A differential effect of bone morphogenetic protein-2 and vascular endothelial growth factor release timing on osteogenesis at ectopic and orthotopic sites in a large-animal model

Tissue Engineering - Part A

Volumn 18, Issue 19-20, 2012, Pages 2052-2062

  Geuze, Ruth E ^a   Theyse, Lars F H ^b   Kempen, Diederik H R ^a   Hazewinkel, Herman A W ^b   Kraak, Helen Y A ^a   Öner, F Cumhur ^a   Dhert, Wouter J A ^a,b   Alblas, Jacqueline ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM PHOSPHATE; COPOLYMERS; DYNAMICS; FLUORESCENCE MICROSCOPY; TISSUE ENGINEERING;

ANGIOGENESIS; BEAGLE DOG; BILATERAL CONTROL; BIPHASIC CALCIUM PHOSPHATES; BONE FORMATION; BONE GROWTH; BONE MORPHOGENETIC PROTEIN-2; BONE MORPHOGENETIC PROTEINS; BONE TISSUE ENGINEERING; DELIVERY VEHICLE; DIFFERENTIAL EFFECT; DUAL RELEASE; ECTOPIC BONES; FLUOROCHROMES; GROWTH FACTOR; HISTOMORPHOMETRY; IN-VIVO; LOCATION DEPENDENTS; MICRO-PARTICLES; ORTHOTOPIC; OSTEOGENESIS; OSTEOGENICITY; PARASPINAL MUSCLES; POLY(LACTIC-CO-GLYCOLIC ACID); RELEASE PROFILES; SUSTAINED RELEASE; VASCULAR ENDOTHELIAL GROWTH FACTOR; VEGF RELEASE;

BONE;

ANIMALIA; CANIS FAMILIARIS;

BONE MORPHOGENETIC PROTEIN 2; LACTIC ACID; POLYGLYCOLIC ACID; POLYLACTIC ACID POLYGLYCOLIC ACID COPOLYMER; POLYLACTIC ACID-POLYGLYCOLIC ACID COPOLYMER; TISSUE SCAFFOLD; VASCULOTROPIN A;

ANIMAL; ARTICLE; BONE DEVELOPMENT; CHEMISTRY; DOG; DRUG EFFECT; METHODOLOGY; TISSUE ENGINEERING;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; DOGS; LACTIC ACID; OSTEOGENESIS; POLYGLYCOLIC ACID; TISSUE ENGINEERING; TISSUE SCAFFOLDS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84867025157     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2011.0560     Document Type: Article

References (55)

