Osteogenic differentiation of an osteoblast precursor cell line using composite PCL-gelatin-nHAp electrospun nanofiber mesh

References

• Balcik, C.; Tokdemir, T.; Senkoylu, A.; Koc, N.; Timucin, M.; Akin, S.; Korkusuz, P.; Korkusuz, F. Early Weight Bearing of Porous HA/TCP (60/40) Ceramics in Vivo: A Longitudinal Study in a Segmental Bone Defect Model of Rabbit. Acta Biomater. 2007, 3, 985–996. DOI: https://doi.org/10.1016/j.actbio.2007.04.004.
   PubMed Web of Science ®Google Scholar
• Thian, E. S.; Huang, J.; Best, S. M.; Barber, Z. H.; Bonfield, W. Novel Silicon-Doped Hydroxyapatite (Si-HA) for Biomedical Coatings: An In Vitro Study Using Acellular Simulated Body Fluid. J. Biomed. Mater. Res. Part B Appl. Biomater. 2006, 76, 326–333.
   PubMed Web of Science ®Google Scholar
• Heise, U.; Osborn, J. F.; Duwe, F. Hydroxyapatite Ceramic as a Bone Substitute. Int. Orthop. 1990, 14, 329–338.
   PubMed Web of Science ®Google Scholar
• Shadanbaz, S.; Dias, G. J. Calcium Phosphate Coatings on Magnesium Alloys for Biomedical Applications: A Review. Acta Biomater. 2012, 8, 20–30. DOI: https://doi.org/10.1016/j.actbio.2011.10.016.
   PubMed Web of Science ®Google Scholar
• Liu, B.; Lun, D. X. Current Application of β-tricalcium phosphate composites in orthopaedics. Orthop. Surg. 2012, 4, 139–144. DOI: https://doi.org/10.1111/j.1757-7861.2012.00189.x.
   PubMedGoogle Scholar
• Vallittu, P. K.; Narhi, T. O.; Hupa, L. Fiber Glass-Bioactive Glass Composite for Bone Replacing and Bone Anchoring Implants. Dent. Mater. 2015, 31, 371–381. DOI: https://doi.org/10.1016/j.dental.2015.01.003.
   PubMed Web of Science ®Google Scholar
• Eglin, D.; Alini, M. Degradable Polymeric Materials for Osteosynthesis: Tutorial. Eur. Cell. Mater. 2008, 16, 80–91. DOI: https://doi.org/10.22203/eCM.v016a09.
   PubMed Web of Science ®Google Scholar
• Christensen, F. B.; Dalstra, M.; Sejling, F.; Overgaard, S.; Bunger, C. Titanium-Alloy Enhances Bone-Pedicle Screw Fixation: mechanical and Histomorphometrical Results of Titanium-Alloy versus Stainless Steel. Eur Spine J. 2000, 9, 97–103. DOI: https://doi.org/10.1007/s005860050218.
   PubMed Web of Science ®Google Scholar
• van der Stok, J.; Koolen, M. K.; de Maat, M. P.; Yavari, S. A.; Alblas, J.; Patka, P.; Verhaar, J. A.; van Lieshout, E. M.; Zadpoor, A. A.; Weinans, H.; Jahr, H. Full Regeneration of Segmental Bone Defects Using Porous Titanium Implants Loaded with BMP-2 Containing Fibrin Gels. Eur. Cell. Mater. 2015, 29, 141. DOI: https://doi.org/10.22203/eCM.v029a11.
   PubMed Web of Science ®Google Scholar
• Tomlinson, A. W.; Comerford, E. J.; Birch, R. S.; Innes, J. F.; Walton, M. B. Mechanical Performance in Axial Compression of a Titanium Polyaxial Locking Plate System in a Fracture Gap Model. Vet. Comp. Orthop. Traumatol. 2015, 28, 88–94.
   PubMed Web of Science ®Google Scholar
• Al-Moraissi, E. A.; Ellis, E. 3rd, Biodegradable and Titanium Osteosynthesis Provide Similar Stability for Orthognathic Surgery. J. Oral Maxillofac. Surg. 2015, 73, 1795–1808. DOI: https://doi.org/10.1016/j.joms.2015.01.035.
