, Z. Bone regeneration with active angiogenesis by basic fibroblast growth factor gene transfected mesenchymal stem cells seeded on porous beta-TCP ceramic scaffolds. Biomed Mater 1, 93, 2006.
27. Keramaris, N.C., Calori, G.M., Nikolaou, V.S., Schemitsch, E.H., and Giannoudis, P.V. Fracture vascularity and bone healing: a systematic review of the role of VEGF. Injury 39, S45, 2008.
28. Kempen, D.H., Lu, L., Heijink, A., Hefferan, T.E., Creemers, L.B., and Maran, A. Effect of local sequential VEGF and BMP-2 delivery on ectopic and orthotopic bone regeneration. Biomaterials 30, 2816, 2009.
29. Patel, Z.S., Young, S., Tabata, Y., Jansen, J.A., Wong, M.E., and Mikos, A.G. Dual delivery of an angiogenic and an osteogenic growth factor for bone regeneration in a critical size defect model. Bone 43, 931, 2008.
30. Abukawa, H., Shin, M., Williams, W.B., Vacanti, J.P., Kaban, L.B., and Troulis, M.J. Reconstruction of mandibular defects with autologous tissue-engineered bone. Oral Maxillofac Surg 62, 601, 2004.
31. Nguyen, L.H., Annabi, N., Nikkhah, M., Bae, H., Binan, L., and Park, S. Vascularized bone tissue engineering: approaches for potential improvement. Tissue Eng Part B Rev 18, 363, 2012.
32. Johnson, E.O., Troupis, T., and Soucacos, P.N. Tissueengineered vascularized bone grafts: basic science and clinical relevance to trauma and reconstructive microsurgery. Microsurgery 31, 176, 2011.
33. Scott, M.A., Levi, B., Askarinam, A., Nguyen, A., Rackohn, T., and Ting, K. Brief review of models of ectopic bone formation. Stem Cells Dev 21, 655, 2012.
34. Sun, J.S., Wu, S.Y., and Lin, F.H. The role of musclederived stem cells in bone tissue engineering. Biomaterials 26, 3953, 2005.
35. Young, S., Patel, Z.S., Kretlow, J.D., Murphy, M.B., Mountziaris, P.M. and Baggett, L.S. Dose effect of dual delivery of vascular endothelial growth factor and bone morphogenetic protein-2 on bone regeneration in a rat critical-size defect model. Tissue Eng Part A 15, 2347, 2009.
36. Fiedler, J., Leucht, F., Waltenberger, J., Dehio, C., and Brenner, R.E. VEGF-A and PlGF-1 stimulate chemotactic migration of human mesenchymal progenitor cells. Biochem Biophys Res Commun 334, 561, 2005.
37. Deckers, M.M., Karperien, M., van der Bent, C., Yamashita, T., Papapoulos, S.E., and Löwik, C.W. Expression of vascular endothelial growth factors and their receptors during osteoblast differentiation. Endocrinology 141, 1667, 2000.
38. Wernike, E., Montjovent, M.O., Liu, Y., Wismeijer, D., Hunziker, E.B., and Siebenrock, K.A. VEGF incorporated into calcium phosphate ceramics promotes vascularisation and bone formation in vivo. Eur Cell Mater 19, 30, 2010.
39. Terheyden, H., Lang, N.P., Bierbaum, S., and Stadlinger, B. Osseointegration-communication of cells. Clin Oral Implants Res 23, 1127, 2012.
40. Crisan, M., Yap, S., Casteilla, L., Chen, C.W., Corselli, M., and Peaúlt, B. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3, 301, 2008.
41. Matsuo, K., and Irie, N. Osteoclast-osteoblast communication. Arch Biochem Biophys 473, 201, 2008.
42. Sims, N.A., and Gooi, J.H. Bone remodeling: multiple cellular interactions required for coupling of bone formation and resorption. Semin Cell Dev Biol 19, 444, 2008.
43. Logeart-Avramoglou, D., Oudina, K., Bourguignon, M., Delpierre, L., Nicola, M.A., and Petite, H. In vitro and in vivo bioluminescent quantification of viable stem cells in engineered constructs. Tissue Eng Part C 16, 447, 2010.
44. Becquart, P., Cambon-Binder, A., Monfoulet, L.E., Bourguignon, M., Petite, H., and Logeart-Avramoglou, D. Ischemia is the prime but not the only cause of human multipotent stromal cell death in tissue-engineered constructs in vivo. Tissue Eng Part A 18, 2084, 2012.