1. Silber, J.S., Anderson, D.G., Daffner, S.D., Brislin, B.T., Le-land, J.M., Hilibrand, A.S., Vaccaro, A.R., and Albert, T.J. Donor site morbidity after anterior iliac crest bone harvest for single-level anterior cervical discectomy and fusion. Spine 28, 134, 2003.
2. Finkemeier, C.G. Bone-grafting and bone-graft substitutes. J Bone Joint Surg Am 84-A, 454, 2002.
3. Reddi, A.H., and Haudenschild, D.R. BMP Family. Maryland Heights, MO: Elsevier Academic Press, 2000, p. 747.
4. Wozney, J.M., and Rosen, V. Bone morphogenetic protein and bone morphogenetic protein gene family in bone formation and repair. Clin Orthop Relat Res 346, 26, 1998.
5. Rengachary, S.S. Bone morphogenetic proteins: basic concepts. Neurosurg Focus 13, e2, 2002.
6. Wozney, J.M. Overview of bone morphogenetic proteins. Spine (Phila Pa 1976) 27, S2, 2002.
7. Bessa, P.C., Casal, M., and Reis, R.L. Bone morphogenetic proteins in tissue engineering: the road from laboratory to clinic, part II (BMP delivery). J Tissue Eng Regen Med 2, 81, 2008.
8. Bessa, P.C., Casal, M., and Reis, R.L. Bone morphogenetic proteins in tissue engineering: the road from the laboratory to the clinic, part I (basic concepts). J Tissue Eng Regen Med 2, 1, 2008.
9. Kang, Q., Sun, M.H., Cheng, H., Peng, Y., Montag, A.G., Deyrup, A.T., Jiang, W., Luu, H.H., Luo, J., Szatkowski, J.P., Vanichakarn, P., Park, J.Y., Li, Y., Haydon, R.C., and He, T.C. Characterization of the distinct orthotopic bone-forming activity of 14 BMPs using recombinant adenovirus-mediated gene delivery. Gene Ther 11, 1312, 2004.
10. Nilsson, O.S., Urist, M.R., Dawson, E.G., Schmalzried, T.P., and Finerman, G.A. Bone repair induced by bone morpho-genetic protein in ulnar defects in dogs. J Bone Joint Surg Br 68, 635, 1986.
11. Wang, E.A., Rosen, V., D'Alessandro, J.S., Bauduy, M., Cordes, P., Harada, T., Israel, D.I., Hewick, R.M., Kerns, K.M., LaPan, P., and et al. Recombinant human bone mor-phogenetic protein induces bone formation. Proc Natl Acad Sci U S A 87, 2220, 1990.
12. Hanada, K., Solchaga, L.A., Caplan, A.I., Hering, T.M., Goldberg, V.M., Yoo, J.U., and Johnstone, B. BMP-2 induction and TGF-beta 1 modulation of rat periosteal cell chon-drogenesis. J Cell Biochem 81, 284, 2001.
13. Bostrom, M.P., Lane, J.M., Berberian, W.S., Missri, A.A., Tomin, E., Weiland, A., Doty, S.B., Glaser, D., and Rosen, V.M. Immunolocalization and expression of bone morphogenetic proteins 2 and 4 in fracture healing. J Orthop Res 13, 357, 1995.
14. Govender, S., Csimma, C., Genant, H.K., Valentin-Opran, A., Amit, Y., Arbel, R., Aro, H., Atar, D., Bishay, M., Borner, M.G., Chiron, P., Choong, P., Cinats, J., Courtenay, B., Fei-bel, R., Geulette, B., Gravel, C., Haas, N., Raschke, M., Hammacher, E., van der Velde, D., Hardy, P., Holt, M., Josten, C., Ketterl, R.L., Lindeque, B., Lob, G., Mathevon, H., McCoy, G., Marsh, D., Miller, R., Munting, E., Oevre, S., Nordsletten, L., Patel, A., Pohl, A., Rennie, W., Reynders, P., Rommens, P.M., Rondia, J., Rossouw, W.C., Daneel, P.J., Ruff, S., Ruter, A., Santavirta, S., Schildhauer, T.A., Gekle, C., Schnettler, R., Segal, D., Seiler, H., Snowdowne, R.B., Stapert, J., Taglang, G., Verdonk, R., Vogels, L., Weckbach, A., Wentzensen, A., and Wisniewski, T. Recombinant human bone morphogenetic protein-2 for treatment of open tibial fractures: a prospective, controlled, randomized study of four hundred and fifty patients. J Bone Joint Surg Am 84-A, 2123, 2002.
15. Friedlaender, G.E., Perry, C.R., Cole, J.D., Cook, S.D., Cier-ny, G., Muschler, G.F., Zych, G.A., Calhoun, J.H., LaForte, A.J., and Yin, S. Osteogenic protein-1 (bone morphogenetic protein-7) in the treatment of tibial nonunions. J Bone Joint Surg Am 83-A Suppl 1, S151, 2001.
16. Uludag, H., D'Augusta, D., Palmer, R., Timony, G., and Wozney, J. Characterization of rhBMP-2 pharmacokinetics implanted with biomaterial carriers in the rat ectopic model. J Biomed Mater Res 46, 193, 1999.
17. Cho, T.J., Gerstenfeld, L.C., and Einhorn, T.A. Differential temporal expression of members of the transforming growth factor beta superfamily during murine fracture healing. J Bone Miner Res 17, 513, 2002.
