Bone regeneration induced by an in situ gel-forming poloxamine, bone morphogenetic protein-2 system

Journal of Biomedical Nanotechnology

Volumn 10, Issue 6, 2014, Pages 959-969

  Rodriguez Evora M ^a   Reyes, R ^a   Alvarez Lorenzo, C ^b   Concheiro, A ^b   Delgado, A ^a   Evora C ^a  

^a UNIVERSIDAD DE LA LAGUNA   (Spain)

^b UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

BMP 2; Bone regeneration; Controlled release; Critical bone defect; In situ gelling; In vivo release kinetics; PLGA microspheres; Poloxamine; Scaffold; Syringeability

Indexed keywords

BIOCOMPATIBILITY; BONE; DEFECTS; HYDROGELS; MICROSPHERES; SCAFFOLDS;

BMP-2; BONE DEFECT; BONE REGENERATION; CONTROLLED RELEASE; IN-SITU-GELLING; IN-VIVO; PLGA MICROSPHERES; POLOXAMINES; SYRINGEABILITY;

SCAFFOLDS (BIOLOGY);

BONE MORPHOGENETIC PROTEIN 2; IODINE 125; MICROSPHERE; POLOXAMINE; POLYGLACTIN; POLYMER; TETRONIC 1307; TETRONIC 908; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCOMPATIBILITY; BIOLOGICAL ACTIVITY; BONE REGENERATION; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; HYDROGEL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; ISOTOPE LABELING; MESENCHYMAL STEM CELL; NONHUMAN; OSSIFICATION; POLOXAMINE GELS; RAT; SKULL DEFECT; VISCOELASTICITY;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; BONE REGENERATION; DIFFUSION; DRUG IMPLANTS; ETHYLENEDIAMINES; GELS; MALE; NANOCAPSULES; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; SKULL FRACTURES; TREATMENT OUTCOME;

EID: 84898478863     PISSN: 15507033     EISSN: 15507041     Source Type: Journal    
DOI: 10.1166/jbn.2014.1801     Document Type: Article

References (46)