   PubMed Web of Science ®Google Scholar
• Paeng, J. Y.; Hong, J.; Kim, C. S.; Kim, M. J. Comparative Study of Skeletal Stability between Bicortical Resorbable and Titanium Screw Fixation after Sagittal Split Ramus Osteotomy for Mandibular prognathism. J. Craniomaxillofac. Surg. 2012, 40, 660–664. DOI: https://doi.org/10.1016/j.jcms.2011.11.001.
   PubMed Web of Science ®Google Scholar
• Jo, J. Y.; Jeong, S. I.; Shin, Y. M.; Kang, S. S.; Kim, S. E.; Jeong, C. M.; Huh, J. B. Sequential Delivery of BMP-2 and BMP-7 for Bone Regeneration Using a Heparinized Collagen Membrane. Int. J. Oral Maxillofac. Surg. 2015, 44, 921–928. DOI: https://doi.org/10.1016/j.ijom.2015.02.015.
   PubMed Web of Science ®Google Scholar
• Geiger, M.; Li, R. H.; Friess, W. Collagen Sponges for Bone Regeneration with rhBMP-2. Adv. Drug Deliv. Rev. 2003, 55, 1613–1629. DOI: https://doi.org/10.1016/j.addr.2003.08.010.
   PubMed Web of Science ®Google Scholar
• John, A.; Hong, L.; Ikada, Y.; Tabata, Y. A Trial to Prepare Biodegradable Collagen-Hydroxyapatite Composites for Bone Repair. J. Biomater. Sci. Polym. Ed. 2001, 12, 689–705. DOI: https://doi.org/10.1163/156856201316883485.
   PubMed Web of Science ®Google Scholar
• Chung, K. M.; Salkin, L. M.; Stein, M. D.; Freedman, A. L. Clinical Evaluation of a Biodegradable Collagen Membrane in Guided Tissue Regeneration. J. Periodontol. 1990, 61, 732–736. DOI: https://doi.org/10.1902/jop.1990.61.12.732.
   PubMed Web of Science ®Google Scholar
• Liu, X.; Ma, P. X. Polymeric Scaffolds for Bone Tissue Engineering. Ann. Biomed. Eng. 2004, 32, 477–486. DOI: https://doi.org/10.1023/B:ABME.0000017544.36001.8e.
   PubMed Web of Science ®Google Scholar
• Silva, G. A.; Coutinho, O. P.; Ducheyne, P.; Reis, R. L. Materials in Particulate Form for Tissue Engineering. 2. Applications in Bone. J. Tissue Eng. Regen. Med. 2007, 1, 97–109. DOI: https://doi.org/10.1002/term.1.
   PubMed Web of Science ®Google Scholar
• Lee, E. J.; Jun, S. H.; Kim, H. E.; Kim, H. W.; Koh, Y. H.; Jang, J. H. Silica Xerogel-Chitosan Nano-Hybrids for Use as Drug Eluting Bone Replacement. J. Mater. Sci. Mater. Med. 2010, 21, 207–214. DOI: https://doi.org/10.1007/s10856-009-3835-9.
   PubMed Web of Science ®Google Scholar
• Tormala, P. Biodegradable Self-Reinforced Composite Materials; Manufacturing Structure and Mechanical Properties. Clin. Mater. 1992, 10, 29. DOI: https://doi.org/10.1016/0267-6605(92)90081-4.
   PubMedGoogle Scholar
• Linhart, W.; Peters, F.; Lehmann, W.; Schwarz, K.; Schilling, A. F.; Amling, M.; Rueger, J. M.; Epple, M. Biologically and Chemically Optimized Composites of Carbonated Apatite and Polyglycolide as Bone Substitution Materials. J. Biomed. Mater. Res. 2001, 54, 162–171. DOI: https://doi.org/10.1002/1097-4636(200102)54:2<162::AID-JBM2>3.0.CO;2-3.
   PubMed Web of Science ®Google Scholar
• Niu, X.; Feng, Q.; Wang, M.; Guo, X.; Zheng, Q. Porous nano-HA/Collagen/PLLA Scaffold Containing Chitosan Microspheres for Controlled Delivery of Synthetic Peptide Derived from BMP-2. J. Control. Release. 2009, 134, 111–117. DOI: https://doi.org/10.1016/j.jconrel.2008.11.020.
