Sequential VEGF and BMP-2 releasing PLA-PEG-PLA scaffolds for bone tissue engineering: I. Design and in vitro tests

References

• Angelopoulou A, Voulgari E, Diamanti EK, Gournis D, Avgoustakis K. 2015. Graphene oxide stabilized by PLA-PEG copolymers for the controlled delivery of paclitaxel. Eur J Pharm Biopharm. 93:18–26.
   PubMed Web of Science ®Google Scholar
• Aydin HM, Korkusuz P, Vargel I, Kılıç E, Güzel E, Çavuşoğlu T, Uçgan D, Pişkin E. 2011. A 6-month in vivo study of polymer/mesenchymal stem cell constructs for cranial defects. J Bioact Compat Polym. 26:207–221.
   Web of Science ®Google Scholar
• Bhat S, Kumar A. 2012. Cell proliferation on three-dimensional chitosan-agarose-gelatin cryogel scaffolds for tissue engineering applications. J Biosci Bioeng. 114:663–670.
   PubMed Web of Science ®Google Scholar
• Bölgen N, Korkusuz P, Vargel İ, Kılıç E, Güzel E, Çavuşoğlu T, Uçkan D, Pişkin E. 2014. Stem cell suspension injected HEMA-lactate-dextran cryogels for regeneration of critical sized bone defects. Artif Cells Nanomed Biotechnol. 42:70–77.
   PubMed Web of Science ®Google Scholar
• Bölgen N, Plieva F, Galaev IY, Mattiasson B, Pişkin E. 2007. Cryogelation for preparation of novel biodegradable tissue-engineering scaffolds. J Biomater Sci Polym Ed. 18:1165–1179.
   PubMed Web of Science ®Google Scholar
• Chen G, Ushida T, Tateishi T. 2002. Scaffold design for tissue engineering. Macromol Biosci. 2:67–77.
   Web of Science ®Google Scholar
• Cho TJ, Gerstenfeld LC, Einhorn TA. 2002. Differential temporal expression of members of the transforming growth factor β superfamily during murine fracture healing. J Bone Miner Res. 17:513–520.
   PubMed Web of Science ®Google Scholar
• Deckers MM, van Bezooijen RL, van der Horst G, Hoogendam J, van der Bent C, Papapoulos SE, Löwik CW. 2002. Bone morphogenetic proteins stimulate angiogenesis through osteoblast-derived vascular endothelial growth factor A. Endocrinology. 143:1545–1553.
   PubMed Web of Science ®Google Scholar
• Do Kim H, Bae EH, Kwon IC, Pal RR, Do Nam J, Lee DS. 2004. Effect of PEG-PLLA diblock copolymer on macroporous PLLA scaffolds by thermally induced phase separation. Biomaterials. 25:2319–2329.
   PubMed Web of Science ®Google Scholar
• Eckardt H, Ding M, Lind M, Hansen ES, Christensen KS, Hvid I. 2005. Recombinant human vascular endothelial growth factor enhances bone healing in an experimental nonunion model. J Bone Joint Surg Br Vol. 87:1434–1438.
   PubMedGoogle Scholar
• Eczacıoğlu N. 2015. Production of porous PLA-PEG copolymer tissue scaffolds releasing VEGF165 and BMP-2 sequentially in mandibular bone defects [master of science dissertation]. [Tokat (Turkey)]: Gaziosmanpaşa University.
   Google Scholar
• Eğri S. 2009. Synthesis/characterization of poly(L-lactide/ɛ-caprolactone)-polyethyleneglycol terpolymers and investigation of applicability of porous scaffolds made of these polymers within tissue engineering concept [doctoral dissertation]. [Ankara (Turkey)]: Hacettepe University.
   Google Scholar
• Gerstenfeld LC, Cullinane DM, Barnes GL, Graves DT, Einhorn TA. 2003. Fracture healing as a post‐natal developmental process: molecular, spatial, and temporal aspects of its regulation. J Cell Biochem. 88:873–884.
   PubMed Web of Science ®Google Scholar
• Groeneveld EH, Burger EH. 2000. Bone morphogenetic proteins in human bone regeneration. Eur J Endocrinol. 142:9–21.
   PubMed Web of Science ®Google Scholar
• Harwood PJ, Newman JB, Michael AL. 2010. (ii) An update on fracture healing and non-union. Orthop Trauma. 24:9–23.
   Web of Science ®Google Scholar
• Hou Q, Grijpma DW, Feijen J. 2003. Porous polymeric structures for tissue engineering prepared by a coagulation, compression moulding and salt leaching technique. Biomaterials. 24:1937–1947.
   PubMed Web of Science ®Google Scholar
• Huang YC, Kaigler D, Rice KG, Krebsbach PH, Mooney DJ. 2005. Combined angiogenic and osteogenic factor delivery enhances bone marrow stromal cell‐driven bone regeneration. J Bone Miner Res. 20:848–857.
   PubMed Web of Science ®Google Scholar
• Kaigler D, Krebsbach PH, West ER, Horger K, Huang YC, Mooney DJ. 2005. Endothelial cell modulation of bone marrow stromal cell osteogenic potential. FASEB J. 19:665–667.