18. Bouletreau, P.J., Warren, S.M., Spector, J.A., Peled, Z.M., Gerrets, R.P., Greenwald, J.A., and Longaker, M.T. Hypoxia and VEGF up-regulate BMP-2 mRNA and protein expression in microvascular endothelial cells: implications for fracture healing. Plast Reconstr Surg 109, 2384, 2002.
19. Komatsu, D.E., and Hadjiargyrou, M. Activation of the transcription factor HIF-1 and its target genes, VEGF, HO-1, iNOS, during fracture repair. Bone 34, 680, 2004.
20. Maes, C., Stockmans, I., Moermans, K., Van Looveren, R., Smets, N., Carmeliet, P., Bouillon, R., and Carmeliet, G. Soluble VEGF isoforms are essential for establishing epiph-yseal vascularization and regulating chondrocyte development and survival. J Clin Invest 113, 188, 2004.
21. Street, J., Bao, M., deGuzman, L., Bunting, S., Peale, F.V., Jr., Ferrara, N., Steinmetz, H., Hoeffel, J., Cleland, J.L., Daugh-erty, A., van Bruggen, N., Redmond, H.P., Carano, R.A., and Filvaroff, E.H. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci U S A 99, 9656, 2002.
22. Kaigler, D., Wang, Z., Horger, K., Mooney, D.J., and Krebsbach, P.H. VEGF scaffolds enhance angiogenesis and bone regeneration in irradiated osseous defects. J Bone Miner Res 21, 735, 2006.
23. Eckardt, H., Ding, M., Lind, M., Hansen, E.S., Christensen, K.S., and Hvid, I. Recombinant human vascular endothelial growth factor enhances bone healing in an experimental nonunion model. J Bone Joint Surg Br 87, 1434, 2005.
24. Villars, F., Guillotin, B., Amedee, T., Dutoya, S., Bordenave, L., Bareille, R., and Amedee, J. Effect of HUVEC on human osteoprogenitor cell differentiation needs heterotypic gap junction communication. Am J Physiol Cell Physiol 282, C775, 2002.
25. Gerber, H.P., Vu, T.H., Ryan, A.M., Kowalski, J., Werb, Z., and Ferrara, N. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochon-dral bone formation. Nat Med 5, 623, 1999.
26. Peng, H., Wright, V., Usas, A., Gearhart, B., Shen, H.C., Cummins, J., and Huard, J. Synergistic enhancement of bone formation and healing by stem cell-expressed VEGF and bone morphogenetic protein-4. J Clin Invest 110, 751, 2002.
27. Mayr-Wohlfart, U., Waltenberger, J., Hausser, H., Kessler, S., Gunther, K.P., Dehio, C., Puhl, W., and Brenner, R.E. Vascular endothelial growth factor stimulates chemotactic migration of primary human osteoblasts. Bone 30, 472, 2002.
28. Engsig, M.T., Chen, Q.J., Vu, T.H., Pedersen, A.C., Ther-kidsen, B., Lund, L.R., Henriksen, K., Lenhard, T., Foged, N.T., Werb, Z., and Delaisse, J.M. Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for os-teoclast recruitment into developing long bones. J Cell Biol 151, 879, 2000.
29. 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.
30. Akeno, N., Czyzyk-Krzeska, M.F., Gross, T.S., and Clemens, T.L. Hypoxia induces vascular endothelial growth factor gene transcription in human osteoblast-like cells through the hypoxia-inducible factor-2alpha. Endocrinology 142, 959, 2001.
31. Kempen, D.H., Creemers, L.B., Alblas, J., Lu, L., Verbout, A.J., Yaszemski, M.J., and Dhert, W.J. Growth factor interactions in bone regeneration. Tissue Eng Part B Rev 16, 551, 2010.
32. Seeherman, H., Wozney, J., and Li, R. Bone morphogenetic protein delivery systems. Spine (Phila Pa 1976) 27, S16, 2002.
33. 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.
34. Peng, H., Usas, A., Olshanski, A., Ho, A.M., Gearhart, B., Cooper, G.M., and Huard, J. VEGF improves, whereas sFlt1 inhibits, BMP2-induced bone formation and bone healing through modulation of angiogenesis. J Bone Miner Res 20, 2017, 2005.
35. Roldan, J.C., Detsch, R., Schaefer, S., Chang, E., Kelantan, M., Waiss, W., Reichert, T.E., Gurtner, G.C., and Deisinger, U. Bone formation and degradation of a highly porous bi-phasic calcium phosphate ceramic in presence of BMP-7, VEGF and mesenchymal stem cells in an ectopic mouse model. J Craniomaxillofac Surg 38, 423, 2010.
36. Kanczler, J.M., Ginty, P.J., White, L., Clarke, N.M., Howdle, S.M., Shakesheff, K.M., and Oreffo, R.O. The effect of the delivery of vascular endothelial growth factor and bone morphogenic protein-2 to osteoprogenitor cell populations on bone formation. Biomaterials 31, 1242, 2009.
37. Zhang, W., Wang, X., Wang, S., Zhao, J., Xu, L., Zhu, C., Zeng, D., Chen, J., Zhang, Z., Kaplan, D.L., and Jiang, X. The use of injectable sonication-induced silk hydrogel for VEGF(165) and BMP-2 delivery for elevation of the maxillary sinus floor. Biomaterials 32, 9415, 2011.