   PubMed Web of Science ®Google Scholar
• Lagoa, A. L.; Wedemeyer, C.; von Knoch, M.; Loer, F.; Epple, M. A Strut Graft Substitute Consisting of a Metal Core and a Polymer Surface. J. Mater. Sci. Mater. Med. 2008, 19, 417–424. DOI: https://doi.org/10.1007/s10856-006-0022-0.
   PubMed Web of Science ®Google Scholar
• Ignatius, A. A.; Claes, L. E. In Vitro Biocompatibility of Bioresorbable Polymers: Poly(L, DL-Lactide) and Poly(L-Lactide-co-Glycolide. Biomaterials. 1996, 17, 831–839. DOI: https://doi.org/10.1016/0142-9612(96)81421-9.
   PubMed Web of Science ®Google Scholar
• Vainionpaa, S.; Kilpikari, J.; Laiho, J.; Helevirta, P.; Rokkanen, P.; Tormala, P. Strength and Strength Retention in Vitro, of Absorbable, Self-Reinforced Polyglycolide (PGA) Rods for Fracture Fixation. Biomaterials. 1987, 8, 46–48. DOI: https://doi.org/10.1016/0142-9612(87)90028-7.
   PubMed Web of Science ®Google Scholar
• Ji, Y.; Xu, G. P.; Zhang, Z. P.; Xia, J. J.; Yan, J. L.; Pan, S. H. BMP-2/PLGA Delayed-Release Microspheres Composite Graft, Selection of Bone Particulate Diameters, and Prevention of Aseptic Inflammation for Bone Tissue Engineering. Ann. Biomed. Eng. 2010, 38, 632–639. DOI: https://doi.org/10.1007/s10439-009-9888-6.
   PubMed Web of Science ®Google Scholar
• Fei, Z.; Hu, Y.; Wu, D.; Wu, H.; Lu, R.; Bai, J.; Song, H. Preparation and Property of a Novel Bone Graft Composite Consisting of rhBMP-2 Loaded PLGA Microspheres and Calcium Phosphate Cement. J. Mater. Sci. Mater. Med. 2008, 19, 1109–1116. DOI: https://doi.org/10.1007/s10856-007-3050-5.
   PubMed Web of Science ®Google Scholar
• Ingavle, G. C.; Gionet-Gonzales, M.; Vorwald, C. E.; Bohannon, L. K.; Clark, K.; Galuppo, L. D.; Leach, J. K. Injectable Mineralized Microsphere-Loaded Composite Hydrogels for Bone Repair in a Sheep Bone Defect Model. Biomaterials. 2019, 197, 119–128. DOI: https://doi.org/10.1016/j.biomaterials.2019.01.005.
   PubMed Web of Science ®Google Scholar
• Ingavle, G.; Avadhanam, V.; Zheng, Y.; Liu, C.; Sandeman, S. Biomineralised Interpenetrating Network Hydrogels for Bone Tissue Engineering. Bioinspired. Biomimetic Nanobiomater. 2016, 5, 12–23. DOI: https://doi.org/10.1680/jbibn.15.00013.
   Web of Science ®Google Scholar
• Black, C. R.; Goriainov, V.; Gibbs, D.; Kanczler, J.; Tare, R. S.; Oreffo, R. O. Bone Tissue Engineering. Curr. Mol. Biol. Rep. 2015, 1, 132–140. DOI: https://doi.org/10.1007/s40610-015-0022-2.
   PubMedGoogle Scholar
• De Witte, T. M.; Fratila-Apachitei, L. E.; Zadpoor, A. A.; Peppas, N. A. Bone Tissue Engineering via Growth Factor Delivery: From Scaffolds to Complex Matrices. Regen. Biomater. 2018, 5, 197–211. DOI: https://doi.org/10.1093/rb/rby013.
   PubMed Web of Science ®Google Scholar
• Morris, A. H.; Stamer, D. K.; Kyriakides, T. R. The Host Response to Naturally-Derived Extracellular Matrix Biomaterials. Semin. Immunol. 2017, 29, 72–91. DOI: https://doi.org/10.1016/j.smim.2017.01.002.
   PubMed Web of Science ®Google Scholar
• Liu, Y.; Lim, J.; Teoh, S. H. Review: development of Clinically Relevant Scaffolds for Vascularised Bone Tissue Engineering. Biotechnol. Adv. 2013, 31, 688–705. DOI: https://doi.org/10.1016/j.biotechadv.2012.10.003.