   PubMed Web of Science ®Google Scholar
• Kaigler D, Wang Z, Horger K, Mooney DJ, Krebsbach PH. 2006. VEGF scaffolds enhance angiogenesis and bone regeneration in irradiated osseous defects. J Bone Miner Res. 21:735–744.
   PubMed Web of Science ®Google Scholar
• Kanczler JM, Ginty PJ, White L, Clarke NM, Howdle SM, Shakesheff KM, Oreffo RO. 2010. The effect of the delivery of vascular endothelial growth factor and bone morphogenic protein-2 to osteoprogenitor cell populations on bone formation. Biomaterials. 31:1242–1250.
   PubMed Web of Science ®Google Scholar
• Kang Q, Sun MH, Cheng H, Peng Y, Montag AG, Deyrup AT, et al. 2004. Characterization of the distinct orthotopic bone-forming activity of 14 BMPs using recombinant adenovirus-mediated gene delivery. Gene Ther. 11:1312–1320.
   PubMed Web of Science ®Google Scholar
• Kempen DH, Lu L, Classic KL, Hefferan TE, Creemers LB, Maran A, Dhert WJ, Yaszemski MJ. 2008a. Non-invasive screening method for simultaneous evaluation of in vivo growth factor release profiles from multiple ectopic bone tissue engineering implants. J Control Release. 130:15–21.
   PubMed Web of Science ®Google Scholar
• Kempen DH, Lu L, Hefferan TE, Creemers LB, Maran A, Classic KL, Dhert WJ, Yaszemski MJ. 2008b. Retention of in vitro and in vivo BMP-2 bioactivities in sustained delivery vehicles for bone tissue engineering. Biomaterials. 29:3245–3252.
   PubMed Web of Science ®Google Scholar
• Kempen DH, Lu L, Heijink A, Hefferan TE, Creemers LB, Maran A, Yaszemski MJ, Dhert WJ. 2009. Effect of local sequential VEGF and BMP-2 delivery on ectopic and orthotopic bone regeneration. Biomaterials. 30:2816–2825.
   PubMed Web of Science ®Google Scholar
• Komatsu DE, Hadjiargyrou M. 2004. Activation of the transcription factor HIF-1 and its target genes, VEGF, HO-1, iNOS, during fracture repair. Bone. 34:680–688.
   PubMed Web of Science ®Google Scholar
• Kozawa O, Matsuno H, Uematsu T. 2001. Involvement of p70 S6 kinase in bone morphogenetic protein signaling: vascular endothelial growth factor synthesis by bone morphogenetic protein‐4 in osteoblasts. J Cell Biochem. 81:430–436.
   PubMed Web of Science ®Google Scholar
• Lannutti J, Reneker D, Ma T, Tomasko D, Farson D. 2007. Electrospinning for tissue engineering scaffolds. Mater Sci Eng C. 27:504–509.
   Web of Science ®Google Scholar
• Lee WC, Li YC, Chu I. 2006. Amphiphilic poly (D, L‐lactic acid)/poly (ethylene glycol)/poly (D, L‐lactic acid) nanogels for controlled release of hydrophobic drugs. Macromol Biosci. 6:846–854.
   PubMed Web of Science ®Google Scholar
• Li JZ, Li H, Sasaki T, Holman D, Beres B, Dumont RJ, et al. 2003. Osteogenic potential of five different recombinant human bone morphogenetic protein adenoviral vectors in the rat. Gene Ther. 10:1735–1743.
   PubMed Web of Science ®Google Scholar
• Liu X, Ma PX. 2004. Polymeric scaffolds for bone tissue engineering. Ann Biomed Eng. 32:477–486.
   PubMed Web of Science ®Google Scholar
• Lozinsky V, Plieva FM, Galaev YU, Mattiasson B, et al. 2002. The potential of polymeric cryogels in bioseparation. Bioseparation. 10:163–188.
   Google Scholar
• Mattiasson B, Galaev I, Lozinsky V, Plieva F. 2005. U.S. Patent No. US 20050019770 A1. Washington (DC): U.S. Patent and Trademark Office.
   Google Scholar
• Niikura T, Hak DJ, Reddi AH. 2006. Global gene profiling reveals a downregulation of BMP gene expression in experimental atrophic nonunions compared to standard healing fractures. J Orthop Res. 24:1463–1471.
   PubMed Web of Science ®Google Scholar
• Ozturk BY, Inci I, Egri S, Ozturk AM, Yetkin H, Goktas G, et al. 2013. The treatment of segmental bone defects in rabbit tibiae with vascular endothelial growth factor (VEGF)-loaded gelatin/hydroxyapatite “cryogel” scaffold. Eur J Orthop Surg Traumatol. 23:767–774.
   PubMedGoogle Scholar
• Patel ZS, Young S, Tabata Y, Jansen JA, Wong ME, Mikos AG. 2008. Dual delivery of an angiogenic and an osteogenic growth factor for bone regeneration in a critical size defect model. Bone. 43:931–940.
