Novel therapeutic core-shell hydrogel scaffolds with sequential delivery of cobalt and bone morphogenetic protein-2 for synergistic bone regeneration

Acta Biomaterialia

Volumn 23, Issue , 2015, Pages 295-308

  Perez, Roman A ^a,b   Kim, Joong Hyun ^a,b   Buitrago, Jennifer O ^a,b   Wall, Ivan B ^b,c   Kim, Hae Won ^a,b,d  

^a BK21 Plus NBM Global Research Center for Regenerative Medicine   (South Korea)

^b Dankook University   (South Korea)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d Dankook University   (South Korea)

Author keywords

Angiogenesis; Bone formation; Osteogenesis; Sequential delivery; Therapeutic scaffolds

Indexed keywords

BONE; CELL CULTURE; COBALT; GENE EXPRESSION; HYDROGELS; ION IMPLANTATION; SCAFFOLDS (BIOLOGY); SHELLS (STRUCTURES); TISSUE REGENERATION;

ANGIOGENESIS; BONE FORMATION; BONE MORPHOGENETIC PROTEIN-2; BONE REGENERATION; CO IONS; CORE SHELL; OSTEOGENESIS; OSTEOGENIC; SEQUENTIAL DELIVERY; THERAPEUTIC SCAFFOLD;

PROTEINS;

BONE MORPHOGENETIC PROTEIN 2; CD31 ANTIGEN; COBALT; HYPOXIA INDUCIBLE FACTOR 1ALPHA; VASCULOTROPIN; BMP2 PROTEIN, HUMAN; DRUG COMBINATION; DRUG IMPLANT; HYDROGEL;

ADULT; ANGIOGENESIS; ANIMAL CELL; ARTICLE; BONE DENSITY; BONE DEVELOPMENT; BONE MASS; BONE REGENERATION; CONTROLLED STUDY; CROSS LINKING; GENE EXPRESSION; HYDROGEL; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; UPREGULATION; ADMINISTRATION AND DOSAGE; ANIMAL; CHEMISTRY; DEVICE FAILURE ANALYSIS; DRUG COMBINATION; DRUG EFFECTS; DRUG IMPLANT; DRUG POTENTIATION; MALE; PATHOPHYSIOLOGY; PROSTHESIS DESIGN; RADIOGRAPHY; SKULL FRACTURES; SPRAGUE DAWLEY RAT; TISSUE SCAFFOLD; TREATMENT OUTCOME;

RATTUS;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; BONE REGENERATION; COBALT; DRUG COMBINATIONS; DRUG IMPLANTS; DRUG SYNERGISM; EQUIPMENT FAILURE ANALYSIS; HYDROGELS; MALE; PROSTHESIS DESIGN; RATS; RATS, SPRAGUE-DAWLEY; SKULL FRACTURES; TISSUE SCAFFOLDS; TREATMENT OUTCOME;

EID: 84938197884     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2015.06.002     Document Type: Article

References (37)