   PubMed Web of Science ®Google Scholar
• Shrivats, A. R.; McDermott, M. C.; Hollinger, J. O. Bone Tissue Engineering: State of the Union. Drug Discov. Today. 2014, 19, 781–786. DOI: https://doi.org/10.1016/j.drudis.2014.04.010.
   PubMed Web of Science ®Google Scholar
• Lee, H.; Yeo, M.; Ahn, S.; Kang, D. O.; Jang, C. H.; Lee, H.; Park, G. M.; Kim, G. H. Designed Hybrid Scaffolds Consisting of Polycaprolactone Microstrands and Electrospun Collagen-Nanofibers for Bone Tissue Regeneration. J. Biomed. Mater. Res. Part B Appl. Biomater. 2011, 97, 263–270.
   PubMed Web of Science ®Google Scholar
• Kang, H. G.; Kim, S. Y.; Lee, Y. M. Novel Porous Gelatin Scaffolds by Overrun/Particle Leaching Process for Tissue Engineering Applications. J. Biomed. Mater. Res. Part B Appl. Biomater. 2006, 79, 388–397.
   PubMed Web of Science ®Google Scholar
• Khan, Y. M.; Katti, D. S.; Laurencin, C. T. Novel Polymer-Synthesized Ceramic Composite-Based System for Bone Repair: An in Vitro Evaluation. J. Biomed. Mater. Res. A. 2004, 69, 728–737.
   PubMed Web of Science ®Google Scholar
• Athanasiou, K. A.; Zhu, C.; Lanctot, D. R.; Agrawal, C. M.; Wang, X. Fundamentals of Biomechanics in Tissue Engineering of Bone. Tissue Eng. 2000, 6, 361–381. DOI: https://doi.org/10.1089/107632700418083.
   PubMedGoogle Scholar
• He, J.; Guo, J.; Jiang, B.; Yao, R.; Wu, Y.; Wu, F. Directing the Osteoblastic and Chondrocytic Differentiations of Mesenchymal Stem Cells: matrix vs. induction Media. Regen. Biomater. 2017, 4, 269–279. DOI: https://doi.org/10.1093/rb/rbx008.
   PubMed Web of Science ®Google Scholar
• Rodrigues, C. V.; Serricella, P.; Linhares, A. B.; Guerdes, R. M.; Borojevic, R.; Rossi, M. A.; Duarte, M. E.; Farina, M. Characterization of a Bovine Collagen-Hydroxyapatite Composite Scaffold for Bone Tissue Engineering. Biomaterials. 2003, 24, 4987–4997. DOI: https://doi.org/10.1016/S0142-9612(03)00410-1.
   PubMed Web of Science ®Google Scholar
• Wahl, D. A.; Czernuszka, J. T. Collagen-Hydroxyapatite Composites for Hard Tissue Repair. Eur. Cell. Mater. 2006, 11, 43–56. DOI: https://doi.org/10.22203/eCM.v011a06.
   PubMed Web of Science ®Google Scholar
• Fernandez-Yague, M. A.; Abbah, S. A.; McNamara, L.; Zeugolis, D. I.; Pandit, A.; Biggs, M. J. Biomimetic Approaches in Bone Tissue Engineering: Integrating Biological and Physicomechanical Strategies. Adv. Drug Deliv. Rev. 2015, 84, 1–29. DOI: https://doi.org/10.1016/j.addr.2014.09.005.
   PubMed Web of Science ®Google Scholar
• Sanaei-Rad, P.; Jafarzadeh Kashi, T. S.; Seyedjafari, E.; Soleimani, M. Enhancement of Stem Cell Differentiation to Osteogenic Lineage on Hydroxyapatite-Coated Hybrid PLGA/Gelatin Nanofiber Scaffolds. Biologicals. 2016, 44, 511–516. DOI: https://doi.org/10.1016/j.biologicals.2016.09.002.
   PubMed Web of Science ®Google Scholar
• Jayaraman, K.; Kotaki, M.; Zhang, Y.; Mo, X.; Ramakrishna, S. Recent Advances in Polymer Nanofibers. J. Nanosci. Nanotechnol. 2004, 4, 52–52.