1. D. Chen, M. Zhao, and G. R. Mundy, Bone morphogenetic proteins. Growth Factors 22, 233 (2004).
2. V. Rosen, BMP2 signaling in bone development and repair. Cytokine Growth Factor Rev. 20, 475 (2009).
3. K. W. Lo, B. D. Ulery, K. M. Ashe, and C. T. Laurencin, Studies of bone morphogenetic protein-based surgical repair. Adv. Drug Deliv. Rev. 64, 1277 (2012).
4. Y. M. Kolambkar, J. D. Boerckel, K. M. Dupont, M. Bajin, N. Huebsch, D. J. Mooney, D. W. Hutmacher, and R. E. Guldberg, Spatiotemporal delivery of bone morphogenetic protein enhances functional repair of segmental bone defects. Bone 49, 485 (2011).
5. A. L. Shimer, F. C. Oner, and A. R. Vaccaro, Spinal reconstruction and bone morphogenetic proteins: Open questions. Injury 40, S32 (2009).
6. K. R. Remya, J. Joseph, S. Mani, A. John, H. K. Varma, and P. Ramesh, Nanohydroxyapatite incorporated electrospun polycaprolactone/ polycaprolactone-polyethyleneglycol-polycaprolactone blend scaffold for bone tissue engineering applications. J. Biomed. Nanotechnol. 9, 1483 (2013).
7. A. Aravamudhan, D. M. Ramos, J. Nip, M. D. Harmon, R. James, M. Deng, C. T. Laurencin, X. Yu, and S. G. Kumbar, Cellulose and collagen derived micro-nano structured scaffolds for bone tissue engineering. J. Biomed. Nanotechnol. 9, 719 (2013).
8. K. I. Jeong, S. G. Kim, J. S. Oh, S. Y. Lee, Y. S. Cho, S. S. Yang, S. C. Park, J. S. You, S. C. Lim, M. A. Jeong, J. S. Kim, and S. Y. Lee, Effect of platelet-rich plasma and platelet-rich fibrin on peri-implant bone defects in dogs. J. Biomed. Nanotechnol. 9, 535 (2013).
9. J. Venkatesan and S. K. Kim, Stimulation of minerals by carbon nanotube grafted glucosamine in mouse mesenchymal stem cells for bone tissue engineering. J. Biomed. Nanotechnol. 8, 676 (2012).
10. K. Bergman, T. Engstrand, S. Piskounova, D. Ossipov, J. Hilborn, and T. Bowden, Injectable cell-free template for bone-tissue formation. J. Biomed. Mater. Res. A 91, 1111 (2009).
11. A. C. Docherty-Skogh, K. Bergman, M. J. Waern, S. Ekman, K. Hultenby, D. Ossipov, J. Hilborn, T. Bowden, and T. Engstrand, Bone morphogenetic protein-2 delivered by hyaluronan-based hydrogel induces massive bone formation and healing of cranial defects in minipigs. Plast. Reconstr. Surg. 125, 383 (2010).
12. J. Kim, I. S. Kim, T. H. Cho, K. B. Lee, S. J. Hwang, G. Tae, I. Noh, S. H. Lee, Y. Park, and K. Sun, Bone regeneration using hyaluronic acid-based hydrogel with bone morphogenic protein-2 and human mesenchymal stem cells. Biomaterials 28, 1830 (2007).
13. J. Patterson, R. Siew, S. W. Herring, A. S. Lin, R. Guldberg, and P. S. Stayton, Hyaluronic acid hydrogels with controlled degradation properties for oriented bone regeneration. Biomaterials 31, 6772 (2010).
14. W. Zhang, X. Wang, S. Wang, J. Zhao, L. Xu, C. Zhu, D. Zeng, J. Chen, Z. Zhang, D. L. Kaplan, and X. Jiang, The use of injectable sonication-induced silk hydrogel forVEGF165andBMP-2delivery for elevation of the maxillary sinus floor. Biomaterials 32, 9415 (2011).
15. E. Martínez-Sanz, D. A. Ossipov, J. Hilborn, S. Larsson, K. B. Jonsson, and O. P. Varghese, Bone reservoir: Injectable hyaluronic acid hydrogel for minimal invasive bone augmentation. J. Control. Release 152, 232 (2011).
16. S. Fu, P. Ni, B. Wang, B. Chu, L. Zheng, F. Luo, J. Luo, and Z. Qian, Injectable and thermo-sensitive PEG-PCL-PEG copolymer/collagen/n-HA hydrogel composite for guided bone regeneration. Biomaterials 33, 4801 (2012).
17. G. Bhakta, B. Rai, Z. X. Lim, J. H. Hui, G. S. Stein, A. J. van Wijnen, V. Nurcombe, G. D. Prestwich, and S. M. Cool, Hyaluronic acid-based hydrogels functionalized with heparin that support controlled release of bioactive BMP-2. Biomaterials 33, 6113 (2012).
18. Q. Wang, S. Jamal, M. S. Detamore, and C. Berkland, PLGA-chitosan/ PLGA-alginate nanoparticles blends as biodegradable colloidal gels for seeding human umbilical cord mesenchymal stem cells. J. Biomed. Mater. Res. Part A 96A, 520 (2011).
19. Q. Wang, J. Wang, Q. Lu, M. S. Detamore, and C. Berkland, Injectable PLGA based colloidal gels for zero-order dexamethasone release in cranial defects. Biomaterials 31, 4980 (2010).
20. A. Rey-Rico, M. Silva, J. Couceiro, A. Concheiro, and C. Alvarez-Lorenzo, Osteogenic efficiency of in situ gelling poloxamine systems with and without bone morphogenetic protein-2. Eur. Cell Mater. 21, 317 (2011).
21. J. Gonzalez-Lopez, C. Alvarez-Lorenzo, P. Taboada, A. Sosnik, I. Sandez-Macho, and A. Concheiro, Self-associative behavior and drug-solubilizing ability of poloxamine (tetronic) block copolymers. Langmuir 24, 10688 (2008).
22. C. Alvarez-Lorenzo, A. Rey-Rico, A. Sosnik, P. Taboada, and A. Concheiro, Poloxamine based nanomaterials for drug delivery. Front. Biosci. 2, 424 (2010).
23. A. Sosnik, B. Leung, A. P. McGuigan, and M. W. Sefton, Collagen/poloxamine hydrogels: Cytocompatibility of embedded HepG2 cells and surface-attached endothelial cells. Tissue Eng. 11, 1807 (2005).
24. A. Sosnik, B. M. Leung, and M. W. Sefton, Lactoylpoloxamine/ collagen matrix for cell-containing tissue engineering modules. J. Biomed. Mater. Res. A 86, 339 (2008).