   PubMed Web of Science ®Google Scholar
• Peng H, Usas A, Olshanski A, Ho AM, Gearhart B, Cooper GM, Huard J. 2005. VEGF improves, whereas sFlt1 inhibits, BMP2-induced bone formation and bone healing through modulation of angiogenesis. J Bone Miner Res. 20:2017–2027.
   PubMed Web of Science ®Google Scholar
• Peng H, Wright V, Usas A, Gearhart B, Shen HC, Cummins J, Huard J. 2002. Synergistic enhancement of bone formation and healing by stem cell-expressed VEGF and bone morphogenetic protein-4. J Clin Invest. 110:751–759.
   PubMed Web of Science ®Google Scholar
• Pufe T, Wildemann B, Petersen W, Mentlein R, Raschke M, Schmidmaier G. 2002. Quantitative measurement of the splice variants 120 and 164 of the angiogenic peptide vascular endothelial growth factor in the time flow of fracture healing: a study in the rat. Cell Tissue Res. 309:387–392.
   PubMed Web of Science ®Google Scholar
• Rashkov I, Manolova N, Li SM, Espartero JL, Vert M. 1996. Synthesis, characterization, and hydrolytic degradation of PLA/PEO/PLA triblock copolymers with short poly (l-lactic acid) chains. Macromolecules. 29:50–56.
   Web of Science ®Google Scholar
• Reignier J, Huneault MA. 2006. Preparation of interconnected poly (ɛ-caprolactone) porous scaffolds by a combination of polymer and salt particulate leaching. Polymer. 47:4703–4717.
   Web of Science ®Google Scholar
• Sampath TK, Maliakal JC, Hauschka PV, Jones WK, Sasak H, Tucker RF, et al. 1992. Recombinant human osteogenic protein-1 (hOP-1) induces new bone formation in vivo with a specific activity comparable with natural bovine osteogenic protein and stimulates osteoblast proliferation and differentiation in vitro. J Biol Chem. 267:20352–20362.
   PubMed Web of Science ®Google Scholar
• Schliephake H. 2002. Bone growth factors in maxillofacial skeletal reconstruction. Int J Oral Maxillofac Surg. 31:469–484.
   PubMed Web of Science ®Google Scholar
• Srivastava RK, Albertsson AC. 2006. Enzyme-catalyzed ring-opening polymerization of seven-membered ring lactones leading to terminal-functionalized and triblock polyesters. Macromolecules. 39:46–54.
   Web of Science ®Google Scholar
• Street J, Bao M, deGuzman L, Bunting S, Peale FV, Ferrara N, et al. 2002. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci USA. 99:9656–9661.
   PubMed Web of Science ®Google Scholar
• Temenoff JS, Mikos AG. 2000. Review: tissue engineering for regeneration of articular cartilage. Biomaterials. 21:431–440.
   PubMed Web of Science ®Google Scholar
• Uchida S, Sakai A, Kudo H, Otomo H, Watanuki M, Tanaka M, Nagashima M, Nakamura T. 2003. Vascular endothelial growth factor is expressed along with its receptors during the healing process of bone and bone marrow after drill-hole injury in rats. Bone. 32:491–501.
   PubMed Web of Science ®Google Scholar
• Wan Y, Chen W, Yang J, Bei J, Wang S. 2003. Biodegradable poly (L-lactide)-poly (ethylene glycol) multiblock copolymer: synthesis and evaluation of cell affinity. Biomaterials. 24:2195–2203.
   PubMed Web of Science ®Google Scholar
• Wang EA, Rosen V, D’Alessandro JS, Bauduy M, Cordes P, Harada T, et al. 1990. Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci USA. 87:2220–2224.
   PubMed Web of Science ®Google Scholar
• Wang P, Liu X, Zhao L, Weir MD, Sun J, Chen W, Man Y, Xu HH. 2015. Bone tissue engineering via human induced pluripotent, umbilical cord and bone marrow mesenchymal stem cells in rat cranium. Acta Biomater. 18:236–248.
   PubMed Web of Science ®Google Scholar
• Wozney JM. 2002. Overview of bone morphogenetic proteins. Spine. 27:S2–S8.
   PubMed Web of Science ®Google Scholar
• Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA. 1988. Novel regulators of bone formation: molecular clones and activities. Science. 242:1528–1534.
   PubMed Web of Science ®Google Scholar
• Xiao RZ, Zeng ZW, Zhou GL, Wang JJ, Li FZ, Wang AM. 2010. Recent advances in PEG-PLA block copolymer nanoparticles. Int J Nanomed. 5:1057.
   PubMed Web of Science ®Google Scholar
• Zhang H, Xia H, Wang J, Li Y. 2009. High intensity focused ultrasound-responsive release behavior of PLA-b-PEG copolymer micelles. J Control Release. 139:31–39.
   PubMed Web of Science ®Google Scholar
• Zhang ZY, Teoh SH, Hui JH, Fisk NM, Choolani M, Chan JK. 2012. The potential of human fetal mesenchymal stem cells for off-the-shelf bone tissue engineering application. Biomaterials. 33:2656–2672.
   PubMed Web of Science ®Google Scholar