1. R.A. Perez, J.E. Won, J.C. Knowles, and H.W. Kim Naturally and synthetic smart composite biomaterials for tissue regeneration Adv. Drug Deliv. Rev. 65 2012 471 496
2. T.A. Einhorn The cell and molecular biology of fracture healing Clin. Orthop. Relat. Res. 355 1998 S7 21
3. Y.R. Yun, J.H. Jang, E. Jeon, W. Kang, J.E. Won, H.W. Kim, and et al. Administration of growth factors for bone regeneration Regen. Med. 7 2012 369 385
4. S. Singh, B.M. Wu, and J.C. Dunn The enhancement of VEGF-mediated angiogenesis by polycaprolactone scaffolds with surface cross-linked heparin Biomaterials 32 2011 2059 2069
5. Z.S. Patel, S. Young, Y. Tabata, J.A. Jansen, M.E. Wong, and A.G. Mikos Dual delivery of an angiogenic and an osteogenic growth factor for bone regeneration in a critical size defect model Bone 43 2008 931 940
6. D.H. Kempen, L. Lu, A. Heijink, T.E. Heffran, L.B. Creemers, A. Maran, and et al. Effect of local sequential VEGF and BMP-2 delivery on ectopic and orthopic bone regeneration Biomaterials 30 2009 2816 2825
7. N.J. Shah, M.L. Macdonald, Y.M. Beben, R.F. Padera, R.E. Samuel, and P.T. Hammond Tunable dual growth factor delivery from polyelectrolyte multilayer films Biomaterials 32 2011 6183 6193
8. R.A. Perez, and H.W. Kim Core-shell deigned scaffolds of alginate/alpha-tricalcium phosphate for the loading and delivery of biological proteins J. Biomed. Mater. Res. A 101 2013 1103 1112
9. R.A. Perez, M. Kim, T.H. Kim, J.H. Kim, J.H. Lee, J.H. Park, and et al. Utilizing core-shell fibrous collagen-alginate hydrogel cell delivery system for bone tissue engineering Tissue Eng. Part A 20 2014 103 114
10. Y. Yuan, G. Hilliard, T. Ferguson, and D.E. Millhorn Cobalt inhibits the interaction between hypoxia-inducible factor-alpha and von Hippel-Lindau protein by direct binding to hypoxia-inducible factor-alpha J. Biol. Chem. 278 2003 15911 15916
11. A. Namiki, E. Brogi, M. Kearney, E.A. Kim, T. Wu, T. Couffinhal, and et al. Hypoxia Induces vascular endothelial growth factor in cultured human endothelial cells J. Biol. Chem. 270 1995 31189 31195
12. M. Zhang, C. Wu, H. Li, J. Yuen, J. Chang, and Y. Xiao Preparation, characterization and in vitro angiogenic capacity of cobalt substituted β-tricalcium phosphate ceramics J. Mater. Chem. 22 2012 21686 21694
13. I. Machida-Sano, Y. Matsuda, and H. Namiki In vitro adhesion of human dermal fibroblasts on iron crosslinked alginate films Biomed. Mater. 4 2009 025008
14. I. Machida-Sano, S. Ogawa, H. Ueda, Y. Kimura, N. Satoh, and H. Namiki Effects of composition of iron-cross-linked alginate hydrogels for cultivation of human dermal fibroblasts Int. J. Biomat. 2012 ID 820513
15. W. Fan, R. Crawford, and Y. Xiao Enhancing in vivo vascularized bone formation by cobalt chloride-treated bone marrow stromal cells in a tissue engineered periosteum model Biomaterials 31 2010 3580 3589
16. H.L. Zeng, Q. Zhong, Y.L. Qin, Q.Q. Bu, X.A. Han, H.T. Jia, and et al. Hypoxia-mimetic agents inhibit proliferation and alter the morphology of human umbilical cord derived mesenchymal stem cells BMC Cell Biol. 12 2011 32
17. R.A. Perez, S. Del Valle, G. Altankov, and M.P. Ginebra Porous hydroxyapatite and gelatin/hydroxyapatite microspheres obtained by calcium phosphate cement emulsion J. Biomed. Mater. Res. B 97 2011 156 166
18. R.A. Perez, K. Riccardi, G. Altankov, and M.-P. Ginebra Dynamic cell culture on calcium phosphate microcarriers for bone tissue engineering applications J. Tissue Eng. 5 2014 2041731414543965
19. J.H. Jang, Y. Ku, C.P. Chung, and S.J. Heo Enhanced fibronectin-mediated cell adhesion of human osteoblast by fibroblast growth factor, FGF-2 Biotechno. Lett. 24 2002 1659 1663