38. Kempen, D.H., Lu, L., Heijink, A., Hefferan, T.E., Creemers, L.B., Maran, A., Yaszemski, M.J., and Dhert, W.J. Effect of local sequential VEGF and BMP-2 delivery on ectopic and orthotopic bone regeneration. Biomaterials 30, 2816, 2009.
39. Kempen, D.H., Lu, L., Classic, K.L., Hefferan, T.E., Cree-mers, L.B., Maran, A., Dhert, W.J., and Yaszemski, M.J. Non-invasive screening method for simultaneous evaluation of in vivo growth factor release profiles from multiple ectopic bone tissue engineering implants. J Control Release 130, 15, 2008.
40. Oldham, J.B., Lu, L., Zhu, X., Porter, B.D., Hefferan, T.E., Larson, D.R., Currier, B.L., Mikos, A.G., and Yaszemski, M.J. Biological activity of rhBMP-2 released from PLGA micro-spheres. J Biomech Eng 122, 289, 2000.
41. Kempen, D.H., Lu, L., Hefferan, T.E., Creemers, L.B., Maran, A., Classic, K.L., Dhert, W.J., and Yaszemski, M.J. Retention of in vitro and in vivo BMP-2 bioactivities in sustained delivery vehicles for bone tissue engineering. Biomaterials 29, 3245, 2008.
42. Rui, J., Dadsetan, M., Runge, M.B., Spinner, R.J., Yaszemski, M.J., Windebank, A.J., and Wang, H. Controlled release of vascular endothelial growth factor using poly-lactic-co-glycolic acid microspheres: in vitro characterization and application in polycaprolactone fumarate nerve conduits. Acta Biomater 8, 511, 2012.
43. Takahashi, Y., Yamamoto, M., and Tabata, Y. Enhanced osteoinduction by controlled release of bone morphogenetic protein-2 from biodegradable sponge composed of gelatin and beta-tricalcium phosphate. Biomaterials 26, 4856, 2005.
44. Theyse, L.F., Oosterlaken-Dijksterhuis, M.A., van Doorn, J., Dhert, W.J., and Hazewinkel, H.A. Growth hormone stimulates bone healing in a critical-sized bone defect model. Clin Orthop Relat Res 446, 259, 2006.
45. van Gaalen, S.M., Kruyt, M.C., Geuze, R.E., de Bruijn, J.D., Alblas, J., and Dhert, W.J. Use of fluorochrome labels in in vivo bone tissue engineering research. Tissue Eng Part B Rev 16, 209, 2010.
46. Kim, T.K., and Burgess, D.J. Pharmacokinetic characterization of 14C-vascular endothelial growth factor controlled release microspheres using a rat model. J Pharm Pharmacol 54, 897, 2002.
47. Yamamoto, M., Takahashi, Y., and Tabata, Y. Controlled release by biodegradable hydrogels enhances the ectopic bone formation of bone morphogenetic protein. Biomaterials 24, 4375, 2003.
48. Yamamoto, M., Ikada, Y., and Tabata, Y. Controlled release of growth factors based on biodegradation of gelatin hy-drogel. J Biomater Sci Polym Ed 12, 77, 2001.
49. Deckers, M.M., Karperien, M., van der Bent, C., Yamashita, T., Papapoulos, S.E., and Lowik, C.W. Expression of vascular endothelial growth factors and their receptors during osteoblast differentiation. Endocrinology 141, 1667, 2000.
50. Young, S., Patel, Z.S., Kretlow, J.D., Murphy, M.B., Mount-ziaris, P.M., Baggett, L.S., Ueda, H., Tabata, Y., Jansen, J.A., Wong, M., and Mikos, A.G. 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.
51. Kakudo, N., Kusumoto, K., Wang, Y.B., Iguchi, Y., and Ogawa, Y. Immunolocalization of vascular endothelial growth factor on intramuscular ectopic osteoinduction by bone morphogenetic protein-2. Life Sci 79, 1847, 2006.
52. Wang, D.S., Yamazaki, K., Nohtomi, K., Shizume, K., Oh-sumi, K., Shibuya, M., Demura, H., and Sato, K. Increase of vascular endothelial growth factor mRNA expression by 1, 25-dihydroxyvitamin D3 in human osteoblast-like cells. J Bone Miner Res 11, 472, 1996.
53. Pintucci, G., Moscatelli, D., Saponara, F., Biernacki, P.R., Baumann, F.G., Bizekis, C., Galloway, A.C., Basilico, C., and Mignatti, P. Lack of ERK activation and cell migration in FGF-2-deficient endothelial cells. FASEB J 16, 598, 2002.
54. Anitua, E., Andia, I., Ardanza, B., Nurden, P., and Nurden, A.T. Autologous platelets as a source of proteins for healing and tissue regeneration. Thromb Haemost 91, 4, 2004.
55. Kruyt, M.C., de Bruijn, J.D., Wilson, C.E., Oner, F.C., van Blitterswijk, C.A., Verbout, A.J., and Dhert, W.J. Viable os-teogenic cells are obligatory for tissue-engineered ectopic bone formation in goats. Tissue Eng 9, 327, 2003.