   PubMed Web of Science ®Google Scholar
• Doshi, J.; H, R. D. Electrospinning Process and Application of Electrospun Fibers. J. Electrostat. 1995, 35, 151–160. DOI: https://doi.org/10.1016/0304-3886(95)00041-8.
   Web of Science ®Google Scholar
• Ingavle, G. C.; Leach, J. K. Advancements in Electrospinning of Polymeric Nanofibrous Scaffolds for Tissue Engineering. Tissue Eng. Part B Rev. 2014, 20, 277–293. DOI: https://doi.org/10.1089/ten.teb.2013.0276.
   PubMed Web of Science ®Google Scholar
• Law, J. X.; Liau, L. L.; Saim, A.; Yang, Y.; Idrus, R. Electrospun Collagen Nanofibers and Their Applications in Skin Tissue Engineering. Tissue Eng. Regen. Med. 2017, 14, 699–718. DOI: https://doi.org/10.1007/s13770-017-0075-9.
   PubMed Web of Science ®Google Scholar
• Matsumoto, T.; Kawakami, M.; Kuribayashi, K.; Takenaka, T.; Minamide, A.; Tamaki, T. Effects of Sintered Bovine Bone on Cell Proliferation, Collagen Synthesis, and Osteoblastic Expression in MC3T3-E1 Osteoblast-like Cells. J. Orthop. Res. 1999, 17, 586–592. DOI: https://doi.org/10.1002/jor.1100170419.
   PubMed Web of Science ®Google Scholar
• El-Ghannam, A.; Ducheyne, P.; Shapiro, I. M. Porous Bioactive Glass and Hydroxyapatite Ceramic Affect Bone Cell Function in Vitro along Different Time Lines. J. Biomed. Mater. Res. 1997, 36, 167–180. DOI: https://doi.org/10.1002/(SICI)1097-4636(199708)36:2<167::AID-JBM5>3.0.CO;2-I.
   PubMed Web of Science ®Google Scholar
• Guo, Z.; Xu, J.; Ding, S.; Li, H.; Zhou, C.; Li, L. In Vitro Evaluation of Random and Aligned Polycaprolactone/Gelatin Fibers via Electrospinning for Bone Tissue Engineering. J. Biomater. Sci. Polym. Ed. 2015, 26, 989–1001. DOI: https://doi.org/10.1080/09205063.2015.1065598.
   PubMed Web of Science ®Google Scholar
• Ren, K.; Wang, Y.; Sun, T.; Yue, W.; Zhang, H. Electrospun PCL/Gelatin Composite Nanofiber Structures for Effective Guided Bone Regeneration Membranes. Mater. Sci. Eng. C Mater Biol. Appl. 2017, 78, 324–332. DOI: https://doi.org/10.1016/j.msec.2017.04.084.
   PubMed Web of Science ®Google Scholar
• Safaeijavan, R.; Soleimani, M.; Divsalar, A.; Eidi, A.; Ardeshirylajimi, A. Biological Behavior Study of Gelatin Coated PCL Nanofiberous Electrospun Scaffolds Using Fibroblasts. J. Paramed. Sci. 2015, 5, 67.
   Google Scholar
• Rezaei, A.; Mohammadi, M. R. In Vitro Study of Hydroxyapatite/Polycaprolactone (HA/PCL) Nanocomposite Synthesized by an in Situ Sol-Gel Process. Mater. Sci. Eng. C Mater. Biol. Appl. 2013, 33, 390–396. DOI: https://doi.org/10.1016/j.msec.2012.09.004.
   PubMed Web of Science ®Google Scholar
• Kim, B. R.; Nguyen, T. B.; Min, Y. K.; Lee, B. T. In Vitro and in Vivo Studies of BMP-2-Loaded PCL-gelatin-BCP Electrospun Scaffolds. Tissue Eng. Part A. 2014, 20, 3279–3289. DOI: https://doi.org/10.1089/ten.tea.2014.0081.
   PubMed Web of Science ®Google Scholar
• Rong, D.; Chen, P.; Yang, Y.; Li, Q.; Wan, W.; Fang, X.; Zhang, J.; Han, Z.; Tian, J.; Ouyang, J. Fabrication of Gelatin/PCL Electrospun Fiber Mat with Bone Powder and the Study of Its Biocompatibility. JFB. 2016, 7, 6. DOI: https://doi.org/10.3390/jfb7010006.