25. E. C. Ciucurel and M. W. Sefton, A poloxamine-polylysine acrylate scaffold for modular tissue engineering. J. Biomater. Sci. Polym. Ed. 22, 2515 (2011).
26. E. Cho, J. S. Lee, and K. Webb, Formulation and characterization of poloxamine-based hydrogels as tissue sealants. Acta Biomater. 8, 2223 (2012).
27. A. Dog̃an, M. E. Yalvaç, F. Şahin, A. V. Kabanov, A. Palotás, and A. A. Rizvanov, Differentiation of human stem cells is promoted by amphiphilic pluronic block copolymers. Int. J. Nanomedicine 7, 4849 (2012).
28. A. M. Puga, A. Rey-Rico, B. Magariños, C. Alvarez-Lorenzo, and A. Concheiro, Hot melt poly-ε-caprolactone/poloxamine implantable matrices for sustained delivery of ciprofloxacin. Acta Biomater. 8, 1507 (2012).
29. A. Hernandez, R. Reyes, E. Sanchez, M. Rodríguez-Évora, A. Delgado, and C. Évora, In vivo osteogenic response to different ratios of BMP-2 and VEGF released from a biodegradable porous system. J. Biomed. Mater. Res. Part A 100A, 2382 (2012).
30. Z. Huang, P. G. Ren, T. Ma, R. L. Smith, and S. B. Goodman, Modulating osteogenesis of mesenchymal stem cells by modifying growth factor availability. Cytokine 51, 305 (2010).
31. B. De la Riva, C. Nowak, E. Sanchez, A. Hernandez, M. Schulz-Siegmund, M. K. Pec, A. Delgado, and C. Evora, VEGF-controlled release within a bone defect from alginate/chitosan/PLA-H scaffolds. Eur. J. Pharm. Biopharm. 73, 50 (2009).
32. M. Rodríguez-Évora, A. Delgado, R. Reyes, A. Hernández-Daranas, I. Soriano, J. San Román, and C. Évora, Osteogenic effect of local, long versus short term BMP-2 delivery from a novel SPU-PLGA-bTCP concentric system in a critical size defect in rats. Eur. J. Pharm. Sci. 49, 873 (2013).
33. J. J. Delgado, C. Evora, E. Sanchez, M. Baro, and A. Delgado, Validation of a method for non-invasive in vivo measurement of growth factor release from a local delivery system in bone. J. Control. Release 114, 223 (2006).
34. J. D. Moore and H. H. Flanner, Mathematical comparison of dissolution profiles. Pharm. Technol. 20, 64 (1996).
35. U. S. Department of Health and Human Services Food and Drug Administration Center for Drug Evaluation and Research (CDER). Guidance for Industry. Waiver of In Vivo Bioavailability and Bioequivalence Studies for Bioequivalence Studies for Immediate-Release Solid Oral Dosage Forms Based on a Biopharmaceutics Classification System. August (2000), www.fda.gov/downloads/ Drugs/GuidanceComplianceRegulatoryInformation/Guidances/UCM070246.pdf.
36. A. Hernández, E. Sánchez, I. Soriano, R. Reyes, A. Delgado, and C. Evora, Material-related effects of BMP-2 delivery systems on bone regeneration. Acta Biomater. 8, 781 (2012).
37. C. Chaibundit, N. M. P. S. Ricardo, F. M. L. L. Costa, S. G. Yeates, and C. Booth, Micellization and gelation of mixed copolymers P123 and F127 in aqueous solution. Langmuir 23, 9229 (2007).
38. D. S. Jones, B. C. O. Muldoon, A. D. Woolfson, G. P. Andrews, C. P. Mccoy, and F. D. Sanderson, Moisture-activated rheological structuring of nonaqueous poloxamine poly(acrylic acid) systems designed as novel biomedical implants. J. Pharm. Sci. 99, 1838 (2010).
39. I. M. Pelin, S. S. Maeir, G. C. Chitanu, and V. Bulacovschi, Preparation and characterization of a hydroxyapatitecollagen composite as component for injectable bone substitute. Mat. Sci. Eng. C-Mater. 29, 2188 (2009).
40. G. Woerle, B. Siekmann, M. H. J. Koch, and H. Bunje, Transformation of vesicular into cubic nanoparticles by autoclaving of aqueous monoolein/poloxamer dispersions. Eur. J. Pharm. Sci. 27, 44 (2006).
41. S. Piskounova, L. Gedda, G. Hulsart-Billström, J. Hilborn, and T. Bowden, Characterization of recombinant human bone morphogenetic protein-2 delivery from injectable hyaluronan-based hydrogels by means of (125) I-radiolabelling. J. Tissue Eng. Regen. Med. (2012), doi: 10.1002/term.1584.
42. H. K. Kim, W. S. Shim, S. E. Kim, K. H. Lee, E. Kang, J. H. Kim, K. Kim, I. C. Kwon, and D. S. Lee, Injectable in situ-forming pH/thermo-sensitive hydrogel for bone tissue engineering. Tissue Eng. Part A 15, 923 (2009).
43. G. Bhakta, B. Rai, Z. X. Lim, J. H. Hui, G. S. Stein, A. J. van Wijnen, V. Nurcombe, G. D. Prestwich, and S. M. Cool, Hyaluronic acid-based hydrogels functionalized with heparin that support controlled release of bioactive BMP-2. Biomaterials 33, 6113 (2012).
44. M. Kisiel, M. M. Martino, M. Ventura, J. A. Hubbell, J. Hilborn, and D. A. Ossipov, Improving the osteogenic potential of BMP-2 with hyaluronic acid hydrogel modified with integrin-specific fibronectin fragment. Biomaterials 34, 704 (2013).
45. G. Hulsart-Billström, K. Bergman, B. Andersson, J. Hilborn, S. Larsson, and K. B. Jonsson, A uni-cortical femoral defect model in the rat: Evaluation using injectable hyaluronan hydrogel as a carrier for bone morphogenetic protein-2. J. Tissue Eng. Regen. Med. (2012), doi: 10.1002/term.1655.
46. S. Jo, S. Kim, T. H. Cho, E. Shin, S. J. Hwang, and I. Noh, Effects of recombinant human bone morphogenic protein-2 and human bone marrow-derived stromal cells on in vivo bone regeneration of chitosan-poly(ethylene oxide) hydrogel. J. Biomed. Mater. Res. Part A 101, 892 (2013).