20. K. Schmidt-Bleek, H. Schell, J. Lienau, N. Schulz, P. Hoff, M. Pfaff, and et al. Initial immune reaction and angiogenesis in bone healing J. Tissue Eng. Regen. Med. 2012 10.1002/term.1505
21. S. Young, Z.S. Patel, J.D. Kretlow, M.B. Murphy, P.M. Mountziaris, L.S. Baggett, and et al. 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 2009 2347 2362
22. J. Kanczler, P. Ginty, L. White, N. Clarke, S. Howdle, K. Shakesheff, and et al. The effect of the delivery of vascular endothelial growth factor and bone morphogenic protein-2 to osteoprogenitor cell populations on bone formation Biomaterials 31 2010 1241 1250
23. R.A. Perez, and H.W. Kim Core-shell designed scaffolds for drug delivery and tissue engineering Acta Biomater. 21 2015 2 9
24. W. Fan, R. Crawford, and Y. Xiao Enhancing in vivo vascularized bone formation by cobalt chloride-treated bone marrow stromal cells in a tissue engineered periosteum model Biomaterials 31 2010 3580 3589
25. C. Wu, Y. Zhou, W. Fan, P. Han, J. Chang, J. Yuen, and et al. Hypoxia-mimicking mesoporous bioactive glass scaffolds with controllable cobalt ion release for bone tissue engineering Biomaterials 33 2012 2076 2085
26. E. Jeon, Y.R. Yun, H.W. Kim, and J.H. Jang Engineering and application of collagen-binding fibroblast growth factor 2 for sustained release J. Biomed. Mater. Res. A 2013 10.1002/jbm.a.34689
27. J.H. Lee, J.H. Park, M. Eltohamy, R. Perez, E.J. Lee, and H.W. Kim Collagen gel combined with mesoporous nanoparticles loading growth factor as a feasible therapeutic three-dimensional depot for neural tissue engineering RSC Adv. 3 2013 24202 24214
28. H. Ren, Y. Cao, Q. Zhao, J. Li, C. Zhou, L. Liao, and et al. Proliferation and differentiation of bone marrow stromal cells under hypoxic conditions Biochem. Biophys. Res. Commun. 347 2006 12 21
29. D.A. Steinbrech, B.J. Mehrara, P.B. Saadeh, J.A. Greenwald, J.A. Spector, G.K. Gittes, and et al. VEGF expression in an osteoblast-like cell line is regulated by a hypoxia response mechanism Am. J. Physiol. Cell Physiol. 278 2000 C853 C860
30. A. Hoeben, B. Landuyt, M.S. Highley, H. Wildiers, A.T. Van Oosterom, and E. De Bruijn Vascular endothelial growth factor and angiogenesis Pharm. Rev. 56 2004 549 580
31. K. Janeczek Portalska, A. Leferink, N. Groen, H. Fernandes, L. Moroni, and et al. Endothelial differentiation of mesenchymal stromal cells PLoS ONE 7 2012 e46842
32. V. Razban, A.S. Lotfi, M. Soleimani, H. Ahmadi, M. Massumi, S. Khajeh, and et al. HIF-1α Overexpression induces angiogenesis in mesenchymal stem cells Biores. Open Access. 1 2012 174 183
33. T. Iwasea, N. Nagaya, T. Fujii, T. Itoh, S. Murakami, and T. Matsumoto Comparison of angiogenic potency between mesenchymal stem cells and mononuclear cells in a rat model of hind limb ischemia Cardiovasc. Res. 66 2005 543 551
34. Hoch. Al, B.Y. Blinder, D.C. Genetos, and J.K. Leach Differentiation-dependent secretion of proangiogenic factors by mesenchymal stem cells PLoS One 7 2012 e35579
35. K. Uematsu, M. Nagata, T. Kawase, K. Suzuki, R. Takagi, and H. Ohgushi Application of stem-cell media to explant culture of human periosteum: An optimal approach for preparing osteogenic cell material J. Tissue Eng. 4 2013 2041731413509646
36. E.J. Sheehy, C.T. Buckley, and D.J. Kelly Oxygen tension regulates the osteogenic, chondrogenic and endochondral phenotype of bone marrow derived mesenchymal stem cells Biochem. Biophys. Res. Commun. 417 2012 305 310
37. D.P. Lennon, J.M. Edmison, and A.I. Caplan Cultivation of rat marrowderived mesenchymal stem cells in reduced oxygen tension: effects on in vitro and in vivo osteochondrogenesis J. Cell Physiol. 187 2001 345 355