   Google Scholar
• Sattary, M.; Rafienia, M.; Khorasani, M. T.; Salehi, H. The Effect of Collector Type on the Physical, Chemical, and Biological Properties of Polycaprolactone/Gelatin/Nano-Hydroxyapatite Electrospun Scaffold. J. Biomed. Mater. Res. Part B Appl. Biomater. 2019, 107, 933–950. DOI: https://doi.org/10.1002/jbm.b.34188.
   PubMed Web of Science ®Google Scholar
• Czekanska, E. M.; Stoddart, M. J.; Richards, R. G.; Hayes, J. S. In Search of an Osteoblast Cell Model for in Vitro Research. Eur. Cell. Mater. 2012, 24, 1–17. DOI: https://doi.org/10.22203/eCM.v024a01.
   PubMed Web of Science ®Google Scholar
• Davis, H. E.; Rao, R. R.; He, J.; Leach, J. K. Biomimetic Scaffolds Fabricated from Apatite-Coated Polymer Microspheres. J. Biomed. Mater. Res A. 2009, 90, 1021–1031.
   PubMed Web of Science ®Google Scholar
• He, J. W.; Genetos, D. C.; Yellowley, C. E.; Leach, J. K. Oxygen Tension Differentially Influences Osteogenic Differentiation of Human Adipose Stem Cells in 2D and 3D Cultures. J. Cell. Biochem. 2010, 110, 87–96.
   PubMed Web of Science ®Google Scholar
• Zhao, L.; He, C.; Gao, Y.; Cen, L.; Cui, L.; Cao, Y. Preparation and Cytocompatibility of PLGA Scaffolds with Controllable Fiber Morphology and Diameter Using Electrospinning Method. J. Biomed. Mater. Res. Part B Appl. Biomater. 2008, 87, 26–34.
   PubMed Web of Science ®Google Scholar
• Ji, Y.; Ghosh, K.; Shu, X. Z.; Li, B.; Sokolov, J. C.; Prestwich, G. D.; Clark, R. A.; Rafailovich, M. H. Electrospun Three-Dimensional Hyaluronic Acid Nanofibrous Scaffolds. Biomaterials. 2006, 27, 3782–3792. DOI: https://doi.org/10.1016/j.biomaterials.2006.02.037.
   PubMed Web of Science ®Google Scholar
• Webb, K.; Hlady, V.; Tresco, P. A. Relationships among Cell Attachment, Spreading, Cytoskeletal Organization, and Migration Rate for Anchorage-Dependent Cells on Model Surface. J. Biomed. Mater. Res. 2000, 49, 362–368. DOI: https://doi.org/10.1002/(SICI)1097-4636(20000305)49:3<362::AID-JBM9>3.0.CO;2-S.
   PubMed Web of Science ®Google Scholar
• Ba Linh, N. T.; Min, Y. K.; Lee, B. T. Hybrid Hydroxyapatite Nanoparticles-Loaded PCL/GE Blend Fibers for Bone Tissue Engineering. J. Biomater. Sci. Polym. Ed. 2013, 24, 520–538. DOI: https://doi.org/10.1080/09205063.2012.697696.
   PubMed Web of Science ®Google Scholar
• Hassan, M. I.; Sultana, N.; Hamdan, S. Bioactivity Assessment of Poly (ε-Caprolactone)/Hydroxyapatite Electrospunfibers for Bone Tissue Engineering Application. J. Nanomater. 2014, 2014, 1–6.
   Web of Science ®Google Scholar
• Orimo, H.; Shimada, T. The Role of Tissue-Nonspecific Alkaline Phosphatase in the Phosphate-Induced Activation of Alkaline Phosphatase and Mineralization in SaOS-2 Human Osteoblast-like Cells. Mol. Cell. Biochem. 2008, 315, 51–60. DOI: https://doi.org/10.1007/s11010-008-9788-3.
   PubMed Web of Science ®Google Scholar
• Golub, E. E.; Harrison, G.; Taylor, A. G.; Camper, S.; Shapiro, I. M. The Role of Alkaline Phosphatase in Cartilage Mineralization. Bone Miner. 1992, 17, 273–278. DOI: https://doi.org/10.1016/0169-6009(92)90750-8.
   PubMedGoogle Scholar